LICE (Phthiraptera)

Lice are a menace to humans, pets, and livestock, not only because of their blood-feeding or chewing habits, but also because of their ability to transmit pathogens. The human body louse has been indirectly responsible for influencing human history through its ability to transmit the causative agent of epidemic typhus. However, most of the 3200 known species of lice are ectoparasites of wild birds or mammals and have no known medical or veterinary importance. The order Phthiraptera is divided into two main taxonomic groups: the Anoplura (sucking lice) and Mallophaga (chewing or biting lice). All members of the Anoplura are obligate, hematophagous ectoparasites of placental mammals, whereas the more diverse.

Mallophaga include species that are obligate associates of birds, marsupials, and placental mammals. Although certain chewing lice imbibe blood, most species ingest host feathers, fur, skin, or skin products. Because of the different feeding strategies of the two groups, the blood-feeding Anoplura are far more important than the Mallophaga in transmitting pathogens to their hosts.

TAXONOMY

Major taxonomic syntheses for the sucldng lice include a series of eight volumes by Ferris (1919-1935) that remains the most comprehensive treatment of this group on a worldwide basis. Ferris (1951) updated much of his earlier work in a shorter overview of the group. Kim et al. (1986) have compiled an authoritative manual and identification guide for the sucking lice of North America. Durden and Musser (1994a) provide a taxonomic checldist for the sucking lice of the world, with host records and geographical distribution for each species. The chewing lice are taxonomically less well known than are the sucking lice, and few authoritative identification guides are available. These include a synopsis of the lice associated with laboratory animals (Kim et al. 1973), guides to the lice of domestic animals (Tuff 1977, Price and Graham 1997), and an identification guide to the lice of sub-Saharan Africa (Ledger 1980). These publications provide information on both sucking lice and chewing lice. Checklists of the Mallophaga of the world (Hopkins and Clay 1952) and of North America (Emerson 1972) are useful taxonomic references for this group.

Because of the relatively high degree of host specificity exhibited by both chewing and sucking lice, several host-parasite checklists have been prepared. These include a detailed list of both anopluran and mallophagan lice associated with mammals (Hopkins 1949), a hostparasite list for North American Mallophaga (Emerson 1972), a world host-parasite list for the chewing lice of mammals (Emerson and Price 1981 ), and a host-parasite checklist for the Anoplura of the world (Durden and Musser 1994b).

About 550 species of sucking lice have been described (Durden and Musser 1994a), all of which parasitize placental mammals; these lice are currently assigned to 50 genera and 15 families. About 2650 valid species of Mallophaga have been described; most of these are associated with birds, but about 400 (ca. 15%) parasitize mammals. The Mallophaga can be divided into 3 suborders (Table I), 11 families, and 205 genera.

The Mallophaga are divided into the following three groups (suborders of most authors): Amblycera (seven families, ca. 76 genera, and ca. 850 species), Ischnocera (three families, ca. 130 genera, and ca. 1800 species), and Rhyncophthirina (one family, 1 genus, and 3 species) (Figs. 4.1 and 4.5). However, there has been disagreement regarding the taxonomic rank of these three groups and their relationships to the Anoplura. Many current classifications treat the Phthiraptera as an order and assign suborder (or superfamily) rank to each of the Anoplura, Amblycera, Ischnocera, and Rhyncophthirina. Other classifications treat the Anoplura and Mallophaga as separate orders. Unfortunately, recent phylogenetic analyses of lice based on cladistic principles have produced contradictory results and have failed to resolve this issue. Regardless of current taxonomic interpretations, it is widely agreed that both sucking and chewing lice originated from a common nonparasitic ancestral group closely related to the order Psocoptera (book lice and bark lice). These two groups diverged in the late Jurassic or early Cretaceous Period, 100-150 million years ago.

Sucking lice of medical importance are assigned to two families, the Pediculidae and Pthiridae, whereas sucking lice of veterinary importance are assigned to five families: the Haematopinidae, Hoplopleuridae, Linognathidae, Pedicinidae, and Polyplacidae (Table II). Only one species of chewing louse, the dog biting louse, in the family Trichodectidae, has public health importance. Mallophaga of veterinary significance are typically placed in five families: the Boopiidae, Gyropidae, Menoponidae, Philopteridae, and Trichodectidae (Table I).

Classification and Hosts of Chewing Lice (Mallophaga) of Medical and Veterinary Importance

MORPHOLOGY

Lice are small (0.4-10 mm in the adult stage), wingless, dorso-ventrally flattened insects. The elongate abdomen possesses sclerotized dorsal, ventral, and/or lateral plates in many lice (Fig. 4.2); these provide some rigidity to the abdomen when it is distended by a blood meal or other food source. In adult lice the abdomen has 11 segments and terminates in genitalia and associated sclerotized plates. In females, the genitalia are accompanied by finger-like gonopods, which serve to guide, manipulate, and glue eggs onto host hair or feathers. The abdomen is adorned with numerous setae in most lice. Immature lice closely resemble adults but are smaller, have fewer setae,

(A) Ishnocera; (B)Anoplura; (C)Amblycera; (D) Rhynchopthirina.
FIGURE 4.1 Head and mouthparts ofrepresentatives of each ofthe four principal groups oflice. (A) Ishnocera; (B)Anoplura; (C)Amblycera; (D) Rhynchopthirina. (A, from Price and Graham, 1997; B and D, from Ferris, 1931; C, from Bedford, 1932)

and lack genitalia. After each nymphal molt, the abdomen is beset with progressively more setae, and the overall size of the louse increases.

The male genitalia in lice (Fig. 4.3) are relatively large and conspicuous, sometimes occupying almost half the length of the abdomen. The terminal, extrusable, sclerotized pseudopenis (aedeagus) is supported anteriorly by a basal apodeme. Laterally, it is bordered by a pair of chitinized parameres. Two or four testes are connected to the vas deferens, which coalesces posteriorly to form the vesicula seminalis. In the female, the vagina leads to a large uterus, to which several ovarioles supporting eggs in various stages of development are connected by the oviducts. Two or more large accessory glands, which secrete materials to coat the eggs, and a single spermatheca, in which sperm is stored, are situated posteriorly in the abdomen. Except for the human body louse, all lice cement their eggs, called nits, onto the hair or feathers of their host. Eggs are usually subcylindrical, with rounded ends and a terminal cap, the operculum (Fig. 4.4). On the top of the operculum is a patch of holes or areas with thin cuticle, called micropyles, through which the developing embryo respires. Most of the egg is heavily chitinized, which helps to protect the embryo from mechanical damage and desiccation. A suture of thin cuticle encircles the base of the operculum. At the time of hatching, the first-instar nymph emerges from the egg by cracldng this suture and pushing off the operculum.

In chewing lice, the head is broader than the thorax (Fig. 4.5). Amblyceran chewing lice have four-segmented antennae and have retained the maxillary palps characteristic of their psocopteran-like ancestor. However, ischnoceran chewing lice have three to five antennal segments and lack maxillary palps. In the Amblycera, the antennae are concealed in lateral grooves, whereas in the Ischnocera and Rhyncophthirina, the antennae are free from the head (Figs. 4.1 and 4.5).

There is a gradation in the specialization of the mouthparts and of the internal skeleton of the head, or tentorium, from the psocopteran-like ancestor of the lice through the Amblycera, Ischnocera, Rhyncophthirina, and Anoplura. Although mallophagan lice all possess chewing mouthparts (Fig. 4.6), the components and mechanics of these mouthparts differ for each group. In the Amblycera, the opposable mandibles move in a vertical plane, or perpendicular to the ventral surface of the head, whereas in the Ischnocera they move more or less horizontally. In contrast, the Rhyncophthirina possess tiny mandibles that are situated at the tip of an elongated rostrum (Figs. 4.1D and 4.5F). Through extreme

Classification and Hosts of Sucking Lice (Anoplura) of Medical and Veterinary Importance

modifications, members of the chewing louse genus Trochilocoetes (parasites of humming birds) have evolved mouthparts that can function as sucking organs.

The thorax in chewing lice usually appears as two, and occasionally three, segments. Chewing lice possess one or two simple claws on each leg; species that parasitize highly mobile hosts, especially birds, typically have two claws.

In sucking lice (Figs. 4.2 and 4.7) the head is slender and narrower than the thorax. Anoplura have three- to five-segmented antennae and lack maxillary palps. Eyes are reduced or absent in most sucking lice but are well developed in the medically important genera Pediculus and Pthirus (Fig. 4.7A, B), and ocular points, or eyeless projections posterior to the antennae, are characteristic of sucking lice in the genus Haematopinus (Fig. 4.7E).

As indicated by their name, anopluran mouthparts function as sucking devices during blood feeding

A generalized sucking louse (Anoplura), showing dorsal (left) and ventral (right) morphology.
FIGURE 4.2 A generalized sucking louse (Anoplura), showing dorsal (left) and ventral (right) morphology. (From Ignoffo, 1959.)

(Fig. 4.8). At rest, the mouthparts are withdrawn into the head and are protected by the snoutlike haustellum, representing the highly modified labrum. The haustellum is armed with tiny recurved teeth which hook into the host skin during feeding. The stylets, consisting of a serrated labium, the hypopharynx, and two maxillae, then puncture a small blood vessel (Fig. 4.8). The hypopharynx is a hollow tube through which saliva (containing anticoagulants and enzymes) is secreted. The maxillae oppose each other and are curved to form a food canal through which host blood is imbibed (Fig. 4.9).

In sucking lice, all three thoracic segments are fused and appear as one segment. In most species, the legs terminate in highly specialized claws for grasping the host

Internal abdominal anatomy of a male human body louse (Pediculus humanus humanus).
HGURE 4.3 Internal abdominal anatomy of a male human body louse (Pediculus humanus humanus). (From Ferris, 1951.)
Eggs (nits) of representative lice. (A) Chicken body louse, Menacanthus stramineus; (B) Oval guineapig louse, Gyropus ovalis; (C) Pigeon louse, Columbicola columbae; (D) Cattle biting louse, Bovicola bovis; (E) Elephant louse, Haematomyzus elephantis; (F) Human head louse, Pediculus humanus capitis. (From Marshall, 1981).
FIGURE 4.4 Eggs (nits) of representative lice. (A) Chicken body louse, Menacanthus stramineus; (B) Oval guineapig louse, Gyropus ovalis; (C) Pigeon louse, Columbicola columbae; (D) Cattle biting louse, Bovicola bovis; (E) Elephant louse, Haematomyzus elephantis; (F) Human head louse, Pediculus humanus capitis. (From Marshall, 1981).

pelage. These tibio-tarsal claws consist of a curved tarsal element which opposes a tibial spur (Fig. 4.10) to enclose a space that typically corresponds to the diameter of the host hair.

The internal anatomy of lice (Fig. 4.3) is best known for the human body louse. As in most hematophagous insects, strong cibarial and esophageal muscles produce a sucking action during blood feeding. The esophagus leads to a spacious midgut composed primarily of the ventriculus. The posterior region of the midgut is narrow and forms a connection between the ventriculus and the hindgut. Ventrally, mycetomes containing symbiotic microorganisms connect to the ventriculus.

LIFE HISTORY

Lice are hemimetabolous insects. Following the egg stage, there are three nymphal instars, the last of which molts to an adult. Although there is wide variation between species, the egg stage typically lasts for 4-15 days and each nymphal instar for 3-8 days; adults live for up to 35 days. Under optimal conditions many species of lice can complete 10-12 generations per year, but this is rarely achieved in nature. Host grooming, resistance, molting and feather loss, hibernation, and hormonal changes, as well as predators (especially insectivorous birds on large ungulates), parasites and parasitoids, and unfavorable weather conditions can reduce the number of louse generations.

Fecundities for fertilized female lice vary from 0.2 to 10 eggs per day. Males are unknown in some parthenogenetic species, whereas they typically constitute less than 5% of the adult population in the cattle biting louse and less than 1% in the horse biting louse.

BEHAVIOR AND ECOLOGY

Blood from the host is essential for the successful development and survival of all sucldng lice. Anoplura are vessel feeders, or solenophages, that imbibe blood through a hollow dorsal stylet derived from the hypopharynx (Fig. 4.9). Contraction of powerful cibarial and pharyngeal muscles create a sucking reaction for imbibing blood.

Chewing lice feed by the biting or scraping action of the mandibles. Bird-infesting chewing lice typically use their mandibles to sever small pieces of feather, which drop onto the labrum and are then forced into the mouth. Chewing lice which infest mammals use their mandibles in a similar manner to feed on host fur. Many chewing lice that infest birds and mammals can also feed on other integumental products, such as skin debris and secretions. Some species of chewing lice are obligate, or more frequently facultative, hematophages. Even those species of chewing lice that imbibe blood scrape the host integument until it bleeds. The rhyncophthirinan Haematomyzus elephantis, which parasitizes both African and Asian elephants, feeds in this manner.

Chewing lice (Mallophaga) of veterinary importance, showing dorsal morphology (left) and ventral morphology (right) in each case. Not drawn to scale. (A) Heterodoxus spiniger, male, from carnivores; (B) Tricholipeurus parallelus, female, from New World deer; (C) Sheepbiting louse (Bovicola bovis), female; (D) Dog-biting louse (Trichodectes canis), female; (E) Catbiting louse (Felicola subrostrata), male; (F) Elephant louse (Haematomyzus elephantis), male. (A-E, from Emerson and Price, 1975; F, from Werneck, 1950)
FIGURE 4.5 Chewing lice (Mallophaga) of veterinary importance, showing dorsal morphology (left) and ventral morphology (right) in each case. Not drawn to scale. (A) Heterodoxus spiniger, male, from carnivores; (B) Tricholipeurus parallelus, female, from New World deer; (C) Sheepbiting louse (Bovicola bovis), female; (D) Dog-biting louse (Trichodectes canis), female; (E) Catbiting louse (Felicola subrostrata), male; (F) Elephant louse (Haematomyzus elephantis), male. (A-E, from Emerson and Price, 1975; F, from Werneck, 1950)
Generalized mouthparts of an amblyceran chewing louse (Mallophaga). (A) Ventral view of head; (B) labium and associated structures; (C) mandibles. (Drawn by Margo Duncan)
FIGURE 4.6 Generalized mouthparts of an amblyceran chewing louse (Mallophaga). (A) Ventral view of head; (B) labium and associated structures; (C) mandibles. (Drawn by Margo Duncan)

Symbionts are thought to be present in all lice that imbibe blood. Symbionts in the mycetomes (Fig. 4.3) aid in blood meal digestion, and lice deprived of them die after a few days; female lice lacking symbionts also become sterile. In female human body lice, some symbionts migrate to the ovary, where they are transferred transovarially to the next generation of lice.

Lice in general exhibit host specificity, some to such a degree that they parasitize only one species of host. The hog louse, slender guineapig louse, large turkey louse, and several additional species listed in Tables I and II all are typical parasites of a single host species.

Host specificity is broader in some lice. Some lice of veterinary importance parasitize two or more closely related hosts. Examples include the three species which parasitize domestic dogs: Linognathus setosus, Trichodectes

Sucking lice (Anoplura) of medical and veterinary importance, showing dorsal morphology (left) and ventral morphology (right) in each case. Not drawn to scale. (A) Human body louse (Pediculus humanus humanus), female; (B) Human crab louse (Phthirus pubis), female; (C) Flying squirrel louse (Neohaematopinus sciuropteri), male; (D) Spirted rat louse (Polyplax spinulosa), male; (E) Hog louse (Haematopinus suis), female; (F) Little blue cattle louse (Solenoptes capillatus), male; (G) Dog sucking louse (Linognathus setosus), male; (H) Longnosed cattle louse (L. vituli), female. (From Ferris, 1923-1935.)
FIGURE 4.7 Sucking lice (Anoplura) of medical and veterinary importance, showing dorsal morphology (left) and ventral morphology (right) in each case. Not drawn to scale. (A) Human body louse (Pediculus humanus humanus), female; (B) Human crab louse (Phthirus pubis), female; (C) Flying squirrel louse (Neohaematopinus sciuropteri), male; (D) Spirted rat louse (Polyplax spinulosa), male; (E) Hog louse (Haematopinus suis), female; (F) Little blue cattle louse (Solenoptes capillatus), male; (G) Dog sucking louse (Linognathus setosus), male; (H) Longnosed cattle louse (L. vituli), female. (From Ferris, 1923-1935.)
Head region of a sucking louse (Anoplura) feeding on a host, showing components of mouthparts and associated internal structures. (Original by Margo Duncan.)
FIGURE 4.8 Head region of a sucking louse (Anoplura) feeding on a host, showing components of mouthparts and associated internal structures. (Original by Margo Duncan.)
Cross-section through the mouthparts of a sucking louse (Anoplura). (Original by Margo Duncan.)
FIGURE 4.9 Cross-section through the mouthparts of a sucking louse (Anoplura). (Original by Margo Duncan.)

canis, and Heterodoxus spiniger. These lice also parasitize foxes, wolves, coyotes, and occasionally other carnivores. Similarly, the horse sucking louse (Haematopinus asini), parasitizes horses, donkeys, asses, mules, and zebras, whereas L. africanus parasitizes both sheep and goats. At least six species of chewing lice are found on domestic fowl, all of them parasitizing chickens, but some also feeding on turkeys, guinea fowl, pea fowl, or pheasants (Table I). Lice found on atypical hosts are termed stragglers.

Some sucking lice, such as the three taxa that parasitize humans, the sheep foot louse, and the sheep face louse, are not only host specific, but also infest specific body areas, from which they can spread in severe infestations. Many chewing lice, particularly species that parasitize birds, also exhibit both host specificity and site specificity; examples include several species that are found on domestic fowl, and species confined to turkeys, geese, and ducks (Table I). Lice inhabiting different body regions on the same host typically have evolved morphological adaptations in response to specific attributes of the host site. These include characteristics such as morphological differences of the pelage, thickness of the skin, availability of blood vessels, and grooming or preening activities of the host. Site specificity in chewing lice is most prevalent in the more sedentary, specialized Ischnocera than in the mostly mobile, morphologically unspecialized Amblycera. For example, on many bird hosts, roundbodied ischnocerans with large heads and mandibles are predominately found on the head and neck. Elongate forms with narrow heads and small mandibles tend to inhabit the wing feathers, whereas morphologically intermediate forms occur on the back and other parts of the body.

Some chewing lice inhabit highly specialized host sites. These include members of the amblyceran genus Piagetiella, which are found inside the oral pouches of pelicans, and members of several amblyceran genera, including Actornithophilus and Colpocephalum, which live inside feather quills. Several bird species are parasitized by 5 or more different species of site-specific chewing lice, and up to 12 species may be found on the neotropical bird Crypturellus soul (a tinamou).

Site specificity is less well documented for sucking lice. However, domestic cattle may be parasitized by as many as five anopluran species, each predominating on particular parts of the body. Similarly, some Old World squirrels and rats can support up to six species of sucking lice.

Because of the importance of maintaining a permanent or close association with the host, lice have evolved specialized host-attachment mechanisms to resist grooming activities of the host. The robust tibio-tarsal claws of sucking lice (Fig. 4.10) are very important in securing them to their hosts. Various arrangements of hooks and spines, especially on the heads of lice that parasitize arboreal or flying hosts, such as squirrels and birds, also aid in host attachment. Mandibles are important attachment appendages in ischnoceran and rhyncophthirinan chewing lice. In some species of Bovicola, a notch in the first antenhal segment encircles a host hair to facilitate attachment.

Tibio-tarsal claws and antenna of Linognathus africanis (Anoplura): scanning electron micrograph.
FIGURE 4.10 Tibio-tarsal claws and antenna of Linognathus africanis (Anoplura): scanning electron micrograph. (From Price and Graham, 1997.)

A few lice even possess ctenidia (“combs”) that are convergently similar in morphology to those characteristic of many fleas. They occur most notably among lice that parasitize coarse-furred, arboreal, or flying hosts. Additionally, chewing lice that parasitize arboreal or flying hosts often have larger, more robust claws than do their counterparts that parasitize terrestrial hosts.

Because of their reliance on host availability, lice are subjected to special problems with respect to their longterm survival. MI sucking lice are obligate blood-feeders; even a few hours away from the host can prove fatal to some species. Some chewing lice also are hematophages and similarly cannot survive prolonged periods off the host. However, many chewing lice, particularly those that subsist on feathers, fur, or other skin products, can survive for several days away from the host. For example, the cattle biting louse can survive for up to 11 days (this species will feed on host skin scrapings), and Menacanthusspp. of poultry can survive for up to 3 days off the host. Off-host survival is generally greater at low temperatures and high humidities. At 26~ and 65% relative humidity (RH), 4% of human body lice die within 24 hr, 20% within 40 hr, and 84% within 48 hr. At 75% RH, a small proportion of sheep foot lice survives for 17 days at 2~ whereas most die within 7 days at 22~ Recently fed lice generally survive longer than unfed lice away from the host. Mthough most lice are morphologically adapted for host attachment and are disadvantaged when dislodged, the generalist nature of some amblyceran chewing lice better equips them for locating another host by crawling across the substrate. Amblycerans are more likely than other lice to be encountered away from the host, accounting for observations of these lice on bird eggs or in unoccupied nests and roosts.

Host grooming is an important cause of louse mortality. Laboratory mice infested by the mouse louse, for example, usually limit their louse populations to 10 or fewer individuals per mouse by regular grooming. Prevention of self-grooming or mutual grooming by impaired preening action of the teeth or limbs of such mice can result in heavy infestations of more than 100 lice. Similarly, impaired preening due to beak injuries in birds can result in tremendous increases of louse populations. Biting, scratching, and licking also reduce louse populations on several domestic animals.

Whereas most species of lice on small and mediumsized mammals exhibit only minor seasonal differences in population levels, some lice associated with larger animals show clear seasonal trends. Some of these population changes have been attributed to host molting, fur density and length, hormone levels in the blood meal, or climatological factors such as intense summer heat, sunlight, or desiccation. On domestic ungulates in temperate regions, louse populations typically peak during the winter or early spring and decline during the summer. An exception to this trend is the cattle tail louse, whose populations peak during the summer.

Another important aspect of louse behavior is the mode of transfer between hosts. Direct host contact appears to be the primary mechanism for louse exchange. Transfer of lice from an infested mother to her offspring during suclding (in mammals) or during nest sharing (in birds and mammals) is an important mode of transfer. Several species of lice that parasitize livestock transfer during suclding, including the sheep face louse and the sheep biting louse, both of which move from infested ewes to their lambs at this time. Lice can also transfer during other forms of physical contact between hosts, such as mating or fighting. Transfer of lice between hosts also can occur between hosts that are not in contact. The sheep foot louse, for example, can survive for several days off the host and reach a new host by crawling across pasture land. Nests of birds and mammals can act as foci for louse transfer, but these are infrequent sites of transfer.

Dispersal of some lice occurs via phoresy, in which they temporarily attach to other arthropods and are carried from one host to another (Fig. 4.11). During phoresy, most lice attach to larger, more mobile bloodfeeding arthropods, usually a fly, such as a hippoboscid or muscoid. Phoresy is particularly common among ischnoceran chewing lice. Movement of the mouthparts in a horizontal plane better facilitates their attachment to a fly than in the amblycerans, in which mouthparts move in a vertical plane. Phoresy is rare among sucking lice. This is

Two ischnoceran chewing lice (Mallophaga) phoretic on a hippoboscid fly, attached by their mandibles to the posterior abdomen.
FIGURE 4.11 Two ischnoceran chewing lice (Mallophaga) phoretic on a hippoboscid fly, attached by their mandibles to the posterior abdomen. (From Rothschild and Clay, 1952).

probably because attachment to the fly is achieved by the less efficient mechanism of grasping with the tarsal claws.

Mating in lice occurs on the host. It is initiated by the male pushing his body beneath that of the female and curling the tip of his abdomen upward. In the human body louse, the male and female assume a vertical orientation along a hair shaft, with the female supporting the weight of the male as he grasps her with his anterior claws. Most lice appear to exhibit similar orientation behavior during mating. Notable exceptions include the crab louse of humans, in which both sexes continue to clasp with their claws a host hair, rather than each other, during mating; and the hog louse, in which the male strokes the head of the female during copulation. Some male ischnoceran chewing lice possess modified hooklike antennal segments, with which they grasp the female during copulation.

Oviposition behavior by female lice involves crawling to the base of a host hair or feather and cementing one egg at a time close to the skin surface. Two pairs of fingerlike gonopods direct the egg into a precise location and orientation as a cement substance is secreted around the egg and hair base. Optimal temperature requirements for developing louse embryos inside eggs are very narrow, usually within a fraction of a degree, such as may occur on a precise area on the host body. For this reason, female lice typically oviposit preferentially on an area of the host that meets these requirements.

LICE OF MEDICAL INTEREST

Three taxa of sucking lice parasitize humans throughout the world: the body louse, head louse, and crab louse (pubic louse). All are specific ectoparasites of humans; rarely, dogs or other companion animals may have temporary, selflimiting infestations.

Human head and body lice are closely related and can interbreed to produce fertile offspring in the laboratory. For this reason, they generally are recognized as separate subspecies of Pediculus humanus, as in this chapter. Nevertheless, they rarely interbreed in nature, which has prompted some epidemiologists to treat them as separate species, P. humanus (body louse) and P. capitis (head louse).

Human body louse (Pediculus humanus humanus)

The human body louse (Figs. 4.7A and 4.12) or cootie was once an almost ubiquitous companion of humans. Today it is less common, especially in developed nations. Body lice persist as a significant problem in less developed nations in parts of Africa, Asia, and Central and South America. This is significant because P.h. humanus is the only louse of humans that is known

FIGURE 4.12 Human body lice (Pediculus humanus humanus) feeding on a human. (Courtesy of Elton J. Hansens.)
FIGURE 4.12 Human body lice (Pediculus humanus humanus) feeding on a human. (Courtesy of Elton J. Hansens.)

to naturally transmit pathogens. The large-scale reduction in body louse infestations worldwide has led to a concomitant decrease in the prevalence of human louse-borne diseases. However, situations that result in human overcrowding and unsanitary conditions (e.g., wars, famines, and natural disasters) can lead to a resurgence of body louse infestations, often accompanied by one or more louse-borne diseases.

Adult human body lice (Figs. 4.7A and 4.12) are 2.3-3.6 mm long. Under optimal conditions their populations can multiply dramatically if unchecked; e.g., if clothes of infested individuals are not changed and washed in hot water at regular intervals. In unusually severe infestations, populations of more than 30,000 body lice on one person have been recorded. Body lice typically infest articles of clothing and crawl onto the body only to feed. Females lay an average of four or five eggs per day, and these typically hatch after 8 days. Unique among lice, females oviposit not on hair, but on clothing (Fig. 4.13), especially along seams

FIGURE 4.13 Eggs of the human body louse (Pediculus humanus humanus) attached to clothing. (Courtesy ofElton J. Hansens.)
FIGURE 4.13 Eggs of the human body louse (Pediculus humanus humanus) attached to clothing. (Courtesy ofElton J. Hansens.)ฃ

and creases. Each nymphal instar lasts for 3-5 days, and adults can live for up to 30 days.

Biting by body lice often causes intense irritation, with each bite site typically developing into a small red papule with a tiny central clot. The bites usually itch for several days but occasionally for a week or more. Persons exposed to numerous bites over long periods often become desensitized and show little or no reaction to subsequent bites. Persons with chronic body louse infestations may develop a generalized skin thickening and discoloration called Vagabond disease or Hobo disease, names depicting a lifestyle that can promote infestation by body lice. Several additional symptoms may accompany chronic infestations. These include lymphadenopathy (swollen lymph nodes), edema, increased body temperature often accompanied by fever, a diffuse rash, headache, joint pain, and muscle stiffness.

Some people develop allergies to body lice. Occasionally, patients experience a generalized dermatitis in response to one bite or small numbers of bites. A form of asthmatic bronchitis has similarly been recorded in response to allergy to louse infestations. Secondary infections such as impetigo or blood poisoning can also result from body louse infestations.

Body lice tend to leave persons with elevated body temperatures and may crawl across the substrate to infest a nearby person. This has epidemiological significance because high body temperatures of lousy persons often result from fever caused by infection with louseborne pathogens.

Human head louse (Pediculus humanus cap#is)

The human head louse is virtually indistinguishable from the human body louse on the basis of morphological characters and its life cycle. Unless a series of specimens is available for analysis it is often impossible to separate the two subspecies. Generally, adult head lice are slightly smaller (2.1-3.3 mm in length) than body lice.

As indicated by their name, human head lice typically infest the scalp and head region, rather than other areas of the body infested by body lice. Females attach their eggs to the base of individual hairs. As the hair grows, the eggs become further displaced from the scalp. An indication of how long a patient has been infested can be gleaned by measuring the farthest distance of eggs from the scalp and comparing this to the growth rate of hair.

Today, head lice are far more frequently encountered than body lice, especially in developed countries. Transmission occurs by person-to-person contact and via shared objects such as combs, brushes, headphones, and caps. School-age children are at high risk because they are often more likely to share such items. Some school districts in the United States and Britain have infestation prevalences approaching 50% in students. It has been estimated that 6-12 million people, principally children, are infested with head lice annually in the United States. Some ethnic groups, such as persons of African origin, have coarser head hairs and are less prone to head louse infestations. The reason for this is simply that the tibio-tarsal claws of these lice cannot efficiently grip the thicker hairs.

Although head lice are not known to transmit pathogens, heavy infestations can cause severe irritation. As is the case with human body lice, the resultant scratching often leads to secondary infections such as impetigo, pyoderma, or blood poisoning. Severe head louse infestations occasionally result in the formation of scabby crusts beneath which the lice tend to aggregate. Enlarged lymph nodes in the neck region may accompany such infestations.

Human crab louse (Pthirus pubis)

The crab louse, or pubic louse, is a medium-sized (1.1- 1.8 mm long), squat louse (Fig. 4.7B), with robust tibio-tarsal claws used for grasping thick hairs, especially those in the pubic region. It also may infest coarse hairs on other parts of the body, such as the eyebrows, eyelashes, chest hairs, beards, moustaches, and armpits. This louse typically transfers between human partners during sexual intercourse and other intimate contact; in France, crab lice are described as “papillons d’amour” (butterflies of love). Transfer via infested bed linen or toilet seats can also occur. This is uncommon, however, because crab lice can survive for only a few hours off the host.

Female crab lice lay an average of three eggs per day. Eggs hatch after 7-8 days; the three nymphal instars together last for 13-17 days. Under optimal conditions the generation time is 20-25 days. The intense itching caused by these lice is often accompanied by purplish lesions at bite sites and by small blood spots from squashed lice or louse feces on underwear. Crab lice are widely distributed and relatively common throughout the world. They are not known to transmit any pathogens. One epidemiological study, however, revealed a positive relationship between infection with hepatitis B virus and crab louse infestation.

LICE OF VETERINARY INTEREST

A wide variety of lice infests domestic, livestock, and laboratory animals (Tables I and II). Many hosts, particularly small rodents, often support few if any lice, whereas large hosts such as livestock animals, including poultry, may be parasitized by very large numbers of lice. For example, fewer than 10 mouse lice (Polyplax serrata) on a house mouse are a typical burden, but more than a million lice may be present on extremely heavily infested sheep, cattle, horses, or other large animals.

LICE OF CATTLE

Lice are a major problem in cattle operations worldwide. Domestic cattle are parasitized by six species of lice: three species of Haematopinus, one of Linognathus, one of Solenopotes, and one of Bovicola. Domestic Asiatic buffalo are typically parasitized by H. tuberculatus (Tables I and II).

Females of the cosmopolitan cattle biting louse (Bovicola bovis) lay an average of 0.7 eggs per day, which hatch 7-10 days later. Each nymphal instar lasts 5-6 days, and adult longevity can be as long as 10 weeks. Preferred host sites for this louse are the base of the tail, the shoulders, and the top line of the back, but lice may also populate the pollard in severe infestations.

The longnosed cattle louse (L. vituli) (Fig. 4.7H) also is a worldwide pest. Females deposit about one egg per day, and the life cycle is completed in about 21 days. This louse is most common on calves and dairy stock; it rarely occurs in large numbers on mature cattle. Preferred infestation sites are the dewlap and shoulders; declining spring populations are often confined to the shoulders.

The little blue cattle louse (Solenopotes capillatus) (Fig. 4.7F) also has a worldwide distribution. Females lay one or two eggs per day; oviposition typically causes the hairs on which eggs are laid to bend. Eggs hatch after about 10 days, and adulthood is reached about 11 days later. Clusters of S. capillatus typically occur on the muzzle, dewlap, and neck of mature cattle. Aggregations of this louse may surround the eyes in severely infested animals, giving a spectacled appearance to the host.

The cosmopolitan shortnosed cattle louse ( H. eurysternus) is the largest louse found on North American cattle; adults measure 3.5-4.7 mm in length. Females lay one to four eggs per day for about 2 weeks, nymphs reach adulthood in about 14 days, and adult longevity is 10-15 days. This louse is more common on mature cattle than on young animals. Preferred infestation sites are the top of the neck, the dewlap, and brisket. However, in severe infestations, the entire region from the base of the horns to the base of the tail can be infested. In North America, H. eurysternus is most prevalent in the Great Plains and Rocky Mountain regions.

The cattle tail louse ( H. quadripertusus) parasitizes cattle in the warmer regions of the world. It was inadvertently introduced into the United States, where it now occurs in the Gulf Coast states. Females of this louse oviposit on the tail hairs, which become matted with eggs in severe infestations. Infested tail heads may be shed under these circumstances. Eggs hatch after 9-25 days, depending on the season. Under optimal conditions, the entire life cycle can be as short as 25 days. Nymphs migrate over the host body surface, but adults are typically confined to the tail head. Unlike other cattle lice, H. quadripertusus is most abundant during the summer.

Except for H. quadripertusus, cattle lice increase in numbers during the winter and early spring in temperate regions. During summer, lice persist on 1-2% of the members of a herd; these chronically infested animals typically reinfest other herd members during the winter. Bulls and older cows often serve as reservoirs of lice. Bulls have longer, thicker hair and massive shoulders and neck that compromise self-grooming. During summer, a small number of lice can survive on the cooler ear tips, where lethal temperatures are rarely reached.

LICE OF OTHER LIVESTOCK ANIMALS

Horses, donkeys, hogs, goats, and sheep are parasitized by one or more species of louse (Tables I and II). Except for hogs, all of these animals are parasitized by both sucking lice and chewing lice. The horse biting louse (B. equi) is the most important louse of equids worldwide. Females of this louse oviposit on fine hairs, avoiding the coarse hairs of the mane and tail. This louse typically infests the side of the neck, the flanks, and tail base but can infest most of the body (except the mane, tail, ears, and lower legs) in severe infestations. Longhaired horse breeds are more prone to infestation by B. equi.

Domestic swine are parasitized by the hog louse (H. suis) (Fig. 4.7E). This is a large species in which adult females measure ca. 5 mm in length. Hog lice usually frequent skin folds of the head (especially the ears), neck, shoulders, and flanks of swine. Female hog lice lay an average of 3.6 eggs per day. These are deposited singly on hairs along the lower parts of the body, in skin folds on the neck, and on and in the ears. Eggs typically hatch 13-15 days later; each nymphal instar lasts 4-6 days. Adult hog louse longevity can be up to 40 days, and 6-15 generations can be completed per year, depending on environmental conditions.

Domestic sheep and goats are parasitized by several species of sucking lice and chewing lice (Tables I and II). One of these, L. africanus, parasitizes both hosts. Lice of sheep and goats, especially chewing lice, are economically important wherever these livestock animals are farmed, but especially in Australia, New Zealand, and the United States. Females of the sheep biting louse (B. ovis) lay one or two eggs per day and can live for up to 30 days; each nymphal instar lasts 5-9 days. B. ovis mainly infests the back and upper parts of the body but may populate the entire body in severe infestations. This louse causes intense irritation, and infested sheep typically rub against fences and trees, tearing the fleece and greatly reducing its value. Sucldng louse infestations of sheep rarely cause major economic problems.

LICE OF CATS AND DOGS

Domestic cats are parasitized by one species of chewing louse, whereas dogs are parasitized by two species of chewing lice and one species of sucking louse. All four species seem to be distributed worldwide, but none is a common associate of healthy cats or dogs in North America.

The cat biting louse (Felicola subrostrata) (Fig. 4.5E) parasitizes both domestic and wild cats. It may occur almost anywhere on the body. Both the dog biting louse ( T. canis) (Fig. 4.5D) and the dog sucking louse (L. setosus) (Fig. 4.7G) parasitize dogs and closely related wild canids. For example, T. canis also parasitizes coyotes, foxes, and wolves. A second species of chewing louse of dogs is Heterodoxus spiniger (Fig. 4.5A), which evolved in Australasia from marsupial-infesting lice and apparently switched to dingo hosts. It now parasitizes various canids and other carnivores throughout the world. T. can# usually infests the head, neck, and tail region of dogs, where it attaches to the base of a hair using its claws or mandibles. L. setosus occurs primarily on the head and neck and may be especially common beneath collars. H. spiniger can typically be found anywhere on its host.

LICE OF LABORATORY ANIMALS

The principal species of lice that parasitize laboratory mammals have been described by Kim et al. (1973). These lice also parasitize feral populations of their respective hosts. The house mouse (Mus musculus) is often parasitized by the mouse louse (P. serrata). Populations of this louse are typically low, with 10 or fewer lice per infested mouse, unless self-grooming or mutual host grooming is compromised. Eggs of this louse typically hatch 7 days after oviposition. Together the three nymphal instars last only 6 days under optimal conditions, which can result in a generation time as short as 13 days. Domestic rats are often parasitized by the spined rat louse (P. spinulosa) (Fig. 4.7D) and the tropical rat louse (Hoplopleura pacifica). Common hosts include the black rat (Rattus rattus) and the Norway rat (R. norvegicus). The spined rat louse parasitizes these hosts throughout the world, whereas the tropical rat louse is confined to tropical, subtropical, or warm temperate regions, including the southern United States.

Laboratory rabbits are parasitized by the rabbit louse (Haemodipsus ventricosis). This louse originated in Europe but has accompanied its host and been introduced throughout the world.

LICE OF POULTRY AND OTHER BIRDS

At least nine species of chewing lice commonly infest poultry (Table I) in various parts of the world. Individual birds can be parasitized by multiple species, each of which often occupies a preferred host site. The chicken body louse (Menacanthus stramineus) (Fig. 4.14) is the most common and destructive louse of domestic chickens. It has a worldwide distribution and often reaches pest proportions. Adults measure 3-3.5 mm in length. Females lay one or two eggs per day, cementing them in clusters at the bases of feathers, especially around the vent. Eggs typically hatch after 4-5 days. Each nymphal instar lasts about 3 days, and the generation time typically is 13-14 days. These lice are most abundant on the sparsely feathered vent, breast, and thigh regions. Several other chewing lice are pests of poultry more or less throughout the world (Table I). Adults of the shaft louse (Menopon gallinae) measure ca. 2 mm in length, and females deposit eggs singly at the base of the shaft on thigh and breast feathers. Eggs of the wing louse (Lipeurus capon#) hatch 4-7 days after the female has cemented them to the base of a feather. Nymphal stages of this species each last 5-18 days; generation time typically is 18-27 days, and females can live up to 36 days. Females of the chicken head louse (Cuclutogaster heterographus) attach their eggs to the bases of downy feathers. Eggs hatch after 5-7 days, each nymphal instar lasts 6-14 days, and average generation time is 35 days.

FIGURE 4.14 Chicken body lice (Menacanthus stramineus) on a chicken. (Courtesy of Nancy C. Hinlde.)
FIGURE 4.14 Chicken body lice (Menacanthus stramineus) on a chicken. (Courtesy of Nancy C. Hinlde.)

Poultry lice typically transfer to new birds by direct host contact. However, because most species can survive for several hours or days off the host, they also can infest new hosts during transportation in inadequately disinfected cages or vehicles.

PUBLIC HEALTH IMPORTANCE

Three important pathogens are transmitted to humans by body lice. These are the agents of epidemic typhus, trench fever, and louse-borne relapsing fever. Today, the prevalence and importance of all three of these louse-borne diseases are low compared to times when human body lice were an integral part of human life. However, trench fever has emerged as an opportunistic disease of immunocompromised individuals, including persons who are positive for human immunodeficiency virus (HIV).

EPIDEMIC TYPHUS

Epidemic typhus is a rickettsial disease caused by infection with Rickettsia prowazekii. It is also known as louseborne fever, jail fever, and exanthematic typhus. The disease persists in several parts of the world, most notably in Burundi, Democratic Republic of Congo, Ethiopia, Nigeria, Rwanda, and areas of northeastern and central Africa, Russia, Central and South America, and northern China. Epidemic typhus is largely a disease of cool climates, including higher elevations in the tropics. It thrives in conditions of widespread body louse infestations, overcrowding, and poor sanitary conditions. Epidemic typhus apparently was absent from the New World until the 1500s, when the Spanish introduced the disease. One resulting epidemic in 1576-1577 killed 2 million Indians in the Mexican highlands alone. The vector of R. prowazekii is the human body louse. Lice become infected when they feed on a person with circulating /L prowazekii in the blood. Infective rickettsiae invade cells that line the louse gut and multiply there, eventually causing the cells to rupture. Liberated rickettsiae either reinvade gut cells or are voided in the louse feces. Other louse tissues typically do not become infected. Because salivary glands and ovaries are not invaded, anterior-station and transovarial transmission do not occur. Infection of susceptible humans occurs via louse feces (posterior-station transmission) when infectious rickettsiae are scratched into the skin in response to louse bites. R. prowazekii can remain viable in dried louse feces for 60 days. Infection by inhalation of dried louse feces or by crushed lice are less frequent means of contracting the disease.

Transmission of R. prowazekii by body lice was first demonstrated by Charles Nicolle, working at the Institut Pasteur in Tunis in 1909. During these studies, Nicolle accidentally became infected with epidemic typhus, from which he fortunately recovered. He was awarded the Nobel prize in 1928 for his groundbreaking work on typhus. Several other typhus workers also were infected with R. prowazekii during laboratory experiments. The American researcher Howard T. Ricketts, working in Mexico, and Czech scientist Stanislaus yon Prowazek, working in Europe, both died from their infections and were recognized posthumously when the etiologic agent was named. Infection with R. prowazekii is ultimately fatal to body lice as progressively more and more infected gut cells are ruptured. Infective rickettsiae are first excreted in louse feces 3-5 days after the infective blood meal. Lice usually succumb to infection 7-14 days after the infectious blood meal, although some may survive to 20 days. The disease caused by infection with R. prowazekii and transmitted by body lice is called classic epidemic typhus because it was the first form of the disease to be recognized. Disease onset occurs relatively soon after infection by a body louse in classic epidemic typhus. Symptoms generally appear after an incubation period of 10-14 days. Abrupt onset of fever, accompanied by malaise, muscle and head aches, cough, and general weakness, usually occurs at this time. A blotchy rash spreads from the abdomen to the chest and then often across most of the body, typically within 4-7 days following the initial symptoms. The rash rarely spreads to the face, palms, and soles, and then only in severe cases. Headache, rash, prostration, and delirium intensify as the infection progresses. Coma and very low blood pressure often signal fatal cases. A case fatality rate of 10-20% is characteristic of most untreated epidemics, although figures approaching 50% have been recorded. Diagnosis of epidemic typhus involves the demonstration of positive serology, usually by microimmunofluorescence. DNA primers specific to R. prowazekii can also be amplified by polymerase chain reaction from infected persons or lice. One-time antibreak biotic treatment, especially with doxycycline, tetracycline, or chloramphenicol, usually results in rapid and complete recovery. Vaccines are available but are not considered to be sufficiently effective for widespread HSC. Persons that recover from epidemic typhus typically harbor R. prowazekii in lymph nodes or other tissues for months or years. This enables the pathogen to again invade other body tissues to cause disease seemingly at any time. This form of the disease is called recrudescent typhus or Brill-Zinsser disease. The latter name recognizes two pioneers in the study of epidemic typhus: Nathan Brill, who first recognized and described recrudescent typhus in 1910, and Hans Zinsser, who demonstrated in 1934 that it is a form of epidemic typhus. Zinsser’s (1935) book Rats, Lice, and History is a pioneering account of the study of epidemic typhus in general.

Recrudescent typhus was widespread during the 19th and early 20th centuries in some of the larger cities along the east coast of the United States (e.g., Boston, New York, and Philadelphia). At that time, immigrants from regions that were rampant with epidemic typhus, such as eastern Europe, presented with Brill-Zinsser disease after being infected initially in their country of origin. Some of these patients experienced relapses more than 30 years after their initial exposure, with no overt signs of infection with R. prowazekii between the two disease episodes. Because infestation with body lice was still a relatively common occurrence during that period, the lice further disseminated the infection to other humans, causing local outbreaks. The last outbreak of epidemic typhus in North America occurred in Philadelphia in 1877. Today, even recrudescent typhus is a rare occurrence in North America. However, this form of typhus is still common in parts of Africa, Asia, South America, and, occasionally, in eastern Europe. The southern flying squirrel ( Glaucomys volans) has been identified as a reservoir of R. prowazekii in the United States, where it has been found to be infected in Virginia during vertebrate serosurveys for Rocky Mountain spotted fever. Since the initial isolations from flying squirrels in 1963, R. prowazekii has been recorded in flying squirrels and their ectoparasites in several states, especially eastern and southern states. Peak seroprevalence (about 90%) in the squirrels occurs during late autumn and winter, when fleas and sucldng lice are also most abundant on these hosts. Although several ectoparasites can imbibe R. prowazekii when feeding on infected flying squirrels, only the sucldng louse Neohaematopinus sciuropteri (Fig. 4.7C) is known to maintain the infection and transmit the pathogen to uninfected squirrels. Several cases of human infection have been documented in which the patients recalled having contact with flying squirrels, especially during the winter months when these rodents commonly occupy attics of houses. To distinguish this form of the disease from classic and recrudescent typhus, it is called sporadic epidemic typhus or sylvatic epidemic typhus. Many details, such as the prevalence and mode of human infection, remain unresolved. Because the louse N. sciuropteri does not feed on humans, it is speculated that human disease occurs when infectious, aerosolized particles of infected louse feces are inhaled from attics or other sites occupied by infected flying squirrels. Except for flying squirrels in North America, humans are the only proven reservoirs of R. prowazekii. Widespread reports published in the 1950s to 1970s that various species of ticks and livestock animals harbored R. prowazekii have since been disproved. Historically, epidemic typhus has been the most widespread and devastating of the louse-borne diseases. Zinsser (1935) and Snyder (1966) have documented the history of this disease and highlighted how major epidemics have influenced human history. For example, the great outbreak of disease at Athens in 430 BC, which significantly influenced the course of Greek history, appears to have been caused by epidemic typhus. Napoleon’s vast army of 1812 was defeated more by epidemic typhus than by opposing Russian forces. Soon thereafter (ca. 1816- 1819), 700,000 cases of epidemic typhus occurred in Ireland. Combined with the potato famine of that period, this encouraged many people to emigrate to North America; some of these people carried infected lice or latent infections with them. During World War II, several military operations in North Africa and the Mediterranean region were hampered by outbreaks of epidemic typhus. One epidemic in Naples in 1943 resuited in over 1400 cases and 200 deaths. This outbreak is particularly noteworthy because it was the first epidemic of the disease to be interrupted by human intervention through widespread application of the insecticide dichlorodiphenyltrichloroethane (DDT) to louseinfested persons. Today, epidemic typhus is much less of a health threat than it once was. This is largely because few people, especially in developed countries, are currently infested by body lice. Higher sanitary standards, less overcrowding, regular laundering and frequent changes of clothes, effective pesticides, and medical advances have contributed to the demise of this disease. Nevertheless, epidemic typhus has the potential to re-emerge. This is evidenced by the largest outbreak of epidemic typhus since World War II that affected about half a million people living in refugee camps in Burundi in 1997-1998. Similarly, more than 5600 cases were recorded in China during 1999. Additional information about epidemic typhus is provided by the Pan American Health Organization/World Health Organization (1973), McDade (1987), and Azad (1988).

LOUSE-BORNE RELAPSING FEVER

Also known as epidemic relapsing fever, this disease is caused by the spirochete bacterium Borrelia recurrentis. This pathogen is transmitted to humans by the human body louse, as first demonstrated by Sergent and Foley in 1910. Clinical symptoms include the sudden onset of fever, headache, muscle ache, anorexia, dizziness, nausea, coughing, and vomiting. Thrombocytopenia (a decrease in blood platelets) also can occur and cause bleeding, which may initially be confused for a symptom of a hemorrhagic fever. Episodes of fever last 2-12 days (average, 4 days), typically followed by periods of 2-8 days (average, 4 days) without fever, with two to five relapses being usual. As the disease progresses, the liver and spleen enlarge rapidly, leading to abdominal discomfort and labored, painful breathing as the lungs and diaphragm are compressed. At this stage, most patients remain quietly prostrate with a glazed expression, often shivering and taking shallow breaths. Mortality rates for untreated outbreaks range from 5 to 40%. Antibiotic treatment is with penicillin or tetracycline. Humans are the sole known reservoir of B. recurrentis. Body lice become infected when they feed on an infected person with circulating spirochetes. Most of the spirochetes perish when they reach the louse gut, but a few survive to penetrate the gut wall, where they multiply to massive populations in the louse hemolymph, nerves, and muscle tissue. Spirochetes do not invade the salivary glands or ovarian tissues and are not voided in louse feces. Therefore, transmission to humans occurs only when infected lice are crushed during scratching, which allows the spirochetes in infectious hemolymph to invade the body through abrasions and other skin lesions. However, B. recurrentisis also capable of penetrating intact skin. As with R. prowazekii infections, body lice are killed as a result of infection with B. recurrentis. An intriguing history of human epidemics of louseborne relapsing fever is provided by Bryceson et al. (1970). Hippocrates described an epidemic of ” caucus,” or “ardent fever,” in Thasos, Greece, which can clearly be identified by its clinical symptoms as this malady. During 1727-1729, an outbreak in England killed all inhabitants of many villages. During the present century, an epidemic that spread from eastern Europe into Russia during 1919-1923 resulted in 13 million cases and 5 million deaths. Millions also were infected during an epidemic that swept across North Africa in the 1920s. Several major epidemics subsequently have occurred in Africa, with up to 100,000 fatalities being recorded for some of them. During and immediately after World War II, more than a million persons were infected in Europe alone. The only current epidemic of louse-borne relapsing fever is in Ethiopia, where 1000-5000 cases are reported annually, accounting for ca. 95% of the world’s recorded infections. Other smaller loci occur intermittently in other regions, such as Burundi, Rwanda, Sudan, Uganda, People’s Republic of China, the Balkans, Central America, and the Peruvian Andes. Resurgence of this disease under conditions of warfare or famine is an ominous possibility. Additional information on louseborne relapsing fever is provided by Bryceson et al. (1970).

TRENCH FEVER

Also known as five-day fever and wolhynia, trench fever is caused by infection with the bacterium Bartonella (formerly Rochalimaea) quintana. Like the two preceding diseases, the agent is transmitted by the human body louse. Human infections range from asymptomatic through mild to severe, although fatal cases are rare. Clinical symptoms are nonspecific and include headache, muscle aches, fever, and nausea. The disease can be cyclic, with several relapses often occurring. Previously infected persons often maintain a cryptic infection which can cause relapses years later, with the potential for spread to other persons if they are infested with body lice. Effective antibiotic treatment of patients involves administering drugs such as doxycycline or tetracycline. Lice become infected with B. quintana after feeding on the blood of an infected person. The pathogen multiplies in the lumen of the louse midgut and in the cuticular margins of the midgut epithelial cells. Viable rickettsiae are voided in louse feces, and transmission to humans occurs by the posterior-station route when louse bites are scratched. B. quintana can remain infective in dried louse feces for several months, contributing to aerosol transmission as an alternative route of transmission. Transovarial transmission does not occur in the louse vector. Infection is not detrimental to lice and does not affect their longevity. Trench fever was first recognized as a clinical entity in 1916 as an infection of European troops engaging in trench warfare during World War I. At that time, more than 200,000 cases were recorded in British troops alone. Between the two world wars, trench fever declined in importance but re-emerged in epidemic proportions in troops stationed in Europe during World War II. Because of the presence of asymptomatic human infections, the current distribution of trench fever is difficult to determine. However, since World War II, infections have been recorded in several European and African nations, Japan, the People’s Republic of China, Mexico, Bolivia, and Canada. Until recently, B. quintana was considered to be transmitted solely by body lice. However, several homeless or immunocompromised people, including HIV-positive individuals, particularly in North America and Europe, have presented with opportunistic B. quintana infections. This is manifested not as trench fever but as vascular tissue lesions, liver pathology, chronically swollen lymph nodes, and inflammation of the lining of the heart. Because some of these patients were not infested by body lice, an alternate mode of pathogen transmission may have been involved.

Pathogens Transmitted by Lice

HUMAN LICE AS INTERMEDIATE HOSTS OF TAPEWORMS

Occasionally humans become infested with the doublepored tapeworm (Dipylidium caninum). Although carnivores are the normal definitive hosts for this parasite, humans can be infested if they accidentally ingest dog biting lice (T. canis), which serve as intermediate hosts. Although this would appear to be an unlikely event, infants, especially babies playing on carpets or other areas frequented by a family dog, may touch an infested louse with sticky fingers which may then be put into their mouth, thus initiating an infestation.

VETERINARY IMPORTANCE

Several chewing lice and sucking lice parasitize domestic animals (Tables I, II). Although louse populations are usually low on these hosts, lice can sometimes multiply to extremely high numbers, particularly on very young, old, or sick animals. Often this is because hosts are unable to effectively groom themselves or they are immunocompromised. Except for the possibility of pathogen transmission, small numbers of lice typically cause little harm to the host. However, large numbers of lice can be debilitating by causing anemia, dermatitis, allergic responses, hair or feather loss, and other disorders. Lice also induce intensive host grooming, which can lead to the formation of hair balls in the stomach, especially in cats and canes. A few pathogens are lmown to be transmitted to domestic animals by lice (Table III). The most important of these are the viral agent of swinepox and the bacterial agents of murine haemobartonellosis and murine eperythrozoonosis, all of which are widely distributed. In addition to those listed in Table III, several pathogens have been detected in various species of lice, but there is no current evidence that lice are vectors of these organisms.

LICE OF LIVESTOCK

Although louse populations of a few hundred individuals commonly occur on healthy livestock, sometimes these numbers can reach into the thousands or, rarely, to more than a million per animal. It is under thc latter conditions that detrimental effects to the host occur. These include restlessness, pruritus, anemia, low weight gain, low milk yield, dermatitis, hide or fleece damagc, skin crusting or scabbing, and lameness. Large louse populations on domestic stock typically develop on juvenile, senile, sick, nutritionally deprived, or immunocompromised hosts.

Sucking louse infestations of cattle, such as those caused by the shortnosed cattle louse (Haematopinus eurysternus), the cattle tail louse (H. quadripertusus), and the longnosed cattle louse ( Linognathus vituli) (Fig. 4.7H), can cause serious damage to the host. This can be manifested as frequent rubbing of infested areas, hair loss, scab formation, slow recovery from disease or trauma, and low weight gain. Younger animals are typically more severely affected than older cattle. Mixed infestations of both chewing and sucking lice on cattle, or of both lice and nematodes, can affect weight gains more severely than single infestations. In single or mixed infestations, weight gains are typically lower in stressed cattle and those on low-nutrition diets. Sometimes, cattle sucking lice cause severe anemia, abortions, or even death. Irritation can be caused by small numbers of lice in sensitive cattle and usually results in frequent rubbing and subsequent hide damage. This rubbing also damages livestock facilities. Severely infested cattle often have patches of bare skin and a greasy appearance which results from crushing lice and their feces during rubbing. Under laboratory or confined conditions, at least three pathogens can be transmitted by cattle sucking lice, i.e., the causative agents of bovine anaplasmosis, dermatomycosis (ringworm) (Table III), and, rarely, theileriosis. The importance of cattie lice in transmitting any of these pathogens in nature is unknown but presumed to be low. Lice of horses and other equids typically do not greatly debilitate their hosts except when they are present in large numbers. Pruritus, hair loss, and coat deterioration may occur in severely infested animals. Horses with severe louse infestations are nervous and irritable; they typically rub against objects, kicking and stamping. Hair can be rubbed from the neck, shoulders, flanks, and tail base, resulting in an unkempt appearance that may affect the value of the horse. No pathogens are known to be transmitted by equid lice. Hog lice can imbibe significant volumes of blood from hogs, especially piglets, which often have larger infestations than adult pigs. Hog-louse feeding sites often cause intense irritation, leading their hosts to rub vigorously against objects, which can result in hair loss and reddened or crusty skin lesions. Haematopinus suis is a vector of the virus that causes swinepox (Table III), a serious and potentially fatal disease characterized by large pockmark lesions, mainly on the belly of infected animals. Some studies have implicated this louse as a vector of Eperythrozoon suis and E. parvum, causative agents of swine eperythrozoonosis, and of African swine fevervirus. However, transmission of these pathogens by lice appears to be rare, if it occurs at all, in nature. All species of lice that parasitize sheep and goats (Tables I and II) can cause debilitation, even when present in relatively small numbers, because of the potential

FIGURE 4.15 Fleece damage (wool slippage) in a sheep, caused by severe infestation with Linognathus africanus (Anoplura). (Courtesy of John E. Lloyd)
FIGURE 4.15 Fleece damage (wool slippage) in a sheep, caused by severe infestation with Linognathus africanus (Anoplura). (Courtesy of John E. Lloyd)

damage which they can cause to fleece and wool (Fig. 4.15). Some sheep develop hypersensitivity to the sheep biting louse (Bovicola ovis) (Fig. 4.16). This louse causes most sheep fleece devaluation worldwide and is the major cause of cockle, an economically disfiguring condition of sheep fleece that is particularly prevalent in New Zealand. Any increase in skin lesions or body rubbing in response to lice generally devalues wool or mohair. Different breeds of sheep and goats exhibit contrasting levels of resistance or tolerance to infestation by lice.

LICE OF CATS AND DOGS

Louse infestations of cats and dogs are most noticeable on sick or senile hosts. Under these conditions, louse populations can increase dramatically. Severe infestations of any of the four species involved usually cause host restlessness, scratching, skin inflammation, a ruffled or matted coat, and hair loss. The dog biting louse ( T. canis) is an intermediate host of the double-pored tapeworm (D. caninum) (Table III). Lice become infected when they ingest viable D. caninum eggs from dried host feces. The tapeworm develops into a cysticercoid stage in the louse, where it remains quiescent unless the louse is ingested by a dog, usually during grooming. In the dog gut, the cysticercoid is liberated and metamorphoses into an adult tapeworm. The dog sucking louse (L. setosus) has been shown to harbor immatures of the filarial nematode Dipetalonema reconditum, which parasitizes dogs, but whether or not these lice are efficient vectors remains unknown.

FIGURE 4.16 Sheep-biting louse (Bovicola ovis), showing prothorax and head with mandibles characteristically grasping a host hair: scanning electron micrograph. (From Price and Graham, 1997)
FIGURE 4.16 Sheep-biting louse (Bovicola ovis), showing prothorax and head with mandibles characteristically grasping a host hair: scanning electron micrograph. (From Price and Graham, 1997)

LICE OF LABORATORY ANIMALS

Some lice that parasitize laboratory animals initiate serious health problems by causing pruritus, skin lesions, scab formation, anemia, and hair loss. Others are vectors of pathogens that can cause severe problems in animal colonies (Table III). The mouse louse (P. serrata) is a vector of the bacterium Eperythrozoon coccoides, which causes murine eperythrozoonosis, a potentially lethal infection of mice that occurs worldwide. Infection of this blood parasite in mice can either be inapparent or result in severe anemia. Transmission of this pathogen in louse-infested mouse colonies is usually rapid. The spined rat louse (P. spinulosa) is a vector of the bacterium Haemobartonella muris, which causes murine haemobartonellosis (Table III), another potentially fatal blood infection that can cause severe anemia in laboratory rats. Laboratory and wild guinea pigs are parasitized by two species of chewing lice, the slender guineapig louse Gliricola porcelli) and the ovalguineapig louse ( Gyropus ovalis). Small numbers of these lice cause no noticeable harm, whereas large populations can cause host unthriftihess, scratching (especially behind the ears), hair loss, and a ruffled coat. Large infestations of the rabbit louse ( Haemodipsus ventricosis) can cause severe itching and scratching, which results in the host rubbing against its cage, often resulting in hair loss. Young rabbits are more adversely affected than are adults and may experience retarded growth as a consequence of infestation by H. ventricosis. The rabbit louse is also a vector of the causative agent of tularemia among wild rabbit populations (Table III).

LICE OF POULTRY AND OTHER BIRDS

Although louse populations may be very large on domestic fowl, including domestic chickens, turkeys, guinea fowl, pea fowl, and pheasants, no pathogens are known to be transmitted by these lice. Large populations often occur on birds with damaged beaks whose grooming ability is significantly impaired. The chicken body louse (Menacanthus stramineus) (Fig. 4.14) often causes significant skin irritation and reddening through its persistent feeding. Occasionally the skin or soft quills bleed from their gnawing and scraping action, with the lice readily imbibing the resultant blood. The shaft louse (Menopon gallinae) also causes significant losses to the poultry industry, including deaths of young birds with heavy infestations. Large infestations of chicken body lice, shaft lice, and other poultry lice may be injurious to the host by causing feather loss, lameness, low weight gains, inferior laying capacity, or even death. The vast majority of chewing lice are parasites of wild or peridomestic birds. Several of these lice are suspected vectors of avian pathogens. Some chewing lice of aquatic birds, including geese and swans, are vectors offilarial nematodes (Table III). Pet parrots, parakeets, budgerigars, and other birds also are subject to infestation by chewing lice, which is usually noticed only by the associated host scratching and by ruffled or lost feathers. Large populations of these lice can debilitate their hosts. Ranch birds, such as ostriches, emus, and rheas, are prone to similar adverse effects caused by their associated chewing lice.

PREVENTION AND CONTROL

Several techniques have been used in attempts to rid humans and animals of lice and louse-borne diseases. Preventing physical contact between lousy persons or animals and the items they contact, as well as various chemical, hormonal, and biological control mechanisms, comprise the current arsenal of techniques. Chemicals used to kill lice are called pediculicides. Clothes of persons with body lice should be changed frequently, preferably daily, and washed in very hot, soapy water to kill lice and nits. Washing associated bed linen in this manner is also advisable. Infested people should also receive a concurrent whole-body treatment with a pediculicide. Overcrowded and unsanitary conditions should be avoided whenever possible during outbreaks of human body lice and louse-borne diseases because it is under these situations that both can thrive. Crab lice can often be avoided by refraining from multiple sexual partners and changing or laundering bed linen slept on by infested persons. Pediculicides should be applied to the pubic area and to any other infested body regions. To reduce the spread of head lice, the sharing of combs, hats, earphones, and blankets, especially by children, should be discouraged. Often, parents of children with head lice are notified to keep youngsters away from school or other gatherings until the infestation has been eliminated. If the parents are also infested, this can further involve ridding the entire family of lice to prevent reinfestations. Various pediculicidal shampoos, lotions, and gels are widely available for controlling head lice. These treatments typically kill all nymphal and adult lice, but only a small proportion of viable louse eggs. Therefore, treatments should be repeated at weekly intervals for 2-4 weeks in order to kill any recently hatched lice. Hatched or dead nits which remain glued to hair may be unsightly or embarrassing, and these can be removed with a fine-toothed louse comb. Louse combs have been used, in various forms, since antiquity to remove head lice (Mumcuoglu 1996). A wide range of pediculicides is commercially available. Although its use is now banned in many developed countries, the organochlorine DDT is widely used, especially in less developed countries, for controlling human and animal lice. Several alternative pediculicides, such as lindane, chlorpyrifos, diazinon, malathion, permethrin, or pyrethrins, are currently used throughout the world. Pediculicides can be used in powders, fogs, or sprays to treat furniture or premises for lice. Several general parasiticides show promise as pediculicides. Avermectins such as abamectin, doramectin, and ivermectin can kill human body lice and livestock lice. Prescribed doses of these compounds can be administered orally, by injection, or as topical applications of powders, dusts, and pour-ons. However, many of these compounds have not yet been approved for use on humans. The development of novel control agents for lice is a constant process because resistance to various pediculicides has developed in lice in many parts of the world (Burgess 1995, Mumcuoglu 1996).

Lice of livestock can be controlled by both husbandry practices and chemical intervention. Providing a high-energy diet, especially to cattle, can be an effective louse control strategy. If possible, it is important to keep animals in uncrowded conditions and to spot-treat or quarantine any infested individuals until they have been successfully deloused. Various formulations and applications of pediculicides are typically used to control lice on livestock. Insecticidal dusts, powders, sprays, dips, ear tags, tail tags, resin strips, gut boluses, collars, pour-ons, lotions, and injections are widely used products. Infested animals should be treated twice weekly for 2-4 weeks. Insecticidal dust bags or back rubbers can be used as selfdosing rubbing stations for cattle and other livestock. Because louse populations on livestock are typically greater during the winter months, pediculicides are usually best applied to them in the late fall. Fall systemic treatments of cattle for both lice and bots are often administered. Shearing wool from sheep removes up to 80% of the lice present on infested animals. Pets, laboratory animals, and poultry can be treated for lice in several ways. Pets such as dogs and cats can be dipped or bathed with a pediculicidal lotion or shampoo. Various oral or topically applied insecticides used for controlling fleas on pets also are efficacious against lice. Similarly, flea combs also remove lice from pets. Poultry and laboratory animals can be treated with pediculicidal dusts or sprays. Although host treatment is most efficacious, bedding materials and cages can also be treated. Insecticidal feed additives are also available. Insecticideimpregnated resin strips can be added to cages of poultry or laboratory animals to control lice. The bacterium Bacillus thuringiensis and the nematodes Steinernema carpocapsae and S. glaseri, which are effective biological control agents against numerous arthropods, can also be used to kill livestock lice. Some juvenile hormone analogs and insect growth regulators such as diflubenzuron have similarly shown promise as pediculicides. With respect to louse-borne diseases, vaccines have been developed only against epidemic typhus, and none is completely safe or currently approved for widespread use. The live attenuated E-strain vaccine has been administered to humans, particularly in certain African nations, in attempts to quell epidemic typhus outbreaks. However, this vaccine actually caused disease in some patients and did not always prevent subsequent infection.

Cockroaches (Blattaria)

Cockroaches are among the oldest and most primitive of insects. They evolved about 350 million years ago during the Silurian Period, diverging together with the manrids from an ancestral stock that also gave rise to termites (Boudreaux 1979). Cockroaches are recognized as the order Blattaria. Although the majority of species are feral and not directly associated with people, a few species have evolved in proximity to human habitations, where they have adapted to indoor environments. Their omnivorous feeding behavior, facilitated by their unspecialized chewing mouthparts, has contributed to a close physical relationship between cockroach populations and humans, with resultant chronic exposure of humans to these pests. The presence of some species in the home (e.g., German and brownbanded cockroaches) often is an indicator of poor sanitation or substandard housekeeping.

Although they are primarily nuisance pests, their presence can have important health implications. Cockroaches are generalists that feed on virtually any organic substance grown, manufactured, stored, excreted, or discarded by humans. Consequently, food supplies are at risk of contamination by pathogens associated with cockroaches. Because species that infest structures typically have high reproductive rates, humans commonly are exposed to high levels of potentially allergenic proteins associated with cockroaches, which can lead to significant respiratory ailments. Cockroaches also can serve as intermediate hosts of parasites that debilitate domestic animals.

TAXONOMY

There are about 4000 species of cockroaches worldwide. About 70 species occur in the United States, 24 of which have been introduced from other parts of the world. According to Atldnson et al. (1991), 17 of these species are pests of varying degrees. There are five cockroach families, three of which include most of the pest species: Blattidae, Blattellidae, and Blaberidae. Species in the Cryptocercidae are unusual in that they have gut symbionts similar to those found in termites, and they live in family groups in decaying logs. Members of the Polyphagidae include those dwelling in arid regions, where they are capable of moving rapidly through sand. Species in these two families are rarely pests. The family Blatfidae includes relatively large cockroaches that are the most common peridomestic pests throughout much of the world. Blattellid cockroaches range in length from less than 25 mm (e.g., Supella and Blattella) to 35-40 mm (e.g., Periplaneta and Parcoblatta spp.). Parcoblatta species are feral, occasionally invading homes but seldom reproducing indoors. Blaberid cockroaches range greatly in size and include some of the more unusual species, such as the Cuban cockroach, which is green as an adult, and the Surinam cockroach, which is parthenogenetic in North America. Nearly all of the blaberids that occur in the United States are restricted to subtropical regions and have minor medical or veterinary significance. Taxonomic keys for adults are provided by McKittrick (1964), Cornwell (1968), Roth (1985), and Heifer (1987). A pictorial key for identifying the egg cases of common cockroaches is provided by Scott and Borom (1964).

MORPHOLOGY

Cockroaches have retained their basic ancestral form. The Blattaria are distinguished from other insect orders by morphological characters associated with wing size and venation, biting/chewing mouthparts, and prominent cerci. They differ from other orthopteroid insects by having hind femora which are not enlarged, cerci typically with eight or more segments, a body that is dorsoventrally flattened and generally ovoid, and a head that is largely concealed from above by a relatively large pronotum.

A common indicator of cockroach infestations is their egg cases, or oothecae (singular ootheca), purse-shaped capsules that typically contain 5-40 embryos (Fig. 3.1). Coloration ranges from light brown to chestnut brown, depending on the degree of sclerotization. A keel that runs the anterior length of the ootheca permits transport of water and air to the developing embryos. Each embryo is contained in a separate compartment that may or may not be obvious externally. In some species (e.g., German and brownbanded cockroaches) lateral, anterior-to-posterior indentations denote the individual developing embryos. Others have only weak lateral indentations (e.g., brown and smokybrown cockroaches), and still others have no lateral indentations but differ in their symmetry (e.g., Oriental, American, and Australian cockroaches).

The mouthparts of cockroach nymphs and adults are characterized by strongly toothed mandibles for biting and chewing. Maxillary and labial palps are well developed, with five and three segments, respectively. Antennae are long and whiplike, originate directly below the middle of the compound eyes, and consist of numerous small segments. The arrangement of three ocelli near the

Cockroach oothecae (egg cases). A, Australian cockroach (Periplaneta australasiae); B, Brown cockroach (P. brunnea); C, Smokybrown cockroach (P. fuliginosa); D, Oriental cockroach (Blatta orientalis); E, American cockroach (P. americana); F, Brownbanded cockroach (Supella longipalpa); G, German cockroach (Blattella germanica). (Courtesy of the US Public Health Service)
FIGURE 3.1 Cockroach oothecae (egg cases). A, Australian cockroach (Periplaneta australasiae); B, Brown cockroach (P. brunnea); C, Smokybrown cockroach (P. fuliginosa); D, Oriental cockroach (Blatta orientalis); E, American cockroach (P. americana); F, Brownbanded cockroach (Supella longipalpa); G, German cockroach (Blattella germanica). (Courtesy of the US Public Health Service)

antennal sockets is variable: they are well developed in winged species (macropterous) but rudimentary or lacking in species with reduced wings (brachypter0us) or those lacking wings altogether (apterous).

Adults generally have two pairs of wings that are folded fanwise at rest. The front wings, called tegmina (singular tegmen), are typically hardened and translucent, with well-defined veins. The hind wings are membranous and larger. In some species, such as the wood cockroaches (e.g., Parcoblatta species), females are brachypterous and incapable of flight, whereas males are macropterous. Other species, such as the Florida woods cockroach (Eurycot# floridana), have only vestigial wing buds as adult males and females. In cockroaches, all three pairs of legs are well developed, with large coxae and slender, long segments that aid in the rapid running that is characteristic of these insects. Each femur has two longitudinal keels that typically are armed with spines. The tibiae are often heavily spined and are used for defense against predators. Each tarsus consists of five segments with a pair of claws and may bear a padlike arolium that aids in walking on smooth surfaces. Ventral pads, or pulvilli, are present on tarsomeres 1-4. A pair of caudal cerci have small ventral hairs that are sensitive to vibrations caused by lowfrequency sound and air movement; their stimulation initiates an escape response.

The posterior end of the abdomen of some nymphs and all males bears a pair of styli (singular stylus) between the cerci, arising from the sternum of the ninth abdominal segment. In winged species, the styli may be apparent only when viewed ventrally. The structure of the styli serves to distinguish males from females. Generally the males also can be recognized by their more slender bodies, with laterally tapered and dorsally flattened external genitalia (terminalia). The terminalia of the more robust females are notably broader than in males and bear a conspicuous subgenital plate that is rounded or keel-like when viewed ventrally. Associated with this plate is a relatively large genital chamber (genital pouch) in which the ootheca develops. For a more detailed description of cockroach genitalia, see McI~ttrick (1964) or Cornwell (1968). Nymphal stages are similar in appearance to adults, but they lack wings, have incompletely developed genitalia, and may vary markedly in color from the adult.

LIFE HISTORY

Cockroaches are paurometabolous insects. The immature cockroaches generally are similar in appearance to the adults except for their undeveloped sexual organs and lack of fully developed wings (Fig. 3.2). Reproduction in cockroaches is typically sexual, although parthenogenesis is reported in a few species. Comparative life history data for some of the more common cockroach pests are provided in Table I.

In cockroaches, embryogenesis and oviposition occur in one of three ways. Most species are oviparous, including

Developmental stages of cockroaches, represented by Periplaneta brunnea. Left to right: first, second, third, and fourth nymphal instars; adult female, adult male. (Courtesy of Daniel R. Suiter)
FIGURE 3.2 Developmental stages of cockroaches, represented by Periplaneta brunnea. Left to right: first, second, third, and fourth nymphal instars; adult female, adult male. (Courtesy of Daniel R. Suiter)

all Periplaneta species and the Oriental and brownbanded cockroaches. Eggs of oviparous species are protected inside a thick-walled, impermeable ootheca which is deposited soon after it is formed. Embryonic development occurs external to the female. The German cockroach is oviparous, but the female carries the ootheca protruding from the genital chamber until just hours before hatching occurs. The ootheca is softer than in Periplaneta species, allowing uptake of water and nutrients from the genital pouch. A few cockroaches, such as Blaberus species and the Surinam cockroach, are pseudo-ovoviviparous, in that females produce an ootheca which is extruded, rotated, and then retracted into the genital pouch. The eggs are incubated internally until hatching. The only known pseudo-viviparous species is Diploptera punctata, a pest species in Hawaii; the embryos hatch while still in the genital pouch. Embryogenesis takes 1-8 weeks, depending on the species.

The number of nymphal instars varies from 5 to 13, depending on the species, nutritional sources, and microclimate. Development of pestiferous species through the nymphal stadia requires from 6-7 weeks for German cockroaches to well over a year for Periplaneta species and other larger cockroaches. Typically, the nymphs exhibit strong aggregation tendencies, governed largely by aggregation pheromones. These pheromones act as locomotory inhibitors; when cockroaches perceive the pheromone they become relatively stationary. Studies of various species have shown that development to the adult stage is quicker when nymphs are reared in groups rather

I Life Histories of Selected Common Species of Cockroaches, Showing the High Degree of Variability Within Species Due to Environmental Temperatures and Nutritional Availability

 

than in isolation. However, aggregation does have a biological cost; those reared in groups typically are smaller in size, and cannibalism may occur. Longevity of cockroaches varies from several weeks to over a year.

BEHAVIOR AND ECOLOGY

Mating in cockroaches generally is preceded by courtship behavior facilitated by sex pheromones. In some species a blend of volatile compounds is produced by virgin females to attract and orient males (e.g., Periplaneta species and the brownbanded cockroach). In the German cockroach, the sex pheromone is a blend of nonvolatile and volatile cuticular components that elicits courtship by males following palpation of the female’s integument by the male’s antennae. Once courtship is initiated in the male, he turns away from the female and raises his wings to expose dorsal tergalglands; the female feeds on pheromones from these glands as the male grasps her genitalia with his pair of caudal claspers. Most species copulate in an end-to-end position. During the hour or so that follows, a spermatophore is formed and passed from the male into the genital chamber of the female. Only about 20% of females mate again after the first gonotrophic cycle.

Cockroaches can be categorized ecologically as domestic, peridomestic, or feral. Domestic species live almost exclusively indoors and are largely dependent on humans for resources (food, water, and harborage) for survival. They rarely are able to maintain themselves outdoors. Although this group contains the smallest number of species, it presents the greatest concern to human health. Domestic species include the German and brownbanded cockroaches. Peridomestic species are those which survive in or around human habitation. Although they do not require humans for their survival, they are adept at exploiting the amenities of civilization. This group is represented by American, Australian, brown, and smokybrown cockroaches (all Periplaneta species), the oriental cockroach, and the Florida woods cockroach. Feral species are those in which survival is independent of humans. This group includes more than 95% of all species in the world. Only a few occur indoors as occasional and inadvertent invaders that typically do not survive in a domestic environment. They are of little or no medical importance.

Cockroach behavior and survival are strongly influenced by their need for food, water, and safe harborage from potential predators and detrimental microclimates. They are omnivorous and will consume virtually any organic matter, including fresh and processed foods, stored products, and even book bindings and pastes on stamps and wallpaper when more typical foodstuffs are not available. Cockroaches have the same general problems with water balance as do other terrestrial arthropods. Their relatively small size results in a high surface area to volume ratio and a high risk of losing water through respiration, oral and anal routes, or the cuticle. Temperature, air flow, relative humidity, and availability of liquid water greatly affect water regulation.

As a result of these physiological considerations, physical constraints of the environment usually determine habitat preferences of cockroaches in and around structures. Oriental and American cockroaches, for example, require high moisture and occur in damp terrestrial environments such as septic tanks and municipal sewer systems. Brown, smokybrown, and Florida woods cockroaches occur in a wider range of habitats associated with trees, wood and leaf piles, wall voids, and foundation blocks of buildings. Brownbanded cockroaches are more tolerant of drier conditions and commonly occur in kitchens, pantries, and bedrooms. German cockroaches occupy harborages near food and water. Consequently, they are found primarily in kitchens and pantries, and secondarily in bathrooms, when their populations are high. In mixed populations of German and brownbanded cockroaches, the German cockroach tends to outcompete the brownbanded cockroach within 9 months.

Cockroaches are adept crawlers and are capable of rapid movement even across windows and ceilings. Flight ability varies with species. Some are incapable of flight except for crude, downward gliding used as an escape behavior. Others are weak fliers, occasionally seen flying indoors when disturbed. Still others are relatively strong fliers that are particularly active at sunset, when they may be attracted indoors by lights and brightly lit surfaces. Attraction to light is especially common in the Asian, Surinam, and Cuban cockroaches and in many of the wood cockroaches (Parc0blatta species).

Pestiferous cockroaches that occur indoors are typically nocturnal and tend to avoid lighted areas. This enables them to increase their numbers and become established in structures before human occupants even become aware of their presence.

COMMON COCKROACH SPECIES

The following 11 species of cockroaches are commonly encountered by homeowners in the United States and are the ones most frequently brought to the attention of medical entomologists.

Oriental cockroach (Blatta orientalis)

This peridomestic cockroach (Fig. 3.3) is believed to have originated in northern Africa and from there spread to Europe and western Asia, South America, and North America. It is a relatively lethargic species that prefers cooler temperatures than does the German cockroach and is primarily a concern in temperate regions of the world. Adults are black and 25-33 mm long. Males are winged but do not fly, and females are

Oriental cockroach (Blattella orientalis), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.3 Oriental cockroach (Blattella orientalis), female. (Courtesy of the University of Florida/IFAS)
American cockroach (Periplaneta americana), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.4 American cockroach (Periplaneta americana), female. (Courtesy of the University of Florida/IFAS)

brachypterous. Their tarsi lack aroliar pads, precluding this cockroach from climbing on smooth vertical surfaces. Oothecae are 8-10mm long, each typically containing 16 eggs. Also commonly lmown as waterbug, this species is usually associated with damp or wet conditions, such as those found in decaying wood, heavy ground cover (e.g., ivy) , water meter boxes, and the lower levels of structures. It infests garbage chutes of apartment complexes, sometimes reaching upper floors. Development is slow compared to that of most other species, requiring about a year depending on temperature conditions. Adults may live for many months. Mobility is fairly restricted, malting control easier than for most other species. This species is rarely seen during the daytime.

American cockroach (Periplaneta americana)

The American cockroach (Fig. 3.4) is a large species with adults 34-53 mm in length. It is reddish brown, with substantial variation in light and dark patterns on the pronotum. Adults are winged and capable of flight. Nymphs typically complete development in 13- 14months while undergoing 13molts. Adults live an average of 15 months, but longevity may exceed 2 years. Females drop or glue their oothecae (8 mm long) to substrates within a few hours or days of formation. Each ootheca has 12-16 embryos. A female generally produces 6-14 egg cases during her life (mean of 9).

The American cockroach is perhaps the most cosmopolitan peridomestic pest species. Together with other closely related Periplaneta species, P. americana is believed to have spread from tropical Africa to North America and the Caribbean on ships engaged in slave trading. Today this species infests most of the lower latitudes of both hemispheres and extends significantly into the more temperate regions of the world.

The habitats of this species are quite variable. American cockroaches infest landfills, municipal sewage systems, storm drainage systems, septic tanks, crawl spaces beneath buildings, attics, tree holes, canopies of palm trees, voids in walls, ships, electronic equipment, caves, and mines. Studies conducted in Arizona indicated movement by a number of individuals several hundred meters through sewer systems and into neighboring homes. This species often can be seen at night on roofs and in air stacks or vents of sewage systems, through which they enter homes and commercial buildings. Entrance also is gained to homes through laundry vent pipes and unscreened or unfiltered attic ventilation systems. This cockroach is known to move from crawl spaces of hospitals via pipe chases into operating theaters, patients’ rooms, storage facilities, and food preparation areas. Consequently, the potential of this cockroach for disseminating pathogenic microorganisms can be a significant concern for health care personnel.

Australian cockroach (Periplaneta australasiae)

Adult body coloration is similar to that of the American cockroach, but with paler lateral markings on the upper edges of the tegmina (Fig. 3.5). The pronotum is tinged with similar coloration. Adults are slightly smaller than American cockroaches, measuring 32- 35 mm in length. Females mature in about 1 year and typically live for another 4-6 months. A female can produce 20-30 oothecae during her lifetime; the ootheca is about 11 mm long and contains about 24embryos. Embryonic development requires about 40 days. Nymphs are strikingly mottled, distinguishing them from nymphs of other Periplaneta species.

This peridomestic species requires somewhat warmer temperatures than the American cockroach and does not occur in temperate areas other than in greenhouses and

Australian cockroach (Periplaneta australasiae), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.5 Australian cockroach (Periplaneta australasiae), female. (Courtesy of the University of Florida/IFAS)
Brown cockroach (Periplaneta brunnea), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.6 Brown cockroach (Periplaneta brunnea), female. (Courtesy of the University of Florida/IFAS)

other pseudotropical environs. In the United States, outdoor populations are well established in Florida and along the coastal areas of Louisiana, Mississippi, Alabama, and Georgia. It commonly is found in environments similar to those inhabited by the smokybrown cockroach. In situations where both species occur (e.g., tree holes, attics), the Australian cockroach tends to displace the smokybrown. It can be a serious pest in greenhouses and other tropical environments in more temperate latitudes, where it can cause feeding damage to plants, notably seedlings.

Brown cockroach (Periplaneta brunnea)

The brown cockroach (Fig. 3.6) is smaller than the American cockroach (33-38 mm), and its pronotal markings are more muted. The most apparent diagnostic characteristic for separating these two species is the shape of the last segment of the cercus; in the brown cockroach, the length is about equal to the width, whereas in the American cockroach the length is about 3 times the width. The ootheca of the brown cockroach usually is larger (7-13 vs 8 ram) and contains more embryos (24 vs 16). The brown cockroach affixes its oothecae to substrates using salivary secretions. They give the ootheca a grayish hue not typical of other Periplaneta species that attach their oothecae with salivary secretions. This species is more subtropical than the American cockroach, occurring throughout the southeastern United States, where it infests homes and outbuildings. It is less frequently associated with sewage than is the American cockroach. Because of its similar appearance to the American cockroach, it is often misidentified and may be more widely distributed than is commonly recognized. In Florida, P. brunnea is commonly found in canopies of palm trees and attics. It also readily infests various natural cavities and those in human-associated structures. The oothecae can be useful in differentiating species infesting buildings. Most

Smokybrown cockroach (Periplaneta fuliginosa), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.7 Smokybrown cockroach (Periplaneta fuliginosa), female. (Courtesy of the University of Florida/IFAS)

cockroach oothecae persist in the environment after the nymphs have emerged and provide a history of infestation.

Smokybrown cockroach (Periplanetafuliginosa)

The smokybrown cockroach (Fig. 3.7) has become a major peridomestic pest throughout the southern United States, including southern California, and extends as far north as the Midwestern states. It can be differentiated from the American cockroach by its slightly smaller size (25-33 ram) and uniform dark coloration. Mthough developmental times are quite variable, individuals mature in about 10 months. Adults may live for more than a year. Females produce several oothecae, which are 10-11 mm in length with 20 embryos, at 11-day intervals.

Primary loci for this peridomestic species in the southeastern United States are tree holes, canopies of palm trees, loose mulches such as pine straw or pine bark, and firewood piles. Within structures, P. futiginosa seeks the ecological equivalent of tree holes–areas characterized as dark, warm, protective, and moist, with little air flow and near food resources. These include the soffits (eves) of underventilated attics, behind wall panels, the interstices of block walls, false ceilings, pantries, and storage areas. From these harborages, individuals forage for food and water, generally returning to the same refugia. Mark-release-recapture studies using baited live traps have shown that the median distance traveled between successive recaptures is less than I m but that some adults may forage at distances of more than 30 m.

Florida woods cockroach (Eurycotisfloridana)

This cockroach is restricted to a relatively small area of the United States along the Gulf of Mexico from

Florida woods cockroach (Eurycotisfloridana), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.8 Florida woods cockroach (Eurycotisfloridana), female. (Courtesy of the University of Florida/IFAS)

eastern Louisiana to southeastern Georgia. It is mentioned here only because of its defensive capabilities. It is a large, dark-reddish brown to black cockroach (Fig. 3.8), 30-40 mm long. Although small wing pads are evident, adults are apterous and are relatively slow moving. Oothecae are 13-16 mm long and contain about 22 embryos. E. floridana occurs in firewood piles, mulches, tree holes, attics, wall voids, and outbuildings. Last-instar nymphs and adults, if alarmed, can spray a noxious mix of aliphatic compounds that are both odoriferous and caustic. If this is sprayed into the eyes or onto soft tissues, a temporary burning sensation is experienced. Domestic dogs and cats quicldy learn to avoid this species. Among its common names are the Florida cockroach, the Florida woods roach, the Florida stinkroach, and palmettobug. The last term also is commonly used for other Pcriplaneta species.

Brownbanded cockroach (Supella longipalpa)

Like the German cockroach, this domestic species probably originated in tropical Africa, where it occurs both indoors and outdoors. In North America and Europe it is confined almost exclusively to indoor environments of heated structures. In warm climates, infestations occur particularly in apartments without air conditioning and in business establishments with relatively high ambient temperatures, such as pet stores and animal-care facilities. Adults are similar in size to the those of the German cockroach (13-14.5 mm long) but lack pronotal stripes. Adults have two dark bands of horizontal stripes on the wings (Fig. 3.9), whereas nymphs have two prominent bands running across the mesonotum and first abdominal segment. The brownbanded cockroach derives its name from these bands.

Brownbanded cockroach (Supella longipalpa), female. (Courtesy of the University of Florida/IFAS)
FIGURE 3.9 Brownbanded cockroach (Supella longipalpa), female. (Courtesy of the University of Florida/IFAS)

Populations tend to occur in the nonfood areas of homes, such as bedrooms, living rooms, and closets. Male brownbanded cockroaches occasionally fly and are attracted to lights. Members of this species seek harborage higher within rooms than do German cockroaches. The ootheca is small, only 5 mm long, with an average of 18 embryos and an incubation time of 35-80 days. Females deposit their oothecae by affixing them to furniture, in closets, on or behind picture frames, and in bedding. Transporting S. longipalpa with furniture to new locales is common. Although this species occurs with other cockroaches in homes, the German cockroach often outcompetes it within a few months.

German cockroach (Blattellagermanica)

This cockroach also is known as the steamily in Great Britain. It is believed to have originated in northern or eastern Africa, or Asia, and has spread from there via commerce. The German cockroach is considered to be the most important domestic pest species throughout the developed world. Adults are about 16 mm long, with two dark, longitudinal bands on the pronotum (Fig. 3.10). It requires warm (optimally 30-33°C), moist conditions near adequate food resources. It primarily inhabits kitchens and pantries, with secondary foci in bathrooms, bedrooms, and other living spaces in heavily infested structures. Although this species is nocturnal, like most other cockroaches, some individuals may be seen moving about on walls and in cupboards during the daylight hours where infestations are heavy. Their wing musculature is vestigial, making them unable to fly except for short, gliding, downward movements. B. germanica does not readily move between buildings; however, it does occur in garbage collection containers and outbuildings near heavily infested structures.

German cockroach (Blattella german#a), female. (Courtesy of the University of Florida/IFAS)
HGURE 3.10 German cockroach (Blattella german#a), female. (Courtesy of the University of Florida/IFAS)

The German cockroach has a high reproductive potential. Females produce an ootheca (6-9 ram) containing about 30 embryos within 7-10 days after molting to the adult, or about 2-3 days after mating. The female carries the egg case until a few hours before hatching of the nymphs, preventing access of any oothecal parasitoids or predators. Oothecae are produced at intervals of 20- 25 days, with a female producing 4-8 oothecae during her lifetime. Nymphs complete their development in 7- 12 weeks.

This species is the main cockroach pest in most households and apartment complexes. Control is difficult, in part because of their movement between apartments through plumbing chases in shared or adjacent walls. Researchers studying over 1,000 apartments in Florida concluded that the median number of cockroaches per apartment was >13,000. This high biotic potential makes this species a major nuisance, as well as a pest with implications for human health.

Asian cockroach (Blattella asahinai)

The Asian cockroach is closely related to the German cockroach, from which it is difficult to distinguish morphologically. In fact, Asian and German cockroaches are capable of hybridizing and producing fertile off’- spring, which further complicates their identifications. Techniques have been developed to differentiate these two species and their hybrids based on cuticular hydrocarbons in the waxy layer of the integument.

Despite their morphological similarity, B. asahinai differs from B. germanica in several aspects of its behavior and ecology. It is both a feral and a peridomestic species. Nymphs of the Asian cockroach commonly occur, sometimes in large numbers, in leaf litter and in areas of rich ground cover or well-maintained lawns. Unlike the German cockroach, the adults fly readily and are most active beginning at sunset, when they fly to light-colored walls or brightly lit areas. This behavior can make invasion a nightly occurrence in homes near heavily infested areas. Flight does not occur when temperatures at sunset are below 21°C.

Like those of the German cockroach, Asian cockroach females carry their oothecae until shortly before they are ready to hatch. The ootheca is similar in size and contains the same number of embryos as does that of the German cockroach (38-44). Nymphs are smaller than their B. germanica counterparts and are somewhat paler in appearance. Development from egg to adult requires about 65 days, with females producing up to six oothecae during their life span. Adults also are slightly smaller than those of B. germanica (average of 13 vs 16mm).

The Asian cockroach was first described in 1981 from specimens collected in sugar-cane fields on the Japanese island of Okinawa. When it was first discovered in the United States in 1986, the Asian cockroach was found only locally in three counties in Florida, from Tampa to Lakeland; populations already had become established, with densities as high as 250,000 per hectare. By 1993, this species had spread to at least 30 Florida counties and had infested citrus groves throughout the central part of the state. It feeds on succulent early growth of citrus nursery stock, tassels of sweet corn, strawberries, cabbage, tomatoes, and other agricultural products, although there has been no evidence of significant economic damage.

Infestations of apartments by B. asahinai have become common in central Florida. This cockroach also has become an increasing problem in warehouses, department stores, hotels, fast-food establishments, automobile dealerships, and other businesses with hours of operation that extend beyond dusk.

Surinam cockroach (Pycnoscelus surinamensis)

This species is believed to have originated in the Indo- Malayan region. It commonly occurs in the southeastern United States from North Carolina to Texas. The adults are fairly stout, 18-25 mm in length, with shiny brown wings and a black body (Fig. 3.11). Nymphs characteristically have shiny black anterior abdominal segments, whereas the posterior segments are dull black and roughened. In North America this species is unusual in that it is parthenogenetic, producing only female offspring; elsewhere both males and females are found. The ootheca is 12-15 mm long, is poorly sclerotized, and contains about 26 embryos. Oothecae are retained inside the genital chamber, from which the nymphs emerge in about 35 days. Females produce an average of three oothecae and live about 10 months in the laboratory. This cockroach commonly burrows into compost piles and the thatch of lawns. Transfer

Surinam cockroach (Pycnoscelussurinamensis). (Courtesy of the University of Florida/IFAS)
FIGURE 3.11 Surinam cockroach (Pycnoscelussurinamensis). (Courtesy of the University of Florida/IFAS)

of fresh mulch into the home for potting plants can result in household infestations. Adult females fly and are attracted to light. They are most likely to be noticed by homeowners at night when they fly into brightly lit television screens. This species commonly is transported in commercial mulch to more temperate areas of the United States, where it has been known to infest greenhouses, indoor plantings in shopping malls, and ZOOS.

Cuban cockroach (Panchlora nivea)

This medium-sized cockroach (22-24 mm in length) is unusual in that the adults are pale green. The nymphs are dark brown and are found in leaf litter and decaying wood piles. Adults are strong fliers and are attracted to lights. Panchlora nivea is believed to be native to the Caribbean basin, Mexico, Central America, and northern South America. In the United States it occurs commonly in Florida and coastal Louisiana and Texas. This cockroach often is seen in the evening, resting on windows and glass patio doors, apparently drawn to the brightness of indoor lighting.

PUBLIC HEALTH IMPORTANCE

Cockroaches infesting human dwellings and workplaces represent a more intimate and chronic association than do most other pests of medical/veterinary importance. High populations of any cockroach species may adversely affect human health in several ways. These include contamination of food with their excrement, dissemination of pathogens, induced allergies, psychological stress, and bites. Mthough documentation of bites is limited, there are reports of cockroaches feeding on fingernails, eyelashes, skin calluses of hands and feet, and food residues about the faces of sleeping humans, causing blisters and small wounds (Roth and Willis 1957, 1960). There are other accounts of bites around the mouths of infants in heavily infested homes and even in hospitals. American and Australian cockroaches are the most often implicated species. Bites by the Oriental cockroach have resulted in inflammation of the skin, degeneration of epithelial cells, and subsequent necrosis of the involved tissues.

While many individuals develop a tolerance for cockroach infestations, others may experience psychological stress. The level of stress tends to be proportional to the size of the cockroaches and the magnitude of the infestation. An aversion to cockroaches may be so strong that some people become irrational in their behavior, imagining a severe infestation even when there is none. This illusion of abundant cockroaches has caused some families to move out of their homes. High cockroach populations also produce a characteristic odor that can be unpleasant or even nauseating to some people. Foodstuffs may become contaminated with the excrement of cockroaches, which, on subsequent ingestion, may cause vomiting and diarrhea.

The presence of cockroaches in homes does not necessarily imply poor housekeeping. Peridomestic species such as the American and the Oriental cockroach commonly infest municipal sewage systems or septic tanks and may move into homes through sewage lines. Any of the Periplaneta species may develop high outdoor populations, inducing individuals to seek less crowded environments. At such times, they often enter homes through attic vents, breaches in construction joints, or through crawl spaces. This tends to occur in early fall. While they are active at night the smokybrown cockroach, Asian cockroach, and feral wood roaches (Parcoblatta species) often find their way into even the best-kept homes. Adults frequently alight on doors illuminated by entrance lights, or on window screens of lighted rooms. Entrance is gained once the door is opened or by squeezing past window-screen frames.

Poor housekeeping and unsanitary conditions contribute significantly to cockroach infestations. The German cockroach and, to a lesser degree, the brownbanded cockroach are the principal bane of apartment dwellers. Their survival is enhanced by crowded living quarters, associated clutter, and the accumulated organic debris associated with food preparation. Construction practices used to build apartment complexes (e.g., common wiring ducts, sewage lines, and refuse areas) can contribute to the spread of cockroaches in multiunit dwellings.

Bacteria adhering to tarsus of German cockroach (Blattellagermanica). (From Gazivoda and Fish 1985)
FIGURE 3.12 Bacteria adhering to tarsus of German cockroach (Blattellagermanica). (From Gazivoda and Fish 1985)

PATHOGENIC AGENTS

The significance of cockroaches in public health remains controversial despite the logical assumption that they play a role in transmitting pathogenic agents. Given that cockroaches are so closely associated with humans and poor sanitation, the potential for acquiring and mechanically transmitting disease agents is very real. They are capable of transmitting microorganisms (Fig. 3.12) and other disease agents indirectly by contaminating foods or food preparation surfaces.

Table II lists pathogenic organisms that have been isolated from cockroaches in domestic or peridomestic environments. At least 32 species of bacteria in 16 genera are represented. These include such pathogens as Bacillus subtilis, a causative agent of conjunctivitis; Escherichia coli and 9 strains of Salmonella, causative agents of diarrhea, gastroenteritis, and food poisoning; Salmonella typhi, the causative agent of typhoid; and 4 Proteus species, which commonly infect wounds. These isolations primarily have involved American, German, and Oriental cockroaches. Cockroaches also have been found harboring the eggs of 7 helminth species, at least 17 fungal species, 3 protozoan species, and 2 strains ofpoliomyelitic virus (Brenner et al,. 1987; Koehler et al., 1990, Brenner 1995). Researchers in Costa Rica have shown that Australian, American, and Madeira cockroaches become infected with the protozoan Toxoplasmagondii after eating feces of infected cats. This suggests the possibility of cockroach involvement in the maintenance and dissemination of this parasite, which causes toxoplasmosis in humans, cats, and other animals.

Mthough many pathogens have been recovered from natural populations of cockroaches, this does not necessarily mean that cockroaches serve as their vectors. Isolation of pathogens from cockroaches simply may be

Bacteria Pathogenic to Humans That Have Been Isolated from Field-Collected Cockroaches

indicative of the natural microbial fauna and flora in our domestic environment. Under certain circumstances, however, cockroaches have the potential for serving as secondary vectors of agents that normally are transmitted by other means. Anecdotal accounts associating diseases in humans with the occurrence of cockroaches and microbes lend some credence to the hypothesis that these pests can serve as vectors. Burgess (1982) reported the isolation from German cockroaches of a serotype of S. dysenteriae that was responsible for an outbreak of dysentery in Northern Ireland. Mackerras and Mackerras (1948) isolated S. bovis-morbificans and S. typhimurium from cockroaches captured in a hospital ward where gastroenteritis, attributed to the former organism, was common. In subsequent experimental studies, Salmonella organisms remained viable in the feces of cockroaches for as long as 40 days postinfection (Mackerras and Mackerras 1949). Some of the most compelling circumstantial evidence suggesting that cockroaches may be vectors was noted in a correlation between cases of infectious hepatitis and cockroach control at a housing project during 1956- 1962 in southern California (Tarshis 1962). The study area involved more than 580 apartments and 2800 persons; 95% of the apartments had German cockroaches and a lesser infestation of brownbanded and Oriental cockroaches. After pest control measures were initiated, the incidence of endemic infectious hepatitis decreased for i year. When treatments were discontinued during the following year because the insecticide was offensive to apartment dwellers, the cockroach population increased, accompanied by a corresponding increase in the incidence of hepatitis. Effective control measures were applied for the following 2 years, and cockroach populations and cases of infectious hepatitis dropped dramatically while hepatitis rates remained high in nearby housing projects where no pest control measures were conducted.

INTERMEDIATE HOSTS

Cockroaches can serve as intermediate hosts for animal parasites (Table III). Roth and Willis (1960) published an extensive list of biotic associations between cockroaches and parasitic organisms that potentially infest humans. The eggs of seven species of helminths have been found naturally associated with cockroaches. These include hookworms (Ancylostoma duodenale and Necator americanus), giant human roundworm (Ascaris lumbricoides), other Ascaris species, pinworm (Enterobius vermicularis), tapeworms ( Hymenolepis species), and the whipworm Trichuris trichuria. Development of these helminths in cockroaches has not been observed. These relationships probably represent incidental associations with the omnivorous feeding behavior of cockroaches.

However, cockroaches may serve as potential reservoirs and possible vectors through mechanical transfer in areas where a high incidence of these pathogens in humans is accompanied by substantial cockroach infestations. Human infestations by spirurid nematodes associated with cockroaches are known only for the cattle gullet worm (Gongylonema pulchrum) in the United States, Europe, Asia, and Africa and for the stomach worm Abbreviata caucasia in Africa, Israel, Colombia, and Chile. Human cases involving these parasites are rare and cause no pathology.

COCKROACH ALLERGIES

It is only in recent years that the importance of cockroach allergies has been recognized. Allergic reactions result after initial sensitization to antigens following inhalation, ingestion, dermal abrasion, or injection. Allergens produced by cockroaches are rapidly being recognized as one of the more significant indoor allergens of modernized societies. Among asthmatics, about half are allergic to cockroaches. This rate is exceeded only by allergies to house-dust mites. Sensitivity to cockroaches also affects about 10% of nonallergic individuals, suggesting a subclinical level of allergy.

Symptoms exhibited by persons allergic to cockroaches are similar to those described by Wirtz (1980), who reported on occupational allergies in entomologists. They include sneezing and a runny nose, skin reactions, and eye irritation in about two-thirds of the cases. In the more severe cases, individuals may experience difficulty breathing or, even more alarming, anaphylactic shock following exposure to cockroaches. Such allergic reactions can be life-threatening (Brenner et al., 1991).

In recent years, research has focused on determining the specific components of cockroaches that cause allergy. Laboratory technicians exhibit strong allergies to cast skins and excrement of German cockroaches, whereas most patients seen at allergy clinics react primarily to cast skins and whole-body extracts of German cockroaches. Once an individual has become hypersensitized, he or she may experience severe respiratory distress simply by entering a room where cockroaches are held.

Several proteins that can cause human allergies have been identified in the German cockroach. Different exposure histories are likely to result in allergies to different proteins. Cast sldns, excrement, and partially consumed food of cockroaches, in addition to living cockroaches, all produce allergenic proteins. Some are extremely persistent and can survive boiling water, ultraviolet light, and harsh pH changes, remaining allergenically potent for decades. Traditionally, whole-body extracts have been used to screen for allergens in sldn tests and in bronchial challenges for diagnosing cockroach allergies

Cockroaches as Intermediate Hosts of Parasites of Veterinary Importance

(Fig. 3.13). However, use of more specific antigens that become aerosolized in cockroach-infested homes may be more appropriate, as this is likely to be the sensitizing material. Studies with laboratory colonies have shown that a population of several thousand German cockroaches produced several micrograms of aerosolized proteins in 48 hr. Consequently, the presence of cockroaches may have profound respiratory implications for asthmatic occupants of infested structures. For a general discussion on aerosolized arthropod allergens, see Solomon and Mathews (1988).

Development of an allergy to one insect species can result in broad cross-reactivity to other arthropods, including shrimp, lobster, crab and crawfish, sowbugs (isopods), and house-dust mites. Chronic indoor exposure to cockroach allergens, therefore, may have significant and widespread effects on human health.

VETERIN/ dkY IMPORTANCE

Cockroaches serve as intermediate hosts for a number of parasitic worms of animals (Table III). Most of these relationships are of no economic importance. The majority of the parasites are nematodes in the order Spirurida, all members of which use arthropods as intermediate hosts. Species infesting dogs and cats, among other hosts, attach to the mucosa of the gastrointestinal tract, where erosion of tissue may occur at the points of attachment.

Apparatus for conducting allergen tests using cockroaches. (Courtesy of R. J. Brenner, USDA/ARS)
FIGURE 3.13 Apparatus for conducting allergen tests using cockroaches. (Courtesy of R. J. Brenner, USDA/ARS)

Although serious damage seldom occurs, anemia and slow growth may result. Several cockroach-associated nematodes occur in Europe and North America. The esophageal worms Physaloptera rara and P. praeputialis are the most widespread species in the United States. They develop in the German cockroach, field crickets, and several species of beetles.

Poultry also are parasitized by nematodes which undergo development in cockroaches. The Surinam cockroach is the intermediate host for the poultry eye worms Oxyspirura mansoni and O. parvorum. Both occur in many parts of the world. In the United States, their distribution is limited to Florida and Louisiana. The German cockroach has been incriminated as the intermediate host for chicken and turkey parasites, including the stomach worms Tetrameres americana, T. fissispina, and Cyrnea colini; C. colini also develops in the American cockroach. C. colini apparently causes no significant damage to poultry, but Oxyspirura species can cause pathology ranging from mild conjunctivitis to severe ophthalmia with seriously impaired vision. T. fissispina can cause severe damage to the proventriculus of infested birds.

Several nematode parasites of rats and cattle utilize cockroaches as intermediate hosts (Table III). These include G. neoplasticum and Mastophorus muris in rodents. Both genera occur widely in the United States, where they cause no known pathological problems. The gullet worm of cattle, G. pulchrum, has been shown experimentally to undergo development in the German cockroach, although the usual arthropod hosts are coprophagous beetles.

Exotic zoo animals also can become infested with parasitic nematodes for which cockroaches serve as possible intermediate hosts. Protospirura bonnei and P. muricola, for example, have been found in cockroaches collected in cages of monkeys. In a case of “wasting disease” in a colony of common marmosets, more than 50% of German and brownbanded cockroaches captured in the animal room in which they were housed contained the coiled larvae of Trichospirura leptostoma in muscle cells (Beglinger et al., 1988).

Acanthocephalans (thorny-headed worms) commonly infest primates in zoos and research facilities. Prosthenorchis elegans and P. spirula occur naturally in South and Central America. Their natural intermediate hosts are unknown. In captivity, primates become infected after eating any of several cockroach species in which the intermediate stages of the parasite have completed development. Heavily infested primates frequently die within a few days. The proboscis of acanthocephalan adults commonly penetrates the intestines of the primate host, causing secondary infections, perforation of the gut wall, and peritonitis.

One pentastomid (tongue worm), Raillietiella hemidactyli, develops in cockroaches and reptilian hosts. In Singapore, infested geckos are a common occurrence in houses where heavy infestations of R. hemidactyli larvae have been found in American cockroaches. Remnants of cockroaches are found commonly in the guts of these lizards.

For additional information on the veterinary importance of cockroaches, see Chitwood and Chitwood (1950), Roth and Willis (1957), Levine (1968), and Noble and Noble (1976).

PREVENTION AND CONTROL

Traditionally, cockroaches have been controlled using a variety of toxic chemicals applied as residual pesticides to harborage sites or areas frequented by foraging individuals (see Ebling, 1975 and Rust et. al., 1995). Most materials are neurotoxins that disrupt the nervous system, causing locomotory and respiratory failure. These include organophosphates, carbamates, botanicals such as pyrethrins, and pyrethroids. Formulations include wettable powders, emulsifiable concentrates, crack-andcrevice aerosols, dusts, and baits. Several other materials with different modes of action also are currently in use. When ingested, boric acid (delivered as a fine powder or a dilute solution) damages the gut epithelium of cockroaches and kills them by interfering with nutrient absorption. Inorganic silica dust is absorptive, reducing cuticular lipids and causing desiccation. Active ingredients with other modes of action, such as hydramethylnon and sulfluramid, are metabolic inhibitors which disrupt the conversion of food to energy.

The use of baits containing many of the active ingredients mentioned above have been used extensively to control cockroaches. These baits are used indoors in the form of child-resistant bait stations to reduce human exposure. Other bait formulations of gels or pastes are used in crackand- crevice treatments, making them inaccessible to children and pets. Scatter baits are commonly used outdoors to treat mulches and other landscaping materials that harbor cockroaches.

Insect growth regulators (IGRs) can be used to prevent cockroaches from reaching maturity. Two commonly used IGRs are juvenile hormone analogs and chitin synthesis inhibitors. Juvenile hormone analogs regulate morphological maturation and reproductive processes. They are highly specific to arthropods, have very low mammalian toxicity, and are effective at exceptionally low rates of application. Such compounds include hydroprene and fenoxycarb. Chitin synthesis inhibitors prevent normal formation of chitin during molting. These compounds cause many of the affected nymphs to die during the molting process. Males that survive to the adult stage often have reduced life expectancies, whereas females tend to abort their oothecae.

Integrated pest management, which incorporates various control techniques, has contributed significantly to successful control of cockroaches. This approach uses nontoxic agents, such as sticky traps, vacuum devices, diatomaceous earth, or silica-gel repellents and desiccants, and manipulation of harborage sites to reduce or prevent infestations. Desiccants and dusts should be used only in geographic areas or situations with relatively low humidity; high humidity causes these materials to clump and lose their effectiveness. Building designs and construction techniques can significantly influence cockroach survival. By manipulating microclimates in discrete areas of structures frequented by cockroaches, homes and other buildings can be rendered less hospitable to pest species while at the same time greatly reducing aerosolized allergens. Nontoxic repellents can be used to deny access of cockroaches to specific areas.

Biological control of cockroaches has drawn increased attention in recent years. Among the natural agents that have been investigated are parasitic wasps, nematodes, and sporulating fungi. Females of the eulophid wasp Aprostocetus hagenowii and the evaniid wasp Comperia merceti deposit their eggs in the oothecae of certain peridomestic cockroaches. Major shortcomings in utilizing these wasps are difficulties involved in their mass production and the fact that they do not completely eliminate cockroach infestations. However, A. hagenowii has been shown to reduce populations of the peridomestic Periplaneta species following inundative or augmentative releases of this wasp. C. merceti parasitizes oothecae of the brownbanded cockroach and is the only known parasitoid of a domestic species. The use of parasitic nematodes (e.g., Steinernema carpocapsae) and several fungal pathogens that have been isolated from cockroaches has not yet proved to be effective as a practical management tool. Another drawback to their use is the allergenic nature of several components of nematodes and many sporulating fungi that can become airborne and, upon inhalation, cause asthmatic responses in humans.

Models have been developed for predicting population foci of peridomestic cockroaches based on physical characteristics of residential properties (Smith et al., 1995). However, the use of such models is limited by the scope of the data base used in its development and the complexity of the model itself. The use of traps to detect foci of cockroaches and the analysis of trap counts to determine cockroach abundance and distributional patterns can be helpful in assessing the extent of infestations and monitoring the effectiveness of control programs (Brenner and Pierce 1991).

Epidemiology of Vector-Borne Diseases

COMPONENTS OF TRANSMISSION CYCLES

The components of a transmission cycle of an arthropodborne disease are (1) a vertebrate host which develops a level of infection with the parasite that is infectious to a vector, (2) an arthropod host or vector that acquires the parasite from the infected host and is capable of transmission, and (3) one or more vertebrate hosts that are susceptible to infection with the parasite after being fed upon by the vector (Fig. 2.1). Vector-borne parasites have evolved

Components of the transmission cycle of an anthroponosis such as malaria or louse-borne typhus. (Original by Margo Duncan)

mechanisms for tolerating high constant body temperatures and evading the complex immune systems of the vertebrate hosts as well as for tolerating variable body temperatures and avoiding the very different defensive mechanisms of the arthropod vectors. Asexual parasites, such as viruses and bacteria, employ essentially the same life form to infect both vertebrate and arthropod hosts, whereas more highly evolved heterosexual parasites, such as protozoa and helminths, have different life stages in their vertebrate and arthropod hosts. Some asexual parasites, such as the plague bacillus, intermittently may bypass the arthropod host and be transmitted directly from one vertebrate host to another.

Among sexually reproducing parasites, the host in which gametocyte union occurs is called the definitive host, whereas the host in which asexual reproduction occurs is called the intermediate host. Vertebrates or arthropods can serve as either definitive or intermediate hosts, depending upon the life cycle of the parasite. For example, humans are the definitive host for the filarial worm, Wuchereria bancrofti, because adult male and female worms mate within the human lymphatic system, whereas the mosquito vector, Culex quinquefasciatus, is the intermediate host where development occurs without reproduction. In contrast, humans are the intermediate host of the Plasmodium protozoan that causes malaria, because only asexual reproduction occurs in the human host; gametocytes produced in the human host unite only in the gut of the definitive mosquito host.

A disease is the response of the host to infection with the parasite and can occur in either vertebrate or arthropod hosts. Immunity includes all properties of the host that confer resistance to infection and play an important role in determining host suitability and the extent of disease or illness. Some species or individuals within species populations have natural immunity and are refractory to infection. Natural immunity does not require that the host have previous contact with the parasite, but it may be age dependent. For example, humans do not become infected with avian malaria parasites, even though infective Culex mosquito vectors feed frequently on humans. Conversely, mosquitoes do not become infected with the measles or poliomyelitis viruses that infect humans, even though these viruses undoubtedly are ingested by mosquitoes blood feeding on viremic hosts.

Individuals within populations become infected with parasites, recover, and in the process actively acquire immunity. This acquired immunity to the parasite ranges from transient to lifelong and may provide partial to complete permanent protection. A partial immune response may permit continued infection but may reduce the severity of disease, whereas complete protection results in a cure and usually prevents immediate reinfection.

Acquired immunity may be humeral and result in the rapid formation of antibodies, or it may be cellular and result in the activation of T cells and macrophages. Antibodies consist of five classes of proteins called immunoglobulins that have specific functions in host immunity. Immunoglobulin G (IgG) is most common, comprising over 85% of the immunoglobulins present in the sera of normal individuals. The IgGs are relatively small proteins and typically develop to high concentrations several weeks after infection; they may persist at detectable and protective levels for years. In contrast, IgMs are large macroglobulins that appear shortly after infection but decay rapidly. For the laboratory diagnosis of many diseases, serum samples typically are tested during periods of acute illness and convalescence, 2 to 4 weeks later. A fourfold increase in parasite-specific IgG antibody concentration in these paired sera provides diagnostic serological evidence of infection. The presence of elevated concentrations of IgM presumptively implies current or recent infection. T cells and macrophages are several classes of cells that are responsible for the recognition and elimination of parasites. In long-lived vertebrate hosts, acquired immunity may decline over time, eventually allowing reinfection.

Clinically, the host response to infection ranges from inapparent or asymptomatic to mildly symptomatic to acute. Generally it is beneficial for the parasite if the host tolerates infection and permits parasite reproduction and/or development without becoming severely ill and dying before infecting additional vectors.

THE VERTEBRATE HOST

One or more primary vertebrate hosts are essential for the maintenance of parasite transmission, whereas secondary or incidental hosts are not essential to maintain transmission but may contribute to parasite amplification. Amplification refers to the general increase in the number of parasites present in a given area. An amplifying host increases the number of parasites and therefore the number of infected vectors. Amplifying hosts typically do not remain infected for long periods of time and may develop disease. A reservoir host supports parasite development, remains infected for long periods, and serves as a source of vector infection, but it usually does not develop acute disease.

Attributes of a primary vertebrate host include accessibility, susceptibility, and transmissibility.

Accessibility. The vertebrate host must be abundant and fed upon frequently by vectors. Host seasonality, diel activity, and habitat selection determine availability in time and space to host-seeking vectors. For example, the avian hosts of eastern equine encephalomyelitis (EEE) virus generally begin nesting in swamps coincidentally with the emergence of the first spring generation of the mosquito vector, Culiseta melanura, thereby bringing EEE virus, susceptible avian hosts, and mosquitoes together in time and space. Diel activity patterns also may be critical. For example, larvae (microfilariae) of W. bancrofti move to the peripheral circulatory system of the human host during specific hours of the night that coincide with the biting rhythm of the mosquito vector, Cx. quinquefasciatus. Historically, epidemics of vector-borne diseases have been associated with increases in human accessibility to vectors during wars, natural disasters, environmental changes, or human migrations.

Susceptibility. Once exposed, a primary host must be susceptible to infection and permit the development and reproduction of the parasite. Dead-end hosts either do not support a level of infection sufficient to infect vectors or become extremely ill and die before the parasite can complete development, enter the peripheral circulatory system or other tissues, and infect additional vectors. Ideal reservoir hosts permit parasites to survive in the peripheral circulatory system (or other suitable tissues) in sufficient numbers for sufficiently long time periods to be an effective source for vector infection. Asexual parasites, such as viruses and bacteria, typically produce intensive infections that produce large numbers of infectious organisms for relatively short periods during which the host either succumbs to infection or develops protective immunity. In the case of EEE virus, for example, 1 ml of blood from an infected bird may contain as many as 101~ virus particles during both day and night for a 2- to 5-day period; birds that survive such infections typically develop long-lasting, protective immunity. In contrast, highly evolved parasites produce comparatively few individuals during a longer period. W. bancrofti, for example, maintains comparatively few microfilaria in the bloodstream (usually < 10 microfilaria per cubic millimeter of blood), which circulate most abundantly in the peripheral blood during periods of the day when the mosquito vectors blood feed. However, because both the worms and the human host are long-lived, transmission is enhanced by repeated exposure rather than by an intense parasite presentation over a period of a few days. Infection with > 100 microfilaria per female mosquito may prove fatal for the vector; therefore, in this case, limiting the number of parasites that infect the vector may increase the probability of transmission.

Transmissibility. Suitable numbers of susceptible vertebrate hosts must be available to become infected and thereby maintain the parasite. Transmission rates typically decrease concurrently with a reduction in the number of susceptible (i.e., nonimmune) individuals remaining in the host population. The epidemic threshold refers to the number of susceptible individuals required for epidemic transmission to occur, whereas the endemic threshold refers to the number of susceptible individuals required for parasite persistence. These numerical thresholds vary depending on the immunology and dynamics of infection in the host population. Therefore, suitable hosts must be abundant and either not develop lasting immunity or have a relatively rapid reproductive rate, ensuring the rapid recruitment of susceptibles into the population. In the case of malaria, for example, the parasite elicits an immune response that rarely is completely protective, and the host remains susceptible to reinfection. In contrast, encephalitis virus infections of passerine birds typically produce lifelong protection, but bird life expectancy is short and the population replacement rate is rapid, ensuring the constant renewal of susceptible hosts.

THE ARTHROPOD VECTOR

Literally, a vectoris a “carrier” of a parasite from one host to another. An effective vector generally exhibits characteristics that complement those listed above for the vertebrate hosts and include host selection, infection, and transmission.

Host selection. A suitable vector must be abundant and feed frequently upon infective vertebrate hosts during periods when stages of the parasite are circulating in the peripheral blood or other tissues accessible to the vector. Host-seeking or biting activity during the wrong time or at the wrong place on the wrong host will reduce contact with infective hosts and reduce the efficiency of transmission. Patterns of host selection determine the types of parasites to which vectors are exposed. Anthropophagic vectors feed selectively on humans and are important in the transmission of human parasites. Anthropophagic vectors which readily enter houses to feed on humans or to rest on the interior surfaces are termed endophilic (literally, “inside loving”). Vectors which rarely enter houses are termed exophilic (i.e., “outside loving”). Zoophagic vectors feed primarily on vertebrates other than humans. Mammalophagic vectors blood feed primarily on mammals and are important in the maintenance of mammalian parasites. In contrast, ornithophagic vectors feed primarily on avian hosts and are important in the maintenance of avian parasites. There is a distinction between vectors attracted to a host and those which successfully blood feed on the host. Mammalophagic vectors therefore represent a subset of those mammalophilic vectors that are attracted to mammalian hosts.

Infection. The vector must be susceptible to infection and survive long enough for the parasite to complete multiplication and/or development. Not all arthropods that ingest parasites support parasite maturation, dissemination, and transmission. For example, the mosquito Cx. quinquefasciatus occasionally becomes infected with western equine encephalomyelitis (WEE) virus; however, because this virus rarely escapes the midgut, this species rarely transmits WEE virus. Some arthropods are susceptible to infection under laboratory conditions, but in nature they seldom feed on infected vertebrate hosts and/or survive long enough to allow parasite development. The transmission rate is the number of new infections per unit of time and is dependent upon the rate of parasite development to the infective stage and the frequency of blood feeding by the vector. Because many arthropod vectors are poildlothermic and contact their homeothermic vertebrate hosts intermittently, parasite transmission rates frequently are dependent upon ambient temperature. Therefore, transmission rates for many parasites are more rapid at tropical than at temperate latitudes, and at temperate latitudes they progress most rapidly during summer. The frequency of host contact and, therefore, the transmission rate also depend upon the life history of the vector. For example, epidemics of malaria in the tropics transmitted by a mosquito that feeds at 2-day intervals progress faster than epidemics of Lyme disease at temperate latitudes, where the spirochetes are transmitted to humans principally by the nymphal stage of a hard tick vector that may have one generation and one blood meal per life stage per year.

Transmission. Once infected, the vector must exhibit a high probability of refeeding on one or more susceptible hosts to ensure the transmission of the parasite. Diversion of vectors to nonsusceptible or dead-end hosts dampens transmission effectiveness. The term zooprophylaxis (literally, “animal protection”) arose to describe the diversion of Anopheles infected with human malaria parasites from humans to cattle, a dead-end host for the parasites. With zooprophylaxis the dead-end host typically exhibits natural immunity, in which host tissues are unacceptable to parasites and do not permit growth or reproduction. Alternatively, transmission to a dead-end host may result in serious illness, because the host-parasite relationship has not coevolved to the point of tolerance by the dead-end host. WEE virus, for example, can cause serious illness in humans, which are considered to be a dead-end host because they rarely produce a viremia sufficient to infect mosquitoes.

MODES OF TRANSMISSION

The transmission of parasites by vectors may be vertical or horizontal. Vertical transmission is the passage of parasites directly to subsequent life stages or generations within vector populations. Horizontal transmission describes the passage of parasites between vector and vertebrate hosts.

VERTICAL TRANSMISSION

Three types of vertical transmission are possible within vector populations: transstadial, transgenerational, and venereal transmission.

Transstadial transmission is the sequential passage of parasites acquired during one life stage or stadium through the molt to the next stage(s) or stadium. Transstadial transmission is essential for the survival of parasites transmitted by mites and hard ticks that blood feed once during each life stage and die after oviposition. Lyme disease spirochetes, for example, that are acquired by larval ticks must be passed transstadially to the nymphal stage before transmission to vertebrates.

Transgenerational transmission is defined as the vertical passage of parasites by an infected parent to its offspring. Some parasites may be maintained transgenerationally for multiple generations, whereas others require horizontal transmission for amplification. Transgenerational transmission normally occurs transovarially (through the ovary) after the parasites infect the ovarian germinal tissue. In this situation most of the progeny are infected. Other parasites do not actually infect the ovary and, although they are passed on to their progeny, transmission is not truly transovarial. This situation is usually less efficient and only a small percentage of the progeny are infected. Transgenerational transmission in vectors such as mosquitoes also must include transstadial transmission, because the immature life stages do not blood feed.

Venereal transmission is the passage of parasites between male and female vectors and is relatively rare. Venereal transmission usually is limited to transovarially infected males who infect females during insemination, which, in turn, infect their progeny during fertilization.

La Crosse virus (Fig. 2.2) is an example of a vertically maintained parasite where the arthropod host serves as the reservoir. This virus is maintained by transgenerational transmission within clones of infected Aedes triseriatus mosquitoes and is amplified by horizontal transmission among squirrels and chipmunks. Because this temperate mosquito rarely has more than two generations per year, La Crosse virus spends long periods in infected vectors and relatively short periods in infected vertebrate hosts. Females infected vertically or horizontally transmit their infection transovarially to first-instar larvae. These larvae transmit the virus transstadially through the four larval stadia and the pupal stage to the adults. These transgenerationally infected females then take a blood meal and oviposit infected eggs, often in the same tree hole from which they emerged. Some blood meal

Modes of transmission of a vertically maintained parasite, La Crosse encephalitis virus.

hosts become viremic and amplify the number of infected Ae. triseriatus females by horizontal transmission. Venereal transmission of the virus from transgenerationally infected males to uninfected females has been demonstrated in the laboratory and may serve to establish new clones of infected females in nature.

HORIZONTAL TRANSMISSION

Horizontal transmission is essential for the maintenance of almost all vector-borne parasites and is accomplished by either anterior (biting) or posterior (defecation) routes. Anterior-station transmission occurs when parasites are liberated from the mouthparts or salivary glands during blood feeding (e.g., malaria parasites, encephalitis viruses, filarial worms). Posterior-station (or stercorarian) transmission occurs when parasites remain within the gut and are transmitted via contaminated feces. The trypanosome that causes Chagas disease, for example, develops to the infective stage within the hindgut and is discharged onto the host skin when the triatomid vector defecates during feeding. Irritation resulting from salivary proteins introduced into the host during feeding causes the host to scratch the bite and rub the parasite into the wound. Louse-borne relapsing fever and typhus fever rickettsia also employ posterior-station modes of transmission.

There are four types of horizontal transmission, depending upon the role of the arthropod in the life cycle of the parasite: mechanical, multiplicative, developmental, and cyclodevelopmental.

Mechanical transmission occurs when the parasite is transmitted among vertebrate hosts without amplification or development within the vector, usually by contaminated mouthparts. Arthropods that are associated intimately with their vertebrate hosts and feed at frequent intervals have a greater probability of transmitting parasites mechanically. The role of the arthropod is essentially an extension of contact transmission between vertebrate hosts. Eye gnats, for example, have rasping, sponging mouthparts and feed repeatedly at the mucous membranes of a variety of vertebrate hosts, malting them an effective mechanical vector of the bacteria which cause conjunctivitis or “pink eye.” Mechanical transmission also may be accomplished by contaminated mouthparts if the vector is interrupted while blood feeding and then immediately refeeds on a second host in an attempt to complete the blood meal.

Multiplicative (or propagative) transmission occurs when the parasite multiplies asexually within the vector and is transmitted only after a suitable incubation period is completed. In this case, the parasite does not undergo metamorphosis and the form transmitted is indistinguishable from the form ingested with the blood meal. St. Louis encephalitis (SLE) virus, for example, is not transmitted until the virus replicates within and passes through the midgut, is disseminated throughout the hemocoel, and enters and replicates within the salivary glands. However, the form of the virus does not change throughout this process.

Developmental transmission occurs when the parasite develops and metamorphoses, but does not multiply, within the vector. Microfilariae of W. bancrofti, for example, are ingested with the blood meal, penetrate the mosquito gut, move to the flight muscles, where they molt twice, and then move to the mouthparts, where they remain until they are deposited during blood feeding. These filarial worms do not reproduce asexually within the mosquito vector; i.e., the number of worms available for transmission is always equal to or less than the number ingested.

Cyclodevelopmental transmission occurs when the parasite metamorphoses and reproduces asexually within the arthropod vector. In the life cycle of the malaria parasite, for example, gametocytes that are ingested with the blood meal unite within the mosquito gut and then change to an invasive form that penetrates the gut and forms an asexually reproducing stage on the outside of the gut wall. Following asexual reproduction, this stage ruptures and liberates infective forms that move to the salivary glands, from where they are transmitted during the next blood meal.

The extrinsic incubation period is the time interval between vector infection and parasite transmission when the parasite is away from the vertebrate host. The intrinsic incubation period is the time from infection to the onset of symptoms in the vertebrate host. Repeated lag periods of consistent duration between clusters of new cases at the onset of epidemics were first noticed by early epidemiologists who coined the term extrinsic incubation. These intervals actually represent the combined duration of extrinsic and intrinsic incubation periods.

The duration of the extrinsic incubation period is typically temperature dependent. The rate of parasite development normally increases as a linear degree-day function of ambient temperature between upper and lower thresholds. After being ingested by the mosquito vector, WEE virus, for example, must enter and multiply in cells of the midgut, escape the gut, be disseminated throughout the hemocoel, and then infect the salivary glands, after which the virus may be transmitted by bite. Under hot summer conditions, this process may be completed within 4 days, and the vector mosquito, Cx. tarsalis, is capable of transmitting the virus during the next blood meal. In contrast, under cooler spring conditions transmission may be delayed until the third blood meal. Some parasites may increase the frequency of vector blood feeding and thereby enhance transmission. The plague bacillus, for example, remains within and eventually blocks the gut of the most efficient flea vector, Xenopsylla cheopis. Regurgitation occurs during blood feeding, causing vector starvation and, therefore, transmission at progressively more closely spaced intervals before the vector succumbs to starvation.

TRANSMISSION CYCLES

Transmission cycles vary considerably depending upon their complexity and the role of humans as hosts for the parasite. A vector-borne anthroponosis is a disease resulting from a parasite that normally infects only humans and one or more anthropophagic vectors (Fig. 2.1). Malaria, some forms of filariasis, and louse-borne typhus are examples of anthroponoses with transmission cycles that involve humans and host-specific vectors. Humans serve as reservoir hosts for these parasites, which may persist for years as chronic infections. Vectors of anthroponoses selectively blood feed upon humans and are associated with domestic or peridomestic environments. Widespread transmission of an anthroponosis with an increase in the number of diagnosed human cases during a specified period of time is called an epidemic. When human cases reappear consistently in time and space, transmission is said to be endemic.

Zoonoses are diseases of animals that occasionally infect humans. Likewise, ornithonoses are diseases of wild birds that are transmitted occasionally to humans. In most vector-borne zoonoses, humans are not an essential component of the transmission cycle, but rather become infected when bitten by a vector that fed previously on an infected animal host. Although humans frequently become ill, they rarely circulate sufficient numbers of parasites to infect vectors and thus are termed dead-end hosts. The enzootic transmission cycle is the basic, or primary, animal cycle (literally “in animals”). When levels of enzootic transmission escalate, transmission may become epizootic (an outbreak of disease among animals). Transmission from the enzootic cycle to dead-end hosts is called tangential transmission (i.e., at a tangent from the basic transmission cycle). Often different vectors are responsible for enzootic, epizootic, and tangential transmission. Bridge vectors transmit parasites tangentially between different enzootic and dead-end host species. Human involvement in zoonoses may depend on the establishment of a secondary amplification cycle among vertebrate hosts inhabiting the peridomestic environment.

WEE virus is a zoonosis that exemplifies primary and secondary transmission cycles and tangential transmission to man and equines (Fig. 2.3). In California, WEE virus amplification occurs in a primary enzootic transmission cycle that consists of several species of passerine birds and Cx. tarsal# mosquitoes. In addition to birds, Cx. tarsalis blood feed on a variety of mammals, including rabbits. Rabbits, especially jackrabbits, develop sufficient viremia to infect some Cx. tarsalis and Ae. melanimon mosquitoes, thereby initiating a secondary zoonotic transmission cycle. WEE virus activity in the secondary Aedes-rabbit cycle usually has been detected after

Components of the transmission cycles of a zoonosis such as western equine encephalomyelitis (WEE) virus. (Original by Margo Duncan)

amplification in the primary Cx. tarsalis-bird cycle. Both Cx. tarsalis and Ae. melanimon transmit the virus tangentially to humans and equines, which are dead-end hosts for the virus.

INTERSEASONAL MAINTENANCE

An important aspect of the ecology of vector-borne parasites is the mechanism(s) by which they persist between transmission seasons or outbreaks. Parasite transmission typically is most efficient when weather conditions are suitable for vector activity and population growth. In temperate latitudes, overwintering of parasites becomes problematic when vertebrate or arthropod hosts either enter a winter dormancy or migrate. Similar problems face tropical parasites when transmission is interrupted by prolonged dry or wet seasons. The apparent seasonality that is characteristic of most vector-borne parasites may be due to either the periodic amplification of a constantly present parasite or to the consistent reintroduction of parasites following focal extinction.

Mechanisms of parasite maintenance during periods of unfavorable weather include the following:

Continued transmission by vectors. During periods of unfavorable weather, vectors may remain active and continue to transmit parasites, although transmission rates may be slowed by cold temperature or low vector abundance. In temperate latitudes with cold winters, transmission may continue at a slow rate, because the frequency of blood feeding and rate ofparasite maturation in the vector is diminished. In tropical latitudes, widespread transmission may be terminated during extended dry seasons that reduce vector abundance and survival. In both instances, transmission may be restricted spatially and involve only a small portion of the vertebrate host population. Human infections during adverse periods usually are highly clumped and may be restricted to members of the same household.

Infected vectors. Many vectors enter a state of dormancy as non-blood-feeding immatures or adults. Vertically infected vectors typically remain infected for life and therefore may maintain parasites during periods when horizontal transmission is interrupted. California encephalitis virus, for example, is maintained during winter and drought periods within the transovarially infected eggs of its vector, Ae. melanimon. Infected eggs of this floodwater mosquito may remain dormant and infected for up to several years and are able to withstand winter cold, summer heat, and extended dry periods. Inundation of eggs during spring or summer produces broods of adult mosquitoes that are infected at emergence. Similarly, vectors that inhabit the nests of migratory hosts such as cliff swallows often remain alive and infected for extended periods until their hosts return.

Infected vertebrate hosts. Parasite maintenance may be accomplished by infected reservoir hosts that either continue to produce stages infective for vectors or harbor inactive stages of the parasite and then relapse or recrudesce during the season when vectors are blood feeding. Adult filarial worms, for example, continue to produce microfilariae throughout their lifetime, regardless of the population dynamics or seasonality of the mosquito vector. In contrast, some Korean strains of vivax malaria overwinter as dormant stages in the liver of the human host and then relapse in spring, concurrent with the termination of diapause by the mosquito vector(s).

Alternatively, parasites may become regionally extinct during unfavorable weather periods and then are reintroduced from distant refugia. Two possible mechanisms may allow the reintroduction of parasites:

Migratory vertebrate hosts. Many bird species overwinter in the tropics and return to temperate or subarctic breeding sites each spring, potentially bringing with them infections acquired at tropical or southern latitudes. It also is possible that the stress of long flights and ensuing reproduction triggers relapses of chronic infections. In addition, many large herbivores migrate annually between summer (or wet) and winter (or dry) pastures, bringing with them an array of parasites. Rapid longrange human or commercial transportation is another possible mode for vector and parasite introduction. The seasonal transport of agricultural products and the movements of migratory agricultural workers may result in the appearance of seasonality.

Weather fronts. Infected vectors may be carried long distances by prevailing weather fronts. Consistent weather patterns, such as the sweep of the southeastern monsoon from the Indian Ocean across the Indian subcontinent, may passively transport infected vectors over hundreds of kilometers. The onset of WEE virus activity in the north central United States and Canada has been attributed to the dispersal of infected mosquitoes by storm fronts.

VECTOR INCRIMINATION

To understand the epidemiology of vector-borne disease, it is essential to establish which arthropod(s) is/are the primary vector(s) responsible for parasite transmission. Partial or incomplete vector incrimination has resulted in the misdirection of control efforts at arthropod species that do not play a substantial role in either enzootic maintenance or epidemic transmission. Vector incrimination combines field and laboratory data that measure field infection rates, vector competence, and vectorial capacity.

Infection rates. The collection of infected arthropods in nature is an important first step in identifying potential vectors, because it indicates that the candidate species feeds on vertebrate hosts carrying the parasite. Infection data may be expressed as a percentage at one point in time or an infection prevalence (i.e., number of vectors infected/number examined x 100). The more commonly employed infection rate refers to infection incidence and includes change over a specified time period. When the infection prevalence is low and arthropods are tested in groups or pools, data are referred to as a minimum infection rate (number of pools of vectors positive/ total specimens tested/unit of time x 100 or 1000). Minimum infection rates are relative values with ranges delineated by pool size. For example, minimum infection rates of vectors tested in pools consisting of 50 individuals each must range from 0 to 20 per 1000 females tested.

It is important to distinguish between infected hosts harboring a parasite and infective hosts capable of transmission. In developmental and cyclodevelopmental vectors, the infective stages may be distinguished by location in the vector, morphology, or biochemical properties. Distinguishing infective from noninfective vectors is difficult, if not impossible, with viral or bacterial infections, because the parasite form does not change. The ability to transmit may be implied by testing selected body parts, such as the cephalothorax, salivary glands, or head. With some tick pathogens, however, parasite movement to the mouthparts does not occur until several hours after attachment. As mentioned previously, the transmission rate is the number of new infections per time period. When standardized per unit of population size, the transmission rate may be expressed as an incidence. The annual parasite incidence is the number of new infections per year per 1000 population.

The entomological inoculation rate is the number of potentially infective bites per unit of time. This frequently is determined from the human or host biting rate and the proportion of vectors that are infective and is calculated as bites per human per time period x infectivity prevalence.

Vector competence is defined as the susceptibility of an arthropod species to infection with a parasite and its ability to transmit this acquired infection. Vector competence is determined quantitatively by feeding the candidate arthropod vector on a vertebrate host circulating the infective stage of the parasite, incubating the bloodfed arthropod under suitable ambient conditions, refeeding the arthropod on a noninfected susceptible vertebrate host, and then examining this host to determine if it became infected. Because it often is difficult to maintain natural vertebrate hosts in the laboratory and control the concentration of parasites in the peripheral circulatory system, laboratory hosts or artificial feeding systems frequently are used to expose the vector to the parasites. Susceptibility to infection may be expressed as the percentage of arthropods that became infected among those blood feeding. When the arthropod is fed on a range of parasite concentrations, susceptibility may be expressed as the median infectious dose required to infect 50% of blood-fed arthropods. The ability to transmit may be expressed either as the percentage of feeding females that transmitted or the percentage of hosts that became infected.

Failure of a blood-fed arthropod to become infected with or transmit a parasite may be attributed to the presence of one or more barriers to infection. For parasites transmitted by bite, the arthropod midgut provides the most important barrier. Often parasites will grow in a nonvector species if they are inoculated into the hemocoel, thereby by-passing this gut barrier. After penetrating and escaping from the midgut, the parasite then must multiply and/or mature and be disseminated to the salivary glands or mouthparts. Arthropod cellular or humeral immunity may clear the infection at this point, creating a dissemination barrier. Even after dissemination to the salivary glands, the parasite may not be able to infect or be transmitted from the salivary glands due to the presence of salivary gland infection or salivary gland escape barriers, respectively.

For parasites transmitted at the posterior station, vector competence may be expressed as the percentage of infected vectors passing infective stages of the parasite in their feces.

The concept of vectorial capacity summarizes quantitatively the basic ecological attributes of the vector relative to parasite transmission. Although developed for mosquito vectors of malaria parasites and most easily applied to anthroponoses, the model provides a framework to conceptualize how the ecological components of the transmission cycle of many vector-borne parasites interact.

Vectorial capacity is expressed by the formula:

C= ma2(pn)/(-lnP),

where C is the vectorial capacity as new infections per infection per day, ma is the bites per human per day, a is the human biting habit, P is the probability of daily survival, and n is the extrinsic incubation period (in days).

The biting rate (ma) frequently is estimated by collecting vectors as they attempt to blood feed and is expressed as bites per human per day or night (e.g., 10 mosquitoes per human per night). The human biting habit (a) combines vector feeding frequency and host selection. The feeding frequency is the length of time between blood meals and frequently is expressed as the inverse of the length of the gonotrophic cycle. Host selection patterns are determined by testing blood-fed vectors to determine what percentage fed on humans or the primary reservoir. Therefore, if the blood feeding frequency is 2 days and if 50% of host-seeking vectors feed on humans, a = (1/2 days) x (0.5) = 0.25. In this example, ma 2 = 10 bites/human/night x 0.25 = 2.5; a is repeated because infected vectors must refeed to transmit.

The probability of the vector surviving through the extrinsic incubation period of the parasite, pn, requires information on the probability of vector survival (P) and the duration of the extrinsic incubation period (n). P is estimated either vertically, by age-grading the vector population, or horizontally, by marking cohorts and monitoring their death rate over time. In Diptera, P may be estimated vertically from the parity rate (proportion of parous females per number examined). In practice, P = (parity rate) 1/~, where g is the length of the gonotrophic cycle. The extrinsic incubation period may be estimated from ambient temperature from data gathered during vector competence experiments by testing the time from infection to transmission for infected vectors incubated at different temperatures. Continuing our example, if P = 0.8 and n = 10 days, then the duration of infective life is Pn/(-lnP) = 0.81~ x 0.8) = 0.48. Therefore C = 2.5 x 0.48, or 1.2 parasite transmissions per infective host per day.

SURVEILLANCE

The number of cases of most vector-borne diseases typically varies over both time and space. Information on the number of cases can be gathered from morbidity and mortality records maintained by state or national governmental agencies for the human population. Morbidity data are records of illness, whereas mortality data are records of the cause of death. These data vary greatly in their quality and timeliness, depending upon the accuracy of determining the cause of illness or death and the rapidity of reporting. In the United States, the occurrence of confirmed cases of many vector-borne diseases, including yellow fever, plague, malaria, and encephalitis, must by law be reported to municipal health authorities. However, infections with many arthropod-borne parasites, including Lyme disease and the mosquito-borne encephalitides, frequently are asymptomatic or present variable clinical symptoms and therefore remain largely undiagnosed and underreported. The frequency of case detection and accuracy of reporting systems are dependent on the type of surveillance employed and the ability of the medical or veterinary community to recognize suggestive symptoms and request appropriate confirmatory laboratory tests. In addition, some laboratory tests vary in their specificity and sensitivity, thus complicating the interpretation of laboratory results. Cases may be classified as suspect or presumptive, based on the physician’s clinical diagnosis, or confirmed, based on a diagnostic rise in specific antibodies or the direct observation (or isolation) of the parasite from the case. Surveillance for clinical cases may be active or passive.

Active surveillance involves active case detection in which health workers visit communities and seek out and test suspect cases. In malaria control programs, for example, a field worker visits every household biweekly or monthly and collects blood films from all persons with a current or recent fever. Fever patients are treated with antimalarial drugs presumptively, and these suspected cases are confirmed by detection of malaria parasites in a blood smear. Confirmed cases are revisited and additional medication administered, if necessary. This surveillance provides population infection rates regardless of case classification criteria.

Most surveillance programs rely on passive surveillance, which utilizes passive case detection to identify clinical human or veterinary cases. In this system, individuals seeking medical attention at primary health care organizations, such as physicians’ offices, hospitals, and clinics, are diagnosed by an attending physician who requests appropriate confirmatory laboratory tests. However, because many arthropod-borne diseases present a variety of nonspecific symptoms (e.g., headache, fever, general malaise, arthralgia), cases frequently may be missed or not specifically diagnosed. In mosquito-borne viral infections the patient often spontaneously recovers, and cases frequently are listed under fevers of unknown origin or aseptic (or viral) meningitis without a specific diagnosis. In a passive case-detection system, it is the responsibility of the attending physician to request laboratory confirmation of suspect clinical cases and then to notify the regional public health epidemiologist that a case of a vector-borne disease has been documented.

The reporting system for clinical cases of vector-borne diseases must be evaluated carefully when interpreting surveillance data. This evaluation should take into account the disease, its frequency of producing clinically recognizable symptoms, the sensitivity and specificity of confirmatory laboratory tests, and the type and extent of the reporting system. Usually programs that focus on the surveillance of a specific disease and employ active case detection provide the most reliable epidemiological information. In contrast, broad-based community health care systems that rely on passive case detection typically produce the least reliable information, especially for relatively rare vector-borne diseases with nonspecific symptoms.

Diseases that are always present or reappear consistently at a similar level during a specific transmission season are classified as endemic. The number of cases in a population is expressed as incidence or prevalence. Population is defined as the number of individuals at risk from infection in a given geographical area at a given time. Incidence is the number of new cases per unit of population per unit of time. Incidence data are derived from two or more successive samples spaced over time. Prevalence is the frequency of both old and new infections among members of a population. Prevalence typically is determined by a single point in time estimate and frequently is expressed as the percentage of the population tested that was found to have been infected.

The level of parasite endemicity in a population may be graded as hypoendemic (low), mesoendemic (medium), or hyperendemic (high), depending upon the incidence of infection and/or the immune status of the population. In malaria surveys, for example, the percentage of children with palpable spleens and the annual parasite incidence are used to characterize the level of endemicity. In endemic disease, the percentage of individuals with sera positive for IgG-class antibodies typically increases as a linear function of age or residence history, whereas in hypoendemic disease with intermittent transmission, this function is disjunct, with certain age groups expressing elevated positivity rates. The occurrence of an extraordinarily large number of human infections or cases is termed an epidemic. Health agencies, such as the World Health Organization, typically monitor incidence data to establish criteria necessary to classify the level of endemicity and to decide when an epidemic is under way. A geographically widespread epidemic on a continental scale is called a pandemic.

Serological surveys(or serosurveys) are a useful epidemiological tool for determining the cumulative infection experience of a population with one or more parasiteand host-related factors affecting the efficiency or risk of transmission, and reinfection rates. When coupled with morbidity data, serosurveys provide information on the ratio of apparent to inapparent infections. Random sampling during serosurveys representatively collects data on the entire population and may provide ecological information retrospectively by analysis of data collected concurrently with each serum sample. This information may assign risk factors for infection, such as sex, occupation, and residence history, or it may help in ascertaining age-related differences in susceptibility to disease. Stratified sampling is not random and targets a specific cohort or subpopulation. Although stratified samples may have greater sensitivity in detecting rare or contiguously distributed parasites, the data are not readily extrapolated to infection or disease trends in the entire population. Repeated serological testing of the same individuals within a population can determine the time and place of infection by determining when individuals first become seropositive, i.e., serologically positive with circulating antibodies against a specific parasite. This change from seronegative to seropositive is called a seroconversion.

Forecasting the risk of human infection usually is accomplished by monitoring environmental factors, vector abundance, the level of transmission within the primary and/or amplification cycles, and the numbers of human or domestic animal cases. As a general rule, the accuracy of forecasting is related inversely to the time and distance of the predictive parameter from the detection of human cases. Surveillance activities typically include the time series monitoring of environmental conditions, vector abundance, enzootic transmission rates, and clinical cases.

Environmental conditions. Unusually wet or warm weather may indicate favorable conditions for vector activity or population increases, concurrently increasing the risk of parasite transmission. Parameters frequently monitored include temperature, rainfall, snow pack (predictive of vernal flooding), and agricultural irrigation schedules.

Vector abundance. Standardized sampling at fixed sites and time intervals can be used to compare temporal and spatial changes in vector abundance that are useful in detecting an increased risk of parasite transmission. Extraordinary increases in vector abundance and survival may forecast accurately increased enzootic transmission and, to a lesser extent, epidemics.

Enzootic transmission rates. Monitoring the level of parasite infection in vector or vertebrate populations provides direct evidence that the parasite is present and being actively transmitted (Fig. 2.4). The level of transmission usually is directly predictive of the risk of human or domestic animal involvement. Enzootic transmission activity may be monitored by vector infection rates, vertebrate-host infection rates, sentinel seroconversion rates, and clinical cases.

Vector infection rates. Sampling vectors and testing them for parasites determines the level of infection in the vector population (Fig. 2.4, C and D). When vectors are tested individually, prevalence data are expressed as percentages; e.g., 10 females infected per 50 tested is a 20% infection rate. When combined with abundance estimates, infection rates also may be expressed as infected vectors per sampling unit per time interval; 100 bites per human per night x 0.2 infection rate – 20 infective bites per human per night. These data provide an index of the transmission rate. When infection rates are low and vector populations large, vectors usually are tested in lots or pools. It is statistically advantageous to keep the pool size constant and thus keep the chance of detecting

Mosquito-borne encephalitis surveillance in southern California. (A) Coop with 10 sentinel chickens; (B) Taking blood sample from chicken; (C) Hanging mosquito trap on permanent standard (components from left to right are trap motor and fan assembly with collecting carton, dry-ice bait in a Styrofoam container, and battery); (D) Sorting mosquito collections by species to estimate relative abundance.

infection the same. Because there may be more than one infected vector per pool, infection rates are expressed as a minimum infection rate = positive pools/total individuals tested x 100 or 1000.

Vertebrate-host infection rates. Introduced zoonoses, such as sylvatic plague in North American rodents, frequently produce elevated mortality that may be used to monitor epizootics of these parasites over time and space. In contrast, endemic zoonoses rarely result in vertebrate host mortality. Testing reservoir or amplifying hosts for infection is necessary to monitor the level of enzootic parasite transmission. Stratified sampling for these parasites (directly by parasite isolation or indirectly by seroprevalence) usually focuses on the young of the year to determine ongoing transmission. For example, examining nestling birds for viremia can provide information on the level of enzootic encephalitis virus transmission.

Monitoring the incidence of newly infected individuals in a population over time is necessary to detect increased transmission activity. Because many parasites are difficult to detect or are present only for a limited time period, sampling frequently emphasizes the monitoring of seropositivity. Monitoring the IgM antibody, which rises rapidly after infection and decays relatively quickly, can indicate the level of recent infection, whereas monitoring the IgG antibody documents the population’s historical experience with the parasite. Sampling, marldng, releasing, recapturing, and resampling wild animals is most useful in providing information on the time and place of infection in free-roaming animal populations.

Sentinel seroconversion rates. Sentinels typically are animals that can be monitored over time to quantify the prevalence of a parasite. Trapping wild animals or birds is labor intensive, and determining seroprevalence may provide little information on the time and place of infection, especially if the host has a large home range. To circumvent this problem, caged or tethered natural hosts or suitable domestic animals of known infection history are placed in sensitive habitat and repeatedly bled to detect infection. A suitable sentinel should be fed upon frequently by the primary vector species, be easy to diagnose when infected, be unable to infect additional vectors (i.e., not serve as an amplifying host), not succumb to infection, and be inexpensive to maintain and easy to bleed or otherwise sample for infection. Chickens, for example, are useful sentinels in mosquito-borne encephalitis virus surveillance programs (Fig. 2.4, A and B). Flocks of seronegative chickens are placed at farmhouses and then bled weekly or biweeldy to determine seroconversions to viruses such as WEE or SLE. Because the chickens are confined and the date of seroconversion known, the time and place of infection is determined, while the number seroconverting estimates the intensity of transmission.

Clinical cases. Detecting infection among domestic animals may be an important indication that an epizootic transmission is under way and that the risk of human infection has become elevated. Domestic animals often are more exposed to vectors than are humans and thus provide a more sensitive indication of parasite transmission. Clinical human cases in rural areas in close association with primary transmission cycles may be predictive of future epidemic transmission in urban settings.

Vector-borne diseases frequently affect only a small percentage of the human population, and therefore vector control remains the intervention method of choice. Control programs attempt to maintain vector abundance below thresholds necessary for the transmission of parasites to humans or domestic animals. When these programs fail, personal protection by repellents or insecticideimpregnated clothing, bed nets, or curtains is often the only recourse. Vaccination may be a viable alternative method of control for specific vector-borne diseases, if the vaccine imparts lasting immunity as in the case of yellow fever virus. However, many parasites, such as malaria, have evolved to the point where infection elicits a weak immune response that provides only shortterm and marginal protection. The need for continued revaccination at short intervals severely limits their global usefulness, especially in developing countries. Although breakthroughs in chemotherapy have been useful in case management, it remains the mandate of the medical/ veterinary entomologist to devise strategies which combine epidemiological and ecological information to effectively reduce or eliminate the risk of vector-borne diseases.

Medical Entomology

GENERAL ENTOMOLOGY

Basic concepts of entomology, such as morphology, taxonomy and systematics, developmental biology, and ecology, provide important background information for medical and veterinary entomologists. General entomology books which the reader will find helpful in this regard include Borror et al. (1989), Gullan and Cranston (1994), Oillot (1995), Elzinga (1997), Chapman (1998), and Romoser and Stoffolano (1998). References that provide a more taxonomic or biodiversity-oriented approach to general entomology include works by Arnett (1993), Richards and Davies (1994), Bosik (1997), and Daly et al. (1998). General insect morphology is detailed in Snodgrass (1993), whereas a useful glossary of general entomology is Torre-Bueno (1962). Texts on urban entomology, the study of insect pests in houses, buildings, and urban areas, which also has relevance to medical-veterinary entomology, have been prepared by Ebeling (1975), Hickin (1985), MaUis (1997), and Robinson (1996). General texts on acarology include works by Krantz (1978), Woolley (1987), Evans (1992) and Walter and Proctor (1999).

MEDICAL-VETERINARY ENTOMOLOGY LITERATURE

Textbooks or monographs pertaining to medical entomology, veterinary entomology, or the combined discipline of medical-veterinary entomology are listed under these headings at the end of this chapter. Most of these publications emphasize arthropod morphology, biology, systematics, and disease relationships, whereas some of the more recent texts, such as Beaty and Marquardt (1996) and Crampton et al. (1997), emphasize molecular aspects of medical-veterinary entomology. Other works are helpful regarding common names of arthropods of medicalveterinary importance (Pittaway 1992), surveillance techniques (Bram 1978), control measures (Drummond et al. 1988), or ectoparasites (Andrews 1977, Marshall 1981, Kim 1985, Uilenberg 1994, Barnard and Durden 1999). Publications that devote substantial sections to arthropods associated with wildlife and the pathogens they transmit include Davis and Anderson (1971), Davidson et al. (1981), Fowler (1986) and Davidson and Nettles (1997).

Several journals and periodicals are devoted primarily to medical and/or veterinary entomology. These include the Journal of Medical Entomology, published by the Entomological Society of America (Lanham, MD); Medical and Veterinary Entomology, published by the Royal Entomological Society of London (UK); Journal of Vector Ecology, published by the Society of Vector Ecologists (Corona, CA); Vector Borne and Zoonotic Diseases, published by Mary Ann Liebert, Inc., Larchmont, New York; and Review of Medical and Veterinary Entomology, published by CAB International (Wallingford, UK). Journals specializing in parasitology, tropical medicine, or wildlife diseases that also include articles on medical-veterinary entomology include Parasitology, published by the British Society for Parasitology; Journal of Parasitology, published by the American Society of Parasitologists (Lawrence, KS); Parasite-Journal de la Societe Franfaise de Parasitologie, published by PRINCEPS Editions (Paris, France); Advances in Disease Vector Research, published by Springer-Verlag (New York); Bulletin of the World Health Organization, published by the World Health Organization (Geneva, Switzerland); Journal of Wildlife Diseases, published by the Wildlife Disease Association (Lawrence, KS); Emerging Infectious Diseases, published by the Centers for Disease Control and Prevention (Atlanta, GA); the American Journal of Tropical Medicine and Hygiene, published by the American Society of Tropical Medicine and Hygiene (Northbrook, IL); and Memorias Do Instituto Oswaldo Cruz; published by the Instituto Oswaldo Cruz (Rio de Janeiro, Brazil). Various Internet Web sites pertaining to medical-veterinary entomology can also be accessed for useful information.

HISTORY OF MEDICALVETERINARY ENTOMOLOGY

Problems caused by biting and annoying arthropods and the pathogens they transmit have been the subject of writers since antiquity (Service 1978). Homer (mid-8th century BC), Aristophanes (ca. 448-380 BC), Aristotle (384-322 BC), Plautus (ca. 254-184 BC), Columella (5 BC to AD 65), and Pliny (AD 23-79) all wrote about the nuisance caused by flies, mosquitoes, lice, and/or bedbugs. However, the study of modern medicalveterinary entomology is usually recognized as beginning in the late 19th century, when blood-sucking arthropods were first proven to be vectors of human and animal pathogens.

Englishman Patrick Manson ( 1844-1922 ) was the first to demonstrate pathogen transmission by a blood-feeding arthropod. Working in China in 1877, he showed that the mosquito Culex pipiensfatigans is a vector of Wuchereria bancrofti, the causative agent of Bancroftian filariasis. Following this landmark discovery, the role of various blood-feeding arthropods in transmitting pathogens was recognized in relatively rapid succession.

In 1891, Americans Theobald Smith (1859-1934) and F. L. Kilbourne (1858-1936) implicated the cattle tick, Boophilus annulatus, as a vector of Babesia bigemina, the causative agent of Texas cattle fever (bovine babesiosis/piroplasmosis). This paved the way for a highly successful B. annulatus-eradication program in the United States directed by the US Department of Agriculture. The eradication of this tick resulted in the projected goal: the elimination of indigenous cases of Texas cattle fever throughout the southern United States.

In 1898, Englishman Sir Ronald Ross (1857-1932), working in India, demonstrated the role of mosquitoes as vectors of avian malarial parasites from diseased to healthy sparrows. Also in 1898, the cyclical development of malarial parasites in anopheline mosquitoes was described by Italian Giovani Grassi (1854-1925). In the same year, Frenchman Paul Louis Simond (1858-1947), working in Pakistan (then part of India), showed that fleas are vectors of the bacterium that causes plague.

In 1848, American physician Josiah Nott (1804- 1873) of Mobile, AL, had published circumstantial evidence that led him to believe that mosquitoes were involved in the transmission of yellow fever virus to humans. In 1881, Cuban-born Scottish physician Carlos Finlay (1833-1915) presented persuasive evidence for his theory that what we know today as the mosquito Aedes aegypti was the vector of this virus. However, it was not until 1900 that American Walter Reed (1851-1902) led the US Yellow Fever Commission at Havanna, Cuba, which proved A. aegypti to be the principal vector of yellow fever virus.

In 1903, Englishman David Bruce (1855-1931) demonstrated the ability of the tsetse fly Glossina palpalis to transmit, during blood-feeding, the trypanosomes that cause African trypanosomiasis.

Other important discoveries continued well into the 20th century. In 1906, American Howard Taylor Ricketts (1871-1910) proved that the Rocky Mountain wood tick, Dermacentor andersoni, is a vector of Rickettsia rickettsii, the causative agent of Rocky Mountain spotted fever. In 1907, F. P. Mackie (1875-1944) showed that human body lice are vectors of Borrelia recurrentis, the spirochete that causes louse-borne (epidemic) relapsing fever. In 1908, Brazilian Carlos Chagas (1879-1934) demonstrated transmission of the agent that causes American trypanosomiasis, later named Chagas disease in his honor, by the cone-nose bug Panstrongylus megistus.

In 1909, Frenchman Charles Nicolle (1866-1936), working in Tunis, showed that human body lice are vectors of Rickettsia prowazekii, the agent of louse-borne (epidemic) typhus.

These important discoveries, as well as others of historical relevance to medical-veterinary entomology, are discussed in more detail in the references listed at the end of this chapter. Because of the chronology of many major discoveries relevant to this topic in the 50-year period starting in 1877, this time has been called the “golden age of medical-veterinary entomology” (Philip and Rozeboom 1973).

IDENTIFICATION AND ….. SYSTEMATICS OF ARTHROPODS OF MEDICAL-VETERINARY IMPORTANCE

Table I provides a list of the eight orders of insects and four orders of arachnids that are of particular interest to medical-veterinary entomologists. Accurate identification of these arthropods is an important first step in determining the types of problems they can cause and, subsequently, in implementing control programs.

Although taxonomy and identification are discussed in more detail with respect to arthropod groups treated in the chapters that follow, some publications provide a broader perspective on the classification, taxonomy,

Principle Orders of Insects and Arachnids of Medical-Veterinary Interest

and/or identification of a range of arthropods of medical-veterinary importance. These include two works published by the US Centers for Disease Control and Prevention (1979, 1994), as well as citations by Service (1988), Hopla et al. (1994), Lago and Goddard (1994), and Davis (1995). Mso, some medical-veterinary entomology books are very taxonomically oriented, with emphasis on identification, e.g., Baker et al. (1956), Smith (1973), Lane and Crosskey (1993), Walker (1995) and Baker (1999).

TYPES OF PROBLEMS CAUSED BY ARTHROPODS

ANNOYANCE

Irrespective of their role as blood-feeders (hematophages), parasites, or vectors of pathogens, certain arthropods cause severe annoyance to humans or other animals because of their biting behavior. These include lice, bedbugs, fleas, deer flies, horse flies, tsetse flies, stable flies, mosquitoes, black flies, biting midges, sand flies, chiggers, and ticks. Some, however, do not bite but instead are annoying because of their abundance, small size, or habit of flying into or around the eyes, ears, and nose. Nonbiting arthropods that cause annoyance include the house fl); chironomid midges, and eye gnats. Large populations of household or filth-associated arthropods, such as houseflies and cockroaches, can also be annoying. Nuisance arthropods are commonly problems for humans at outdoor recreational areas, including parks, lakes, and beaches.

ENVENOMATION

Members of several groups of arthropods can inject venom when they bite or sting. Most notable are bees, wasps, ants, spiders, and scorpions. Others, such as blister beetles and certain caterpillars, produce toxins that can cause problems when they are touched or ingested. Envenomation by these arthropods is discussed in more detail in the respective chapters that follow.

In general, envenomation results in medical or veterinary conditions ranging from mild itching to intense debilitating pain or even to life-threatening encounters due to allergic reactions. Envenomation sites on the skin usually appear as reddened, painful, more or less circular lesions surrounding the bite, sting, or point of venom contact. These areas may become raised and can persist for several days, often causing inflammation of adjacent tissues. Caterpillars that cause envenomation typically secrete toxins from specialized setae that penetrate the skin, causing contact dermatitis. Blisters can also develop at arthropod envenomation sites on contact of the skin with blister beetles (family Meloidae), false blister beetles (family Oedemeridae), and certain rove beetles (family Staphylinidae) which secrete toxins in their body fluids. If meloid beetles are accidentally ingested with fodder by livestock, the resulting systemic reaction can be life threatening.

ALLERGIC REACTIONS

A relatively wide spectrum of allergic reactions can occur in humans or animals exposed to certain arthropods. Many of the species involved also cause envenomation by biting or stinging, with the allergic reaction resulting from an overresponsive host immune system. Bites or stings from arthropods such as lice, bedbugs, fleas, bees, ants, wasps, mosquitoes, and chiggers all can result in allergic host reactions. Contact allergies can occur when certain beetles or caterpillars touch the skin. Respiratory allergies can result from inhaling allergenic air-borne particles from cockroaches, fleas, or other arthropods. The recirculation of air by modern air-handling systems in buildings tends to exacerbate inhalation of insect allergens.

Humans and animals usually react to repeated exposure to bites or stings from the same or antigenically related arthropods in two possible ways, depending on the nature of the antigen or venom inoculated and the sensitivity of the host: (1) desensitization to the bites or stings with repeated exposure and (2) allergic reactions which, in extreme cases, can develop into life-threatening anaphylactic shock. However, a distinct five-stage sequence of reactions typically occurs in most humans when they are repeatedly bitten or stung by the same, or related, species of arthropod over time. Stage 1 involves no skin reaction but leads to development of hypersensitivity. Stage 2 is a delayed-hypersensitivity reaction. Stage 3 is an immediate-sensitivity reaction followed by a delayedhypersensitivity reaction. Stage 4 is immediate reaction only, whereas Stage 5 again involves no reaction (i.e., the victim becomes desensitized). These changes reflect the changing host immune response to prolonged and frequent exposure to the same arthropod or to cross-reactive allergens or venoms.

INVASION OF HOST TISSUES

Some arthropods invade the body tissues of their host. Various degrees of invasion occur, ranging from subcutaneous infestations to invasion of organs such as the lungs and intestine. Invasion of tissues allows arthropods to exploit different host niches and usually involves the immature stages of parasitic arthropods.

The invasion of host tissues by fly larvae, called myiasis, is the most widespread form of host invasion by arthropods. Larvae of many myiasis-causing flies move extensively through the host tissues. As they mature, they select characteristic host sites (e.g., stomach, throat, nasal passages, or various subdermal sites) in which to complete the parasitic phase of their development.

Certain mites also invade the sldn or associated hair follicles and dermal glands. Others infest nasal passages, lungs, and air sacs or stomach, intestines, and other parts of the alimentary tract of their hosts. Examples include scabies mites, follicle mites, nasal mites, lung mites, and a variety of other mites that infest both domestic and wild birds and mammals.

ARTHROPOD-BORNE DISEASES

Table II lists the principle groups of insects and arachnids involved in arthropod-borne diseases and the associated types of pathogens. Among the wide variety ofarthropods that transmit pathogens to humans and other animals, mosquitoes are the most important, followed by ticks. Viruses and bacteria (including rickettsiae) are the most diverse groups of pathogens transmitted by arthropods, followed by protozoa and filarial nematodes.

All of the viruses listed in Table II are arthropodborne viruses, usually referred to as arboviruses, indicating that they are typically transmitted by insects or other arthropod hosts. The study of arboviruses is termed arbovirology.

Pathogens are transmitted by arthropods in two basic ways, either biologically or mechanically. In biological transmission, pathogens undergo development or reproduction in the arthropod host. Examples of diseases that involve biological transmission are malaria, African trypanosomiasis, Chagas disease, leishmaniasis, and lymphatic filariasis. In mechanical transmission, pathogens are transmitted by arthropods via contaminated appendages (usually mouthparts) or regurgitation of an infectious blood meal. Examples of diseases that involve mechanical transmission are equine infectious anemia and myxomatosis. Biological transmission is by far the more common and efficient mechanism for pathogen maintenance and transmission.

A wide range of life-cycle patterns and degrees of host associations is characterized by arthropod vectors. Some ectoparasites, such as sucldng lice, remain on their host for life. Others, such as mosquitoes and most biting flies, have a more fleeting association with the host, with some being associated with it only during the brief acts of host

Examples of Arthropod-Borne Diseases of Medical-Veterinary Importance

location and blood-fEeding. Between these two extremes is a wide range of host associations exhibited by different arthropod groups.

FOOD CONTAMINANTS

Many arthropods can contaminate or spoil food materials. In addition to causing direct damage to food resources, arthropods or their parts (e.g., setae, scales, shed cuticles, or body fragments) may be accidentally ingested. This can lead to toxic or allergic reactions, gastrointestinal myiasis, and other disorders.

Insects such as the house fly may alight on food and regurgitate pathogen-contaminated fluids prior to, or during, feeding. While feeding they also may defecate, contaminating the food with potential pathogens. Because the alimentary tract of arthropods may harbor pathogenic microorganisms, subsequent consumption of the contaminated food can lead to the transmission of these pathogens to humans or other animals. Similarly, the integument of household pests such as flies and cockroaches (particularly their legs and tarsi) can serve as a contact source of pathogens which may be readily transferred to food items. Some of these arthropods previously may have visited fecal matter, garbage heaps, animal secretions, or other potential sources of pathogens, thereby further contributing to health risks.

Additional information on insects and other arthropods that can contaminate food is provided by Olsen et al. (1996) and in reviews by Terbush (1972), Hughes (1976), and Gorham (1975, 1991a,b).

FEAR OF ARTHROPODS

Some people detest arthropods, or infestation by them, to such a degree that they suffer from entomophobia, the fear of insects; arachnophobia, the fear of spiders and other arachnids; or acarophobia, the fear of mites (including ticks). Showing concern or disapproval towards the presence of potentially injurious arthropods is probably a prudent and healthy reaction, but phobic behaviors reflect an unusually severe psychological response. Such persons exhibit more-than-normal fear when they encounter an arthropod, often resorting to excessive or obsessive measures to control the problem (e.g., overtreatment of themselves or their homes with insecticides and other chemical compounds).

DELUSORY PARASITOSIS

A relatively common psychological state occurs in which an individual mistakenly believes that he or she is being bitten by, or infested with, parasites. This is called delusory parasitosis, also referred to as delusionalparasitosis or delusions ofparasitosis. This condition is distinct from simply a fear, or phobia, of insects or other arthropods and represents a more deeply rooted psychological problem. This delusory condition is most frequently experienced by middle-aged or elderly persons, particularly women, and is one of the most difficult situations for entomologists to approach.

Remarkable behavioral traits are sometimes attributed to the parasites by victims. These include descriptions of tiny animals jumping into the eyes when a room is entered or when a lamp is switched on. Some victims have failing eyesight; others may have real symptoms from other conditions such as psoriasis that they may attribute to the imagined parasites. Victims become convinced that the parasites are real, and they often consult a succession of physicians in a futile attempt to secure a diagnosis and satisfactory treatment to resolve the problem. Patients typically produce skin scrapings or samples of such materials as vacuumed debris from carpets, draperies, and window sills, which they believe contain the illusive parasites.

Victims of delusory parasitosis often turn to extension entomologists or medical entomologists as a last resort out of frustration with being unable to resolve their condition through family physicians, allergists, and other medical specialists. Because patients are convinced that arthropods are present, they are usually reluctant to seek counseling or other psychiatric help. Dealing with cases of delusory parasitosis requires careful examination of submitted specimens, tact, and professional discretion on the part of the entomologist. Additional information on delusory parasitosis is provided by Driscoll et al. (1993), Koblenzer (1993), Kushon et al. (1993), Poorbaugh (1993), Webb (1993a,b), Goddard (1995), and Hinkle (2000).

TOXINS AND VENOMS

Many arthropods of medical-veterinary importance produce toxins. Notable among these are scorpions, spiders, bees, wasps, ants, and velvet ants; certain beetles (e.g., blister beetles, some rove beetles, and darkling beetles); and caterpillars, cocoons, and adults of various moths. Additionally, antigenic components in saliva released during blood-feeding by arthropods (e.g., certain fleas, ticks, mosquitoes, and chiggers) cause local or systemic reactions in their hosts.

Toxins produced by arthropods represent a wide range of chemical substances from simple inorganic or organic compounds to complex alkaloids and heterocyclic compounds. The term venom refers to toxins that are injected into animal tissues via specialized structures such as stings, chelicerae (fangs), and spines. Venoms are often complex mixtures of toxins and various pharmacologically active compounds that facilitate the spread and effectiveness of the toxic components. They commonly include amines (e.g., histamine, catecholamines, serotonin), peptides, polypeptides (e.g., kinins), specific proteins, and enzymes (e.g., phospholipase, hyaluronidase, esterases) that vary significantly among different arthropod taxa. Depending on what types of cells or tissues they affect, toxins and venoms can be characterized, for example, as neurotoxins, cytotoxins, or hemotoxins. Frequently they cause such symptoms as pain, itching, swelling, redness, hemorrhaging, or blisters, the severity of which is largely dependent on the particular types and amounts of toxin involved.

Further information on arthropod toxins and venoms is provided by Beard (1960), Roth and Eisner (1962), B/icherl and Buckley (1971), Bettini (1978), Schmidt (1982), Tu (1984), and Meier and White (1995).

HOST DEFENSES

Humans and other animals have developed elaborate means to defend themselves against infestation by arthropods and infection by pathogens they may transmit. Both behavioral and immunological responses are used to resist infestation by arthropods. Behavioral defenses include evasive, offensive, or defensive action against biting flies such as mosquitoes, black flies, ceratopogonids, stable flies, and horse flies. Grooming and preening by animals (e.g., biting, scratching, or licldng) are defensive behaviors used to reduce or prevent infestations by ectoparasites and other potentially harmful arthropods. Host immunological defenses against arthropods vary with different arthropods and with respect to previous exposure to the same or antigenically related taxa. Details concerning such host immune responses are beyond the scope of this book, but some general trends are noteworthy. Repeated feeding attempts by the same or antigenically cross-reactive arthropods often lead to fewer arthropods being able to feed successfully, reduced engorgement weights, greater mortality, and decreased fecundity of female arthropods. Widespread arthropod mortality rarely results. For more information concerning the types of host immune responses and cell types involved against various ectoparasites, see Wikel (1996b)

Many blood-feeding arthropods partially or completely counteract the host immune response by inoculating immunomodulators or immunosuppressive compounds into the bite site. In fact, a wide range of pharmacologically active compounds is known to be released at the bite site by various arthropods (Ribeiro 1995). These compounds range from anticoagulants to prevent the blood from clotting, local analgesics to reduce host pain, apyrase to prevent platelet aggregation and promote capillary location, and various enzymes and other factors for promoting blood or tissue digestion. Some of these compounds are perceived by the host as antigens and may elicit an immune response, whereas others can cause localized or systemic toxic responses and itching.

FORENSIC ENTOMOLOGY

Forensic entomology is the study of arthropods, especially insects, associated with crimes and other aspccts of the courts and judicial system. Forensic cntomology usually involves the identification of insects and other arthropods associated with human remains as an aid to detcrmining the time and place of death.

Time of death can often be ascertained based on the ambient temperature and other weather conditions over the preceding days at the crime site and by correlating this information with the developmental rates of key arthropod species present on, or in, the corpse. These arthropods are typically fly larvae, some of which are important primary and secondary decomposers of animal remains. By knowing developmental times and related information for decomposer species at different temperatures, it often is possible to quite accurately estimate the time of death.

The location where a crime took place, if different from the discovery site, also sometimes can be determined based on the presence of unique arthropods with known distributions that do not include the area where the body was found. Similarly, examination of carefully collected insect evidence can aid in solving other crimes (e.g., the origin of drug shipments and sources of vehicles and other accessories used in crimes) in which there is arthropod evidence involving taxa with characteristic geographical distributions.

Further details on the science of forensic entomology are provided by Vincent et al. (1985), Smith (1986), Erzinclioglu (1989), Carts and Haskell (1990), Catts and Goff ( 1992 ), and Golf (2000).

MINOR ARTHROPOD PROBLEMS OF MEDICAL-VETERINARY INTEREST

In addition to arthropod groups detailed in the chapters that follow, a few arthropods in other groups may have minor, incidental, or occasional significance to human and animal health. These include springtails (order Collembola), bark lice (order Pscoptera), walking sticks (order Phasmida), mayflies (order Ephemeroptera), earwigs (order Dermaptera), thrips (order Thysanoptera), caddisflies (order Trichoptera), centipedes (class Chilopoda), and millipedes (class Diplopoda).

On rare occasions, springtails have been recorded infesting human skin (Scott et al. 1962, Scott 1966). Similarly, some bark lice (psocids) are known to cause allergies or dermatitis in humans (Li and Li 1995, Baz and Monserrat 1999). Certain adult mayflies and caddisflies can cause inhalational allergies, especially when they emerge in large numbers from lakes, rivers, or streams (Seshadri 1955 ).

In addition to various hymenopterans, arachnids, and other venomous arthropods detailed in the following chapters, a few miscellaneous arthropods produce venoms that can cause medical-veterinary problems. These include walking sticks (stick insects) and millipedes, some of which utilize venomous defensive secretions or sprays. Defensive sprays of certain walking sticks can cause conjunctivitis (Stewart 1937), whereas defensive sprays of some millipedes contain hydrochloric acid that can chemically burn the skin and can cause long-term skin discoloration (Radford 1975). Centipedes, especially some of the larger tropical species, can cause envenomation when they “bite” with their poison claws (maxillipeds), which are equipped with poison ducts and glands (Remington 1950).

Thrips, which have tubular mouthparts adapted for sucking plant fluids, occasionally pierce the skin and have been known to imbibe blood (Williams 1921, Hood 1927, Bailey 1936, Arnaud 1970). On rare occasions, earwigs also have been recorded as imbibing blood (Bishopp 1961). Bishopp further noted that earwigs have been known to pierce human skin with their pair of caudal pincers (cerci) and may stay attached for an extended period.

Some miscellaneous arthropods inhabit the feathers of birds or the fur of mammals. The exact nutritional requirements of some of these arthropods remain unknown; most of them, however, do not appear to be true ectoparasites. Representatives of two of the three subordcrs of earwigs (suborders Arixeniina and Hemimerina) live in mammal fur. The Arixeniina are associated with Old World bats, whereas the Hemimerina are found on African cricetomyine rodents (Nakata and Maa 1974). These earwigs may feed on skin secretions or sloughed cells, but their effect on the health of their hosts is poorly understood. Other occasional inhabitants of host pelage, such as various beetles, cheyletid mites, and pseudoscorpions, are predators of ectoparasites and are therefore beneficial to their hosts (Durden 1987).

A few arthropods that are not mentioned in the following chapters can occasionally serve as intermediate hosts of parasites that adversely affect domestic and wild animals. These include certain springtails andpsocids (bark lice) as intermediate hosts of tapeworms (Baz and Monserrat 1999).