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Home , Cochliomyia hominivorax, Cordylobia anthropophaga, Cordylobia rodhaini, Dermatobia hominis, Flesh fly, Myiasis

Parasitology Research (2019) 118:389–397 https://doi.org/10.1007/s00436-018-6145-7

ARTHROPODS AND MEDICAL - REVIEW

Myiasis in —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 refers to the of living humans and vertebrates with larvae that feed on necrotic or vital tissue of the host. Since the invasion of new fly 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 . 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 . Neglect . Climate change . Global warming .

Introduction achieve the therapeutic result (Grassberger and Fleischmann 2002;Sherman2009). However, if an unwanted colonization The medical application of 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 and have tissue-destroying consequences for humans, but can also the removal of necrotic tissue with joint disinfection cause additional or psychosocial problems (Zumpt (Morgan 1995; Bonn 2000; Sherman et al. 2005, 2013; 1965; Hall and Smith 1993;HallandWall1995;Grassberger Čeřovský 2011). For , 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: ) 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 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 (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 bezziana or 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: ), 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 (Grassberger 2002). Facultative parasitic fly species are laying their or larvae on open or necrotic 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 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 stabulans, but the pictures look more like a 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 2015; Hiraoka et al. 2015) (Fig. 2) and other exulcerating spp. (top right) with characteristic green-blue coloring. Flesh flies (be- low), e.g. 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., ;Cor.,;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, Central America; NAm, North America; EAs, myiasis. (C., Calliphora;Chr.,Chrysomya;Coch.,Cochliomyia;Cor., Eastern Asia; SAs, Southern Asia; SEA, South-Eastern Asia; WAs, Cordylobia; L., Lucilia. EA, Eastern Africa; CA, Central Africa; SA, Western Asia; EE, Eastern Europe; SE, Southern Europe; WE, Western Southern Africa; WA, Western Africa; SAm, South America; C, Europe). Species labeled in bold are obligatory parasitic

Calliphoridae

Species

C. Chr. Chr. Chr. Coch. Cor. Cor. L. caesar L. cuprina L. illustris L. sericata vicina bezziana megacephala rufifacies hominivorax anthropophaga rodhaini

EA 11 1 CA 3 SA 2 WA 24 2 SAm 1 52 C2 CAm 1 2 NAm 1 1 5 EAs 10 4 SAs 19 3 9 SEA 4 1 1 1 WA 6 EE & Russia 5 SE 1 1 3 WE 1 2 Total 1 33 2 1 59 41 3 1 3 1 34 392 Parasitol Res (2019) 118:389–397

Table 4 Worldwide species distribution of parasitic bot flies causing EAs, Eastern Asia; SAs, Southern Asia; WAs, Western Asia; NE, myiasis. (H., Hypoderma; NA, Northern Africa; WA, Western Africa; Northern Europe; SE, Southern Europe; WE, Western Europe). Species SAm, South America; CAm, Central America; NAm, North America; labeled in bold are obligatory parasitic

Oesteridae

Species

Cuterebra sp. Dermatobia H. bovis H. lineatum H. sinsense H. tarandi hominis haemorrhoidalis

NA 2 WA 1 SAm 42 CAm 61 NAm 18 2 1 1 1 EAs 1 SAs 21 14 WAs 3 2 17 NE 2 SE 1 13 WE 6 Total 18 108 1 3 3 1 3 54

2005;Oleaetal.2014) as underlying disease, but also due to From these case studies, it can be concluded that myiasis any other primary disease that triggers PAOD. In addition to must be recognized as a problem that affects not only elderly diseases of internal cause, the focus is also on inlaying objects people in need of care or people living on the margins of such as tracheal cannulas, drainages, or pin sites after bone society, e.g., people without a permanent residence or without fractures as supporting triggers (Verettas et al. 2008;Batista- being part of a social network (Francesconi and Lupi 2012; da-Silva et al. 2011). Open (abrasion) wounds after accidents Amendt 2013; Bäuerle et al. 2014), but can basically affect also seem to be generally attractive for flies (Chan et al. 2012; everyone who suffers from a Bwidespread disease^ and/or is Durão et al. 2017). also treated in hospitals or nursing homes.

Table 5 Worldwide species distribution of parasitic flesh flies causing Asia; SEA, South-Eastern Asia; WAs, Western Asia; SE, Southern Europe; myiasis. (S., Sarcophaga;W.,Wohlfahrtia. NA, Northern Africa; SAm, WE, Western Europe). Species labeled in bold are obligatory parasitic South America; NAm, North America; EAs, Eastern Asia; SAs,Southern

Sarcophagidae

Species

S. africa S. agyrostoma S. crassipalpis S. haemorrhoidalis S. dux S. peregrina S. ruficornis W. magnifica W. vigil

NA 1 3 SAm 1 NAm 1 EAs 1 2 SAs 1 SEA 1 WAs 12 SE 1 1 2 6 WE Total 1 1 1 3 1 2 1 22 1 Parasitol Res (2019) 118:389–397 393

skin or the larvae could be removed with forceps. If necessary, a small surgical incision can help (Fig. 3b). A complex de- bridement with subsequent antibiosis is often necessary in cases of traumatic myiasis. The oral and topical off-label ap- plication of has been described as successful in some cases (Pierre-filho et al. 2004;Osorioetal.2006; Clyti et al. 2007). In general, the greater the larval infestation, the more extensive the tissue damage, which in extreme cases can lead to amputation of individual body parts or even death (Grassberger 2002; Bernhardt et al. 2018). Depending on the stage of development of the larvae, it may also be necessary to take protective steps for other pa- tients. Since the larvae actively leave (migrate) their food source at a certain point, they can move several meters to find a place for pupation. If this is not prevented or the pupation site is not detected, a new generation of flies can develop in the care area or on the unit within a relatively short time. To avoid nosocomial myiasis infections and transmission of other pathogens in hospitals and care facilities, the infiltra- tion of adult flies into the building must be prevented, which is Fig. 2 Traumatic myiasis with the Lucilia spp. of the family of why the use of fly screens on the windows from the outside is blow flies caused by squamous cell carcinoma of the back (Wollina 2015) (reprinted with permission of Springer-Verlag: Wiener Medizinische recommended (Mielke 1997; Hogsette and Amendt 2008). In Wochenschrift, Myiasis on squamous cell carcinoma of skin, Wollina, addition, wound dressings must be renewed at regular inter- U. ©(2015)) vals and perishable food should not be stored in the patient care area or left for unnecessarily long periods of time Transmission of infectious diseases by flies (Sherman et al. 2005).

Open wounds or skin defects not only increase the risk of a Myiasis in Europe colonization by flies in form of myiasis; the first contact of flies with a wound could theoretically also lead to infections Between 1997 and 2017, 54 cases of autochthonous myiasis with antimicrobial-resistant (Graham et al. 2009; were published from Europe and therefore have a total share Ranjbar et al. 2016; Schaumburg et al. 2016). A review by of 11.6%. About 57% of European cases come from Southern Onwugamba et al. (2018) showed that extended spectrum Europe, with Italy and Spain as the main areas of focus. The beta-lactamases (ESBL) producing, carbapenem- or colistin- percentage of case reports from Western Europe was only resistant Escherichia coli, Enterococcus faecium,ESBLpro- 2.8% (n = 13) of the total. Additionally, three cases come from ducing Klebsiella pneumoniae, Salmonella enterica,or Northern Europe and six from Eastern Europe & Russia. methicillin-resistant Staphylococcus aureus could be detected Twenty-two of the 54 European cases (40.7%) were caused in and on flies. Although direct transmission of these bacteria by bot flies, 13 cases by flesh flies (24.1%), and 13 cases by between flies and humans as a trigger of disease has not yet blow flies (24.1%). been proven, it seems to be confirmed that flies are at least So far, there seem to be less problems with myiasis in responsible for the transmission of Chlamydia trachomatis, Western Europe. The hospital statistics of the Federal which causes trachoma (Emerson et al. 1999, 2000; Ramesh Statistical Office for example recorded a total of 230 cases et al. 2016). It is therefore conceivable that, in addition to for Germany from 2000 to 2016. Those are approximately myiasis, other infections could also be induced. 13 cases per year. Since 2003, there have been 11 cases of prevention and rehabilitation facilities (Source: Federal Treatment Statistical Office; February 2018). However, both statistics only collect data from patients who are permanently resident Maggots should always be removed, regardless of their poten- in Germany and for whom age and gender have been tially useful, e.g., antibacterial properties (Sherman et al. recorded. 2005). The therapy of myiasis therefore concentrates primar- When interpreting the small numbers, however, it must be ily on the mechanical removal of larvae. For furuncular my- clear that many cases are not documented in hospitals, since iasis (Fig. 3a), it is often reported that a lack of oxygen, e.g., the primary disease is of major concern and myiasis is a sec- by application of petroleum jelly, forced the larvae out of the ondary finding. The number of unreported cases is therefore 394 Parasitol Res (2019) 118:389–397

Fig. 3 Furuncular myiasis with after a trip to Central America (Roller et al. 2005) a and subsequent removal by incision b (reprinted with per- mission of Springer-Verlag: Der Hautarzt, Kutane Myiasis nach Zentralamerikareise, Roller, E. Hengge, U. Richter, J. Ruzicka, T. Schulte, K. W. ©(2005))

likely to be substantially higher. Moreover, fly larvae infec- cases. While there were no special priority countries for Ch. tions are tabooed in society for various reasons, hardly reach bezziana,majorityofcases(n = 17) with O. ovis were reported the public or find their way into scientific literature (Hall et al. from Western Asia with focus on Turkey. 2016). The number of reported species in Asia was the most di- To our knowledge, only two cases of nosocomial myiasis verse of all regions. In total, myiasis cases of nine different fly from (South) Europe have been officially reported in the last families could be documented. In addition to the species al- 20 years (Dutto and Bertero 2011; Dutto et al. 2013). Both ready mentioned, also cases involving cases occurred in Italy with a flesh fly species (Sarcophaga (Diptera: Sarcophagidae), Lucilia sericata (Diperta: africa, Sarcophaga spp.). Mielke (1997) reported in his re- Calliphoridae), and Musca domestica (Diptera: Muscidae) view two cases from Germany that occurred in the 1980s. In were frequently reported. this context, it should be noted that not all nosocomial myiasis cases can be equated with neglect in care. Especially drains Myiasis in Africa and tracheal cannulas for example, which are not changed (several times) daily, always carry an increased risk of myiasis Africa accounts for 52 of the 464 cases (11.2% of the total in the warmer season. share). From Southern, Eastern, and Western Africa, only col- onizations with (n = 40) and Cor. Myiasis in America & Caribbean rodhaini (n = 3) (Diptera: Calliphoridae) which cause furuncular myiasis were reported (Fig. 3a). Cases from Altogether, 208 cases (44.8% of the total share) were reported Northern Africa also include infections with W. magnifica from America and the Caribbean in the last 20 years. From and O. ovis. South America come 104 cases, from Central America 65 cases, 37 from Northern America (including Canada), and Effects of global warming in Western Europe two cases come from the Caribbean. Especially two species, (Diptera: Calliphoridae) and In Western Europe, the vast majority of myiasis-relevant fly Dermatobia hominis (Diptera: Oestridae), caused 155 of 208 species are facultative parasitic. For about 10 years, however, cases (74.5%) with a focus on South and Central America. species that are obligatory parasites or at least close relatives Eighteen of 37 cases from Northern America were caused of such species have been established in Europe. Chrysomya by species belonging to Cuterebra spp. (Diptera: Oestridae). megacephala spread in Southern Europe and for some years A colonization with Cuterebra spp. larvae was not reported but also Chr. albiceps hasspreadindirectiontoCentral from any other region. Europe and can be found in Germany for example. Both spe- cies are closely related to the obligatory parasitic Chr. Myiasis in Asia bezziana (Martínez-Sánchez et al. 2001; Grassberger et al. 2003). If the climate forecasts for Western Europe are correct A total of 150 cases (32.2% of the total share) originated from and temperatures remain constantly above average or even Asia; 63 cases from South Asia, 57 cases from Western Asia, rise (source: European Environment Agency; April 2018), 21 cases from East Asia, and 9 cases from South-East Asia. we will have to consider the invasion of more problematic The most common myiasis-causing blow fly was species in the longer term. The flesh fly W. magnifica is an (Diptera: Calliphoridae), an obligatory obligatory parasitic species that has already spread in parasitic species, with 33 cases in total. The second most com- Southern and Eastern Europe, causing severe problems in mon species was Oestrus ovis (Diptera: Oestridae) with 32 humans and (Çiftçioğlu et al. 1996; Sotiraki et al. Parasitol Res (2019) 118:389–397 395

2010; Giangaspero et al. 2011). It endangers the welfare of Compliance with ethical standards animals, because untreated myiasis can lead to death, but also the husbandry sector suffers considerable financial damage. Conflict of interests The authors declare that they have no competing The fact that dogs are also increasingly hosts and carriers of interests W. magnifica represents an increasing risk to human health (Sotiraki et al. 2010). According to these observations, a case References report from 2006, describing a furuncular myiasis with Cor. anthropophaga, was suspected to have taken place in southern Amendt J (2013) Insektenbefall lebender Menschen – Zeichen der Portugal for the first time (Curtis et al. 2006). This observation Vernachlässigung. In: Klinisch-forensische Medizin. Springer is supported by a case report from 2015 describing also a Vienna, Vienna, pp 493–497 furuncular myiasis with Cor. rodhaini from Portugal (Pezzi Batista-da-Silva JA, Borja GEM, Queiroz MMC (2011) Patient with tra- et al. 2015). This could indicate the spread of the genus from cheostomy parasitized in hospital by larvae of the screwworm, Cochliomyia hominivorax. J Sci 11:1–7. https://doi.org/10. Africa to Europe. 1673/031.011.16301 But not only new obligate parasitic species are spreading Bäuerle L, Kanitz U, Laurich S, Naumovska K, Fröb D, Krebs O, with rising temperatures in Europe, but also facultative para- Wilkens A, Püschell K (2014) Fliegenmadenkrankheit (Myiasis) sitic species, such as nudiseta (Diptera: bei Verwahrlosung alter/kranker Menschen. 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