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Vol. 11 No.2 (2019)

The Journal of Medical Entomology and Parasitology is one of the series issued quarterly by the Egyptian Academic Journal of Biological Sciences. It is an important specialist journal covering the latest advances in that subject. It publishes original research and review papers on all aspects of basic and applied medical entomology, parasitology and host-parasite relationships, including the latest discoveries in parasite biochemistry, molecular biology, genetics, ecology and epidemiology in the content of the biological, medical entomology and veterinary sciences. In addition to that, the journal promotes research on the impact of living organisms on their environment with emphasis on subjects such a resource, depletion, pollution, biodiversity, ecosystem…..etc.

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Citation: Egypt. Acad. J. Biolog. Sci. (E-Medical Entom. & Parasitology Vol.11(2) pp 25-32(2019)

Egypt. Acad. J. Biolog. Sci., 11 (2):25 – 32 (2019) Egyptian Academic Journal of Biological Sciences E. Medical Entom. & Parasitology

ISSN: 2090 – 0783 www.eajbse.journals.ekb.eg

A Brief Review of Myiasis with Special Notes on the Blow ’ Producing Myiasis (F.: )

Eslam M. Hosni*; Mohamed A. Kenawy; Mohamed G. Nasser, Sara A. Al-Ashaal and Magda H. Rady Department of Entomology, Faculty of Science, Ain Shams University, Abbassia, Cairo 11566, Egypt E-mail: [email protected] ARTICLE INFO ABSTRACT Article History One of the most interesting and sophisticated relations that seen in Received:26/8/2019 nature is myiasis which represents the relation between these tiny small Accepted:25/9/2019 larvae of Diptera and another living creature where these larvae feed on ______its tissues. Several previous works discussed the issue of myiasis from Keywords: different aspects. In this work, a brief and comprehensive review of Myiasis, Flies, myiasis including classification of its types, classification of dipterous Calliphoridae, Diptera. larvae that cause it and special notes on family Calliphoridae and its role in causing myiasis. . INTRODUCTION In nature, the relationships among living organisms are very complicated. Significant observations and continuous surveillance allow us to understand this complexity. One of these relations is the association between flies and targeted vertebrate hosts. Although the apparent difficulty, the association could simply be either detrimental or beneficial (Hall and Wall, 1995). Earlier in 1815, Kirby and Spence were the first to use the term “scholechiasis” to describe the diseases caused by larvae. Then in 1840, Hope conceived a new term “Myiasis” which defines the invasion of human and animal bodies with dipterous larvae and referred the terms “scholechiasis” and “canthariasis” to the disease caused by larvae of Lepidoptera and Coleoptera, respectively (Hall and Wall, 1995). Later, De la Torre-Bueno (1937) indicated, in Glossary of Entomology, that myiasis is "The disease or injury caused by the attack of dipterous larvae". Zumpt (1965), gave the practical and accurate definition of term myiasis as " The infestation of live human and vertebrate with dipterous larvae, which, at least/or for a certain period, feed on the host’s dead or living tissue, liquid body- substances, or ingested food”. Myiasis is considered a neglected disease with great economic impacts on animals and humans (Hall et al., 2016). From ancient times till recent days myiasis causing flies occupied Holarctic and Holotropic regions. The power of this widespread is referred to a wide variety of hosts from wild and domestic animals and even humans (Francesconia and Lupi, 2012). Myiasis is widespread throughout the world especially the tropical regions. It usually occurs in both domestic and wild animals and incidentally in humans under certain conditions (Hall and Wall, 1995 and Hassona et al., 2014).

Citation: Egypt. Acad. J. Biolog. Sci. (E-Medical Entom. & Parasitology Vol.11(2) pp 25-32(2019)

26 Eslam M. Hosni et al.

In animals, the odor of infected wounds, producing such condition was performed on decayed organic matters, urine, and feces PubMed and Research Gate documents and attract gravid females to lay their eggs. internet-based articles. In addition, several Then the voracious larvae consume necrotic related web pages were accessed. A total of tissues and pervade healthy ones producing 28 articles were included in this review. deep injury (Zumpt, 1965). In humans, RESULTS AND DISCUSSION although the infestation is rare; about 165 Classification of Myiasis: cases of human myiasis were reported from Two main ways for myiasis 1914 till 2014 (Sing and Sing, 2015). The classification: (1) The Anatomical way predisposing factors like low socioeconomic (Table 1) which is based on infested parts of status, poor hygiene, mental regardless the host's body. It was first proposed by patients without care and drug addicts bishop in 1922 and modified by James in increase the disease incidence. Moreover, the 1947 then by Zumpt in 1965 (Gour et al., pathogenicity of myiasis is asymptomatic 2017) and (2) The Ecological (Biological or and may lead to death due to septicemia and Parasitological) way (Table 2) according to toxemia (Singh and Singh, 2015). the host-parasite relationship or level of This review is objected at providing dependence between dipterous larvae and information related to the types of myiasis hosts (Zumpt, 1965 and Hall and Wall, and its causing flies. Due to the economic 1995). The former classification gives a short and health impacts of this injury to both cut to identify the accused fly species, but animals and humans, efforts have to be the later one portrays the biology of the fly intensified toward control of such fly pests. and permits understanding the evolution of MATERIALS AND METHODS myiasis habit (Hall and Wall, 1995). A review of the available published and unpublished reports on miyasis and flies

Table 1: Anatomical classification of Myiasis; after Hall and wall (1995)

A Brief Review of Myiasis with Special Notes on the Blow Flies’ Producing Myiasis 27

Table 2: Biological (Parasitological or Ecological) classification of myiasis, after Hall and Wall (2016)

Biological (Ecological or Parasitological) Piophila casei (Cheese skipper) and Classification of Myiasis: Tubifera tenax (Rat-tailed maggot) The causing flies are classified into (Kenawy, 2008). three categories: 03. The pseudo- or accidental myiasis 01. The obligatory or specific myiasis produces are those free-living producers which develop only on nonparasitic larvae that are live hosts (Zumpt, 1965 and Hall and accidentally swallowed (Zumpt, Wall, 1995). Such flies select various 1965). Flies of family Muscidae are host organs or tissues in which they common in causing such false deposit eggs or larvae. Examples of myiasis (Nagakura et al., 1991). such flies are Wöhlfartia magnifica Anatomical Classification of Myiasis: and W. vigil (Flesh flies), Oestrus 01. Sanguinivorous Myiasis: This term ovis (Sheep bot fly), Hypoderma concerning dipterous larvae with bovis (Warble fly),Gasterophilus voracious behavior towards blood. intestinalis (Horse bot fly), They are ectoparasitic and able to Cochliomyia hominivorax (New- initiate obligatory myiasis. world screwworm) and Chrysomya Chrysomya bezziana and bezziana (Old-world screw-worm) Auchmeromyia luteola (Congo floor and Dermatobia hominis (Human bot maggot) (Calliphoridae) and fly or the Torsalo) (Kenawy, 2008). Dermatobia hominis (Oestridae) are 02. The facultative or semi-specific sanguinivorous fly larvae (Zumpt, myiasis producers (opportunistic) 1965). which develop on both living and 02. Cutaneous (Wound, Traumatic, decayed organic matters under three Dermal or Sub-dermal) Myiasis: is levels: primary wherein the larvae are the most frequent type of myiasis able to initiate myiasis or secondary (Visciarelli et al., 2007). In this and tertiary when the host becomes condition, obligatory myiasis near the death (James, 1947). Flies dipterous larvae feed on animal tissue attack filthy infected wounds, (epidermis and dermis layers) stimulated by the odor and do not causing wounds. These wounds or attack clean wounds or intact skin. trauma, either caused by or Examples of these flies are others, attract other obligatory or Calliphora spp. (Bluebottle flies) and facultative parasites to cause myiasis Lucilia spp. (Greenbottle flies), (Zumpt, 1965). Flies of families Sarcophaga spp. (Flesh flies), Calliphoridae and Sarcophagidae like 28 Eslam M. Hosni et al.

Cochliomyia hominivorax, Lucilia This type usually receives its name sericata, and Wohlfahrtia magnifica from the anatomical region affected could produce dermal and wound (Francesconia and Lupi, 2012). myiasis (Gour et al., 2017). 06. Ocular (Ophthalmic) Myiasis: 03. Furuncular (Warble) Myiasis: is occurs due to the infestation of host considered a type of cutaneous eyes by dipterous larvae. Eye myiasis and occurs after penetration infestation could be internal, external of the healthy skin by dipterous or in the orbital part. Ophthalmo- larvae causing furuncular lesion or myiasis interna occurs when the nodes. The furuncular lesion is a infestation including the anterior and nodule with a central pore that posterior segment of the eyeball exudates a purulent fluid after larval (Jakobs et al., 1997). In Ophthalmo- infestation. The number of maggots myiasis externa, the infestation is in the furuncular nodes varies restricted to superficial ocular tissues. according to fly species Red eyes, eye pain, and vision loss (Francesconia and Lupi, 2012). The are described as symptoms of Ocular erythematous lesion, pruritus, myiasis (Anane and Hssine, 2010). movement sensation, Chrysomya bezziana, Dermatobia hyperpigmentation, fluid leak from hominis, Lucilia spp. and Cuterbera nodes and night pain are reported as spp. are the common agents of ocular symptoms of furuncular myiasis myiasis (Francesconia and Lupi, (Mahal and Sperling, 2012). The 2012). number of lesions and their 07. Oral Myiasis: was first described by distribution patterns are fly species- Laurence (1909). The incidence of dependent. Cordylobia oral myiasis is associated with poor anthropophaga, Dermatobia hominis, oral hygiene, alcoholism, mental Wohlfahrtia vigil, Wohlfahrtia disability and other clinical forms magnifica, and Cuterebra sp. are like oral trauma and gingival diseases common agents of furuncular myiasis (Hassona et al., 2014). Also, people (Robbins and Khachemoune, 2010). whose mouth remains open for a long 04. Migratory (Creeping) Myiasis: time are susceptible to Oral myiasis occurs when the maggots start to (Sharma et al., 2008). Swelling of migrate for a distant in the host skin mouth, lips and gingival was reported and burrow in it causing obvious as symptoms of Oral myiasis. The migratory lesions. This migration reported species are Chrysomya produces ulcerated epithelium and bezziana, Cochliomyia hominivorax, causes inflammation in dermis layer. Musca domestica, Wohlfahrtia The larvae then diagnosed in the magnifica and Calliphora vicina fibrous cystic sinus tract in dermis (Hassona et al., 2014). layer (Gour et al., 2017). Hypoderma 08. Aural (Otom) Myiasis: includes the bovis (Cattle bot fly) and infestation of the ear by dipterous Gasterophilus intestinalis (Horse bot larvae. Female flies oviposit eggs or fly) are common agents of migratory larvae around the aural cavity (Uzun or creeping myiasis. Unintentionally, et al., 2004). Symptoms vary from humans could be infested by cattle itching, inflammation of auditory and horse bot flies but, the larvae are canal, aural pain to otorrhea and unable to complete their life cycle in bleeding. The most common species human skin (Royce et al., 1999). that cause aural myiasis are 05. Cavity Myiasis: is an infestation of Chrysomya bezziana, Chrysomya body cavities by dipterous larvae. megacephala, Cochliomyia A Brief Review of Myiasis with Special Notes on the Blow Flies’ Producing Myiasis 29

hominivorax and Wohlfahrtia 12. Cerebral Myiasis: is rare, fatal, and magnifica (Francesconia and Lupi, survival rates are low (Terterov et al., 2012). 2010). Species of Hypoderma bovis 09. Nasal Myiasis: occurs when female and Hypoderma lineatum were flies deposit their larvae in the nasal discriminated to cause cerebral cavity while the host is sleeping. In a myiasis (Francesconia and Lupi, study about 252 peoples older than 2012). 50 yrs. were suffering from nasal Calliphoridae and Other Dipterous myiasis (Francesconia and Lupi, Families as Myiasis Producing Agents: 2012). Low socioeconomic status and Order Diptera (Tru flies) currently poor hygiene are predisposing factors includes more than 150,000 described of larval invasion (Francesconia and species in 10,000 genera and about150 Lupi, 2012). Nasal pain, movement families (Pape and Thompson, 2010). sensation, anosmia, nasal discharge, About thirteen families of this order and nasal bleeding are common signs compress all myiasis causing flies. These are of nasal myiasis (Tsang and Lee, Calliphoridae, Oestridae, Sarcophagidae, 2009). Chrysomya bezziana, Muscidae, Gastrophilidae, Phoridae, Cochliomyia hominivorax, Oestrus Drosophilidae, Psychodidae, Stratiomydae, ovis, Lucilia sericata, Wohlfahrtia Scenopinidae, Syrphidae, Piophilidae and magnifica Drosophila melanogaster Dryomyzidae (Singh and Singh, 2015) of and Cephalopina titillator (Camel bot which three families are the major ones: The fly) are the main agents of nasal first one is family Oestridae which contains myiasis (Francesconia and Lupi, 151 species in 28 genera. All species are 2012). obligate parasites in their larval stages. The 10. Intestinal (Enteric) Myiasis: is second family is Sarcophagidae with 2000 widespread in animals rather than species in 400 genera and the third family is humans where the alimentary tract of Calliphoridae (Hall and Wall, 1995). About the mammals from pharynx to anus 80 species of Sarcophagidae and harbors larvae. Symptoms vary from Calliphoridae have been recorded to cause asymptomatic cases to nausea, myiasis (Hall and Wall, 1995). vomiting, abdominal pain and rectal Calliphoridae (blow flies, carrion bleeding (Karabiber et al., 2010). flies, bluebottles, greenbottles, cluster flies) Gasterophilus intestinalis is the (Table 3) is one of the most common and common maggot causing enteric interesting families of Diptera. It is classified myiasis (Singh and Singh, 2015). into 6 subfamilies with 150 genera and about 11. Urinogenital Myiasis: is the 1000 species. Calliphorid flies are infestation of urinogenital area of the characterized by their metallic bodies with host by dipterous larvae. The most blue and green color, while some species are common symptoms are lumbar pain, dull. The members of this family are ureteric obstruction, and dysuria. performing several environmental services The causing flies are Wohlfahrtia including, but not limited to decomposing of magnifica, Sarcophaga dead animal bodies and pollination (Shafqat haemorrhoidalis, Fannia canicularis et al., 2016). On the other hand, several and Sarcophaga carnaria species of the family have medical and (Francesconia and Lupi, 2012). veterinary importance (Stevens, 2003).

30 Eslam M. Hosni et al.

Table 3: Prominent myiasis causing species of family Calliphoridae; after Francesconia and Lupi (2012) Species Parameters Status Description Cochliomyia hominivorax Distribution Through tropical and temperate zones of US, Caribbean (New-World Screwworm) and Latin America. Classification Obligatory wound myiasis. Hosts Mammals. Human Myiasis Cause human wound myiasis and destroy the underlying tissues because of the screw-like feeding fashion of maggots. Chrysomya bezziana Distribution Prefers tropical and subtropical climates and (Old-world Screwworm) widespread throughout tropical Africa, Middle East region, Indian sub-continent, from south-east Asia to China, and from the Philippines to Papua New Guinea. Classification Obligatory wound myiasis. Hosts Sheep and human. Human Myiasis Human wound myiasis cases were reported in a poor region in Africa and Indian sub-continent. Chrysomya megacephala Distribution Has a worldwide distribution especially in Oriental and Australasian regions. Classification Facultative wound myiasis. Hosts Decomposing flesh and feces. Human Myiasis Wound and aural myiasis. Has forensic importance. Chrysomya albiceps and Distribution Native species in Australia. Chrysomya rufifacies Classification Facultative wound myiasis flies. Hosts Primary and secondary myiases in humans and other animals. Human Myiasis Wound and Nasal myiasis. Has forensic importance. Auchmeromyia senegalensis Distribution Mainly distributed in Sub-Saharan Africa. (Congo floor maggot) Classification Sanguinivorous myiasis. Hosts Mammals. Human Myiasis Suck human blood. Lucilia serricata and Distribution Lucilia serricata in North America and Europe and Lucilia cuprina Lucilia cuprina in South Africa and Australia. Classification Facultative wound myiasis. Hosts Prefer dead tissue of sheep and sometimes feed on living tissue. Human Myiasis Facultative wound myiasis. Calliphora sp. Distribution Has a worldwide distribution. Classification Facultative myiasis. Hosts Decomposing flesh of carrions Human Myiasis Calliphora vicina is primary invader causing oral, aural, nasal, intestinal, urinogenital and wound myiasis. Calliphora hilli cause ocular myiasis. Cordylobia anthropophaga Distribution Sub-Saharan Africa and Portugal.. (Tumbu fly) Classification Obligatory cutaneous myiasis Hosts Wild mammals and domestic animals Human Myiasis Furuncular myiasis Cordylobia rodhaini Distribution Tropical Africa especially in humid forests.. (Lund’s fly) Classification Obligatory cutaneous myiasis. Hosts Forest mammals particularly rodents. Human Myiasis Occasionally cause furuncular myiasis Phormia regina and Distribution The northern area of Tropic cancer. Protophormia terranovae Classification Facultative wound myiasis. Hosts Decomposing flesh and Protophormia terranovae is a serious parasite of cattle, sheep, and reindeer Human Myiasis Phormia regina is facultative wound myiasis and has forensic importance.

A Brief Review of Myiasis with Special Notes on the Blow Flies’ Producing Myiasis 31

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ARABIC SUMMARY

مراجعه موجزه وشامله لظاهره التدويد مع القاء الضوء علي الذباب النافخ والتابع لعائله الخوتعيات إسالم محمد حسني؛ محمد أمين قناوي؛ محمد جمال الدين ناصر؛ ماجده حسن راضي قسم غلم الحشرات – كلية العلوم – جامعة عين شمس، العباسيه، القاهره 66566، مصر

تعتبر ظاهره التدويد واحدة من العالقات األكثرتعقيدا و إثارة لالهتمام في الطبيعه. وذلك لطبيعه العالقه المركبه بين طرفين ؛االول هو يرقات الذباب والطرف االخر هو االنسجه الحيه التي تتغذي عليها من العائل الحي. وقد ناقشت العديد من االبحاث العلميه السابقة ظاهره التدويد من جوانب مختلفة. ويعد هذا العمل مراجعة موجزة وشاملة لظاهره التدويد بما في ذلك االقسام واالنواع المختلفه لتلك الظاهره وكذلك ، تصنيف يرقات الخوتعيات من رتبه ثنائيات االجنحه و المسببه لظاهره التدويد.