Abstract
Myiasis refers to the infestation of living humans and vertebrates with fly larvae that feed on necrotic or vital tissue of the host. Since the invasion of new fly species in Europe is currently being observed, which live obligatorily parasitically or are close relatives of such species, the aim of this study is to obtain a global overview of the distribution of myiasis-causing fly species in times of climate change and to assess the possible consequences for Western Europe. A systematic literature search was conducted using Pubmed/Medline for the years 1997 to 2017 and a total of 464 international case reports from 79 countries were evaluated. The described cases were caused by 41 different species. In 99.4% of the cases, it was a colonization by just one species, a maximum of three species were detected in a human. Casuistics from Western Europe mostly describe myiasis as a “holiday souvenir” from tropical regions. Reports of autochthonous cases are rare in comparison to other regions. With regard to rising temperatures and the invasion of new fly species, a noticeable increase in the number of cases in Western Europe is to be assumed, which could be an increasing problem in the clinical area and in care, which is why thorough monitoring for professional identification and treatment seems important in the future.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
04 January 2019
It was brought to the authors’ attention that a citation within the published article was cited incorrectly.
References
Amendt J (2013) Insektenbefall lebender Menschen – Zeichen der Vernachlässigung. In: Klinisch-forensische Medizin. Springer Vienna, Vienna, pp 493–497
Batista-da-Silva JA, Borja GEM, Queiroz MMC (2011) Patient with tracheostomy parasitized in hospital by larvae of the screwworm, Cochliomyia hominivorax. J Insect Sci 11:1–7. https://doi.org/10.1673/031.011.16301
Bäuerle L, Kanitz U, Laurich S, Naumovska K, Fröb D, Krebs O, Wilkens A, Püschell K (2014) Fliegenmadenkrankheit (Myiasis) bei Verwahrlosung alter/kranker Menschen. Arch Kriminol 234:183–192
Bernhardt V, Finkelmeier F, Tal A, Bojunga J, Derwich W, Meier S, Lux C, Verhoff MA, Amendt J (2018) Multispecies blow fly myiasis combined with hypothermia in a man assumed to be dead. Parasitol Res 117:579–583. https://doi.org/10.1007/s00436-017-5691-8
Bonn D (2000) Maggot therapy: an alternative for wound infection. Lancet 356:1174. https://doi.org/10.1016/S0140-6736(05)72870-1
Campbell-Lendrum D, Manga L, Bagayoko M, Sommerfeld J (2015) Climate change and vector-borne diseases: what are the implications for public health research and policy? Philos Trans R Soc Lond B Biol Sci 370:20130552. https://doi.org/10.1098/rstb.2013.0552
Čeřovský V (2011) Lucifensin, a peptide behind the maggot therapy. In: Collection Symposium Series Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Prague, pp 22–26
Chan JCM, Lee JSW, Dai DLK, Woo J (2005) Unusual cases of human myiasis due to old world screwworm fly acquired indoors in Hong Kong. Trans R Soc Trop Med Hyg 99:914–918. https://doi.org/10.1016/j.trstmh.2005.06.020
Chan QE, Hussain MA, Milovic V (2012) Eating out of the hand, maggots – friend or foe? J Plast Reconstr Aesthetic Surg 65:1116–1118. https://doi.org/10.1016/j.bjps.2012.01.014
Çiftçioğlu N, Altintaş K, Haberal M (1996) A case of human orotracheal myiasis caused by Wohlfahrtia magnifica. Parasitol Res 83:34–36. https://doi.org/10.1007/s004360050203
Clyti E, Nacher M, Merrien L, el Guedj M, Roussel M, Sainte-Marie D, Couppié P (2007) Myiasis owing to Dermatobia hominis in a HIV-infected subject: treatment by topical ivermectin. Int J Dermatol 46:52–54. https://doi.org/10.1111/j.1365-4632.2006.03028.x
Curtis SJ, Edwards C, Athulathmuda C, Paul J (2006) Case of the month: cutaneous myiasis in a returning traveller from the Algarve: first report of tumbu maggots, Cordylobia anthropophaga, acquired in Portugal. Emerg Med J 23:236–237. https://doi.org/10.1136/emj.2005.028365
Durão C, Barros A, Campos P (2017) A rare case of digital myiasis. J Infect Public Health 10:886–887. https://doi.org/10.1016/J.JIPH.2016.11.002
Dutto M, Bertero M (2011) Cutaneous superficial myiasis: report of a rare nosocomial parasitic disease caused by Sarcophaga spp. (Diptera, Sarcophagidae). Cent Eur J Public Health 19:232–234
Dutto M, Pellegrino M, Vanin S (2013) Nosocomial myiasis in a patient with diabetes. J Hosp Infect 83:74–76. https://doi.org/10.1016/j.jhin.2012.08.019
Emerson PM, Lindsay SW, Walraven GEL, Faal H, Bøgh C, Lowe K, Bailey RL (1999) Effect of fly control on trachoma and diarrhoea. Lancet 353:1401–1403. https://doi.org/10.1016/S0140-6736(98)09158-2
Emerson PM, Bailey RL, Mahdi OS, Walraven GEL, Lindsay SW (2000) Transmission ecology of the fly Musca sorbens, a putative vector of trachoma. Trans R Soc Trop Med Hyg 94:28–32. https://doi.org/10.1016/S0035-9203(00)90427-9
Francesconi F, Lupi O (2012) Myiasis. Clin Microbiol Rev 25:79–105. https://doi.org/10.1128/CMR.00010-11
Giangaspero A, Traversa D, Trentini R, Scala A, Otranto D (2011) Traumatic myiasis by Wohlfahrtia magnifica in Italy. Vet Parasitol 175:109–112. https://doi.org/10.1016/j.vetpar.2010.09.028
Graham JP, Price LB, Evans SL, Graczyk TK, Silbergeld EK (2009) Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Sci Total Environ 407:2701–2710. https://doi.org/10.1016/j.scitotenv.2008.11.056
Grassberger M (2002) Fliegenmaden: Parasiten und Wundheiler. In: Aspöck H (ed) Amöben, Bandwürmer, Zecken... Parasiten und parasitäre Erkrankungen des Menschen in Mitteleuropa. Biologiezentrum des OÖ. Landesmuseums, Zürich, pp 507–532
Grassberger M, Fleischmann W (2002) The biobag - a new device for the application of medicinal maggots. Dermatology 204:306. https://doi.org/10.1159/000063369
Grassberger M, Friedrich E, Reiter C (2003) The blowfly Chrysomya albiceps (Wiedemann) (Diptera: Calliphoridae) as a new forensic indicator in Central Europe. Int J Legal Med 117:75–81. https://doi.org/10.1007/s00414-002-0323-x
Grzywacz A, Prado Castro C (2012) New records of Fannia Robineau-Desvoidy (Diptera: Fanniidae) collected on pig carrion in Portugal with additional data on the distribution of F. conspecta Rudzinski, 2003
Hall MJR, Smith KGV (1993) Diptera causing myiasis in man. In: Medical insects and arachnids. Springer Netherlands, Dordrecht, pp 429–469
Hall M, Wall R (1995) Myiasis of humans and domestic animals. Adv Parasitol:257–334
Hall MJR, Wall RL, Stevens JR (2016) Traumatic myiasis: a neglected disease in a changing world. Annu Rev Entomol 61:159–176. https://doi.org/10.1146/annurev-ento-010715-023655
Hiraoka H, Ozawa T, Sowa-Osako J, Ichimura T, Kimata-Teramoto I, Isozumi R, Kaneko A, Tsuruta D (2015) Repeated myiasis in a female vulvar squamous cell carcinoma caused by Lucilia sericata and Sarcophaga crassipalpis. J Dermatol 42:840–841. https://doi.org/10.1111/1346-8138.12911
Hogsette JR, Amendt J (2008) Flies. In: Bonnefoy X, Kampen H, Sweeney K (eds) Public health significance of urban pests. World Health Organization, Geneva, pp 209–239
Hokelek H, Akbas E, Guneren LEM, Akbas H, Guneren E et al (2002) Myiasis infestation: a rare complication of decubitus ulcer. Eur J Plast Surg 25:32–34. https://doi.org/10.1007/s00238-001-0331-y
Iqbal J, Hira PR, Marzouk MM, al-Ali F, Shelahi F, Khalid N, Wyatt N, Hall MJ (2011) Pressure sores and myiasis: flesh flies (Diptera: Sarcophagidae) complicating a decubitus ulcer. Ann Trop Med Parasitol 105:91–94. https://doi.org/10.1179/136485910X12851868780469
Ivorra T, Martínez-Sánchez A, Rojo S (2018) Predatory behavior of Synthesiomyia nudiseta larvae (Diptera: Muscidae) on several necrophagous blowfly species (Diptera: Calliphoridae). Int J Legal Med:1–10. https://doi.org/10.1007/s00414-018-1922-5
Kleine C, Schoefer H, Amendt J, Bexten T, Just-Nuebling G (2014) Cutaneous myiasis in a patient with seborrhoeic eczema. Lancet 383:1012. https://doi.org/10.1016/S0140-6736(14)60199-9
Lo Pinto S, Giordani G, Tuccia F, Ventura F, Vanin S (2017) First records of Synthesiomyia nudiseta (Diptera: Muscidae) from forensic cases in Italy. Forensic Sci Int 276:e1–e7. https://doi.org/10.1016/j.forsciint.2017.05.003
Martínez-Sánchez A, Marcos-García MA, Rojo S (2001) First collection of Chrysomya megacephala (Fabr.) in Europe (Diptera: Calliphoridae). Pan-Pac Entomol 77:240–243
Mielke U (1997) Nosocomial myiasis. J Hosp Infect 37:1–5. https://doi.org/10.1016/S0195-6701(97)90067-0
Morgan D (1995) Myiasis: the rise and fall of maggot therapy. J Tissue Viability 5:43–51. https://doi.org/10.1016/S0965-206X(14)80176-9
Morgan ER, Wall R (2009) Climate change and parasitic disease: farmer mitigation? Trends Parasitol 25:308–313. https://doi.org/10.1016/J.PT.2009.03.012
Olea MS, Centeno N, Aybar CAV, Ortega ES, Galante GB, Olea L, Juri MJD (2014) First report of myiasis caused by Cochliomyia hominivorax (Diptera: Calliphoridae) in a diabetic foot ulcer patient in Argentina. Korean J Parasitol 52:89–92. https://doi.org/10.3347/kjp.2014.52.1.89
Onwugamba FC, Fitzgerald JR, Rochon K, Guardabassi L, Alabi A, Kühne S, Grobusch MP, Schaumburg F (2018) The role of “filth flies” in the spread of antimicrobial resistance. Travel Med Infect Dis 22:8–17. https://doi.org/10.1016/j.tmaid.2018.02.007
Osorio J, Moncada L, Molano A, Valderrama S, Gualtero S, Franco-Paredes C (2006) Role of ivermectin in the treatment of severe orbital myiasis due to Cochliomyia hominivorax. Clin Infect Dis 43:e57–e59. https://doi.org/10.1086/507038
Pereyra-Rodríguez JJ, Bernabeu-Wittel J, Conejo-Mir MD, Ruiz-Pérez de Pipaón M, Conejo-Mir J (2010) Treatment of cutaneous myiasis associated with scalp psoriasis in a 13-year-old girl with oral ivermectin. J Am Acad Dermatol 63:908–909. https://doi.org/10.1016/j.jaad.2010.01.042
Pessoa L, Galvão V (2011) Myiasis infestation in advanced oral squamous cell carcinoma. BMJ Case Rep 2011:bcr0420114124. https://doi.org/10.1136/bcr.04.2011.4124
Pezzi M, Cultrera R, Chicca M, Leis M (2015) Furuncular myiasis caused by Cordylobia rodhaini (Diptera: Calliphoridae): a case report and a literature review. J Med Entomol 52:151–155. https://doi.org/10.1093/jme/tju027
Pierre-filho PDTP, Minguini N, Pierre LM, Pierre AM (2004) Use of ivermectin in the treatment of orbital myiasis caused by Cochliomyia hominivorax. Scand J Infect Dis 36:503–505. https://doi.org/10.1080/00365540410020136
Pinos VH, Ortiz-Prado E, Bermeo C, León J, Armijos L, Almeida E (2014) A unique case of facial burn superinfected with Dermatobia hominis larvae resulting in a bilateral enucleation of the eyes. Trop Dr 44:235–237. https://doi.org/10.1177/0049475514531257
Ramesh A, Bristow J, Kovats S, Lindsay SW, Haslam D, Schmidt E, Gilbert C (2016) The impact of climate on the abundance of Musca sorbens, the vector of trachoma. Parasit Vectors 9:48. https://doi.org/10.1186/s13071-016-1330-y
Ranjbar R, Izadi M, Hafshejani TT, Khamesipour F (2016) Molecular detection and antimicrobial resistance of Klebsiella pneumoniae from house flies (Musca domestica) in kitchens, farms, hospitals and slaughterhouses. J Infect Public Health 9:499–505. https://doi.org/10.1016/j.jiph.2015.12.012
Rodrigues FT, Klemig LR, Cardozo MRP, Alves PC, Aguiar VM, Lessa CS (2017) Myiasis associated with an invasive ductal carcinoma of the left breast: case study. Rev Inst Med Trop Sao Paulo 59. https://doi.org/10.1590/s1678-9946201759035
Roller E, Hengge U, Richter J, Ruzicka T, Schulte KW (2005) Kutane Myiasis nach Zentralamerikareise. Hautarzt 56:975–977. https://doi.org/10.1007/s00105-005-1030-6
Schaumburg F, Onwugamba FC, Akulenko R, Peters G, Mellmann A, Köck R, Becker K (2016) A geospatial analysis of flies and the spread of antimicrobial resistant bacteria. Int J Med Microbiol 306:566–571. https://doi.org/10.1016/j.ijmm.2016.06.002
Semenza JC, Suk JE (2017) Vector-borne diseases and climate change: a European perspective. FEMS Microbiol Lett 365. https://doi.org/10.1093/femsle/fnx244
Sherman RA (2009) Maggot therapy takes us back to the future of wound care: new and improved maggot therapy for the 21st century. J Diabetes Sci Technol 3:336–344. https://doi.org/10.1177/193229680900300215
Sherman RA, Roselle G, Bills C, Danko LH, Eldridge N (2005) Healthcare-associated myiasis: prevention and intervention. Infect Control Hosp Epidemiol 26:828–832. https://doi.org/10.1086/502501
Sherman RA, Mumcuoglu KY, Grassberger M, Tantawi TI (2013) Maggot therapy. In: Biotherapy - history, principles and practice. Springer Netherlands, Dordrecht, pp 5–29
Shivekar S, Senthil K, Srinivasan R et al (2008) Intestinal myiasis caused by Muscina stabulans. Indian J Med Microbiol 26:83–85. https://doi.org/10.4103/0255-0857.38869
Smadi R, Amr ZS, Katbeh-Bader A et al (2014) Facial myiasis and canthariasis associated with systemic lupus panniculitis: a case report. Int J Dermatol 53:1365–1369. https://doi.org/10.1111/ijd.12500
Sotiraki S, Farkas R, Hall MJR (2010) Fleshflies in the flesh: epidemiology, population genetics and control of outbreaks of traumatic myiasis in the Mediterranean Basin. Vet Parasitol 174:12–18. https://doi.org/10.1016/j.vetpar.2010.08.010
Velásquez Y, Ivorra T, Grzywacz A, Martínez-Sánchez A, Magaña C, García-Rojo A, Rojo S (2013) Larval morphology, development and forensic importance of Synthesiomyia nudiseta (Diptera: Muscidae) in Europe: a rare species or just overlooked? Bull Entomol Res 103:98–110. https://doi.org/10.1017/S0007485312000491
Verettas D-AJ, Chatzipapas CN, Drosos GI, Xarchas KC, Staikos C, Chloropoulou P, Kazakos KI, Ververidis A (2008) Maggot infestation (myiasis) of external fixation pin sites in diabetic patients. Trans R Soc Trop Med Hyg 102:950–952. https://doi.org/10.1016/j.trstmh.2008.05.011
Wollina U (2015) Myiasis on squamous cell carcinoma of skin. Wien Med Wochenschr 165:79–82. https://doi.org/10.1007/s10354-014-0326-5
Zielke E (1992) Welche Formen der Myiasis sind von Mitteleuropa bekannt — welche sind möglich? Mitt Österr Ges Tropenmed Parasitol 14:249–256
Zumpt F (1965) Myiasis in man and animals in the old world. A textbook for physicians, veterinarians and zoologists. Butterworth & Co Ltd
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no competing interests
Additional information
Handling Editor: Julia Walochnik
Electronic supplementary material
ESM 1
(DOCX 72 kb)
Rights and permissions
About this article
Cite this article
Bernhardt, V., Finkelmeier, F., Verhoff, M.A. et al. Myiasis in humans—a global case report evaluation and literature analysis. Parasitol Res 118, 389–397 (2019). https://doi.org/10.1007/s00436-018-6145-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-6145-7