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Acta Tropica 103 (2007) 186-194

ACTATROPICA

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Non-biting cyclorrhaphan flies (Diptera) as carriers of intestinalhuman parasites in slum areas of Addis Ababa, Ethiopia

Sisay Getachew, Teshome Gebre-Michael *, Berhanu Erko,Meshesha Balkew, Girmay Medhin

AkliIu Lemma Institute ofPathobiology, Addis Ababa University, P.O. Box 1176, Addis Ababa, EthiopiaReceived 20 December 2006; received in revised form 8 May 2007; accepted 11 June 2007

Available online 16 June 2007

Abstract

A study was conducted to determine the role of non-biting cyclorrhaphan flies as carriers of intestinal parasites in slum areasof Addis Ababa from January 2004 to June 2004. A total of 9550 flies, comprising of at least seven species were collected fromfour selected sites and examined for human intestinal parasites using the formol-ether concentration method. The dominant flyspecies was Chrysomya rufifacies (34.9%) followed by Musca domestica (31%), Musca sorbens (20.5.%), Lucina cuprina (6.8%),Sarcophaga sp. (2.8%), Calliphora vicina (2.2%) and Wohlfahrtia sp. (1.8%). Six intestinal helminths (Ascaris lumbricoides,Trichuris trichiura, hookworms, HymenoIepis nana, Taenia spp. and Strongyloides stercoralis) and at least four protozoan parasites(Entamoeba histolytica/dispar, Entamoeba coli, Giardia lamblia and Cryptosporidium sp.) were isolated from both the externaland gut contents of the flies. A. lumbricoides and T. trichiura among the helminths and E. histolytica/dispar and E. coli amdng theprotozoans were the dominant parasites detected both on the external and in the gut contents of the flies, but occurring more in thelatter. Among the flies, C. rufifacies and M. sorbens were the highest carriers of the helminth and protozoan parasites, respectively.The public health significance of these findings is highlighted.(C) 2007 Elsevier B.V. All rights reserved.

Keywords: Non-biting flies; Intestinal human parasites; Mechanical transmission; Ethiopia

1. Introduction

Non-biting cyclorrhaphan flies are often associatedwith domestic dwellings, human and animal excreta andother wastes, especially during the dry season when theybreed prolifically and cause a constant annoyance forhumans. They are equipped with special sensory cellson their antennae that can detect strong compounds suchas ammonia and carbon dioxide emitted from faeces

Corresponding author. Tel.: +251 11 76 30 91;fax: +251 11 75 52 96.

E-mail address: Teshomegm@yahoo.com (T. Gebre-Michael).

0001-706X/$ see front matter (C) 2007 Elsevier B.V. All fights reserved.doi: 10.1016/j.actatropica.2007.06.005

and other decomposing organic materials (Tan et al.,1997). The free interchange that flies have with suchsites ensures that they are laden with disease causingorganisms on their mouthparts, body hairs and stickypads of their feet, as well as in their stomachs, fae-ces and vomitus (Graczyk et al., 2005). Their contactwith any foodstuff or their feeding habits, which ofteninvolves vomiting and defecating, will contaminate foodand utensils with potentially disease causing organisms(Greenberg, 1973). Moreover, the biology and ecol-ogy of non-biting flies suggest that their potential formechanical transmission of intestinal parasites is high.The females can live up to a month, lay up to six eggbatches, and produce up to 12 generations, and travel

S. Getachew et ai. /Acta Tropica 103 (2007) 186-194 187

up to 20 miles towards unsanitary sites (Greenberg,1971).

Several studies in different parts of the world showthat non-biting flies carry different stages of helminthand protozoan parasites. For example, Sulaiman et al.(1988), isolated eggs of Ascaris lumbricoides, Trichuristrichiura andhookworms from fly species of Chrysomya,Sarcophaga and Musca, which were collected fromrefuse dump and peridomestic sites in Malaysia. Doizet al. (2000) incriminated houseflies in the transmis-sion of giardiasis in Spain. More recently in Nigeria,Nmorsi et al. (2006) revealed the presence of both pro-tozoan parasites (Chilomastix mesnili, Cryptosporidiumparvum, Entamoeba histolytica and Isospora belli) andhelminth parasites (A. lumbricoides, Dicrocoelium hos-

pes, Enterobius vermicularis, Strongyloides stercoralisand T. trichiura) in four synanthropic fly species col-lected from various sites.

Most protozoan and helminth parasites are preva-lent in urban and rural areas of Ethiopia (Tedla, 1986;Tesfa-Yohannes and Kloos, 1993; Erko et al., 1998).Although other routes of transmission such as con-

taminated water, carriers and food handlers might bethe major possibilities, the likelihood of non-bitingflies mechanically transmitting these parasites cannot beexcluded. In a large city like Addis Ababa, there are

several potential breeding sites for flies. Some of theseinclude refuse/waste dumps, human and animal excreta.The breeding sites are often seen near residential areas,hotels, restaurants, hospitals, open markets, abattoirs andbutcheries. It is also common to see, in some sections ofthe city, excreta from improper latrines going into the

open sewerage ditches along streets and paths. Children,adults and the homeless in general often defecate outsidehouses in these open areas. These would lead to increasedcontact between flies and pathogen-positive fecal (orwaste) matter. With such obvious opportunities for con-tamination of human food, the chance of being infectedthrough consumption of contaminated and inadequatelycooked foodstuff is thus very high. Similar situations alsoexist in other highly populated urban slums in Ethiopia.Several non-biting cyclorrhaphan flies are involved in themechanical transmission of these pathogens in differentparts of the world (Greenberg, 1973). For example, thehouselfly (Musca domestica), the eye seeking fly (Muscasorbens) and other filth flies are commonly seen forag-ing on and breeding in garbage and other waste matterin Ethiopia. However, information regarding the speciesinvolved and the role of these flies as mechanical carriersand potential transmitters is not available in Ethiopia.

The aim of this study was therefore to determine thespecies of cyclorrhaphan flies frequenting the different

filth conditions (refuse dump, human/animal excreta,market quarters, etc.) in Addis Ababa and assess theirpotential role in mechanical transmission of helminthand protozoan parasites of man.

2. Materials and methods

2.1, Fly collection sites

Addis Ababa, the capital city, is located at an altitudeof 2400 m above sea level having an annual precipita-tion of more than 1000 mm per year and an estimatedpopulation of five million. Open-air defecation is not

uncommon to see in some quarters of the city by chil-dren and adults, especially, the homeless. Small open-airmarkets and inappropriate disposal of wastes are also

common in most parts of the city. For fly collection,potential foraging and breeding sites: garbage heaps,open defecating grounds, open-air small markets andbutcheries close to human dwellings were randomlyselected based on visual fly abundance.

2.2. Collection and identification offlies

At each site, flies were collected bi-monthly for 6months during the dry season (January-June 2004) bytwo persons using sweeping net for a 2 h morning sessionfrom 9.00 to 11.00 am when most flies are active. Fliestrapped were placed in small groups in test tubes, labeledand transported to the laboratory in a cooler box withice packs and stored in the refrigerator at -4C untilidentification and processing for parasite examination.Refrigeration would also minimize the possible cross-

contamination among flies that would otherwise resultfrom mobile and active flies.

2.3. Processing external body offlies for parasiteexamination

All trapped flies were killed by deep freezing or chlo-roform. Flies were then identified (Crosskey and Lane,1993), counted and pooled in batches of 10 (or less)of the same species. Each pool of flies was immersed insterile physiological saline and stirred with an applicatorstick for 5 min and vortexed for 2-3 min to wash-off anyparasitic cysts, eggs or larvae from the external body ofthe flies. The washed flies were then removed with sterileforceps and further processed for examination ofgut con-tents (see below). The suspension from the external bodywash was then processed using formol-ether concen-

tration techniques (Ritchie, 1948). A smear taken fromthe concentrate was examined under the microscope at

188 S. Getachew et al./Acta Tropica 103 (2007) 186-194

10-40 magnification for helminth ova/larvae and forprotozoan cysts and their number recorded.

For detection of Cryptosporidium spp., modifiedZiehl-Neelson staining method was applied as describedby Adegbola et al. (1994). Air-dried smears of flypreparations were fixed with methanol and stained withcarbol-fuchsin for 30 rain. These were then washed withtap water, decolorized with 1% acid alcohol for min,washed with tap water again, counter-stained with 1%methylene blue for min, rinsed in tap water and air-dried finally. The slides were then examined under amicroscope.

2.4. Processing and examination offly gut contentsfor parasites

After the washing procedure of flies described abovefor external parasites, the whole gut of each washedfly was dissected out on autoclaved microscope, slidesunder a stereoscopic microscope using entomologicalneedles and macerated to liberate the lumen contents.To further minimize cross-contamination among flies,the entomological needles and forceps were dipped inethanol and flamed between dissections. The pooled gutcontents of each species were then similarly processedusing formol-ether concentration method for micro-scopic examination of parasite ova, larvae and cysts asdescribed above.

3. Results

3.1. Species composition ofcollected non-bitingcyclorrhaphan flies

A total of 9550 non-biting cyclorrhaphan flies,belonging to 7 species, were collected from January toJune 2004. The dominant species was Chrysomya ruff-facies (34.9%) and least abundant was Wohlfahrtia sp.(1.9%) (Table 1).

tion expressed as number ofparasites per 100 flies variedwith site of collection, fly species and fly body region(external or internal).

3.2.1. C. rufifacies (Calliphoridae)This was the dominant fly species collected and was

most abundant in butchery sites and defecating grounds.It was multiply infected with both helminth and proto-zoan parasites. Among the helminths, it had eggs of A.lumbricoides, T. trichiura, hookworms, H. nana, Taeniasp. and larvae of S. stercoralis on the external body sur-face at rates ranging from 0.2 to 2.0 eggs/larvae per 100flies (Table 1). Similarly, these parasites were detectedin the gut contents of the fly at rates ranging from 0.1 to2.6 eggs/larvae per 100 flies. Defecating grounds werethe most important contaminating habitat with the para-sites. Eggs of A. lumbricoides, were the most prevalentboth on the external body (0.7-2.0 eggs/100 flies) andin the intestinal content (0.9-2.6 eggs/100 flies) fol-lowed by T. trichiura, which were 0.2-1.0 eggs/100 flieson the external body and 0.5-1.4 eggs/100 flies in theintestinal contents. Eggs of H. nana were the least com-mon and only detected in the gut content at the rateof 0.2 eggs/100 flies collected from garbage depositionsites.

Of the protozoan parasites, C. rufifacies carried cystsof E. histolytica/dispar, E. coli, G. lamblia and, Cryp-tosporidium sp. on the external body surface at ratesranging from 0.2 to 1.3 per 100 flies (Table 1). In thegut contents, the same parasites occurred at rates rangingfrom 0.1 to 2.1 cysts per 100 flies (Table 2). As with thehelminths, defecating grounds were the most importantcontaminating habitat for the fly with the protozoan par-asites. Of the protozoan parasites, E. histolytica/disparwas the most prevalent both on the external body (0.6-1.3cysts/100 flies) and in the intestinal content (0.1-2.1cysts/100 flies) followed by E. coli: 1.0-1.2 cysts/100flies on the external and 0.1-1.3 cysts/100 flies in theintestinal contents.

3.2. Flies, their parasites and level ofparasiteburden

Both intestinal helminth and protozoan parasites ofhumans were detected from both the external surfaceand gut contents of the flies collected. Six helminth par-asites were identified: these were A. lumbricoides, T.trichiura, hookworms, Hymenolepis nana, S. stercoralisand Taenia species. The protozoan parasites encounteredin different species of flies were E. histolytica/dispar,Entamoeba coli, Giardia lamblia and Cryptosporidiumspecies (Tables and 2). However, the burden of infec-

3.2.2. Musca domestisca (Muscidae)It was the second dominant fly species collected and

was most abundant in garbage dumps. It carried bothhelminth and protozoan parasites. Among the helminths,it carried eggs of A. lumbricoides, T. trichiura, hook-worms, Taenia sp. and larvae of S. stercoralis on theexternal body surface at rates ranging from 0.1 to 1.7per 100 flies (Table 1). In the intestinal contents, onlyeggs of A. lumbricoides, T. trichiura and Taenia spp.were detected at rates ranging from 0.6 to 2.0 per 100flies (Table 2). Defecating grounds which were the leastpreferred foraging habitats were the most dangerous con-

TableParasite burdens expressed as number of eggs, larvae or cysts per 100 flies detected on the body of trapped flies from different sites in Addis Ababa

Species; number collected (%) Sites of collection Number of flies Helminth parasites per 100 flies Protozoan parasites per 100 fliesdissected

A1 Tt Hw Hn Tae Ss Eh Ec G1 Cry

Chrysomya rufifacies; 3330 (34.9)

Musca domestica; 2960 (31)

Musca sorbens; 1960 (20.5)

Lucilia cuprina; 650 (6.8)

Calliphora vicina; 210 (2.2)

Sarcophaga spp.; 270 (2.8)

Wohlfahrtia spp." 170 (1.8)

Butchery 1260 0.7 0.2 0 0 0.5 0 0 0 0 0.2Garbage 460 0.9 0.7 0 0 0 0 0.6 0 0 0Market 420 0.9 0.4 0.2 0 0 0 1.2 1.2 0.2 0Defecating grounds 1190 2.0 1.0 0 0 0 0.3 1.3 1.0 0.08 0.3

Butchery 660 0.3 0.1 0 0 0.1 0.1 0.1 0.1 0 0.3Garbage 1060 0.2 0.1 0 0 0 0 0.5 0.1 0.2 0Market 760 0.5 0.4 0 0 0 0 0.7 0.9 0 0Defecating grounds 480 1.7 0.8 0.2 0 0 0.2 2.0 1.5 1.0 0.2

Butchery 190 0.5 0 0 0 0 0 0.5 0.5 0 0Garbage 500 0.8 0.6 0 0 0 0.2 1.2 1.0 0 .0Market 670 0.7 0.1 0 0 0 0 0.6 0.7 0.4 0Defecating grounds 600 2 1.0 0.3 0.5 1.0 0.6 2.5 2.0 0.5 1.0

Butchery 200 0.5 0 0 0 0 0 0 0 0 0Garbage 130 0 0 0 0 0 0 0 0 0 0Market 140 0.7 0 0 0 0 0 0 0 0 0Defecating grounds 180 2.2 1.1 0 0 0 0 1.1 0 0 0

Market 80 0 0 0 0 0 0 0 0 0 0Garbage 130 0 0 0 0 0 0 0 0 0 0

Defecating grounds 50 0 0 0 0 0 0 2 0 0 0Butchery 130 0 0 0 0 0 0 0 0 0 0Garbage 90 0 0 0 0 0 0 0 0 1.1 0

Butchery 70 0 0 0 0 0 0 0 0 0 0Defecating grounds 100 0 0 0 0 0 0 0 0 0 0

A1, A. lumbricoides; Tt, T. trichiura; Hw, hookworm; Hn, H. nana; Ta, Taenia spp.; Ss, S. stercoralis; Eh, E. histolytica/dispar; Ec, E. coli; G1, G. lamblia; Cry, Cryptosporidium spp.

Table 2Parasite burdens expressed as number of eggs, larvae or cysts per 100 flies detected in the gut of trapped flies from different sites in Addis Ababa

Species; number collected (%) Sites of collection Number of fliesdissected

Helminth parasites per 100 flies Protozoan parasites per 100 flies

A1 Tt Hw Hn Tae Ss Eh Ec Gl CryChrysomya rufifacies; 3330 (34.9)

Musca domestica; 2960 (31)

Musca sorbens; 1960 (20.5)

Lucilia cuprina" 650 (6.8)

Calliphora vicina; 210 (2.2)

Sarcophaga spp.; 270 (2.8)

Wohlfahrtia spp." 170 (1.8)

Butchery 1260 1.1 0.5 0 0 1.3 0 0.1 0.1 0Garbage 460 1.3 0.7 0 0.2 0 0.2 0.5 0.2 0.5Market 420 0.9 1.4 0 0 0 0 0.9 0.4 lYDefecating grounds 1190 2.6 1.3 0.1 0 1.0 0.1 2.1 .3 0.2

Butchery 660 0.4 0.2 0 0 0.6 0 0.6 0.7 0.2Garbage 1060 0.3 0.2 0 0 0 0 0.7 0.4 0.3Market 760 0.7 0.4 0 0 0 0 0.9 0.5 0Defecating grounds 480 2.0 1.5 0 0 0 0 2.3 2.0 0.3 0.3

Butchery 190 0 0 0 0 0 0 1.5 0.5 0Garbage 500 0 0 0 0 0 0 1.6 1.2 0Market 670 0 0 0 0 0 0 0.9 1.0 0.4Defecating grounds 600 2 1.0 0.3 0.5 1.0 0.6 3.3 2.0 0.3

Butchery 200 1.0 0 0 0 1.0 0 0 0 0Garbage 130 0 0 0 0 0 0 0 0 0Market 140 1.2 0 0 0 0 0 0 0 0Defecating grounds 180 1.8 1.8 0 0 0 0 0 1.1 0

Market 80 0 0 0 0 0 0 0 0 0Garbage 130 0 0 0 0 0 0 0 0 0

Defecating grounds 50 2.0 0 0 0 0 0 2.0 0 0Butchery 130 0.8 0 0 0 0 0 0 0.8 0Garbage 90 1.1 0 0 0 0 0 1.1 0 0

Butchery 70 0 0 0 0 0 0 0 0 0Defecating grounds 100 1.0 0 0 0 0 0 0 0 0

0.5000.1

0.4000

0000.5

0000

00

000

00

A1, A. lumbricoides; Tt, T. trichiura; Hw, hookworm; Hn, H. nana; Ta, Taenia spp.' Ss, S. stercoralis; Eh, E. histolytica/dispar; Ec, E. coli; G1, Giardia lamblia; Cry, Cryptosporidium spp.

S. Getachew et al. /Acta Tropica 103 (2007) 186-194 191

taminating habitats were these parasites. Ofthe helminthparasites detected, A. lumbricoides, was the most preva-lent both on the external body (0.2-1.7 eggs/100 flies)and in the intestinal content (0.3-2.0 eggs/100 flies) fol-lowed by T. trichiura, on the external body (0.1-0.8eggs/100 flies) as well as in the intestinal contents(0.2-1.5 eggs/100 flies). The least abundant was thehookworm (0.2 eggs/100 flies on the external) from fliescollected on defecating grounds.Among the protozoan parasites, M. domestica also

carried cysts of E. histolytica/dispar, E. coli, G. lambliaand Cryptosporidium sp. on the external body at ratesranging from 0.1 to 2.0 per 100 flies (Table 1). Similarly,the same parasites were detected in the gut contents at

rates ranging from 0.2 to 2.3 cysts per 100 flies (Table 2).As with the helminths, defecating grounds were the mostdangerous contaminating habitats with the above para-sites although it was the least preferred foraging habitat.Of these, cysts of E. histolytica/dispar were the mostprevalent both on the external body (0.1-2.0/100 flies)and in the intestinal content (0.6-2.3/100 flies) followedby E. coli which were 0.1-1.5 cysts/100 flies on theexternal body and 0.4-2.0 cysts/100 flies in the intestinalcontent.

3.2.3: Musca sorbens (Muscidae)It was the third most abundant species collected

and was most common in market areas and defecat-ing grounds. It was multiply infested with six helminthand four protozoan parasites. Of the helminths, it car-

ried eggs of A. lumbricoides, T. trichiura, hookworms,Taenia spp., H. nana and larvae of S. stercoralis on theexternal body at rates ranging from 0.1 to 2.0 per 100flies (Table 1). In the gut, the same parasites were alsodetected at rates ranging from 0.6 to 2.0 eggs/larvae per100 flies (Table 2). A. lumbricoides was again the mostprevalent, being found at the rate of 0.5-2.0 eggs/100flies on the external body and 2.0 eggs/100 flies in thegut contents. T. trichiura was the next common helminthparasite at the rate of 0.1-1.0 eggs/100 flies on the exter-nal body; although unexpectdely was much scarcer inthe guts.

M. sorbens also carried protozoan cysts of E. histolyt-ica/dispar, E. coli, G. lamblia and Cryptosporidium sp.on the external body surface at rates ranging from 0.4 to2.5 per 100 flies (Table 1). The same cysts were detectedin the gut contents at rates ranging from 0.4 to 3.3 per100 flies (Table 2). Defecating grounds were the mostdangerous contaminating habitats with the protozoanparasites of which E. histolytica/dispar was again thepredominant parasite both on the external body (0.5-2.5cysts/100 flies) and in the intestinal contents (0.9-3.3

cysts/100 flies) followed by E. coli both on the externalbody and in the intestinal contents (0.5-2.0 cysts/100flies).

3.2.4. Lucilia cuprina (Calliphoridae)It was the fourth most abundant species and was more

common in butchery areas and defecating grounds. Onlytwo helminth parasites (A. lumbricoides and T. trichiura)were recovered from the external body at the rate of0.5-2.2 eggs per 100 flies. The two parasites plus Taenia

sp. were recovered from the gut contents at the rate of1.0 to 1.8 eggs per 100 flies. A. lumbricoides was thedominant parasite both on the external body (0.5-2.2eggs/100 flies) as well as in the gut contents (1.0-1.8eggs/100 flies) followed by T. trichiura, though scarcelyrecovered from a limited number of the flies.

Regarding protozoan parasites, it only carried cystsof E. histolytica/dispar at a rate of 1.1 cysts/100 flies onthe external body and only E. coli from its gut contents(1.1 cysts/100 flies) (Tables and 2).

3.2.5. Calliphora vicina (Calliphoridae)It was the least abundant of all the calliphorids col-

lected and none was found infected either on its external

or internal body (Tables 1 and 2).

3.2.6. Sarcophaga sp. (Sarcophagidae)This was the most abundant of the two species col-

lected in the family and was the fifth common of allspecies collected. None harboured helminths on theexternal body but was only found positive for A. lum-bricoides in the gut contents at the rate of 0.8-2.0 eggsper 100 flies (Tables and 2). Protozoan parasites (E.histolytica/dispar and G. lamblia) were recovered on theexternal body at a rate of 1.1-2.0 cysts per 100 flies, butonly E. histolytica/dispar and E. coli were recovered inthe gut contents at the rate of 0.8-2.0 cysts per 100 flies(Tables and 2). E. histolytica/dispar was most prevalentin both situations.

3.2.7. Wohlfahrtia sp. (Sarcophagidae)It was the least abundant of all flies collected and none

was found infected (Tables and 2).The level of parasite burdens of the three dominant

fly species (C. rufifacies, M. domestica and M. sor-

bens) with helminth and protozoan parasites is depictedin Figs. and 2, respectively. A. lumbricoides was themost abundant hlminth parasite detected followed by T.trichiura both on the external body and in the gut con-

tents, being much higher in the latter. C. rufifacies was

the highest carrier of these parasites in both situations.Likewise, E. histolytica/dispar was the most prevalent

192 S. Getachew et al. /Acta Tropica 103 (2007) 186-194

C. rufifacies [] M. domestica [] M. sorbens

1.81.61.41.2

0.80.60.40.20

Helminths

Fig. 1. The level of human intestinal helminth parasite burden on theexternal body and in the guts of the three dominant flies (Chrysomyiarufifacies, Musca domestica and Musca sorbens). (Note: A1, A. lum-bricoides; Tt, T. trichiura; Hw, hookworm; Hn, H. nana; Ta, Taenia

sp.; Ss, S. stercoralis.)

C. rufifacies M. domestica [] M. sorbens

1.8

.-- 1.6

1.4

1.2

0.8

0.6,

0.4

xterna bodyEtd

GutProtozoan parasites

Fig. 2. The level of human intestinal protozoan parasite burden on theexternal body and in the guts of the three dominant flies (Chrysomyiarufifacies, Musca domestica and Musca sorbens). (Note: Ehd, E. his-tolytica/dispar; Ec, E. coli; G1, Giardia Iamblia; Cry, Cryptosporidiumsp.)

protozoan parasites followed by E. coli, and both were

more common in the gut than on the external body.Unlike the helminths however, the protozoan parasiteswere mostly carried by M. sorbens both on the externalbody and in the gut contents.

4. Discussion

In this study, a total of9550 non-biting cyclorrhaphanflies, belonging to 7 species,

were collected from Januaryto June 2004 from four potential breeding sites. C. ruff-

facies, M. domestica and M. sorbens were found to bethe dominant species.

In most collected flies, females dominated over maleswhich could be due to their active search for suitableoviposition and feeding substrata, although no signifi-cant difference was observed between the sexes in theircapacity as parasite carriers. The high abundance of C.rufifacies in butchery and defecating grounds may be dueto the scavenger feeding habit of the fly (feeding on deadtissue and other maggots) and high preference for liquidfecal matter. Boonchu et al. (2004) have observed thatmetallic flies showed the highest preference for pork vis-cera as compared to sarcophagid and muscoid flies. Thehigh abundance of M. domestica in garbage areas maybe due to the ability to feed on drier food substrate. Eesaand E1-Sibae (1993) also showed that of the five synan-thropic flies collected from different breeding areas, M.domestica was abundant in rubbish dumps, constitutingabout 98% of all the species collected. M. sorbens was

more abundant near defecating grounds, market areas

and garbage dumps and could be due to its higher feed-ing preference for human fecal materials which are oftenseen in the vicinity.

Domestic filth flies of the families Calliphoridae,Muscidae and Sarcophagidae have close association withman and several investigators in different countries havereported various pathogenic organisms in a number offly species and their potential as mechanical vectors ofthese intestinal parasites.

In Rio de Janeiro (Brazil), de Oliveira et al. (2002) iso-lated Ascaris sp., Trichuris sp., Toxascaris sp., Toxocara

sp., Capillaria sp., and others from C. megacephala andM. domestica on their body surface and in their intestinalcontents. These fly species were found to carry eggs ofthe above helminth parasites in slum areas of metropoli-tan Manila, the Philippines (Monzon et al., 1991), and a

significant proportion of C. megacephala was found pos-itive compared to M. domestica. Furthermore, Umecheand Mandah (1989) examinded 5000 houseflies col-lected from markets and residential areas in Nigeria anddetected A. lumbricoides ova, S. stercoralis larvae andToxocara ova in varying degree of prevalence.

The present study, the first of its kind in Ethiopia,revealed that eggs/larvae of six intestinal helminth par-asites [A. Iumbricoides, T. trichiura, hookworms, H.

nana, Taenia sp. and S. stercoralis] were detected on

the external body surfaces as well as in the gut lumensof non-biting cyclorrhaphan flies. The former twohelminths were the predominant parasites isolated. It wasalso shown that C. rufifacies, the predominant speciescomprising 34.9% of all flies trapped, was the major car-

tier of these parasites. More infested flies of the species

S. Getachew et al. /Acta Tropica 103 (2007) 186-194 193

came from collections made near defecating grounds andthis was probably the major source of contamination forC. rufifacies. This is somewhat similar to the observa-tion in Malaysia by Sulaiman et al. (1988) where the

same species and a related species (C. megacephala)were found to be major carriers of A. lumbricoides andT. trichiura eggs mostly in their guts. However, the den-sities of these parasites in the Malaysian flies was muchhigher than the Ethiopian species.

In addition, synanthropic flies (M. domestica inparticular) have also been incriminated as potentialmechanical vectors of different protozoan parasites suchas Sarcocystis spp., Toxoplasma gondii, Isospora spp.,Giardia spp., E. coli, E. histolytica, Endolimax nana,Trichomonas spp., Hammondia spp. and C. parvum else-where (Graczyk et al., 1999a,b, 2000, 2003, 2005). In thepresent study too, at least four species of human proto-zoan parasites: E. histolytica/dispar, E. coli, G. lamblia,Cryptosporidiurn sp. were detected in various fly speciescollected. The former two species occurred more fre-quently than the others. As in helminth parasites, theprotozoan cysts were more abundant in the gut contentsthan on the external body surface of the flies. The majorcarrier of the most frequent protozoan cysts was M. sor-

hens followed by M. domestica coming from defecatinggrounds. M. sorbens was the third most abundant speciesand made up 22.6% of the flies trapped. M. sorbensbreeds mainly on human and animal faeces but forageson the human face and moist skin as a result of which is awell known mechanical vector of trachoma (Emerson etal., 2000, 2001). C. parvum is an anthropozoonotic par-asite which significantly contributes to the mortality ofimmunocomporomised people. The pathogen can alsoseverely debilitate healthy individuals in which infec-tions can be initiated by as few as 30 oocysts, and inpeople with impaired immune system, a single oocystcan initiate infection (Graczyk et al., 2000). Filth flies cantransport oocysts of C. parvum on their external surfacesand in their digestive tracts and contaminate food stuffvia mechanical dislodgment, fecal deposition and regur-gitation (vomits) of oocysts (Graczyk et al., 2003, 2005).In the present work, although less frequent than the otherprotozoan parasites, Cryptosporidium sp. (presumablyC. parvum) were extracted from both the external surfaceas well as gut content of M. domestica, C. rufifacies andM. sorbens collected at different sites. Thus, the presentwork also indicated that filth flies with access to a sub-strata containing oocysts of this and other parasites can

transport these pathogens in their digestive tracts and ontheir external body surface and potentially could contam-inate food of inhabitants near the sites where flies havebeen collected. It has been shown that houseflies caught

on refuse dumps in six areas of Ibadan (Nigeria) were

found to harbour intestinal parasitic cysts and eggs intheir alimentary canal which were similar to those foundin the faeces of the community living in the environment(Dipeolu, 1977).

These parasites are common and occur in variousdegrees of prevalence in children and adults both inurban and rural Ethiopia (Tedla, 1986; Tesfa-Yohannesand Kloos, 1993; Erko et al., 1998). The likelihood ofnon-biting cyclorrhaphan flies in mechanical transmis-sion of such intestinal parasites to people is difficult to

prove. However, it seems likely that the tendency ofsomechildren including adults to defecate in exposed situ-ations and the foraging activity of these flies on fecaland other waste matter will lead to contact between fliesand positive faeces. It has also been established thatexternal body parts of flies such as antennae, mouth-parts, legs, gut contents as well as vomits and faeces will

carry pathogens which are ideally situated for diseasetransmission (Graczyk et al., 2003, 2005). With suchobvious opportunities, the chance for contamination ofhuman food and transmission would be high. Eggs adher-ing to the surface of the fly are quickly removed as thefly cleans itself, this beneficial act of auto-sterilizationusually occurs shortly after the fly quits the surface on

which it has been feeding. Oyerinde (1976), workingwith experimentally infected M. domestica found thatlarvae of hookworms survived longer in the gut than onthe external surface of the fly. The present study revealedthat some cycolrrhaphan flies frequenting exposed refusedumps and faeces can carry human enteroparasites in

a big and tropical city like Addis Ababa. It there-fore becomes imperative to urgently institute control

measures of these flies through massive education on

improving the standard of environmental sanitary condi-tions. Control of synanthropic flies is known to coincidewith drastic reductions in outbreaks of food-borne dis-

eases (Graczyk et al., 2005).

Acknowledgements

We would like to thank the University ofAddis Ababafor financial support of this investigation. The excellenttechnical assistance of Kokebe Gebre-Michael, KonjitTadesse, Sisay Dessie and Hussien Mohammed is alsogratefully acknowledged.

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