Introduction to myiasis

Defining myiasis

The term myiasis was first proposed by Hope (1840) to refer to diseases of humans originating specifically with dipterous larvae, as opposed to those caused by insect larvae in general, scholechiasis (Kirby and Spence, 1815). Hope presented a table of myiasis cases which included several from Jamaica resulting from unknown larvae, one of which led to death. Some of the larvae were described as being of an unidentified blue fly; these are almost certainly very early references to myiasis caused by the New World screwworm, Cochliomyia hominivorax (Coquerel).

Myiasis has since been defined as 'the infestation of live vertebrate animals with dipterous larvae, which, at least for a certain period, feed on the host's dead or living tissue, liquid body substances, or ingested food' (Zumpt, 1965). There are two main systems for categorizing myiasis: anatomically, in relation to the location of the infestation on the host (see Table 1); or according to the parasite's level of dependence on the host (see Table 2).

The anatomical system of classification was first proposed by Bishopp (Patton, 1922) and later modified by James (1947), (see Table 1). The system is useful for practical diagnosis (Zumpt, 1965) and so is used below. However, Patton (1922) found it to be unsatisfactory when considering evolutionary and biological relationships, because individual species could be assigned to more than one group and different groups contained species with different levels of dependence on the host. He put forward instead a system based on the degree of parasitism shown by the fly (see Table 2).

Table 1. Classification of myiases according to their anatomical position in or on the host animal

Zumpt

Bishopp

James

SanguinivorousBloodsuckingBloodsucking
Dermal/subdermalTissue-destroyingFuruncular
Subdermal migratoryCreeping
Traumatic/wound
Anal/vaginal
NasopharyngealInfestations of the head passagesNose, mouth and sinuses
Aural
Ocular
IntestinalIntestinal/urogenitalEnteric
Anal/vaginal
UrogenitalIntestinal/urogenitalBladder and urinary passages
Anal/vaginal

Note: The division of myiases into five rows in the first column is based on Zumpt (1965). The second and third columns show the comparable groupings of Bishopp (Patton, 1922) and the modification of these by James (1947).

In Patton's categorisation, there are two main groups of myiasis-causing species: the specific parasites, which must develop on live hosts; and the semi-specific parasites, which usually develop on decaying organic matter, such as carrion, faeces and rotting vegetation, but may also deposit their eggs or larvae on live hosts. Zumpt (1965) termed the specific parasites obligatory and the semi-specific parasites facultative. The facultative species may be further differentiated depending on whether they are able to initiate myiasis (primary species) or only invade after other species have initiated it (secondary and tertiary species) (Kettle, 1984), (see Table 2).

Table 2. Classification of myiases according to the parasitic relationship of the Diptera with the host

Group

Subgroup

Remarks

Specific/obligatory Parasite dependent on host for part of its life cycle
Semi-specific/facultativePrimaryNormally free-living but may initiate myiasis
SecondaryNormally free-living and unable to initiate myiasis but may be involved once animal is infested by other species
TertiaryNormally free-living, but may be involved in myiasis when host is near death
Accidental/pseudomyiasis Normally free-living larvae that may be accidentally ingested and cause pathological reactions

Sources: Patton, 1922; Zumpt, 1965; Kettle, 1984

In addition, Patton (1922) defined a third group of myiasis-causing species, those that cause accidental myiases when their eggs or larvae are ingested by the host. Zumpt (1965) termed these pseudomyiases.

Flies that may be encountered in cases of cutaneous myiasis primarily belong to four families, Calliphoridae, Sarcophagidae, Muscidae, and Oestridae. The first three families are involved primarily in wound or traumatic myiasis.

Wound or traumatic myiasis

The primary purpose for developing this identification key is to aid in identifying cases of traumatic myiasis caused by the three major species of obligate parasites encountered in wound myiasis. The New World screwworm fly, Cochliomyia hominivorax, the Old World screwworm fly, Chrysomya bezziana, and Wohlfahrt's wound myiasis fly, Wohlfahrtia magnifica.

Wound or traumatic myiasis is the infestation by dipterous larvae of primarily the cutaneous tissues in animals and humans, usually at the sites of natural (orifices) and unnatural (wounds) openings into the body. It may be deleterious, as when the obligate and primary species attack the host's healthy tissues or it may be benign, as when secondary species confine their activities to diseased and dead tissue. In the later situation carefully controlled myiasis can even be of benefit to the host in 'maggot therapy' (Sherman et al., 2000).

Calliphoridae

Auchmeromyia

Bloodsucking larvae of the African species Auchmeromyia senegalensis the Congo floor maggot, are atypical myiasis species as they do not live on or in the host, but suck the blood of sleeping humans and burrow-dwelling animals such as warthogs (sanguinivorous myiasis).

Cordylobia

Cordylobia includes three species: C. anthropophaga is the Tumbu fly of Africa which causes a boil-like (furuncular) type of myiasis, particularly of man and dogs. Eggs are deposited on dry, shaded ground, especially if contaminated by urine/faeces, or on drying laundry. Larvae hatch in 1-3 days and remain just under the soil surface until activated by host body heat. They then emerge, burrow into the host and grow for 8-15 days in a furuncle. Antelopes and the African Giant Rat are important hosts of C. rodhaini.

Cochliomyia

The two species of the New World genus, Cochliomyia, most frequently encountered in cases of wound myiasis are C. hominivorax and C. macellaria.  The New World screwworm fly, C. hominivorax, is a true obligate parasite of mammals: females lay eggs at the edges of wounds on living mammals (or on mucous membranes); within 24 hours, larvae emerge and immediately begin to feed on the underlying tissues, burrowing gregariously head-downwards into the wound; larvae reach maturity about 5-7 days after hatching and leave the wound, falling to the ground into which they burrow and pupate.  On completion of development, adult flies emerge from the puparium and mate within 1-3 days.  About four days after mating, females seek a suitable host and lay an average of 200 eggs (range 10-490) in a flat, shingle-like batch. Further batches are laid at intervals of three days with an average of four batches per female. Adult flies live for 2-3 weeks on average and may disperse great distances.  The literature on the New World screwworm is extensive and scattered, but earlier publications may be accessed rapidly by reference to the bibliography of Snow et al (1981).  Larvae of C. macellaria involved in myiasis are only secondary invaders, feeding on the edge or surface of the wound.  A rare case of C. minima myiasis of a dog in Puerto Rico has been described (De León & Fox, 1980).

Chrysomya screwworms

The life cycle of Chrysomya bezziana (Old World screwworm), its habits and the appearance of wounds infested by it are very similar to those of Cochliomyia hominivorax. The two species appear to occupy an exactly equivalent parasitic niche in their natural ranges. Adult female Ch. bezziana only oviposit on live mammals, depositing 150-500 eggs at sites of wounding or in body orifices such as the ear, nose and urinogenital passages. The larvae hatch after 18-24 hours, moult once after 12-18 hours and a second time about 30 hours later.  They feed for 3-4 days and then drop to the ground and pupate. This species has been recorded on 21 host species at a zoo in Malaysia (Spradbery & Vanniasingham, 1980). Similar reports exist for Cochliomyia hominivorax and Wohlfahrtia magnifica.

Chrysomya species other than screwworms

Chrysomya albiceps is a facultative parasite and normally lays its eggs on carcasses. The first instar larvae feed on exudations of the decomposing flesh, but second and third instars are, in addition, predacious, feeding on other blowfly larvae. They may even be cannibalistic. Whilst the eggs are normally laid on carcasses, they may also be laid on neglected wounds where the larvae can cause tissue destruction. Chrysomya albiceps and the similar Ch. rufifacies are frequently involved in secondary myiasis in sheep.

Lucilia

Members of this genus are responsible for the condition known as 'blowfly strike' of sheep in a number of countries including South Africa and Australia, where the species responsible is L. cuprina, and in many temperate areas including Europe and North America, where the important species is L. sericata. Female Lucilia lay their eggs on carcasses, in neglected, suppurating wounds and, in  particular, on the wool of sheep soiled with urine, faeces or blood.  Lucilia sericata has been used to assist the healing of long-term wounds in man, a treatment termed 'maggot therapy' (larva therapy or biosurgery), whereby the larvae ingest necrotic tissues and stimulate the healing process (Sherman & Pechter, 1988; Thomas et al., 1996; Sherman et al., 2000).  Lucilia bufonivora is an obligate parasite of toads and frogs.

Calliphora

The two most important species are C. vicina and C. vomitoria which share similar biologies.  Females are attracted for oviposition to any decaying matter, of which carrion is most suitable.  Calliphora are usually only involved in myiasis as secondary species, but C. vicina> , in particular, may be a primary invader (Zumpt, 1965; Smith, 1986).

Phormia, Protophormia

These closely related genera are, approximately, confined to areas north of the Tropic of Cancer.  The important species are Phormia regina and the more northern Protophormia terraenovae.  They are very similar in appearance and habits, both usually breeding in carrion, but also recorded in wound myiasis.   Protophormia terraenovae may, in particular, be a serious parasite of cattle, sheep and reindeer (James, 1947; Smith, 1986).

Protocalliphora

Flies in the genus Protocalliphora are obligate, blood-feeding parasites of nestling birds in the Old and New Worlds (Sabrosky et al ., 1989) but, in general, their effects are not serious. 

Other Calliphorids causing obligate myiasis

Flies in the genus Booponus develop as larvae in boils under the skin of bovids and deer of the Old World.  In that respect they are somewhat like Cordylobia, but they lay their eggs directly on the host.  Elephantoloemus indicus is the sole representative of its genus and develops in the skin of Indian elephants - many thousands of larvae can impart a honey-comb appearance to the skin due to numerous scars.

Sarcophagidae

Wohlfahrtia

Females are larviparous, depositing first instar larvae rather than eggs. The most important agent of myiasis is W. magnifica an obligate parasite of warm blooded vertebrates in southeastern Europe, southern and Asiatic Russia, the Middle East and North Africa. Some 120-170 larvae are deposited near to wounds or body openings of man and other animals, such as sheep (Farkas et al., 1997), goats, cattle, horses, donkeys, pigs, dogs, camels and geese (see figure on following page). The larvae of Wohlfahrtia magnifica feed and mature in 5-7 days and then leave the wound for pupation (Zumpt, 1965; Kettle, 1984). Wohlfahrtia nuba also infests wounds of livestock in North Africa and the Middle East, but it probably feeds only on dead or diseased tissues rather than on living tissues (James, 1947). Wohlfahrtia vigil and W. meigeni (opaca) are North American species whose larvae tend to penetrate the hosts skin individually producing furuncles like Cordylobia (Alexander, 1984). Wohlfahrtia meigeni can be a serious pest of mink and fox in fur farms in North America (Knowlton, 1941; Gassner & James, 1948).

Sarcophaga, Cistudinomyia

Sarcophaga sensu lato may occasionally be involved in myiasis, but little is known of their larval stages. Sarcophaga cruentata (= haemorrhoidalis) is one of the most common species and breeds mainly in faeces (Zumpt, 1965; Smith, 1986).  Blaesoxipha plinthopyga is reported to be an important facultative myiasis causing sarcophagid (Baumgartner, 1988). Cistudinomyia cistudinis is parasitic on turtles and tortoises, but is probably of little economic importance with infestations rarely being large enough to cause death (Knipling, 1937). Larvae may penetrate at ongoing or previous sites of attachment of tortoise ticks. Calliphorid> species recorded rarely on tortoise and other reptiles are Chrysomya megacephala, Lucilia (Frank, 1981), and Calliphora vicina  (Sales et al., 2003).

Muscidae

Members of the family Muscidae may be involved as secondary invaders, especially the ubiquitous Musca domestica, the common housefly. Species of Fannia are sometimes involved in urinogenital myiasis. Species of Passeromyia are obligate, blood-feeding larval parasites of bird nestlings, feeding from the skin surface or burrowing subcutaneously - they may cause death of the host (Zumpt, 1965). Species of Philornis include similar bloodfeeding or subcutaneous parasites of neotropical birds (Guimarães and Papavero, 1999).

Oestridae

Oestrinae (34 species in 9 genera)

The genus Oestrus has six species parasitising antelopes, sheep and goats, including O. ovis, the very important sheep nasal bot fly. Larvae of O. ovis develop in the head sinuses and nasal passages of sheep and goats in all sheep-farming areas of the world. Effects may be insignificant or may be severe (especially in lambs), with purulent discharge from nostrils, repeated sneezing and shaking of head and breathing difficulties. Can cause opthalmomyiasis in man.

Other genera in the Oestrinae are Cephalopina (1 species which can be a serious problem in camels, C. titillator [Musa et al., 1989]), Cephenemyia> (8 species in Cervidae), Gedoelstia> (2 species in antelopes), Kirkioestrus (2 species in antelopes), Pharyngobolus (1 species in African elephant), Pharyngomyia (2 species in Cervidae), Rhinoestrus (11 species in horses, zebras, pigs, giraffe, hippopotamus, springbuck, sheep) and Tracheomyia (1 species in kangaroos). All are found in the nasal passages of the host excepting Pharyngobolus and Tracheomyia which are found in the trachea.

Gasterophilinae (c. 15 species in 3 genera)

Originally restricted to the Palaearctic and Afrotropical regions, species of the genus of most veterinary importance, Gasterophilus (bot flies, 9 species), now have a worldwide distribution.  Their larvae develop in the digestive tract of horses and zebras. Eggs are stuck to the hairs of the host (or on vegetation, G. pecorum) and, when they hatch, the larvae enter the mouth by their own actions or via the hosts tongue in grooming. Gasterophilus nigrocornis, G. haemorrhoidalis, G. inermis, G. nasalis, G. pecorum, G. intestinalis (eggs laid mainly on inner forelegs and stimulated to emerge by hosts licking - larvae migrate through tongue, second stages move to stomach - heavy infestation may cause irritation of stomach membranes, ulceration, and other stomach disorders).

The two other genera of this sub-family are Gyrostigma (3 species in rhinoceros) and Cobboldia (3 species in elephant).  Gyrostigma attach to the stomach wall and are eventually voided with the faeces, but larvae of Cobboldia move freely in the stomach (mainly between stomach wall and contents) and leave the host via its mouth when mature.

Hypodermatinae (32 species in 11 genera)

Hypoderma (5 species in cattle and Cervidae) are the heel flies, warble flies or cattle grubs whose larvae migrate from sites of oviposition, by a subcutaneous route and in nerve tissues, to the back where they develop in 'warbles' which spoil the host's hide.  Hypoderma bovis pass through connective tissues to spinal column and then to back (there for 5-11 weeks): H. lineatum go to oesophagus, remain there a while, then to back). Hypoderma diana attacks deer in a similar manner. The persistence of the females in laying 300-800 eggs can cause 'gadding' by the hosts: this can result in reduced milk production and failure to gain weight. 

There are seven other genera in the subfamily Hypodermatinae and the larvae of all of them develop in the skin of their hosts in the manner of Hypoderma larvae, i.e., Oestroderma (1 species in pikas), Oestromyia> (5 species in mice, marmots and pikas), Pallasiomyia (1 species in saiga antelope), Pavlovskiata (1 species in goitered antelope), Portschinskia (7 species in mice and pikas), Przhevalskiana> (6 species in gazelles and goats - in the latter host they can be an important veterinary pest) and Strobiloestrus (3 species in Kobus species).

Cuterebrinae (>70 species in 6 to 8 genera)

The most economically important Cuterebrid fly is Dermatobia hominis. Sometimes called the tórsalo, or human bot fly, it is a very serious pest of cattle in South America, the larvae creating boil-like swellings where they enter the skin (Lane et al, 1987). The hides of infested cattle may be worthless. Females catch other species of host-visiting fly and oviposit on them: the fly is then released and transports the eggs to the host (phoretic behaviour).  The selection of host is made by the porter fly and so D. hominis is found in a very wide range of hosts, from mammals to birds.

Species in the genus Cuterebra (>60 species) cause skin myiasis of rodents, lagomorphs and, occasionally, humans throughout the New World (Baird et al, 1989). Four other genera have been synonymised within Cuterebra; Alouattamyia (1 species in howler monkeys), Andinocuterebra (1 species, unknown host), Pseudogametes (2 species, unknown hosts) and Rogenhofera (6 species, unknown host).

Two genera which have been provisionally placed in both Gasterophilinae and Cuterebrinae to date are Neocuterebra (1 species in African elephant, in boils on buttocks, abdominal flanks, chest and thighs - little if any pathological effect) and Ruttenia (1 species in African elephant, in pockets in dermal tissues of the foot, causing slight localized inflammation).

Primary Sources

Hall, M.J.R. (1991). Screwworm flies as agents of wound myiasis.  Pp. 8 17 in, World Animal Review, Special Issue 'New World Screwworm: Response to an Emergency' , October 1991, R.D.S. Branckaert (Ed.) 52 pp.

Hall, M.J.R. & Smith, K.G.V. (1993). Diptera causing myiasis in man. In: Medical Insects and Arachnids, Lane R.P. & Crosskey R.W., eds. Chapman & Hall, London, UK, 429-469.

References

Alexander, J. O'Donel  1984.   Arthropods and human skin> .  422 pp. Springer-Verlag, Berlin, Heidelberg, New York, Tokyo.

Baird, J.K., Baird, C.R. & Sabrosky, C.W.  1989.  North American cuterebrid myiasis. Report of seventeen new infections of human beings and review of the disease.  Journal of the American Academy of Dermatology, 21 , 763-772.

Baumgartner, D.L. 1988.  Review of myiasis (Insecta: Diptera: Calliphoridae, Sarcophagidae) of nearctic wildlife.  Wildlife Rehabilitation,7, 3-46.

De León, D. & Fox, I.  1980.   Canine minima myiasis in Puerto Rico - a case report.  Journal of Agriculture of the University of Puerto Rico> 64 : 126-128.

Farkas, R., Hall, M.J.R. & Kelemen, F.  1997.  Wound myiasis of sheep in Hungary.  Veterinary Parasitology> 69 : 133-144.

Frank, W. 1981.  Ectoparasites.  Chapter 10, pp. 357-383 in, Diseases of the Reptilia, Volume 1 , Cooper, J.E. & Jackson, O.F. (Eds.), xi + 383 + xxxii pp.

Gassner, F.X. & James, M.T.  1948.  The biology and control of the fox maggot, Wohlfahrtia opaca (Coq). Journal of Parasitology 34 , 44-50.

Guimarães, J.H. & Papavero, N.  1999.  Myiasis in man and animals in the neotropical region - Bibliographic database . 308 pp. São Paulo, Plêiade/FAPESP.

Hope, F.W. 1840. On insects and their larvae occasionally found in the human body. Trans. R. Entomol. Soc. London, 2 : 256-271.

James, M.T. 1947. The flies that cause myiasis in man. USDA Misc. Pub. No. 631. 175 pp.
Kettle, D.S. 1984. Medical and veterinary entomology. London and Sydney, Cross Helm. 658 pp.

Kirby, W. & Spence, W. 1815. An introduction to entomology. Vol. 1. London, Longman, Hurst, Rees, Orme & Brown. 512 pp.

Knipling, E.F. 1937.  The biology of Sarcophaga cistudinis Aldrich (Diptera), a species of Sarcophagidae parasitic on turtles and tortoises.  Proceedings of the Entomological Society of Washington  39, 91-101.

Knowlton, G.F. & Hall, D.G.  1941.  Flesh fly kills kit mink.  Journal of Economic Entomology 34 , 216.

Lane, R.P., Lovell, C.R., Griffiths, W.A.D. & Sonnex, T.S.  1987.  Human cutaneous myiasis - a review and report of three cases due to Dermatobia hominis.  Clinical and Experimental Dermatology 12 , 40-45.

Musa, M.T., Harrison, M., Ibrahim, A.M. & Taha, T.O.  1989.  Observations on Sudanese camel nasal myiasis caused by the larvae of Cephalopina titillator.  Revue Élevage Médicine Véterinaire de Pays Tropicaux 42 , 27-31.

Patton, W.S. 1922. Notes on the myiasis producing Diptera of man and animals. Bull. Entomol. Res 12 : 239-261.

Sabrosky, C.W., Bennett, G.F. & Whitworth, T.L.  1989.  Bird blow flies (Protocalliphora) in North America (Diptera: Calliphoridae) with notes on the Palearctic species.  Smithsonian Institution Press, Washington & London, 312 pp.

Sales, M.J., Ferrar, D., Castellà, J., Borràs, D. and HALL, M.J.R. (2003)  Myiasis in two Hermann's tortoises (Testudo hermanni). The Veterinary Record 153, 600-601.

Sherman, R.A. and Pechter, E.A.  1988.  Maggot therapy: a review of the therapeutic applications of fly larvae in human medicine, especially for treating osteomyelitis.  Medical and Veterinary Entomology 2 , 225-230.

Sherman, R.A., Hall, M.J.R. & Thomas, S. (2000) Medicinal maggots: an ancient remedy for some contemporary afflictions.  Annual Review of Entomology 45, 55-81.

Smith, K.G.V. 1986. A manual of forensic entomology> . London, British Museum (Natural History). 205 pp.

Snow, J.W., Siebenaler, A.J. & Newell, F.G.  1981.  Annotated bibliography of the screwworm, Cochliomyia hominivorax  (Coquerel).  United States Department of Agriculture Science and Education Administration Agricultural Reviews and Manuals , Southern Series No. 14, 32pp.

Spradbery, J.P. & Vanniasingham, J.A. 1980.  Incidence of the screw-worm fly, Chrysomya bezziana, at the Zoo Negara, Malaysia. Malaya Veterinary Journal 7 , 28-32.

Thomas, S., Jones, M., Shutler, S. & Jones, S.  1996.  Using larvae in modern wound management.  Journal of Wound Care 5 : 60-69.

Zumpt, F. 1965. Myiasis in man and animals in the Old World. London, Butterworths. 267 pp.