Filth flies and human food-borne protozoan diseases
- Mechanical Transmission of Human Protozoan Parasites by Insects
There are 108 families of Diptera containing over 120,000 species, of which approximately 350 fly species in 29 families have been potentially associated with the spread of food-borne diseases (22). Over 50 species of synanthropic flies have been reported to be associated with unsanitary conditions and involved in dissemination of human pathogens in the environment (22). Of these, 21 species of filth flies have been involved in transmission of human gastrointestinal diseases (22) (see the Introduction). Flies from these families breed in animal manure and human excrement, garbage, animal bedding, and decaying organic matter (5). The ecology and biology of breeding, indiscriminate traveling between filth and human food, and feeding habits of nonbiting flies are similar (5).
Promiscuous-landing synanthropic flies are recognized vectors for a variety of protozoan parasites of public health importance (15, 22). Synanthropic flies, particularly the common house fly (Musca domestica), have been identified as vectors of protozoan parasites such as Sarcocystis spp. (19), Toxoplasma gondii (31), Isospora spp. (17), Giardia spp. (3, 13, 16, 29), Entamoeba coli (17), Entamoeba histolytica/Entamoeba dispar (17), Endolimax nana (17), Pentatrichomonas hominis (17), Hammondia spp. (17), and Cryptosporidium parvum (2, 10, 11, 13, 29). Despite intensive efforts to test synanthropic flies for Cyclospora spp., this pathogen has not yet been recovered from flies (23). Toxoplasma gondii can be mechanically transmitted by Musca domestica and Chrysomya megacephala (31). The flies were able to contaminate milk with Toxoplasma gondii oocysts 48 h after last contact with infectious feces, and infectious oocysts were isolated from flies up to 72 h after contact with contaminated fecal material (31).
The biology and ecology of Musca domestica ensure efficient transmission of human protozoan parasites. Adult female flies can live 15 to 25 days (5) and lay five to six batches of 75 to 150 eggs (5, 15). In temperate climates there can be 10 to 12 fly generations in the summer (5, 15). Winter usually ends the breeding cycle; however, indoors, i.e., barns and houses, flies can develop several generations during the winter months (5, 15). Cattle barns, for example, are sites where house flies can breed throughout the winter (15). Individual flies can travel as far as 20 miles (21); however, the vast majority, over 88%, do not travel more than 2 miles (5), and their movement is generally oriented toward unsanitary sites (15).
Current hazard analysis and critical control point and good manufacturing practice regulations require the exclusion of flies from sites where food is produced or stored (22). However, a reasonable approach to excluding flies from such areas requires differentiation between fly species of public health importance and other species which are not involved in transmission of pathogens (22).
The involvement of nonbiting flies in mechanical transmission of Cryptosporidium parvum has been discovered recently (2, 9-11, 13, 29). Cryptosporidium parvum is an anthropozoonotic protozoan parasite which significantly contributes to the mortality of immunocompromised or immunosuppressed persons (8). Diarrheal disease is initiated by a microscopic stage of this parasite, the oocyst. The pathogen also debilitates healthy, i.e., immunocompetent, individuals, in which the disease can be caused by as few as 10 oocysts (8). It is believed that in those with impaired immune systems, a single oocyst can initiate infection (8). Cryptosporidium parvum is particularly prevalent in preweaned cattle, and cattle manure is a source of the oocysts (8).
Animal manure is a recognized source of anthropozoonotic parasites such as Cryptosporidium spp. and is also a favorite breeding place, food source, and landing site of filth flies (4, 14, 15). Coprophagic and saprophagous flies are proficient vectors of Cryptosporidium spp. because of their breeding and feeding ecology; they also act as an epidemiologic link between animals and humans (14, 15). Cryptosporidium parvum oocysts can be transported by filth flies not only from cattle sources but from any unhygienic or contaminated source, i.e., toilets, abattoirs, trash, carcasses, and sewage (13, 29). Because wild filth flies carry viable Cryptosporidium parvum oocysts acquired naturally from unhygienic sources, they can be involved in the epidemiology of cryptosporidiosis (11). Filth flies can cause human or animal cryptosporidiosis via deposition of infectious oocysts on visited foodstuff (2, 6,9-13, 23, 29). However, such epidemiologic involvement is difficult to prove, as cryptosporidiosis cases that result from fly visitations on food items or raw, preprocessed food products will be classified as food borne (12). Interestingly, food-borne cases of cryptosporidiosis have been extensively documented (1). Winter usually ends the breeding cycle of synanthropic flies; however, indoor flies can develop several generations (14, 15).
The involvement of filth flies, i.e., house flies, in mechanical transmission of Cryptosporidium parvum was first described in 1999 (9), although it had been suggested in 1987 (28). Other insects, i.e., dung beetles, have also been reported to mechanically carry Cryptosporidium parvum oocysts acquired from animal manure or other unhygienic sites (20). Subsequent reports confirmed that filth flies can transport infectious oocysts of Cryptosporidium parvum on their external surfaces and in their digestive tracts (2, 4, 6). Thus, nonbiting flies can serve as mechanical vectors for the human parasite against which no effective prophylaxis or therapy exists (8).
Exposure of adult house flies, Musca domestica, to bovine diarrheal feces with Cryptosporidium parvum oocysts resulted in intense deposition of the oocysts through fecal spots and vomit drops on the visited surfaces, with an average of 108 oocysts per cm2 (9, 10). On average, 267, 131, 32, 19, and 14 oocysts per house fly were eluted from its exoskeleton on days 3, 5, 7, 9, and 11 after emergence, respectively (9). Approximately 320 Cryptosporidium parvum oocysts per pupa were eluted from the external surface of the pupae derived from maggots that bred in a substrate with the bovine feces; oocysts were numerous on the maggots (approximately 150 oocysts/maggot) (9). In another study, over the course of 6 months, wild filth flies (families Muscidae, Sarcophagidae, and Calliphoridae) were collected in barns with and without a calf shedding Cryptosporidium parvum oocysts in diarrheic feces (11).
Oocysts of Cryptosporidium parvum transported on the flies' exoskeletons and eluted from their fecal and vomit droplets were infectious to neonatal mice, which are always used in Cryptosporidium bioassays (11). The mean number of oocysts carried by a fly varied from 4 to 131, and the total oocyst number per weekly collection varied from 56 to approximately 4.56 x 103 (11). Molecular data showed that the oocysts shed by infected calves were carried by flies for at least 3 weeks (11).
In the next study, wild synanthropic flies (Muscidae, Calliphoridae, Lauxaniidae, and Anthomyiidae) caught at cattle dairy farms and cattle waste facilities were tested for Cryptosporidium parvum on their exoskeletons and in their digestive tract by a technique that allows assessment of oocyst viability, fluorescent in situ hybridization (13, 29). Fluorescent in situ hybridization employs fluorescently labeled oligonucleotide probes targeted to species-specific sequences of 18S rRNA (29). As rRNA has a short half-life and is only present in high copy numbers in viable organisms, fluorescent in situ hybridization allows differentiation between viable and nonviable cells and eliminates the need for fluorogenic dyes (13, 29). The vast majority of oocysts, >80%, were viable, and more oocysts were located within the digestive tract than on the exoskeleton (13, 29).
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