The housefly (Musca domestica) is the most common of all domestic flies, accounting for about 91% of all flies in human habitations, and one of the most widely distributed insects found all over the world. It is a known pest that is capable of causing annoyance and carrying various microbial, including parasitic diseases, to man and animals and has been recognized as an important mechanical vector for a variety of pathogenic intestinal parasites including helminths and protozoa in different regions of the world. This is mainly attributed to its structural morphology, filthy, and feeding habits.
Flies are commonly found both indoors and outdoors, especially in unsanitary areas where they persist on excrement, dead animal bodies, and contaminated areas where fecal matter, large amounts of organic waste, and piles of garbage are left exposed and unattended. Furthermore, when infected persons excrete in open areas, there is an increased risk of contact between flies and pathogen-contaminated fecal matter and human/animal foods and drinks. Several studies including those of Sualiman et al. in Tokyo and Getachew et al. in Ethiopia have documented house flies as vectors of eggs of Ascaris lumbricoides, Trichuris trichiura, Enterobius vermicularis, Taenia sp., Hymenolepis nana, Toxocara canis, hookworm larvae, and Strongyloides larvae.
Enteric parasitic infections are still a major health problem globally, especially in developing countries with estimated 3.5 billion people being affected worldwide; of these, about 895 million people are infected with soil-transmitted helminths. About 1.5 million Nigerians suffer from Ascariasis alone and several thousand with Strongyloidiasis, Trichuriasis, Enterobiasis, and hookworm infections.
The high prevalence rate of intestinal helminths in Nigeria, especially among primary school children, was confirmed by Dada-Adegbola et al. who recorded a 68.2% prevalence rate of intestinal helminths among children aged 0–7 years. The prevalence of these parasites infections is a major public health risk because their predisposing factors which include lack of or insufficient access to safe drinking water, unhygienic environment, poor personal hygiene practices, poverty, malnutrition, and ignorance abound in the subregions.
The purpose of this study was to investigate the common filth housefly, M. domestica, for intestinal parasites of medical importance, assess its role in parasitic disease transmission, and make appropriate recommendations toward their management and effective control of the associated parasitic diseases in the community.
MATERIALS AND METHODS
The study area for this work was Calabar South Local Government Area in Calabar, Cross River State, Southern Nigeria, between November 2017 and February 2018. Specific areas in Calabar South were randomly selected for sample collection. The areas were classified as sanitary and insanitary areas. The sanitary areas included restaurants and kitchens, while the insanitary areas included s, garbage dump, and public latrine areas [Figure 1].
Collection and identification of flies
The flies were captured from sanitary and insanitary locations by placing an insect gum trap at each specimen collection site for as long as 1 to 2 h. Each fly trapped was carefully examined using the morphologic criteria and the identification keys to ascertain the species. All flies identified as M. domestica were aseptically transferred, using sterile forceps, from the insect trap into an appropriately labeled, sterile screw-capped specimen bottle. In all, 300 M. domestica specimens (150 from sanitary and 150 from insanitary areas, each pooled in 30 batches of five flies per pool) were selected for the study and transported to the laboratory for processing.
Processing of specimens from sanitary areas for parasites [Figure 2]
External surface of each pooled specimen in a sterile centrifuge tube was washed vigorously with 5 ml of sterile normal saline. Manual shaking technique was used to dislodge the parasites from the exoskeleton of the flies and the washout spun at 3000 rpm for 5 min. Direct smear of the deposit was examined under the microscope with ×10 and ×40 objective lenses for possible parasites.
Each pooled, washed specimen was rinsed with 10% alcohol, air-dried, and the flies crushed in a sterile universal container using sterile forceps. The crushed specimen was emulsified in the universal container with a little quantity of normal saline using an applicator stick. Direct smear microscopy and formol-ether concentration methods were adopted for the detection of helminths’ ova/larvae and protozoan trophozoites/cysts.
Processing of specimens from insanitary areas for parasites
The 150 M. domestica specimens from insanitary locations, pooled in 30 batches of five flies each, were processed separately but with the same procedure as for those from sanitary locations [Figure 2].
Data obtained in this study were analyzed using Statistical Package for the Social Sciences (SPSS, Armonk, NY: IBM Corp., 2012), version 21.0, and Chi-square test at a significant level of P < 0.05 and 95% confidence interval.
Table 1 shows the distribution of parasites in washed and crushed pooled fly specimens. Overall, 28 (46.7%) of the 60 pooled specimens of 5 flies each from both locations examined were positive for parasites with helminths and protozoa having similar frequency (14, 23.3%) each. Statistically significant number of fly specimens carried parasites on their external (washed) surface samples than in their gut (crushed) contents, 23 (76.7%) versus 5 (16.7%), respectively (χ2= 21.60, P = 0.000). Protozoa dominated in the external surface of flies against helminths, 13 (43.3%) versus 10 (33.3%), respectively, while helminths dominated in their gut contents, 4 (13.3%) versus 1 (3.3%), respectively.
Table 2is on the carriage of parasite by fly specimens based on location. Greater number of insanitary specimens (19, 63.3%) were found to carry parasites than sanitary specimens (9, 30.0%). This difference was statistically significant (χ2= 6.40, P = 0.0114). Greater number of the insanitary specimens carried protozoa than those with helminths, 11 (36.7%) versus 8 (26.7%), respectively, whereas more of sanitary specimens carried helminths than protozoa, 6 (20.0%) versus 3 (10.0%), respectively. These differences were statistically insignificant, P > 0.05.
Figure 3 shows the frequency of parasites species in pooled fly specimens. Parasites detected include Entamoeba histolytica/dispar (39.3%), followed by hookworm (21.4%), A. lumbricoides (17.9%), T. trichiura (14.3%), and Giardia intestinalis (7.1%).
The overall number of specimens tested positive for presence of parasites in this study, 46.7%, is higher than 2.9% recorded in Khartoum, Sudan, and 30.9% in Lahore.
Greater number of studied fly specimens carrying parasites on their external surface (76.7%) than in their gut contents (16.7%) is attributed to the insect's habit of wallowing in filth and the possession of external structures well adapted for taking up and carrying of living organisms from the contaminated materials. This differs from the report of Adenusi and Adewoga that the quantity of pathogens present in the gut is usually higher than the quantity present on the body surfaces, suggesting that the flies’ feces and vomitus may also serve as a major route of transmission of pathogens. However, the World Health Organization further explained that pathogens on the outer surface of the housefly may survive for a few hours, while those in the gut could be viable for several days.
Helminths and protozoan parasites being detected in the same ratio (23.3%) for each in this study rhymes with the report of El-Sherbini and El-Sherbini that although bigger cells such as helminth eggs are carried by flies on their external surface, small cystic stages of human infectious intestinal protozoa can be ingested as well as carried on the exoskeleton.
The predominance of protozoan parasites in the external body surface of flies (13, 43.3%) over helminths (10, 33.3%) in this study suggests that most of these flies must have been from the insanitary locations, most of which were shown [Table 2] to carry protozoa than helminths. The disparities could be attributed to the difference in environmental hygiene and contamination.
In the present study, in insanitary and sanitary areas, E. histolytica/dispar, G. intestinalis, A. lumbricoides, Trichuris trichuira, and Ancylostoma duodenale (hookworm) were detected. Recovery of these parasites from studied flies in the study area establishes the role of M. domestica in the transmission of parasitic diseases in this community and the larger society. Its long flight ranges help the spreading of parasites from one area to another including other countries. It serves as a good carrier of disease agents, also due to its predilection for feeding on human and animal wastes, garbage, and human foods. Studies have shown that more than 100 pathogens associated with the housefly may cause disease in humans and animals, including parasitic worms, infantile diarrhea, cholera, and dysentery, as evidenced in previous reports in our study area: that of Usip and Ita[2017) with 26.6% parasite carriage, six types of parasite, E. histolytica/dispar (6.2%) and hookworm (5.6%) being the most frequent among children, aged 6–7 years, and also that of Aleru et al. who found 88% frequency among primary school children with A. lumbricoides as the most frequently detected helminth.
The transference of infection occurs when pathogenic organisms are picked up from garbage, sewage, and other sources of filth by the flies and deposited on human and animal foods through their s and other body parts, their vomitus, and feces.,
A common observation in the study area showed a common problem of lack of good toilet facilities in some houses. Most of the residents were in poor living conditions with low standard of living and used the drainage system and refuse dumps as their toilets. In such conditions, the abundance of houseflies and their menace to public health cannot be overlooked. Previous studies also show that the accumulating of refuse in urban and agricultural areas provides the parasites with new feeding sources, and detected that houseflies take up infectious pathogens from refuse and transmit them purely mechanically.
E. histolytica/dispar being the most frequently encountered parasite in this study is an indication of poor hygiene and sanitation due to poor water supply commonly observed in the study area, as this parasitic disease's transmission is water and hygiene related.; E. histolytica is the pathogenic species of ameba that causes amebiasis or amebic dysentery. The WHO (2010), ranked amebiasis as the third most important parasitic disease, causing 100,000 deaths annually, especially in the developing countries with a major cause of transmission as poor sanitation, particularly where food and water are involved. More than three billion people, which translate to half of the global population, do not have access to proper sanitation. About 3 million children die each year from diseases associated with poor sanitation worldwide. Brooks asserted that in Africa, in tropical Africa in particular, more than half of the population has little or no access to safe drinking water and the people are constantly faced with food insecurity and shortage, which largely contribute to infection with E. histolytica and other enteric parasites and adversely contribute to a high prevalence of diarrheal diseases.
Amebiasis is prevalent in Nigeria, and its widespread prevalence, especially among growing children of school age, has been attributed to a multiple environmental source of transmission.
Limitations of the study
The limitations of this study included limited financial resources which limited its scope. This also led to the pooling of the fly specimens as against processing them individually.
This study has recorded a high rate of carriage of medically important parasites in M. domestica, especially in the insanitary areas of Calabar South, with E. histolytica/dispar being the most frequently encountered. This has confirmed M. domestica as a mechanical vector of these medically important parasites which suggests their role in parasitic disease transmission. Effective control of their population in human and animal habitats and increased public awareness on their health hazards in other to stop these diseases are recommended.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
1. Graczyk JK, Knight R, Eilman RH, Grankold MR. The role of non-biting flies in the epidemiology of human infectious diseases Microbes Infect. 2001;3:231–5
2. Dübendorfer A, Hediger M, Burghardt G, Bopp D. Musca domestica
, a window on the evolution of sex-determining mechanisms in insects Int J Dev Biol. 2002;46:75–9
3. Graczyk TK, Knight R, Tamang L. Mechanical transmission of human protozoan parasites by insects Clin Microbiol Rev. 2005;18:128–32
4. Brazil SM, Steelman CD, Szalanski AL. Detection of pathogen DNA from filth flies (Diptera: Muscidae) using filter paper spot cards J Agric Urban Entomol. 2009;24:13–8
5. Larraín P, Salas C, Salas F. House fly (Musca domestica
L.) (Diptera Muscidae) development in different types of manure Chil J Agric Res. 2008;68:192–7
6. Mayr A. Spread of infectious agents through refuse by domestic, community and field parasites with special reference to human health Zentralbl Bakteriol Mikrobiol Hyg B. 1983;178:53–60
7. Nazni WA, Luke H, Wan Rozita WM, Abdullah AG, Sa’diyah I, Azahari AH, et al Determination of the flight range and dispersal of the house fly, Musca domestica
(L.) using mark release recapture technique Trop Biomed. 2005;22:53–61
8. Szalanski AL, Owens CB, McKay T, Steelman CD. Detection of campylobacter and Escherichia coli
O157: H7 from filth flies by polymerase chain reaction Med Vet Entomol. 2004;18:241–6
9. Sualiman S, Mohammod CG, Marwi MA, Oothuman PYokogawa M. Study on the role of flies in transmitting helminths in a community Collected Papers on the Control of Soil-Transmitted Helminthiasis. 1989;4 Tokyo APCO:59–62
10. Getachew S, Gebre-Michael T, Erko B, Balkew M, Medhin G. Non-biting cyclorrhaphan flies (Diptera) as carriers of intestinal human parasites in slum areas of Addis Ababa, Ethiopia Acta Trop. 2007;103:186–94
11. Taghipour A, Ghodsian S, Jabbari M, Olfatifar M, Abdoli A, Ghaffarifar F. Global prevalence of intestinal parasitic infections and associated risk factors in pregnant women: A systematic review and meta-analysis Trans R Soc Trop Med Hyg. 2021;115:457–70
12. Aleru C, Abbey S, Obisike U, Elekima I, Christian S, Henshaw M. The prevalence of intestinal helminths infections among primary school children in Calabar south local government area, cross rivers state, Nigeria Int J Sci Res. 2016;5:1809–14
13. Dada-Adegbola HO, Oluwatoba AO, Falade CO. Prevalence of multiple intestinal helminths among children in a rural community Afr J Med Med Sci. 2005;34:263–7
14. Ijagbone IF, Olagunju TF. Intestinal helminthe parasites among school children in Iragbiji, Boripe local government area, Osun state, Nigeria Afr J Biomed Res. 2006;9:63–6
15. Prüss-Ustün A, Bartram J, Clasen T, Colford JM Jr, Cumming O, Curtis V, et al Burden of disease from inadequate water, sanitation and hygiene in low- and middle-income settings: A retrospective analysis of data from 145 countries Trop Med Int Health. 2014;19:894–905
16. Dodge HR Diptera: Pictorial Key to Principal Families of Public Health Importance. 1953 Atlanta, Ga, USA U.S. Department of Health, Education and Welfare
17. Ochei J, Kolhatkar L Medical Laboratory Science Theory and Practice. 2000 New Delhi Tata McGraw Hill Publishers:947–9
18. World Health Organization. Manual of Basic Techniques for a Health Laboratory. 20032nd ed Geneva World Health Organization:111–56
19. Ibrahim AM, Ahmed HH, Adam RA, Ahmed A, Elaagip A. Detection of intestinal parasites transmitted mechanically by house flies (Musca domestica
, Diptera: Muscidae) infesting slaughterhouses in Khartoum State, Sudan Int J Trop Dis. 2018;1:011
20. Humayun M, Hussain R, Chaudhry NA, Khan SA, Tayyab M. Prevalence of parasites in house-flies from different areas of Lahore Biomedica. 2002;18:31–3
21. Adenusi AA, Adewoga TO. Studies on the potential and public health importance of non-biting synanthropic flies in the mechanical transmission of human enterohelminths Trans R Soc Trop Med Hyg. 2013;107:812–8
22. World Health Organization. Houseflies. Carriers of Diarrhoeal Diseases and Skin and Eye Infections (PDF). Last accessed on 2017 Sep 25:302–8 Available from: https://wikimili.com/en/Housefly#citeref-WHO39-1
23. El-Sherbini GT, El-Sherbini ET. The role of cockroaches and flies in mechanical transmission of medical important parasites J Entomol Nematol. 2011;3:98–104
24. Axtell RC. Integrated fly -control program for caged-poultry houses J Econ Entomol. 1970;63:400–5
25. Esiet LP, Edet IA. Comparative prevalence of intestinal parasites among children in public and private schools in Calabar south, Calabar, cross river state, Nigeria Am J Res Commun. 2017;5:80–97
26. Hewitt CG The House-Fly: Musca Domestica
Linn: Its Structure, Habits, Development, Relation to Disease and Control. 2011 Canada Cambridge University Press:181–4
27. Service M Medical Entomology for Students. 20084th ed UK Cambridge University Press:140–1
28. World Health Organization (WHO). Kenya-Arid and Semi Arid Lands Sector Wide Program Project. 2010;1 Kenya World Health Organization (WHO):1–4
29. United Nations Children Fund (UNICEF). Kenya Annual Report 2008. Programs; Water Environment and Sanitation. 2009 Kenya UNICEF Kenya:22–3
30. Brooks J Water and Sanitation for 6,000 People in Kenya. A Project Report; Quarterly Update. 2009 United Kingdom Global/Giving Works-Kenya:1–11
31. Ajero CM, Nwoko BE, Nwoke EA, Ukaga CN. Human amoebiasis: Distribution and burden; and the Nigerian environment Int Sci Res J. 2008;1:130–4