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Myiasis in Humans—A Global Case Report Evaluation and Literature Analysis

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Myiasis in Humans—A Global Case Report Evaluation and Literature Analysis Parasitology Research (2019) 118:389–397 https://doi.org/10.1007/s00436-018-6145-7 ARTHROPODS AND MEDICAL ENTOMOLOGY - REVIEW Myiasis in humans—a global case report evaluation and literature analysis Victoria Bernhardt1 & Fabian Finkelmeier2 & Marcel A. Verhoff1 & Jens Amendt1 Received: 9 October 2018 /Accepted: 12 November 2018 /Published online: 19 November 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018 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 Bholiday 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 profes- sional identification and treatment seems important in the future. Keywords Parasitism . Neglect . Climate change . Global warming . Flies Introduction achieve the therapeutic result (Grassberger and Fleischmann 2002;Sherman2009). However, if an unwanted colonization The medical application of maggots in a therapeutic sense is by fly larvae occurs, this is called myiasis and can not only an effective method for the treatment of chronic wounds and have tissue-destroying consequences for humans, but can also the removal of necrotic tissue with joint wound disinfection cause additional infections or psychosocial problems (Zumpt (Morgan 1995; Bonn 2000; Sherman et al. 2005, 2013; 1965; Hall and Smith 1993;HallandWall1995;Grassberger Čeřovský 2011). For maggot therapy, a controlled number of 2002; Sherman et al. 2005; Hogsette and Amendt 2008; sterile fly larvae, which are often fixed in a so-called biobag, Francesconi and Lupi 2012; Hall et al. 2016). In times of are placed on a wound for a defined period of time in order to global warming, not only the invasion of new fly species in Western Europe is to be expected, but also the risk of an increasing number of cases, as a warmer climate leads to an Handling Editor: Julia Walochnik increase of fly generations and thus also to an increasing num- ber of myiasis pathogens (Morgan and Wall 2009). Myiasis Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00436-018-6145-7) contains supplementary can be divided into two categories according to the anatomical material, which is available to authorized users. region as provided by the WHO ICD-10 classification (Table 1) and according to the biology of the parasitic species * Victoria Bernhardt (Zumpt 1965;Zielke1992;HallandWall1995; Hogsette and [email protected] Amendt 2008). Biological classification distinguishes between obligatory 1 Institute of Legal Medicine, University Hospital Frankfurt, and facultative parasitic species. The former, e.g., bot flies Goethe-University, Frankfurt, Main, Germany (Diptera: Oestridae), develop exclusively in living organisms. 2 Department of Medicine I, Gastroenterology, University Hospital But also in blow flies (Diptera: Calliphoridae) and flesh flies Frankfurt, Goethe-University, Frankfurt, Main, Germany (Diptera: Sarcophagidae) (Fig. 1), there are obligatory 390 Parasitol Res (2019) 118:389–397 Table 1 WHO ICD10 classifications of myiasis and its specific forms Methods ICD10-classification Type of myiasis A systematic literature search using Pubmed/Medline with the B87.0 Cutaneous myiasis (also: furuncular myiasis; search term myiasis and the search settings human, case re- incl. creeping myiasis) port, and full text covered the years 1997 to 2017, resulting in B87.1 Wound myiasis (also: traumatic myiasis) 741 publications. Of these, 464 were available and usable. B87.2 Ocular myiasis (externa or interna) Veterinary cases, reviews, or a lack of information on the type B87.3 Nasopharyngeal myiasis of myiasis, fly family or species led to exclusion. Foreign (incl. laryngeal myiasis) language cases (except German and English) were translated B87.4 Aural myiasis by means of DeepL online translator. The year of publication, B87.8 Myiasis of other sites the patient’s age and sex, the country in which the infection (incl. intestinal or genitourinary myiasis) was suspected to have occurred, the fly species, the type of B87.9 Myiasis, unspecified myiasis, the body region, the type of treatment, and any un- derlying diseases were recorded. The online available hospital parasitic species, like Chrysomya bezziana or Wohlfahrtia statistics of the Federal Statistical Office (Germany) were also magnifica for example (Zumpt 1965;Halletal.2016). evaluated according to ICD-10 B87. A descriptive evaluation Facultative parasitic species, which also occur in the families of the data was carried out using SPSS 23.0 (IBM, Ehingen, of blow flies, flesh flies, or house flies (Diptera: Muscidae), nor- Germany). mally develop on rotting organic material (carrion or faces). The colonization of living persons is rather accidental, as flies are Results & discussion attracted by the smell of necrotic tissue, but also by blood, urine, or feces (Grassberger 2002). Facultative parasitic fly species are laying their eggs or larvae on open or necrotic skin areas; inflam- Of at least 12 known fly families that can cause myiasis matory areas of the oral cavity, but also of the throat or nose, can (Zumpt 1965), only three to four families seem to be of higher be affected. Obligatory parasitic fly species, on the other hand, importance according to our analysis. These include blow flies also place their offspring onto the intact mucous membranes (38.8%; Tables 2 and 3), bot flies (41.2% of the cases studied; (Zumpt 1965). Table 4), flesh flies (10.3%; Table 5), and house flies (3.0%). The aim of the present work is to get a global overview of However, the results of the present study are limited by the myiasis-causing species and their distribution in order to as- species identification of the used case reports. In some cases, a sess possible consequences for (Western) Europe in times of correct species identification is at least very doubtful: Pinos climate change. A secondary goal is to detect possible basic or et al. (2014) described a traumatic myiasis with Dermatobia pre-existing diseases that promote colonization by flies and to hominis larvae. But this species only causes furuncular myia- recommend treatment measures. sis with single larvae. Another example can be illustrated by a case report of Smadi et al. (2014). They reported from adhered pupae of Lucilia sericata at the skin of a woman. But this species will not pupariate at the skin of a host. A case report by Shivekar et al. (2008) reports of an intestinal myiasis with Muscina stabulans, but the pictures look more like a flesh fly species. Potential primary diseases and consequences of fly colonization Primary diseases promoting myiasis Traumatic myiasis is often caused by a primary disease or an external injury that promotes colonization by flies (Francesconi and Lupi 2012). A large number of casuistics report of colonizations based on squamous cell carcinoma at different parts of the body (Pessoa and Galvão 2011; Wollina Fig. 1 Flies of the blowfly family: Lucilia spp. (top left) and Calliphora 2015; Hiraoka et al. 2015) (Fig. 2) and other exulcerating spp. (top right) with characteristic green-blue coloring. Flesh flies (be- low), e.g. Sarcophaga spp., show a grayish to black-white coloration. The tumor wounds (Rodrigues et al. 2017). The colonization of abdomen is rather flat to tube-shaped pressure ulcers in the posterior parts of the body is also Parasitol Res (2019) 118:389–397 391 Table 2 Myiasis-causing blow fly species (C., Calliphora;Chr.,Chrysomya; Coch., Cochliomyia;Cor.,Cordylobia;L.,Lucilia) depending on the myiasis category. Species labeled in bold are obligatory parasitic Calliphoridae Aural Cerebral Furuncular Nasal Ophthalmo Ophthalmo Oral Tracheostoma Traumatic Umbilical externa interna C. vicina 1 Chr. bezziana 2127116 Chr. megacephala 2 Chr. rufifacies 1 Coch. hominivorax 1611191272 Cor. 41 anthropophaga Cor. rodhaini 3 L. caesar 1 L. cuprina 3 L. illustris 1 L. sericata 21 82 2 17 frequently reported (Hokelek et al. 2002; Iqbal et al. 2011). But not only skin diseases increase the risk of an infection Other skin diseases such as seborrheic eczema (Kleine et al. by fly larvae, also patients having a peripheral artery occlusive 2014) and psoriasis (Pereyra-Rodríguez et al. 2010) can also disease (PAOD) with further development of a gangrene show promote a colonization. an increased risk. This is mainly due to diabetes (Chan et al. Table 3 Worldwide species distribution of parasitic blow flies causing Caribbean; CAm,
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