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. 2018 Aug 22;18:1049. doi: 10.1186/s12889-018-5934-3

A systematic review of human pathogens carried by the housefly (Musca domestica L.)

Faham Khamesipour 1,2,✉, Kamran Bagheri Lankarani 1, Behnam Honarvar 1, Tebit Emmanuel Kwenti 3,4
PMCID: PMC6104014  PMID: 30134910

Abstract

Background

The synanthropic house fly, Musca domestica (Diptera: Muscidae), is a mechanical vector of pathogens (bacteria, fungi, viruses, and parasites), some of which cause serious diseases in humans and domestic animals. In the present study, a systematic review was done on the types and prevalence of human pathogens carried by the house fly.

Methods

Major health-related electronic databases including PubMed, PubMed Central, Google Scholar, and Science Direct were searched (Last update 31/11/2017) for relevant literature on pathogens that have been isolated from the house fly.

Results

Of the 1718 titles produced by bibliographic search, 99 were included in the review. Among the titles included, 69, 15, 3, 4, 1 and 7 described bacterial, fungi, bacteria+fungi, parasites, parasite+bacteria, and viral pathogens, respectively. Most of the house flies were captured in/around human habitation and animal farms. Pathogens were frequently isolated from body surfaces of the flies. Over 130 pathogens, predominantly bacteria (including some serious and life-threatening species) were identified from the house flies. Numerous publications also reported antimicrobial resistant bacteria and fungi isolated from house flies.

Conclusions

This review showed that house flies carry a large number of pathogens which can cause serious infections in humans and animals. More studies are needed to identify new pathogens carried by the house fly.

Electronic supplementary material

The online version of this article (10.1186/s12889-018-5934-3) contains supplementary material, which is available to authorized users.

Keywords: Bacteria, Fungi, House fly, House fly control, Mechanical transmission, Parasites, Pathogens, Viruses

Background

The house fly, Musca domestica L. (Diptera: Muscidae), is the most common and widespread species of fly in the world. It is said to have originated from the savannahs of Central Asia and spread throughout the world, and can be found in both rural and urban areas of tropical and temperate climates [1, 2]. The house fly belongs to a group of flies often referred to as “filth flies”; the other members belong to the families Calliphoridae and Fanniidae [3]. The house fly has been in existence since the origin of human life [4] and well adapted to life in human habitations [5]. M. domestica is an eusynanthropic, endophilic species, i.e. it lives closely in association with humans and is able to complete its entire lifecycle within habitations of humans and domestic animals [6]. House flies are often found in abundance in areas of human activities such as hospitals, food markets, slaughter houses, food centers or restaurants, poultry and livestock farms where they constitute a nuisance to humans, poultry, livestock and other farm animals, and also act as potential vector of diseases [7].

The house fly is known to carry pathogens that can cause serious and life-threatening diseases in humans and animals. Over 100 pathogens including bacteria, viruses, fungi and parasites (protozoans and metazoans) have been associated with the insect [8, 9]. Molecular analysis revealed that house flies carry very diverse groups of microorganisms [10]. Evidence supporting the role of the house fly in transmission of diseases are mostly circumstantial, with the strongest evidence pointing to the correlation between the rise in incidence of diarrhoea and an increase in the fly population [11–14].

The characteristics of the pathogens carried by house flies depend on the area where the insect is collected; house flies captured from the hospital environment or animal farms (where there is extensive use of antibiotics as growth promoters) commonly carry antimicrobial resistant bacteria and fungi [9, 15–20]. More so, house flies presenting in the hospital environment may also be associated with the transmission of nosocomial infections [9, 21].

House fly causes mechanical transmission of pathogens, which is the most widely recognised mechanism [22–24]. This occurs when pathogens are transmitted from one vertebrate hosts to another without amplification or development of the organism within the vector [22]. House flies usually feed and reproduce in feces, animal manure, carrion and other decaying organic substances, and thus live in intimate association with various microorganisms including human pathogens, which may stick to body surfaces of the fly. The constant back and forth movement of house flies between their breeding sites and human dwellings can lead to the transmission of pathogens to humans and animals.

Currently, there is no systematic review on the pathogens carried by the house fly. The aim of this systematic review was to identify the types and prevalence of human pathogens carried by the house fly.

Methods

For this systematic review, we did a literature search to identify scientific articles reporting pathogens (bacteria, viruses, fungi and parasites) that has been isolated from the house fly (Musca domestica). The current study conforms to the Preferred Reporting Items for Systematic reviews and Meta-analyses (PRISMA) guidelines [25] (Additional file 1).

Search strategy and selection criteria

Relevant studies were searched in health-related electronic databases including PubMed, PubMed Central, Google Scholar and Science Direct using the keywords: House fly OR Musca domestica OR Pathogens OR bacteria OR fungi OR parasites OR viruses.

The search was limited to the studies published in English or containing at least an English abstract until November 2017. Subsequently, the titles and abstracts of the selected articles were examined by 2 reviewers, independently (parallel method) to identify articles reporting pathogens isolated from the house fly. When there was any discrepancy in their report, a third reviewer was invited to resolve the issue. Relevant papers were also manually cross checked in order to identify further references. In the selected articles, the following data were extracted by the first reviewer and checked by the second reviewer. The data included type and species of pathogen isolated, stage of house fly from which pathogen was isolated, frequency of occurrence of pathogen, method used in isolation of pathogen, type of study (field or experimental), site of the house fly from where the pathogen was isolated, nature of pathogen isolated (whether the pathogen was carrying genes that were resistant to antimicrobials or not), and location of capture of the house fly (human residents, animal farms, markets/shops, hospitals etc.). Excluded articles were those reporting pathogens isolated from flies in general without specifying the fly species. The selection process is detailed in Fig.1.

Fig. 1.

Fig. 1

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Flowchart of the selection process for publications included in this review

Risk of bias in individual studies

Level of risk of bias for the study was likely to be high mainly because of differences in study and the methods used to isolate pathogens from the house fly. Most of the studies were not designed to isolate all the types of pathogens. Moreover, studies using molecular methods (PCR and/or sequences) yielded more pathogens compared to studies using standard cultural methods.

Results

Figure 1 (PRISMA flowchart) provides a four-phase study selection process in the present systematic review study. A total of 1718 studies were identified in the initial search. After the title and abstract screening, 131 full- text articles were retrieved. Of these, a final 99 articles were identified for this review [2–24, 26–93]

Seventy-three 73 (73.73%) of the works described bacterial pathogens (Table 1), 18 (18.18%) fungi (Table 2), 5 (5.05%) parasites (Table 3) and 7 (7.07%) described viruses. The selected studies were done in 21 countries and the study period covered the years 1970–2017. Sixty-eight of the studies were field studies (performed on house flies caught in the wild) (68.69%) while 31 were experimental studies (performed in the laboratory) (31.31%). Of the 68 field studies, 12 described pathogens isolated from house flies caught in the wild in Europe, 16 in the Middle East, 15 in Africa, 13 in USA, 10 in Asia, and 2 in South America. Twenty studies (28.88%) reported on house flies that were caught from within human habitation, 28 (28.28%) from animal farms (including poultry, dairy and piggery farms), 10 (10.10%) from the surroundings, 10 (10.10%) from food centers (including cafeteria, restaurants), 7 (7.07%) from markets or shops, 14 (14.14) from hospitals, 7 (7.07%) from dump sites or sanitary landfills while 4 (4.04%) were from gardens or farms.

Table 1.

Bacteria species that have been isolated from house flies, including the site of isolation, the frequencies and their distribution

Bacteria genera Species Medical and/or veterinary importance Geographical occurrence Site of specimen collection Host stage infected Prevalence Lab or field study Site of isolation References
Helicobacter H. pylori Medical Worldwide Laboratory reared Adult – Lab External surfaces/internal organs [70–72]
Campylobacter C. jejuni Medical and veterinary Worldwide Poultry, piggery Adult/larvae 6.2% Field/ Lab External surfaces/internal organs [73, 74, 87, 90]
C. coli Medical and veterinary Worldwide Poultry, piggery Adult 90.1% Field External surfaces/internal organs [74]
Others Medical and veterinary Worldwide Restaurant, refuse dumps, barbecue shops, fruits and food vendors, markets, poultries (broiler farms) Adult – Field External surfaces/internal organs [38, 75]
Salmonella S. typhimurium Medical Worldwide Laboratory experiment Adult – Lab [37]
S. enterica serovar Enteritidis Medical Worldwide Poultry, dumpsters Adult/larvae 6–70% Lab/field External surfaces/internal organs [23, 28, 39]
Others Medical Worldwide Restaurant, refuse dumps, barbecue shops, fruits and food vendors, markets, fish vendors, human habitation Adult 11.8–66.67% Field External surfaces/internal organs [25, 27, 29, 70–72, 91]
Escherichia E. coli Medical Worldwide Human habitation, cafeteria and food centers, hospitals, open fields, poultry farms, slaughter houses, cattle farms, animal hospitals Adult/larvae 10.5–76.3% Field/lab External surfaces/internal organs [2–24, 29–38, 40, 43–46, 48, 89, 92]
Bacillus B. anthrax Medical and veterinary Worldwide Laboratory reared Adult – Lab External surfaces/Internal organs [76]
B. megatarium non Worldwide Cafeteria and food centers Adult 50% Field External surfaces/Internal organs [7]
B. sphaericus Medical Worldwide Cafeteria and food centers Adult 50% Field External surfaces/Internal organs [7]
B. cereus Medical Worldwide Fresh fish Larvae – Field External surfaces/Internal organs [46, 53]
B. alvei Medical Worldwide Cafeteria and food centers Adult 50% Field External surfaces/Internal organs [7]
B. pumilus Medical Worldwide Adult – Field External surfaces/Internal organs [46]
B. thuringiensis non Worldwide Adult – Field External surfaces/Internal organs [46]
Others Medical Worldwide Dairy farms, hospitals, slaughter houses, fruit and food centers Adult 31.1% Field External surfaces [10, 20, 44, 61, 89]
Staphylococcus S. aureus Medical Worldwide Human habitation, fresh fish Adult/ larvae 26.9% Field External surfaces/Internal organs [40, 45, 53, 77, 92]
S. epidermidis Medical Worldwide Human habitation Adult – Field External surfaces/Internal organs [40]
S. sciuri Medical/veterinary Worldwide Dumpsters of restaurants Adult – Field External surfaces [46]
S. saprophyticus Medical Worldwide Dumpsters of restaurants Adult – Field External surfaces [46]
S. xylosus Medical Worldwide Dumpsters of restaurants Adult – Field External surfaces [46]
Others Medical/veterinary Worldwide Poutry, animal farms, garden, garbage/dump areas, restaurants/cafeteria, markets, human habitation, hospitals Adult 22.9–28.2% Field External surfaces/Internal organs [10, 20, 48, 78, 79, 89, 91]
Enterococcus E. faecalis Medical Worldwide Restaurants, piggery farms Adult 55.5–88.2% Field/lab External surfaces/Internal organs [21, 49, 50]
E. faecium Medical Worldwide Restaurants, piggery farms Adult 6.8–12.8% Field/lab External surfaces/Internal organs [49, 50]
E. casseliflavus Medical Worldwide Restaurants, piggery farms Adult 4.9–6.7% Field/lab External surfaces/Internal organs [49, 50]
E. hirae Medical/veterinary Worldwide piggery farms Adult 12.8% Field/lab External surfaces/Internal organs [50]
Aeromonas A. caviae Medical Worldwide Hospitals, streets, slaughter houses (abattoir) Adult 39–78% Field Internal organs [48, 80, 81]
A hydrophila Medical Worldwide Open field Adult – Field Internal organs [82]
Others Medical Worldwide Poutry, animal farms, garden, garbage/dump areas, restaurants/cafeteria, markets, human habitation, hospitals Adult – Field Internal organs [79]
Shigella S. sonnei Medical Worldwide Hospitals, streets, slaughter houses Adult – Field Internal organs [48]
S. dysenteriae Medical Worldwide Dumpsters of restaurants Adult – Field Internal organs [46]
Others Medical Worldwide Poultry, animal farms, garden, garbage/dump areas, restaurants/cafeteria, markets, human habitation, hospitals Adult 4.8–66.67% field External surfaces/ internal organs [11, 13, 29, 38, 40, 43, 79, 91]
Klebsiella K. pneumoniae Medical Worldwide Hospitals, human habitation, slaughter houses Adult 11.3–82% field External surfaces/ internal organs [15, 47, 82]
K. oxytoca Medical Open field Adult – Field External surfaces [83]
Others Medical Poutry, animal farms,garden, garbage/dump areas, restaurants/cafeteria, markets, human habitation, hospitals, slaughter houses, open field Adult – Field External surfaces [40, 44, 48, 61, 79, 89]
Pseudomonas P. aeruginosa Medical Worldwide Dump sites, slaughter houses, open field, human habitation, fresh fish, hospitals Adult/larvae 37% field External surfaces/internal organs [15, 19, 53, 61, 84]
Others Medical Worldwide Hospitals, streets, slaughter houses, Adult 21.8% Field External surfaces/internal organs [44, 48, 92]
Proteus P. mirabilis Medical Worldwide Slaughter houses, hospitals Adult 29.1% field External surfaces/internal organs [15]
P. vulgaris Medical Worldwide Human habitation Adult – Field External surfaces/internal organs [40]
Proteus sp. Medical Worldwide Slaughter houses, dump sites, open fields, human habitations Adult 14.8% Field External surfaces/internal organs [61, 89, 92]
Citrobacter C. freundi Medical Worldwide Cafeteria and food centers, Slaughter houses, hospitals Adult 28.4% field External surfaces/internal organs [7, 15]
Chronobacter C. turicensis, Medical Worldwide Poultry, dumpsters Adult/larvae 14% Field/lab External surfaces/internal organs [23, 28]
C. universalis Medical Worldwide Poultry, dumpsters Adult/larvae – Field/lab External surfaces/internal organs [23, 28]
C. sakazakii Medical Worldwide Poultry, dumpsters Adult/larvae – Field/lab External surfaces/internal organs [23, 28, 46]
Listeria L. monocytogenes Medical Worldwide Poultry, dumpsters Adult/larvae 3–49.4% Field/lab External surfaces/internal organs [23, 28, 54]
Others Medical/veterinary Worldwide Animal farms Adult – Field External surfaces/internal organs [78]
Streptococcus S. pyogenes medical Worldwide Fresh fish, human habitation Adult/larvae – Field External surfaces/internal organs [40, 53]
S. faecalis Medical Worldwide Fresh fish Larvae – Field External surfaces/internal organs [53]
Others Medical Worldwide Hospitals, slaughter houses, streets, dump sites, open fields, human habitation Adult 66.67% Field External surfaces/internal organs [48, 61, 89, 91]
Alternaria Alternaria spp. Medical Worldwide Fresh fish, Human habitation Larvae 1.4–6% Field [15, 53, 55]
Serratia Serratia spp. Medical worldwide Human habitation Adult – Field Internal organs [40]
Enterobacter Enterobacter spp. Medical Worldwide Human habitation Adult – Field Internal organs [40, 89]
Edwardsiella Edwardsiella spp. Medical Worldwide Poultry Adult – field External surfaces/internal organs [43]
Providencia Providencia spp. Medical Worldwide Poultry, animal farms, garden, garbage/dump areas, restaurants/cafeteria, markets, human habitation, hospitals, slaughter houses, open field Adult – Field External surfaces/ internal organs [43, 79]
Vibrio Vibrio cholera non O1 Medical Worldwide Human habitation Adult 45.7% Field Internal organs [29]
Others Medical / veterinary Worldwide Animal farms Adult – Field External surfaces/ internal organs [78]
Morganella M. morgana Medical Worldwide Poutry, animal farms,garden, garbage/dump areas, restaurants/cafeteria, markets, human habitation, hospitals, slaughter houses, open field Adult 16.67% Field External surfaces/Internal organs [7, 79]
Clostridium Clostridium spp. Medical Worldwide Dairy farms Adult – Field Internal organs [10]
Corynebacterium Corynebacterium spp. Medical Worldwide Dairy farms Adult – Field Internal organs [10]
Lactobacillus Lactobacillus spp. Medical Worldwide Dairy farms Adult – Field Internal organs [10]
Yersinia Y. enterocolitica Medical Worldwide Hospitals, streets, slaughter houses Adult – Field Internal organs [48]
Burkholderia B. pseudomallei Medical Worldwide Open field Adult – Field Internal organs [83]
Acinetobacter A. baumanni Medical worldwide Poultry, dumpsters Adult – Field Internal organs [46, 89]
Methylobacterium M. persicinum Medical Worldwide Poultry, dumpsters Adult – Field Internal organs [46]
Micrococcus Micrococcus sp. Medical Worldwide Garbage/dump areas, poultry, restaurants Adult – Field External surfaces/Internal organs [89]
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Table 2.

Fungi species that have been isolated from house flies, including the site of isolation, the frequencies and their distribution

Fungi genera Species Medical, veterinary or agricultural importance Geographical occurrence Site of specimen collection Host stage infected Prevalence Lab or field study Site of isolation References
Cladosporum C. cladosporoides Medical Worldwide Cattles diagnosed with bovine ringworm, animal pens, dump sites Adult/larvae 4.7–85% Field/lab External surfaces [56, 57]
Others Medical Worldwide Human habitation Larvae 0.2 Field External surfaces [53, 55]
Penicillium P. axalicum Medical Worldwide Fresh fish Larvae – Field External surfaces [53]
P. corylophilum Medical Worldwide Animal pens, dump sites Larvae – Field External surfaces [57]
P. fellutanum Medical Worldwide Animal pens, dump sites Larvae 11.9% Field External surfaces [57]
P. verrucosum Medical Worldwide Human habitation Adult – Field External surfaces [60]
P. aurantiogriseum Medical Worldwide Human habitation Adult – Field External surfaces [60]
Others Medical Worldwide Human habitation, Cattles diagnosed with bovine ringworm, hospitals, slaughter houses adult 3.4–21% Field/lab External surfaces [55, 56, 58, 59]
Aspergillus A. flavus Medical Worldwide Animal pens, dump sites, poultry farms, dairy, piggery, slaughter houses, open field Adult/larvae 23.8% Field External surfaces [52, 57, 60]
A niger Medical Worldwide Animal pens, dump sites Adult/larvae 14.4–85.71% Field External surfaces [7, 57]
A fumigatus Medical Worldwide Cafeteria and food centers Adult 85.71 Field External surfaces [7]
A tamari Medical Worldwide Fresh fish Larvae – Field External surfaces [53]
A parasiticus Medical Worldwide Human habitation Adult – Field External surfaces [60]
Others Medical Worldwide Human habitation, Cattles diagnosed with bovine ringworm, hospitals, slaughter houses Adult 2.8–67.4% Field/lab External surfaces [55, 56, 58, 59]
Beauveria B. bassiana Medical Worldwide Poultry farms, dairy, piggery, open field, slaughter houses Adult – Field External surfaces [52]
Mucor M. cirinelloides Medical Worldwide Cafeteria and food centers Adult – Field External surfaces [7]
Others Medical Worldwide Human habitation Adult 2% Field External surfaces [55]
Alternaria A. alternata Medical Worldwide Animal pens, dump sites Adult/larvae 1.4–11.9% Field External surfaces [53, 55, 57, 58]
Fusarium F. oxysporum Medical Worldwide Fresh fish Larvae – Field External surfaces [53]
F. verticilliodes Medical Worldwide Human habitation Adult – Field External surfaces [60]
F. proliferatum Medical Worldwide Human habitation Adult – Field External surfaces [60]
Others Medical Worldwide Animal pens, dump sites, Human habitation, hospitals, slaughter houses Larvae 4.7–17% Field External surfaces [55, 57, 58]
Curvularia C. brachyspora Medical Worldwide Animal pens, dump sites Adult 2.4% Field External surfaces [57]
Mycelia M. sterilia Medical Worldwide Animal pens, dump sites Adult 2.4% Field External surfaces [57]
Candida C. albicans Medical Worldwide Pig pen, Human habitation Adult 44.6% Field External surfaces [51, 54]
C. glabrata Medical Worldwide Human habitation Adult 23% Field External surfaces [51]
C. krusei Medical Worldwide Human habitation Adult 19.6% Field External surfaces [51]
C. tropicalis Medical Worldwide Pig pen, Human habitation Adult 7.4% Field External surfaces [51, 54]
C. dubliniensis Medical Worldwide Human habitation Adult 3.6% Field External surfaces [51]
C. parapsilisis Medical Worldwide Human habitation Adult 1.8% Field External surfaces [51]
Others Medical Worldwide Human habitation Adult 10.5% Field External surfaces [59]
Microsporum M. canis Veterinary Worldwide Laboratory experiment Adult/larvae – Field External surfaces/internal organs [85]
M. gypseum Medical Worldwide Hospitals, slaughter houses Adult – Field External surfaces [58]
Chrysosporium Chrysosporium spp. Medical Worldwide Human habitation Adult 2% Field External surfaces [55]
Curvalaria Curvalaria spp. Agricultural Worldwide Human habitation Adult 0.4% Field External surfaces [55]
Epicoccum Epicoccum spp. Medical Worldwide Human habitation Adult 1% Field External surfaces [55]
Eupenicillium Eupenicillium spp. Medical Worldwide Human habitation Adult 1% Field External surfaces [55]
Moniliella Moniliella spp. Medical and veterinary Worldwide Human habitation Adult 9% Field External surfaces [55]
Nigrospora Nigrospora spp. Agricultural Worldwide Human habitation Adult 1% Field External surfaces [55]
Rhizopus Rhizopus spp. Veterinary Worldwide Human habitation Adult 2% Field External surfaces [55]
Scopulariopsis Scopulariopsis spp. Veterinary Worldwide Human habitation Adult 2% Field External surfaces [55]
Mucorales Mucorales spp. Medical Worldwide Hospitals Adult 11% Field External surfaces [59]
Rhodotorula Rhodotorula spp. Medical/veterinary Worldwide Hospitals Adult 8.4% Field External surfaces [59]
Moniliella M. suaveolans Medical Worldwide Human habitation Adult – Field External surfaces [60]
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Table 3.

Parasites that have been isolated from house flies, including the site of isolation, the frequencies and their distribution

Parasite genera Species Medical or veterinary importance Geographical occurrence Site of specimen collection Host stage infected Prevalence Lab or field study Site of isolation References
Ascaris A. lumbricoides Medical Worldwide Slaughter houses, dump sites, human habitation, open fields Adult 12.6–14.29% Field External surfaces [61–63, 98, 99]
A. suum Veterinary Worldwide piggery Adult 62% Field/lab External surfaces/internal organs [54]
Entamoeba E. histolytica Medical Worldwide Slaughter houses, dump sites, human habitation, open fields Adult 35.43–53.57% Field External surfaces [61–63]
Hookworm Ancylostoma duodenale/Necator americanus Medical Worldwide Slaughter houses, dump sites, human habitation, open fields Adult 8.93% Field External surfaces [61, 62, 64]
Trichuris T. trichiura Medical Worldwide Slaughter houses, dump sites, human habitation, open fields, piggery Adult 12.5–74.0% Field External surfaces [61–64]
T. suis Medical/veterinary Worldwide Piggery Adult – Field/lab External surfaces/internal organs [54]
Strongyloides S. stercoralis Medical Developing countries Slaughter houses, dump sites, human habitation, open fields Adult 10.7% Field External surfaces/internal organs [61]
S. ransomi Veterinary Tropical regions Piggery Adult 21% Field External surfaces [54]
Metastrongylus M. spp Veterinary Worldwide Piggery Adult – Field External surfaces/internal organs [54]
Haematopinus H. suis Veterinary Worldwide Piggery Adult – Field External surfaces/internal organs [54]
Crytosporidium C. parvum Medical/ Veterinary Worldwide Laboratory experiment Adult/larvae – Lab Internal organs [65]
Giardia G. lamblia Medical Developing countries Human habitation, refuse dumps, tomato/vegetable and soft drink shops Adult 23.62% Field External surfaces [3, 63]
Enterobius E. vermicularis Medical Worldwide but more prevalent in developed world Poultry Adult – Field External surfaces [3]
Taenia T. spp. Medical/veterinary Worldwide Human habitation, refuse dumps, tomato/vegetable and soft drink shops Adult 15.75% Field External surfaces [63, 64]
Hymenolepis H. nana Medical Worldwide Human habitation, refuse dumps, tomato/vegetable and soft drink shops Adult 5.51% Field Internal organs [63]
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Pathogens were isolated more frequently from the body surfaces of the flies as reflected from 44 studies (44.44%), followed by 33 studies (33.33%) reporting isolation from both the body surfaces and the gut, while 22 studies (22.22%) indicated isolation from the gut. Most studies reported isolation of pathogens from adult flies 91 (91.92%), followed by larvae 5 (5.05%) and from both the adults and the larvae 3 (3.03%).

The most frequent method used in the isolation of pathogens was standard cultural methods 77 (77.78%), followed by molecular methods (such as polymerase chain reaction [PCR] or sequencing) 14 (14.14%) and other parasitological techniques 8 (8.08%).

Among the bacterial pathogens isolated, 7 studies reported virulent bacteria (8.97%), 14 reported bacteria carrying genes which confer resistance to multiple antibiotics (17.95%), and the enteric bacteria were the most frequently isolated bacteria as shown in 55 studies (70.51%) (Table 1). Among the parasites, Ascaris spp. Entamoeba spp., hookworms and Trichiuris spp. were most frequently reported (Table 2). Among the fungi, Penicillum spp., Aspergillus spp., and Candida spp. were the most frequently reported (Table 3). Very few studies reported on viruses isolated from the house fly, most of which were experimental studies (Table 4).

Table 4.

Viruses that have been isolated from house flies, including the site of isolation, the frequencies and their distribution

Virus family Common name Medical or veterinary importance Geographical occurrence Site of specimen collection Host stage infected Prevalence Lab or field study Site of isolation References
Picornavirus Senecavirus A Medical/veterinary Worldwide Laboratory experiment Adult – Lab Internal organs [65]
Filoviridae Ebola virus Medical West and Central Africa Laboratory experiment Adult – Lab Internal organs [68]
Arteriviridae Porcine reproductive and respirator syndrome virus Veterinary Worldwide Piggery Adult – Lab Internal organs [86]
Orthomyxoviridae Avian Influenza virus H5N1 Veterinary Worldwide Laboratory experiment Adult – Lab Internal organs [66]
Hytrosaviridae Musca domestica salivary gland hypertrophy virus (MdSGHV) Veterinary Worldwide Laboratory experiment Adult 3–24% Lab Internal organs [88]
Paramyxoviridae Newcastle disease virus Medical/veterinary Worldwide Laboratory experiment Adult – Lab Internal organs [67]
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Discussion

This systematic review revealed a total of at least 130 pathogens that have been isolated from the house fly. Bacterial pathogens were by far the most frequently reported, suggesting the house fly may play an important role as vector of bacterial diseases. Fungi were the second most frequently isolated pathogens followed by parasites, and viruses were the least frequent. The differences in the rate of isolation of these pathogens could be attributed to individual biases at the level of the study, pertaining to the method used in the isolation of the pathogens. Most of the articles reviewed used standard cultural methods for the isolation of pathogens, which may have skewed the outcome towards bacterial pathogens; more advanced methods including cell culture and PCR, which are required for the detection of viruses, are expensive and not readily available. This may explain the low number of reports on isolation of viruses from house flies.

Pathogens were more frequently isolated from the body surfaces of house flies, especially from those captured from within human habitations and animal farms. House flies habitually feed on feces, animal manure, carrion and other decaying organic matter. In the process of feeding, pathogens stick on their mouth parts, wings, legs and other body surfaces, which they carry back to human habitations and animal farms, where they live and complete their lifecycle [6]. The constant movement of the house fly back and forth from feces (or other animal waste) to food and drinking water therefore places humans and animals at risk of infection. The frequent isolation of pathogens from the body surfaces of the flies makes it plausible that when house flies transmit pathogens, they only act as mechanical vectors [22–24, 26]. Unlike in biological transmission, there is no multiplication (amplification) of the pathogen in the host in mechanical transmission. However, the fly has been demonstrated to carry sufficient quantity of pathogens on its body surface, enough to cause an infection [27]. The quantity of pathogens present in the gut is usually higher than the quantity present on the body surfaces, suggesting that feces and vomitus may also serve as a major route of transmission of pathogens [28, 94].

Enteric bacteria were the most frequently isolated bacteria [2–24, 27, 29–35, 37–39]. This could be due to the fact that house flies feed mainly on feces and other animal waste, which is a rich source of enteric bacteria. Some of the bacteria isolated from house flies were highly virulent species including enteropathogenic strains such as enteroaggregative E. coli (EAEC), enterohaemorhagic E. coli (EHEC), enterotoxigenic E. coli (ETEC), and enteropathogenic E. coli (EPEC) [18, 29–34], Vibrio cholera and Bacillus anthracis that cause enteric diseases, cholera and anthrax respectively. Others including Klebsiella spp., Pseudomonas, Staphylococci, Streptococci, Clostridium spp. and Enterococci to name just a few, are also important causes of diseases in humans (including nosocomial infection). Furthermore, several studies reported bacteria that were resistant to multiple antibiotics including E. coli (20,35,36), Klebsiella pneumoniae [15, 47] and Pseudomonas aeruginosa [15, 19, 48]. Most of the antibiotic resistant bacteria were isolated from flies caught in and around hospital environments and animal farms (where there is an extensive use of antibiotics as growth promoters) [15, 17–20, 49, 50], suggesting that house flies may also play a role in the dissemination of antibiotic resistant bacteria to different environments [17].

Fungi species frequently isolated from the house fly belonged to the genera: Candida, Aspergillus, and Penicillium [7, 51–60]. Some of these genera (including Candida and Aspergillus) contain fungi species that are important human pathogens, but most others contain fungi species that are of veterinary (e.g. Microsporum, Rhizopus, Scopularipsis and Rhodotorula) and agricultural importance (e.g. Curvalaria and Nigrospora). Furthermore, genera Epicoccum contain fungi species which are important allergens. Some species of fungi that have been isolated from the house fly were resistant to multiple antifungals, example of which includes Candida [51]. Most of the fungi that have been isolated from the house fly were reportedly isolated from the outer cuticle of the insect and rarely from internal organs, feces or vomitus.

Very few studies reported the isolation of parasites from the house fly. Among these studies, almost all the parasites described were isolated from the body surfaces of the flies. The parasites species frequently reported belonged to the genera: Ascaris, Entamoeba, Trichiuris, and the hookworms [61–64]. These parasites commonly cause enteric diseases in humans and their frequent occurrence on the house fly could also be attributed to the food source of the house fly. Parasites of the genera Metastrongylus and Heamatopinus, which are known to be strict pathogens of domestic animals including pigs were also reported [54].

Reports of the isolation of viruses from wild-caught flies are very rare. However, house flies were reported to be capable of carrying a number of viruses in laboratory experiments. The majority of these viruses were of veterinary importance including the Senecavirus A whose natural hosts are pigs and cows [65]; the porcine reproductive and respiratory syndrome virus which causes a disease of pigs called porcine reproductive and respiratory syndrome (PRRS), also referred to as the blue-ear pig disease; Avian influenza virus and Newcastle disease virus which cause diseases in birds including poultry [66, 67]. In addition, one study demonstrates the ability of the house fly to carry the Ebola virus in laboratory experiments [68]. However, its role in the transmission of the virus is still to be confirmed.

Study limitations

Although this systematic review addresses a key gap in the evidence base by identifying the types and prevalence of pathogens carried by the house fly, there are some key limitations in the evidence collected. Firstly, the survival of these pathogens on the house fly and the house fly’s role in the transmission of these pathogens to humans and animals remains largely undefined. Secondly, it is unclear how representative these pathogens reported are of the wider population of pathogens that are carried by the house fly.

Future perspectives

Mechanical transmission of pathogens by arthropods including house flies is often overlooked because too much importance is given to biologically transmitted diseases such as malaria, yellow fever etc. [26]. Nevertheless, there is enough evidence to show that house flies can carry pathogens capable of causing serious diseases in humans and domestic animals, and should therefore be controlled. The control of the house fly can be achieved by physical (such as composting manure [95, 96]), chemical and biological methods. The use of chemical pesticides, which is the most common method today, is fast losing grounds due to the growing resistance by the house fly and other pests, couple to the effects they may have on non-target organisms [97–99], have led to the consideration of other methods, including biological control. Biological control agents including fungi of the genera Metarhizium and Beauveria, and bacteria including Bacillus thuringiensis can be used to control the housefly [93, 97]. Furthermore, the sequencing of the genome of the house fly presents new opportunities for the identification of novel targets for controlling the housefly and also for understanding the mechanism of resistance to insecticides as well as the genetic adaptation of the house fly to high pathogen loads [69].

Conclusion

This review showed that the common house fly is a mechanical vector of a diverse range of pathogens including bacteria, fungi, viruses and parasites. However, more studies on identifying new pathogens and the survival of these pathogens are needed.

Additional file

Additional file 1: (490.9KB, pdf)

PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) Checklist. (PDF 490 kb)

Acknowledgements

We would like to thank Health Policy Research Center (HPRC) of Shiraz University of Medical Sciences. Acknowledgments also go to Dr. Natasha Potgieter and Dr. Farhat Afrin for the kind comments.

Funding

No funding was received.

Availability of data and materials

The original research articles included in this systematic review are publicly available.

Abbreviations

EAEC

Enteroaggregative Escherichia coli

EHEC

Enterohaemorhagic Escherichia coli

EPEC

Enteropathogenic Escherichia coli

ETEC

Enterotoxigenic Escherichia coli

PCR

Polymerase chain reaction

PRRS

Porcine reproductive and respiratory syndrome

Authors’ contributions

FK and KET conceived of the idea and participated in the design of this study. FK, KBL, BH and KET read and approved the final version of the paper.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Additional file 1: (490.9KB, pdf)

PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) Checklist. (PDF 490 kb)

Data Availability Statement

The original research articles included in this systematic review are publicly available.

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