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Summary Summary
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Introduction Introduction
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Life cycles Life cycles
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Classification Classification
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Epidemiology Epidemiology
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Geographical distribution Geographical distribution
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Risk factors Risk factors
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Environmental factors Environmental factors
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Host factors Host factors
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Socio-economic factors Socio-economic factors
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Molecular epidemiology Molecular epidemiology
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Human myiases Human myiases
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Cutaneous and wound myiases Cutaneous and wound myiases
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Ophthalmomyiasis Ophthalmomyiasis
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Human external ophthalmomyiasis, ophthalmomyiasis externa Human external ophthalmomyiasis, ophthalmomyiasis externa
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Human internal ophthalmomyiasis, ophthalmomyiasis interna Human internal ophthalmomyiasis, ophthalmomyiasis interna
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Human orbital ophthalmomyiasis Human orbital ophthalmomyiasis
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Nasal myiasis Nasal myiasis
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Oral myiasis Oral myiasis
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Intestinal myiases (Pseudomyiasis) Intestinal myiases (Pseudomyiasis)
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Aural myiasis Aural myiasis
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Uriogenital myiasis Uriogenital myiasis
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Cerebral myiasis Cerebral myiasis
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Clinical signs Clinical signs
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Diagnosis Diagnosis
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Larval collection and preservation Larval collection and preservation
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Laboratory rearing of larvae Laboratory rearing of larvae
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Immunodiagnostic tools Immunodiagnostic tools
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Other techniques used in myiasis diagnoses Other techniques used in myiasis diagnoses
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Fly identification Fly identification
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Molecular identification Molecular identification
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Treatment Treatment
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Control and prevention Control and prevention
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Quarantine measures, and international and regional cooperation Quarantine measures, and international and regional cooperation
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The insect sterilization technique The insect sterilization technique
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Maggot therapy (Biosurgery) Maggot therapy (Biosurgery)
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Forensic entomology Forensic entomology
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References References
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Cite
Abstract
Human myiases can be caused by over 50 species of dipteran larvae. The numbers of human clinical myiasis reports, reflect their relative importance in the following order; cutaneous, ophthalmomyiases, nasal, oral, intestinal, ear, urogenital, and cerebral myiases. Myiasis producing flies are distributed worldwide, but most reported cases are from warm and developing countries. Molecular techniques have been applied to myiasis fly identification and classification, especially ostrids and calliphorines. Successful elimination programs have been carried out against Hypoderma spp. in the UK and Cochliomyia hominivorax in the USA, Mexico, Central America, Libya and the Caribbean Islands and another is ongoing against Crysomya bezziana in the Middle East. A beneficial myissis “Biosurgery or maggot therapy” is the intentional use of Lucilia sericata larvae applied in specially designed dressings to chronic and MRSA infected wounds. The growing larvae execration/secretion facilitate wound debridement and successfully treated leg and pressure ulcers, wounds associated with diabetes, and many other types of infected wounds in a shorter time compared to conventional treatment. Now knowledge of myiases producing flies is accepted in many countries as a forensic tool.
Summary
Human myiases can be caused by over 50 species of dipteran larvae. The numbers of human clinical myiasis reports, reflect their relative importance in the following order; cutaneous, ophthalmomyiases, nasal, oral, intestinal, ear, urogenital, and cerebral myiases. Myiasis producing flies are distributed worldwide, but most reported cases are from warm and developing countries. Molecular techniques have been applied to myiasis fly identification and classification, especially ostrids and calliphorines. Successful elimination programs have been carried out against Hypoderma spp. in the UK and Cochliomyia hominivorax in the USA, Mexico, Central America, Libya and the Caribbean Islands and another is ongoing against Crysomya bezziana in the Middle East. A beneficial myissis ‘Biosurgery or maggot therapy’ is the intentional use of Lucilia sericata larvae applied in specially designed dressings to chronic and MRSA infected wounds. The growing larvae execration/secretion facilitate wound debridement and successfully treated leg and pressure ulcers, wounds associated with diabetes, and many other types of infected wounds in a shorter time compared to conventional treatment. Now knowledge of myiases producing flies is accepted in many countries as a forensic tool.
Introduction
The biological term ‘myiasis’ was proposed by Hope (1840) to be used only in connection with dipterous larvae occasionally found in the human body. De la Torre-Bueno (1937) added clinical dimension to the term emphasizing the pathological effects of larvae to the definition ‘disease or injury caused by the attack of dipterous larvae’. Zumpt (1965) argued ‘the problem of myiasis must be considered from a biological aspect, and not only from a clinical one’ and produced a more comprehensive definition for myiasis as ‘the infestation of live human and vertebrate animals with the dipterous larvae, which, at least for a certain period, feed on the host’s dead or living tissue, liquid body-substances, or ingested food’.
Dipterous larvae were separated biologically to obligate and facultative parasites. Obligatory parasites are those larvae which normally develop exclusively in or on living vertebrates. Obligatory myiases flies belong to Gastrophilidae, Cutterbridae, Ostridae and Hypodermatidae, such as Gastrophilus spp., Dermatobia hominis, Oestrus ovis and Hypoderma bovis respectively.
The facultative parasites are those larvae which are normally free-living and develop in decaying organic matter, including; carcasses, decomposing vegetables, faeces, manure and sewage. Occasionally and under certain circumstances, such larvae may gain access to the body of a living animal and infest it for a certain period of their life or complete its development. Examples for facultative parasites are blowflies which cause sheep strike (Fig. 68.1) or Musca domestica (House fly) and Eristalis tenax (Drone fly), which may be involved in rectal myiasis.

The life cycle of Blow-fly strike caused by Lucellia sericata and L. cuprina.
Also, myiasis producing flies can be classified into:
Primary flies which initiate strike by laying eggs on living animals,
Secondary flies which lay eggs on animal already struck,
Tertiary flies which lay their eggs when the carcass starts to dry.
Life cycles
The life cycles of most myiasis producing flies are provided by Zumpt (1965) and Beesley (1998). In general myiasis producing flies have similar life cycles which starts with attraction of the adult female fly to the host to deposit either her eggs or larvae on it. Usually attraction occurs due to the odour of decomposing matter, or wound. Bacterial activity appears to be important in preparing favourable conditions. In case of facultative flies (e.g. blowflies), the larvae can obtain the food from either dead carcasses or living animals. The female lays from a few hundred to a few thousands eggs. The larvae hatch after 8 hours to 3 days depending on temperature, humidity and fly species. They grow rapidly and pass two ecdyses. A few days later they will become mature third stage larvae (L3), when they will leave the host and pupate in the soil for three to seven days then hatch as adult flies (Fig. 68.1).
The life cycle of screw-worm blowfly (obligatory flies) is similar to other blowflies but differs in that the female attacks the wound of the live host only and not carcasses. The number of eggs laid by the female is 150–500 and the duration of the life cycle also varies.
The adult Gastrophilus spp. (Gastrophilidae) female fly lays 160–2400 eggs during persistent attacks causing annoyance to horses. They stick their eggs to the hairs of the host. The first stage larvae (L1) are stimulated to emerge by warmth and friction caused by the licking action of the host’s tongue. In some species the hatched L1 can penetrate unbroken skin. In G. pecorum the eggs are laid on the leaves of plants and are ingested by the host. Gasterophilus L1 may penetrate the tongue, lips or the inside of the cheek and begin migrating in tunnels until reaching the third stage larvae (L3) in the stomach, intestine, or rectum of the equine, depending upon the species.
The L1 of G. pecorum and G. haemorrhoidalis can penetrate human skin causing creeping myiasis as they move along under the skin resulting in a prominent indurated track in its course. L1 cannot develop further to the second stage (L2) in man.
The life cycle of Dermatobia hominis (Cutterbridae) is unusual. The female fly captures a day-flying mosquito, or another fly such as Musca spp. or Stomoxys spp., or even certain tick species, and glues its eggs to the other species’s body. When this carrier host feeds on a suitable mammal host, the warmth stimulates the eggs to hatch and within 5–10 minutes the larvae penetrate the host’s skin. Alternatively, the eggs are laid on vegetation or the ground and they hatch when a host brushes past them. A small nodule of host tissue subsequently develops around each larva, with a central breathing pore. As the larvae develop over the following 6–12 weeks they become quite large and a boil-like lesion forms at the site of infection. These lesions often attract screwworms with potentially fatal consequences. Once the larvae are mature they burrow out of the skin and drop to the ground where they pupate.
Females flies of the family Oesteridae, mainly Oestrus ovis are viviparous and deposit about 25 larvae on the nostrils of sheep. These larvae are about 1 mm long, and migrate through the nasal passages to reach the frontal sinuses, feeding on the mucus secretions which are stimulated by their movement. The first ecdysis occurs in the nasal passages and L2 crawl into the frontal sinuses where the final molt takes place. In the nasal sinuses the larvae may remain several weeks before they migrate again to the nostrils and sneezed out to pupate on the ground and the adult fly is generated from the pupated larvae. The female survives only two weeks, but each can deposit up to 500 larvae in the nasal passages of the sheep.
The adult Hypoderma females attach eggs to the hairs of the underside of the body of cattle, the L1 then penetrate the skin via the hair follicles. After a migration of 5–6 months, through the connective tissues via the oesophagus (H. lineatum) or epidural fat (H. bovis) the larvae reach the skin of the back. They then feed for a further 4–6 weeks and moult into the second and third stages reaching the size of 25 mm in a boil. The L3 later falls to the ground to pupate. The larval migration described in cattle sometimes seen in man and horses. Humans usually suffer single larva infestations, and not 20–30 larvae as seen commonly in cattle. H. lineatum is the main species to infect humans and tends to occur in rural children. Hypoderma eggs are laid on the hairs of the body, probably the legs or arms, but L1 are usually seen in the gum or on the scalp, but may also appear in skin of the back, abdomen, chest, or genital region. The L3 can reach 20 mm in length in cattle but usually no more than 5–12 mm long in humans. Reported cases had a larva which broke the surface of the skin just above the right eyebrow, in the parietal and temporal regions of her head (Leclerq 1969). Twenty two cases of human myiasis with Hypoderma larvae causing painful swellings and abscesses were reported from Norway (Zumpt 1965). Intracranial haematomata due to migrating Hypoderma larvae have been recorded in humans and horses. Hypoderma spp. are also incriminated in many ophthalmomyiases cases.
Classification
Myiasis producing flies belong to seven families (Table 68.1).
Family . | Fly name . | Genera . | Species . | Host . | Type of myiasis . | Geographical distribution . | ||
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Muscidae | Common house fly | Musca | Musca domestica | Animals | F | S | C,U,I,A,Or | Worldwide |
Musca sorbens | Animals | F | S | C | ||||
Latrine/lesser housefly | Fannia | Fannia canicularis | Animals | F | S | U,I | ||
Fannia scalaris | Animals | F | S | U,I | ||||
Large house fly | Muscina | M. stabulans | Animals | F | S | U,I | ||
Calliphoridae | Congo floor maggot | Auchmeromyia | A. luteola | pig, hog, ant bears, hyenas | O | P | C, San | Africa south of the Sahara |
Tumbu/Mango fly | Cordylobia | C. anthropophaga | rats, dogs, cata, goats, mice, monkeys, chimpanzees, chicken | O | P | C,Oo,Or | Sub-Saharan Africa, Saudi Arabia | |
Lund’s fly | C. rodhaini | Antelopes, shrews, monkeys, gerbils, rats | O | P | C | Tropical Africa | ||
New-World screwworm | Callitroga (Cochliomyia) | C. hominivorax | Warm-blooded animals | O | S | C,Oo,U,A,Oo,N,Or C | From Belize and Guatemala to Uruguay and northern Chile, West Indies | |
Secondary screwworm | C. macellaria | F | S | C | From south east Canada to Argentina | |||
Old-World screwworm | Chrysomyia | C. bezziana | Warm-blooded animals | O | S | C,Oo,U,A,Oo,Or | Africa, Middle East, Asia, from India and China to Papua New Guinea | |
C. albiceps C. megacephala C. chloropyga C. mallochi C. putoria C. inclinata | Animals | F F F F F F | T S S S S S | C C | Africa, Middle East, Asia Africa, Middle East, Asia | |||
Sheep strike | Lucilia | L. cuprina | Sheep | F | P,S | C,I | Africa, Asia, Australia | |
European sheep blow-flies, fleece-worms | L. sericata | Sheep | F | P,S | C,U,Or,I | Europe, USA | ||
Blowfly | L. ampullacea | Sheep | F | P,S | U | Europe, Japan | ||
Bluebottle flies | Calliphora | C. erthyrocephala C. vicina Microcaliphora varpis C. vomitoria | Sheep Sheep Sheep Sheep | F F F F | P P P S | C,I,U C,I,U C,I,U C,Oo,U | Middle East | |
Mack-blow flies | Phormia | Ph. regina Ph. terrae-novae | Sheep Sheep | F F | P,S P,S | C,I C,I | North America North America, Europe | |
Sarcophagidae | Flesh flies | Sarcophaga | S. haemoridalis, S. tibials S. incisilobata | Warm-blooded animals | F F | S S | C,I,U U | Worldwide Central Europe, Ireland, Asia |
Wohlfahrtia | W. magnifica | Warm-blooded animals | O O | P P | C,Oo,Or,A,N | Mediterranean basin, Middle East, Asiatic Russia, China | ||
W. nuba | O | P | C | From west Africa to Pakistan | ||||
W. vigil | O | P | C | Canada, Northern USA | ||||
Gastrophilidae | Horse bot fly | Gastrophilus | G. pecorum, G. haemorrhoidalis, G. intermis G. nigricornis, | Equine | O | P | Cr Cr Cr | Global, especially the Mediterranean basin, Middle East, South Africa, Central America, Africa, USA |
Cuterebridae | Human bot | Dermatobia | D. hominis | Cattle, mammals | O | P | C,Oo,N,U,CC | Forested areas of the New-World tropics, West Indies |
Rodent botflies | Cuterebra | C. emasculator | Rodent | O | P | C,N | North America | |
Oestridae | Sheep nasal botflies | Oestrus | O. ovis | Sheep, goats | O | P | Eo,Or,A,N | Mediterranean basin, Middle East, India, Russia, South Africa, Central America, USA |
Horse nasal botflies | Rhinoestrus | R. purpureus | Equine | Eo | Russia, Italy, Africa | |||
Hypodermatidae | Cattle grub | Hypoderma | H. bovis | Cattle | O | P | Io, CC | North temperate zone |
or warbles | Hypoderma | H. lineatum | Cattle, horse | O | P | C,Io,Cr, CC | South temporate zone | |
H. diana | Red deer | O | P | C,Cr | Ireland, Scotland, Sweden, northern Europe | |||
Reindeer warble | Oedemagena | O. tarandi | Reindeer | O | P | Oo,Or | Scandinavia, Canada |
Family . | Fly name . | Genera . | Species . | Host . | Type of myiasis . | Geographical distribution . | ||
---|---|---|---|---|---|---|---|---|
Muscidae | Common house fly | Musca | Musca domestica | Animals | F | S | C,U,I,A,Or | Worldwide |
Musca sorbens | Animals | F | S | C | ||||
Latrine/lesser housefly | Fannia | Fannia canicularis | Animals | F | S | U,I | ||
Fannia scalaris | Animals | F | S | U,I | ||||
Large house fly | Muscina | M. stabulans | Animals | F | S | U,I | ||
Calliphoridae | Congo floor maggot | Auchmeromyia | A. luteola | pig, hog, ant bears, hyenas | O | P | C, San | Africa south of the Sahara |
Tumbu/Mango fly | Cordylobia | C. anthropophaga | rats, dogs, cata, goats, mice, monkeys, chimpanzees, chicken | O | P | C,Oo,Or | Sub-Saharan Africa, Saudi Arabia | |
Lund’s fly | C. rodhaini | Antelopes, shrews, monkeys, gerbils, rats | O | P | C | Tropical Africa | ||
New-World screwworm | Callitroga (Cochliomyia) | C. hominivorax | Warm-blooded animals | O | S | C,Oo,U,A,Oo,N,Or C | From Belize and Guatemala to Uruguay and northern Chile, West Indies | |
Secondary screwworm | C. macellaria | F | S | C | From south east Canada to Argentina | |||
Old-World screwworm | Chrysomyia | C. bezziana | Warm-blooded animals | O | S | C,Oo,U,A,Oo,Or | Africa, Middle East, Asia, from India and China to Papua New Guinea | |
C. albiceps C. megacephala C. chloropyga C. mallochi C. putoria C. inclinata | Animals | F F F F F F | T S S S S S | C C | Africa, Middle East, Asia Africa, Middle East, Asia | |||
Sheep strike | Lucilia | L. cuprina | Sheep | F | P,S | C,I | Africa, Asia, Australia | |
European sheep blow-flies, fleece-worms | L. sericata | Sheep | F | P,S | C,U,Or,I | Europe, USA | ||
Blowfly | L. ampullacea | Sheep | F | P,S | U | Europe, Japan | ||
Bluebottle flies | Calliphora | C. erthyrocephala C. vicina Microcaliphora varpis C. vomitoria | Sheep Sheep Sheep Sheep | F F F F | P P P S | C,I,U C,I,U C,I,U C,Oo,U | Middle East | |
Mack-blow flies | Phormia | Ph. regina Ph. terrae-novae | Sheep Sheep | F F | P,S P,S | C,I C,I | North America North America, Europe | |
Sarcophagidae | Flesh flies | Sarcophaga | S. haemoridalis, S. tibials S. incisilobata | Warm-blooded animals | F F | S S | C,I,U U | Worldwide Central Europe, Ireland, Asia |
Wohlfahrtia | W. magnifica | Warm-blooded animals | O O | P P | C,Oo,Or,A,N | Mediterranean basin, Middle East, Asiatic Russia, China | ||
W. nuba | O | P | C | From west Africa to Pakistan | ||||
W. vigil | O | P | C | Canada, Northern USA | ||||
Gastrophilidae | Horse bot fly | Gastrophilus | G. pecorum, G. haemorrhoidalis, G. intermis G. nigricornis, | Equine | O | P | Cr Cr Cr | Global, especially the Mediterranean basin, Middle East, South Africa, Central America, Africa, USA |
Cuterebridae | Human bot | Dermatobia | D. hominis | Cattle, mammals | O | P | C,Oo,N,U,CC | Forested areas of the New-World tropics, West Indies |
Rodent botflies | Cuterebra | C. emasculator | Rodent | O | P | C,N | North America | |
Oestridae | Sheep nasal botflies | Oestrus | O. ovis | Sheep, goats | O | P | Eo,Or,A,N | Mediterranean basin, Middle East, India, Russia, South Africa, Central America, USA |
Horse nasal botflies | Rhinoestrus | R. purpureus | Equine | Eo | Russia, Italy, Africa | |||
Hypodermatidae | Cattle grub | Hypoderma | H. bovis | Cattle | O | P | Io, CC | North temperate zone |
or warbles | Hypoderma | H. lineatum | Cattle, horse | O | P | C,Io,Cr, CC | South temporate zone | |
H. diana | Red deer | O | P | C,Cr | Ireland, Scotland, Sweden, northern Europe | |||
Reindeer warble | Oedemagena | O. tarandi | Reindeer | O | P | Oo,Or | Scandinavia, Canada |
F = Facultative myiases, O = Obligatory myiases, In = Incidental myiasis, P = Primary myiasis, S = Secondary myiasis, T = Tertiary myiasis, C = Cutaneous myiasis, Cr = Creeping myiasis, Eo = External ophthalmomyiasis, Io = Internal ophthalmomyiasis, Oo = Orbital ophthalmomyiasis, N = Nasal myiasis, Or = Oral myiasis, I = Intestinal myiasis, A = Ear myiasis, U = Urogenital myiasis, CC = Cerebral myiasis, San = Sanguinivorous.
Epidemiology
Geographical distribution
Myiasis causing flies are globally distributed, and some can fly considerable distances, e.g. Cochliomyia hominvorax, 300 km, and Crysomya bezziana, 100 km. Endemic areas of some of the more distinctive forms of myiasis are limited to parts of the tropics; however sporadic cases in returned travellers may be encountered in any part of the world (Hall and Wall 1995). Furthermore, with global warming many tropical flies, vectoring many infectious diseases are moving northwards.
Risk factors
Environmental factors
The presence of the myiasis producing fly in a locality supportive of fly abundance and activity are the main determining factors for the occurrence of myiases. The presence and the abundance of the animal hosts of the obligatory myiasis producing flies, the relative abundance of decaying biological materials for the facultative myiasis producing flies, and the suitable climate, mainly temperature and humidity are enhancing factors for the abundance of flies through shorter life cycles, and activities. O. ovis ophthalmomyiasis is prevalent in small ruminant raising areas and oral myiasis occurs mainly in the tropics (Chan et al. 2005).
Wound/cutaneous myiasis is known to be seasonal favouring warm seasons but not extreme temperatures of hot or cold. Cutaneous and wound myiases increase when animal diseases associated with skin lesions and natural opening inflammation and/or contamination with excreta, e.g. foot and mouth disease, diarrhoea, abortion, mange and wounds prevail. Inadequate or breakdown of medical services during wars and natural disasters is associated with human wound myiases.
Microclimate is equally important. For instance, areas detected as unsuitable for Old World Screwworm (OWS) by remote sensing were found to be heavily inhabited with the fly, e.g. Saudi intensive cattle farming, has brought thousands of cattle to the middle of the desert, provided concrete shades and humidifiers for cooling. These projects have changed the local climate, providing concrete resting places and suitable hosts for the fly.
Host factors
Cases of human infections with Lucilia spp. and other blowfly species are almost always associated with personal neglect and incapacity through old age, infancy, or disease. The flies are attracted by the smell of decay, they lay their eggs on the skin or soiled clothing.
People at high risk of myiases are the elderly, the bedridden, those suffering advanced dementia, the wounded, those with poor oral hygiene, those on tube feeding (Chan et al. 2005), those with diabetic foot ulcers, and the psychotic.
Oral Myiasis is associated with poor oral hygiene, alcoholism, senility, suppurating lesions, severe halitosis and other conditions (Droma et al. 2007). It has also been reported in males undertaking outdoor activities more than females (Droma et al. 2007). There are many underlying health disorders that predispose for myiases.
Socio-economic factors
While myiasis by saprophytic larvae is often indicative of poor environmental and personal hygiene, it can occur in unexpected places including well kept homes and hospitals. Nowadays, they are relatively uncommon in high income countries and most human cases are reported from low income countries.
Molecular epidemiology
In spite of the fact that genetic research has focused on diptera (Amendt et al. 2004) little attention was paid to the molecular epidemiology of myiasis producing flies. So far, the genes of subunite I and/or II of the mitochondrial encoded gene for cyto-chrome oxidase has been examined. The mitochondrial encoded 12S rRNA, COI and COII sequences of the two blowflies L. cuprina and L. sericata originating from different geographical regions throughout the world were studied by Stevens and Wall (1996). Morphologically proven L. cuprina specimens from Hawaii were assigned to L. sericata on the basis of mitochondrial sequence data. This result and the analysis of nuclear encoded 28S rDNA sequence reflect hybridization between the two species in Hawaii (Stevens et al. 2002). Specimens of C. vomitoria from the USA and the UK exhibited variability in the D1-D7 region of the nuclear encoded 28S rRNA sequences similar to that found between C. vicina and C. vomitoria in the UK (Stevens and Wall 2001). Recently, a small degree of genetic diversity was found between geographical populations of C. bezziana within the Arabian Gulf region suggesting that a single Gulf colony could be used to implement the sterile insect technique within an integrated control programme (Hall et al. 2009).
Human myiases
Only one fly species, the Congo floor maggot (Aucheromyia leuteola), is exclusively parasitic on man. Most species are zoonotic. With increased use of insecticides in agriculture the number of cases of human myiases has decreased and, at least in otherwise healthy individuals, they are usually restricted to agricultural workers or those living in close proximity to animals. The following clinical types of myiasis are reported with the numbers of the reported clinical cases of the different types of myiasis taken as a reflection of their importance (Table 68.2).
Type of myiasis . | Number of myiases reports . | |
---|---|---|
Key words . | And myiasis . | And human . |
Cutaneous | 250 | 183 |
Ophthalmo | 183 | 154 |
Ocular | 64 | 47 |
Nose | 129 | 66 |
Oral | 122 | 69 |
Intestinal | 122 | 68 |
Gastrointestinal | 33 | 11 |
Ear | 81 | 61 |
Auditory canal | 15 | 13 |
External auricular | 5 | 4 |
Urogenital | 67 | 37 |
Cerebral | 27 | 17 |
Pseudo | 7 | 5 |
Hypodermic | 2 | 2 |
Type of myiasis . | Number of myiases reports . | |
---|---|---|
Key words . | And myiasis . | And human . |
Cutaneous | 250 | 183 |
Ophthalmo | 183 | 154 |
Ocular | 64 | 47 |
Nose | 129 | 66 |
Oral | 122 | 69 |
Intestinal | 122 | 68 |
Gastrointestinal | 33 | 11 |
Ear | 81 | 61 |
Auditory canal | 15 | 13 |
External auricular | 5 | 4 |
Urogenital | 67 | 37 |
Cerebral | 27 | 17 |
Pseudo | 7 | 5 |
Hypodermic | 2 | 2 |
Cutaneous and wound myiases
D. hominis and C. anthropophaga are the main specific cutaneous myiasis flies. The majority of human cases are reported from endemic areas and travellers returning from those areas.
The common wound infesting fly species are; Cochliomyia hominivorax, Chrysomya bezziana, Wahlfahrtia spp., Phormia regina, Phaenicia sericata, Sarcophaga sp., Calliphora sp., and Musca domestica. The infestation is comparatively benign and sometimes beneficial, for the larvae feed on necrotic tissue and produce substances such as allantoin and deoxyribonuclease that facilitate healing. It is common in diabetic foot ulcers (Chan et al. 2005). The clinical signs are intense local reaction, wound widening, foul smell, itching, pricking sensation, induration of surrounding tissues, leakage of brownish serous to bloody exudates, redness and furuncular swelling. Also, first stage larvae may move along under the skin and cause prominent indurated track in its wake causing what is known as creeping myiasis.
Ophthalmomyiasis
Ophthalmomyiasis, or ocular myiasis, is the infestation of the human eye by the larval stage of certain flies of order diptera. This disease is classified into internal, external, and orbital forms, according to the location of the larvae (Kean et al. 1991).
Human external ophthalmomyiasis, ophthalmomyiasis externa
This form of ophthalmomyiasis involves mainly the conjunctiva, the eye lid and is most commonly caused by the larvae of O. ovis (Reingold et al. 1984; Harvey 1986; Heyde et al. 1986; Mazzeo et al. 1987; Amr et al. 1993). The larvae are barely able to penetrate the tissue and do not survive long. Most cases report one larva infestation, but 60 larvae were reported on one occasion (Victor and Bhargva 1998). Larvae were found in the conjunctiva, eye lids, lachrymal sac, and the cornea. The infestation occurs outdoors, in sheepherding areas (Heyde et al. 1986).
Other flies reported to cause ophthalmomyiasis externa are the human botfly, D. hominis, rodent botflies of genus Cuterebra (Wilhelmus 1986; Cogen et al. 1987) and horse botflies of various Gastrophilus species (Medownick et al. 1985). Gedoelstia, normaly a parasite of antelopes, causes a similar type of ocular myiasis in South Africa (Kean et al. 1991) and a case was caused by Sarcophaga crassipalpis (Uni et al. 1999). Clinical signs include; conjunctivitis of variable severity, sensation of suddenly moving foreign body with abrupt itching and lacrimation during warm months in endemic area, even without a history of fly strike. All reported
cases, suffered from oedema, hyperaemia and unspecific irritation of the conjunctiva and some reported purulent conjunctivitis. Also, swollen eyelids with mild to severe oedema of the eye lids and cellulites were described. In addition, haemorrhage, ulceration, pain, larva protruding from an aperture in the eyelid, discharge, excoriation, erythema and laceration of the lacrimal drainage system. Ophthalmomyiasis was reported to associate with Herpes zoster ophthalmicus in a case caused by C. bezziana (Verma et al. 1990) and with short duration pre-septal cellulitis (Bali et al. 2007). Cornea involvement results in the reduction in vision.
Human internal ophthalmomyiasis, ophthalmomyiasis interna
Internal ophthalmomyiasis is most commonly caused by cattle botflies H. bovis and H. lineatum (Mason 1981; Vine and Schatz 1981; Syrdalen et al. 1982; Steahly and Peterson 1982; Edwards et al. 1984). The former is the common species in the cold temperate climatic zone while the latter is more prevalent in the warmer climatic zones, but the areas of distribution of these species overlap (Beaver et al. 1984). When D. hominis larvae enter the eye, signs of visual disturbance, redness of the eyes, haemorrhage of the fundus, retina and other parts of the eye occur and it may lead to unilateral or in severe cases bilateral-blindness. Other reported clinical signs are reversible severe decreased vision or vision loss, floaters (objects in the field of vision that originate in the vitreous), retinal haemorrhages in the funduscopic regions, pain, anterior uveitis and vitritis, mild panuveitis, diffuse stellate keratic precipitates, mild iris heterochromia and atrophy, fine neo-vascularization of the angle, and a mature cataract (Lagacé-Wiens et al. 2008). Also, an ophthalmomyiasis case was associated with Fuchs heterochromic iridocyclitis (Spirn et al. 2006).
Human orbital ophthalmomyiasis
This myiasis is caused by various species of the family calliphoridae. Obligatory species include C. anthropophaga, C. bezziana, W. magnifica, and C. hominivorax. Facultative species include Calliphora vomitoria and C. macellaria (Kean et al. 1991).
Symptoms are caused by the motion, feeding and excretory activity of the larvae and include foreign-body sensation and itching, trauma is the major cause of lachrymal apparatus lesions. Cases are refractive to antibiotics treatments only.
Diagnosis of ophthalmomyiasis is achieved by clinical examination and the use of slit-lamp bio-microscopy, ultrasonography and funduscopic examination.
Treatment is by removal of all larvae. Although some patients extract the fly larva by themselves, larvae may be removed by the cotton swab mounting technique. Suffocation of deeply seated larvae by the use of liberal amounts of topical antibiotic will facilitate their removal. No specific therapy is necessary in some cases. In contrast, surgical extraction may be needed in others. A successful treatment was achieved by oral ivermectin, in addition to antibiotic and topical steroids and cyclo-plegics. The treatment of choice is laser photocoagulation (Currier et al. 1995) or vitrectomy with larva removal and intraocular steroids. Larvae behind the retina could not be photocoagulated. Triamcinolone (0.4 mg) is administered for intraocular inflammation, and antibiotics are given as prophylaxis.
Nasal myiasis
The fly species reported to cause nasal myiasis are; C. bezziana, C. hominivorax, and O. ovis (Zhang et al. 2007). One case was reported to be caused by the fruit fly Drosophila melanogaster (Aydin et al. 2006) and another by Calliphora erythrocephala (Skibsted 1995). Infestation of ear, nose, and throat by the larvae of C. bezziana has been reported from the endemic areas. Among the predisposing factors, atrophic rhinitis is the most common (Kuruvill et al. 2006), followed by leprosy (Thami 1995) and upper respiratory tracts carcinoma (Gopalakrishnan et al. 2008). A case of Non Hodgkins lymphoma of ethmoidal sinus was associated with rhinoorbital myiasis (David et al. 1996).
Also, many nosocomial cases have been reported. The maggots burrow into delicate membranes and feed on underlying structures, causing considerable destruction of tissues, resulting in complications such as extensive erosion of the nose, face, and orbit, with rarely meningitis and death as a result of intracranial involvement (Sharma 1989). Reported complications include; pneumocephalus after atrophic rhinitis with nasal myiasis. Symptoms of rhinal myiasis are the same as in allergic rhinitis (Baldi 1990). Recurrent nasal myiasis was reported and treated successfully by permanent closure of the nostrils (Gupta 1978).
Oral myiasis
Oral myiasis cases have been reported worldwide from Asia, Europe and South America. Most of the cases were described in developing countries and in the tropics, and only rarely in developed countries.
Many fly species cause oral myiasis (Table 68.1). The larvae of W. magnifica were reported to be repeatedly recovered from the mouth and intubation tube of an unconscious patient (Yuca et al. 2005). Infestation may occur directly, by the fly deposition of eggs or larvae or indirectly, by ingestion of contaminated food such as meat. Breast-fed infants may suffer oral myiasis when suckling from mothers with breast myiasis caused by C. anthropophaga (Ogbalu et al. 2006).
A number of underlying medical disorders in patients are associated with oral myiasis. Most described cases had lesions located in the anterior part of the oral cavity, suggesting direct infestation. Other cases involved; the gingiva, lips and the floor of mouth (Droma et al. 2007).
Infestation by multiple larvae is common, though the number of cases is small (Chan et al. 2005). The number of infested larvae in the reported cases, ranged between 3 and > 50 larvae. The age of reported oral myiasis case ranged between 3 and 89 years with a median of 26 years.
Clinically, the patient suffers acute swelling in gingiva, lips, and/or other parts of the oral cavity (Faber and Hendrikx 2006). Although oral myiasis is uncommon, the dental surgeon should be aware of its existence, especially among patients returning from the tropical areas.
Intestinal myiases (Pseudomyiasis)
Reported species of intestinal myiasis where larvae were passed dead or alive on repeated occasions in carefully collected specimens include Eristalis tenax, Musceina stabulans and Leptocera venalicia. Intestinal myiasis may occur by one of the following: eggs or young larvae swallowed with contaminated food or water, faecal specimen may have been contaminated after it was passed and/or retro-infection from eggs or larvae deposited in the anus. The patient may suffer from diarrhoea, vomiting, abdominal pain, colic and fever. Symptoms of gastroenteritis subside after elimination of the larvae.
A whole range of species of diptera have been implicated although how many are cases of genuine parasitism is debatable. Many have undoubtedly arisen through maggots being present in food. During their passage through the gut they may set up some irritation and possibly even tissue damage but they are unable to establish themselves and cannot be considered to be parasitic. In other cases flies, such as Eristalis tenax which normally breed in faeces and rotting matter have laid their eggs around the anus and the larvae feed around the anal orifice and may even move into the rectum. They can cause irritation but they seldom cause physical damage and cannot be looked on as serious parasites. Cases of human myiasis such as these tend to occur among people who neglect personal hygiene through illness, extreme old age or infancy.
Aural myiasis
Aural myiasis is caused by S. haemorrhoidalis, Wohlfahrtia magnifica, screwworms and Lucillia spp. The majority of cases are reported from neonates and children. Cases reported in adults are associated with mental handicap, alcoholics, chronic otitis media, carcinoma and Alzheimer’s disease patients. Symptoms include; purulent and haemorrhagic exudates in the external auditory canal, aural malodour, otalgia, aural itching, roaring sound, tinnitus, furuncle of the external ear, restlessness, and pain (Yuca et al. 2005). The treatment of aural myiasis requires removal of larvae, cleaning affected area with 70% alcohol, 10% chloroform, oil drops, topical ivermectin and normal saline (Yuca et al. 2005).
Uriogenital myiasis
Genuine cases of urinary tract myiasis are rare. Infection presumably occurs when flies oviposit around the urethral meatus. Species most frequently involved is Fannia canicularis (Table 68.1). The clinical signs include; frequent painful urination with pus, mucous and larvae in the urine, painful mixing, and bilateral costo-lumber pain.
Vaginal myiasis is infrequent and usually occurs when poor hygiene is combined with vaginal discharge. Vaginal myiasis has been associated with venereal diseases including trichomoniasis, candidiasis and gonorrhoea.
Cerebral myiasis
Cerebral myiasis is very rare. Three fly species have been described. Two cases involving children were caused by Hypoderma bovis and H. lineatum (Kaleliogˇlu et al. 1989; Semenov 1969). A fatal cerebral myiasis was also caused by D. hominis (Rossi and Zucoloto 1973).
Clinical signs
Clinical signs caused by the larvae vary depending on the causative fly species, and the site of infestation.
Diagnosis
The diagnosis of some myiases is often made by the patient or their carers. Clinical signs may be indicative of some myiasis. Unlike internal myiases, skin myiases are detected by palpation for warble fly in the expected sites. The larvae will appear as nodules of one cm in diameter in the skin which will cause a severe irritation and itching. D. hominis swellings can become itchy and painful, but unless they become infected with bacteria or the larvae enter the eye they are not serious.
Larval collection and preservation
Larvae must be collected from the lesion and include all morphological forms. Divide larvae to be sent to the laboratory to two equal groups. Place one group in water of 90° C for two minutes then transfer to a tube containing 70% alcohol or 10% formalin (Abo-Shehada 2005). Keep the remaining group in a perforated tube.
Label the tubes with the following:
Place of collection,
Species affected,
Date of sample collection,
Name of the veterinarian or physician in charge of the case.
Laboratory rearing of larvae
Larvae of several saprophytic species can be reared simply by putting them on blood agar plates kept at about 30° C. Larvae of most obligate parasitic species require special techniques of rearing.
Immunodiagnostic tools
Many tests (e.g. ELISAs) are easy and affordable tools for the detection of many myiasis-causing larvae on living animals, especially when larvae are undergoing migration and hence otherwise undetectable (rev. in Otranto 2001). However, information on the value of these methods for the diagnosis of nasal and gastrointestinal myiasis is unsatisfactory (Otranto 2001). Likewise, the value of immunodiagnosis of human myiases is questioned.
Other techniques used in myiasis diagnoses
Some techniques were reported to help in diagnosis of myiasis. The use of ultrasound in confirming the larval size and determine method of removal was described (Bowry and Cottingham 1997). The presence of O. ovis larvae in sheep sinuses can be detected by using rhinoscope (estroscope) and a third instar larvae were resolved after endoscopic examination of a nasal infestation (Badia and Lund 1994).
Fly identification
Morphological identification of the myiasis producing fly using early larval stages is very difficult. Identification keys for myiases producing flies are available (Zumpt 1965).
Molecular identification
To overcome the constraints of the classical morphological identification of some myiasis flies highly sensitive molecular assays were developed. Hypervariable DNA regions internal to some mitochondrial and nuclear ribosomal genes were used for the molecular identification of larvae belonging to the families oestridae (Otranto et al. 2003a,b; Otranto and Traversa 2004) and calliphoridae (Stevens and Wall 2001). Molecular identification using the mitochondrial encoded 12S rRNA, COI and COII sequences was achieved for L. cuprina and L. sericata (Stevens and Wall 1996). Similarly, the D1–D7 region of the nuclear encoded 28S rRNA sequences were used to identify C. vicina and C. vomitoria (Stevens and Wall 2001). Mitochondrial and nuclear genes of the four Rhinoestrus morphotypes affecting equids in Italy have been genetically characterized (Otranto et al. 2005a) and a semi-nested PCR assay employing mitochondrial genetic markers were used as molecular diagnostic tool in live animals.
A PCR-RFLP assay was used to differentiate between H. bovis and H. lineatum using the cytochrome oxidase I (COI) gene and restriction enzymes (Otranto et al. 2003) and similar assay was produced for C. hominivorax and C. macellaria. Also, PCR-RFLP assay provided a DNA-based method for identifying C. hominivorax individuals with a mutation in the esterase gene associated with organophosphate resistance (Carvalho et al. 2006).
As R. purpureus may cause ophthalmomyiasis in humans (Peyresblanques 1964), a seminested PCR assay employing a hyper-variable fragment (200 bp) internal to the Rhinoestrus cox1gene encoding the region spanning from external loop 4 (E4) to the carboxy terminal (–COOH), was reported to differentiate between larvae of the two species. The fly DNA was extracted from nasal cotton swab samples.
Treatment
An effective treatment strategy consisted of mechanical removal of larva(e), dressing the affected tissues, and preventing re-infestation and secondary infections. Applying the treatment strategy will vary according to the infestation site. The complete removal of all larvae is essential. A foreign body response may occur against any part of the larvae remaining in the surgical site.
In superficial cases of myiasis, the larvae may be removed by irrigation and/or picked up with a cotton swap or forceps. Larvae in subcutaneous tissue can often be removed through a small incision after preliminary anesthesia of both host and parasite.
Deep infestations around the nose, eyes and ears require specialized surgical treatment. Wound occlusion and suffocation of deeply seated larvae can be achieved by the use of liberal amounts of topical antibiotics. The shape of D. hominis larvae and their curved body spines makes them difficult to extract. Covering the breathing hole of D. hominis with petroleum jelly, grease, fat, or Vaseline induce the larvae to force their own way out of the skin.
The treatment of oral myiasis is by surgical debridement under local anesthesia. Methods of wound occlusion and larvae suffocation were used in the treatment of cutaneous myiasis. Those methods aim at preventing air from the infesting larvae. Application of such methods may shift the aerobic larvae into a more superficial position where it is possible to remove them with ease and less tissue damage (Meinking et al. 2003). These methods are not easily applicable in the oral cavity. So far, lavage and surgical debridement are the only available treatment of choice for oral myiasis.
The patient’s management include:
Surgical exploration and search for larvae,
Removal of all larvae and necrotic tissues,
Topical application of gentian violet,
Oral therapy with ivermectin (6 mg orally),
Patient referred to plastic surgery to repair tissue damage.
Intestinal infestation usually responds to hexylresorcinol or tetrachlorethylene followed by purgation (Morris et al. 1996).
In cutaneous myiasis, the site of infestation may facilitate the entry of Clostridium tetani while removing the larvae using contaminated instruments and therefore vaccination is recommended. Research has shown that doramectin is capable of preventing infestation of wounds for at least 14 days after treatment.
Although many insecticides will kill C. hominivorax larvae, most of these require repeated applications before healing occurs. Under extensive grazing regimes, such as those practiced in parts of the Americas, treatment of individual animals is not practical.
Control and prevention
Provision of effective veterinary services and environmental hygiene are vital for the control and prevention of myiases in man. The veterinary services will provide the measures of controlling major animal diseases with cutaneous and natural orifices inflammation, e.g. FMD and diarrhoeal diseases and causes of wounds. Also, such services will provide treatment and prevention of specific myiasis producing fly infestation, e.g. O. ovis. In addition, the education of farmers to adopt the essential regular animal inspection for early detection of myiasis cases. Proper waste disposal will minimize the alternative breeding sites for the facultative myiasis producing flies, e.g. blowflies.
Quarantine measures, and international and regional cooperation
These measures aim to prevent the spread of fly species, such as screwworm flies, from endemic to non-endemic countries. This is especially important during period of mass importation of animals. For example during the annual Hajj season around seven million livestock are imported to Saudi Arabia over a 2 to 3 weeks period from all over the world including screwworm endemic countries. Inspection of animals at ports of entry and insect control in ships and planes are important measures of control. Animal movements must be controlled during screwworm myiasis outbreaks.
Control of D. hominis has always been similar to that of other fly myiases and involves treatment of cattle with organophosphate or organochlorine insecticides. Trials of doramectin suggest that it may be a more effective and less toxic replacement. Treatment of human cases usually involves surgical removal of the larvae. Chemical control using effective insecticides is vital to reduce the number of flies and mass treat myiasis in infected farm animals. Regular animal inspection for myiasis cases must be done routinely in endemic countries, especially during outbreaks. The control of myiasis in wild animals is a difficult task.
The insect sterilization technique
Insect sterilization technique, also called sterile insect technique (SIT) is a proven effective biological method of control. As a biological method, SIT has attracted a great deal of interest for use in blowfly control because of increasing resistance to available insecticides as well as strict limits on the residual level of insecticides on wool imposed by the European Union. SIT has been proven to be effective in the field for the area-wide control of some insects (Knipling 1960; Krafsur 1998). SIT involves mass-rearing of insects that are then sterilized and released in sufficient numbers. This results in most of the wild females mating with the released sterile males and thus producing non viable eggs. This can result in suppression and subsequent elimination of the target insect population. For C. capitata, SIT has been shown to be most effective if only sterile males are released in the field (McInnis et al. 1994). The use of genetic engineering with the aim of developing a system for controlling female viability in a strain of L. cuprina that would allow a male-only sterile release program was attempted (Scott et al. 2004).
It may prove possible to eliminate or at least control some species by sterile male release and research was conducted towards this end in Australia. C. bezziana does not yet occur in Australia but it is present in Papua New Guinea and there is a real risk that it will be introduced in the near future.
The first major implementation of SIT was in the New World screwworm (NWS) Eradication Program, that successfully eliminated the NWS, from the Continental US, Mexico and much of Central America. Currently, ionizing radiation is used for sterilizing insects, but the safer, more cost-effective transgenic insect techniques could replace this method. Genetic transformation methods (GTM) have been demonstrated in NWS. GTMs help to identify genes and examine gene function in NWS (Allen et al. 2004).
C. hominivorax is restricted principally to North and South America, and the Caribbean Islands. An outbreak of NWS occurred in Libya during the late 1980s but this was eradicated using the sterile male release technique. Educating the public regarding myiasis may help preventing human myiasis (Abdo et al. 2006).
A significant number of human myiasis cases are acquired in nursing homes. Carers of the old and debilitated should be made aware of myiasis prevention measures, especially for those on tube feeding. The use of window screens and electrocuters in nursing homes should be adopted to prevent flies access and kill flies that do enter (Chan et al. 2005).
Medical personnel taking care of old or debilitated patients need to bear in mind the possibility of C. bezziana infestation to be able to make a prompt diagnosis and implement relevant intervention to prevent extensive tissue destruction (Chan et al. 2005).
Maggot therapy (Biosurgery)
Fly larvae can be used medically for the treatment of chronic (slow-healing) or badly-infected wounds. The intentional use of maggots to clean infected wounds has been practised for many years. Their use was first championed during the American Civil War and there was another burst of popularity during the 1920s and 1930s for the treatment of thousands of ex-soldiers from the First World War. The development of antibiotics in the 1940s saw a general demise in the use of maggot therapy (Chen et al. 2007). In the late 1990s, its value became increasingly recognized, at least in the UK, owing to problems of antibiotic resistance and methicillin resistant Staphylococcus aureus (MRSA). In the UK, maggot debridement therapy increased from two treatments a month in 1996 to more than 200 treatments per week in 2007. An estimated 30,000 people have been treated with sterile maggots since the mid 1990s and the demand is growing rapidly throughout the world.
The continual movement of the maggots was thought to stimulate the body to produce serous exudates that flush bacteria from the wound, and healing granulation tissue from viable cells. Likewise, the probing from the hooks was postulated to facilitate wound debridement. Recently, three proteolytic enzyme classes were identified in the maggot execrations/secretions (ES). The ES enzymes are capable of effective wound matrix digestion (Chen et al. 2007). The maggot ES also have inhibitory effect on bacteria including MRSA. In addition to the ammonia secreted by maggots is believed to increase the wound pH and hinder bacterial growth (Robinson 1940). Maggots also feed on and kill bacteria (Mumcuoglu et al. 2001). The ES have various substances which appear to enhance wound healing. For example, in vitro studies on cell cultures have identified substances capable of enhancing the proliferation and growth of human fibroblasts (Horobin et al. 2005).
In the UK, the main centre using maggot therapy is Bridgend General Hospital in South Wales. Currently, Bridgend-based biosurgical company ZooBiotic, is the only supplier of pharmaceutically produced maggots to the healthcare sector in UK and internationally.
Lucilia sericata is the species of fly used most frequently. The larvae are reared under stringently controlled conditions in three rooms. The adult flies are kept in a special room. The eggs are sterilized under aseptic conditions in another and the third room for breeding the larvae. The eggs are deposited on raw liver. Eggs are then transferred to flasks containing a sterile nutrient on which, after hatching, the larvae grow. When the larvae reach the required size (2 mm) they are tested for sterility by incubation in Tryptone Soya Broth and Thioglycollate Broth.
The larvae are applied to the wound in specially designed dressings which confine the larvae and protect the healthy skin from ES. After about 3 to 5 days the larvae reach about 13 mm and they are removed from the wound and destroyed. Some patients may require further treatment, and a fresh batch of larvae is applied.
Biosurgery has proved successful in the treatment of leg and pressure ulcers, wounds associated with diabetes, and many other types of infected wounds. While conventional treatments for these wounds can take months to achieve a successful outcome, maggot therapy usually takes one or two treatments, each lasting 5 days. Thus, it dramatically reduces treatment times and the associated costs (Bonn 2000). Evidence also suggests that it is successful in combating MRSA (Gupta 2008).
Forensic entomology
Another beneficial application of myiasis knowledge is in the field of forensic medicine. Insects including necrophagous dipteran species of the families; Calliphoridae, Fannidae, Muscidae and Sarcophagidae are attracted to the dead carcass within minutes. The presence of larvae on the dead body will provide a mean to estimate the postmortem interval (PMI). The minimum PMI is determined by the age of the insect stage. Now knowledge of myiases producing flies is accepted in many countries as a forensic tool (Amendt et al. 2004).
References
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