Gastrointestinal parasites in captive olive baboons in a UK safari park.

From the safety inside vehicles, Knowsley Safari offers visitors a close-up encounter with captive olive baboons. As exiting vehicles may be contaminated with baboon stool, a comprehensive coprological inspection was conducted to address public health concerns. Baboon stools were obtained from vehicles, and sleeping areas, inclusive of video analysis of baboon­vehicle interactions. A purposely selected 4-day sampling period enabled comparative inspections of 2662 vehicles, with a total of 669 baboon stools examined (371 from vehicles and 298 from sleeping areas). As informed by our pilot study, front-line diagnostic methods were: QUIK-CHEK rapid diagnostic test (RDT) (Giardia and Cryptosporidium), Kato­Katz coproscopy (Trichuris) and charcoal culture (Strongyloides). Some 13.9% of vehicles were contaminated with baboon stool. Prevalence of giardiasis was 37.4% while cryptosporidiosis was <0.01%, however, an absence of faecal cysts by quality control coproscopy, alongside lower than the expected levels of Giardia-specific DNA, judged RDT results as misleading, grossly overestimating prevalence. Prevalence of trichuriasis was 48.0% and strongyloidiasis was 13.7%, a first report of Strongyloides fuelleborni in UK. We advise regular blanket administration(s) of anthelminthics to the colony, exploring pour-on formulations, thereafter, smaller-scale indicator surveys would be adequate.

Entamoeba histolytica infection in humans, chimpanzees and baboons in the Greater Gombe Ecosystem, Tanzania.

Entamoeba histolytica is an enteric parasite that infects approximately 50 million people worldwide. Although E. histolytica is a zoonotic parasite that has the potential to infect nonhuman primates, such transmission is poorly understood. Consequently, this study examined whether E. histolytica is present among humans, chimpanzees and baboons living in the Greater Gombe Ecosystem (GGE), Tanzania. The primary aims were to determine patterns of E. histolytica infection in a system with human-nonhuman primate overlap and to test associations between infection status and potential risk factors of disease. Entamoeba spp. occurred in 60.3% of human, 65.6% of chimpanzee and 88.6% of baboon samples. Entamoeba histolytica occurred in 12.1% of human, 34.1% of chimpanzee and 10.9% of baboon samples. Human E. histolytica infection was associated with gastrointestinal symptoms. This was the first study to confirm the presence of E. histolytica in the GGE. The high sample prevalence of E. histolytica in three sympatric primates suggests that zoonotic transmission is possible and stresses the need for further phylogenetic studies. Interventions targeting better sanitation and hygiene practices for humans living in the GGE can help prevent E. histolytica infection in humans, while also protecting the endangered chimpanzees and other primates in this region.

Oesophagostomiasis in non-human primates of Gombe National Park, Tanzania.

Oesophagostomum sp. is a parasitic nematode that frequently infects wild chimpanzees. Although nodular lesions are commonly associated with infection, some wild chimpanzee populations seem to tolerate Oesophagostomum nodular lesions while those at Gombe and other sites suffer from associated morbidity and mortality. From August 2004 to December 2013, we examined demographic (i.e., age, sex) and individual correlates (i.e., fecal consistency, Oesophagostomum egg production) to Oesophagostomum-associated pathology in 14 individually recognized chimpanzees at Gombe Stream National Park, Tanzania. In addition, we characterized Oesophagostomum-associated pathology in 14 individual sympatric primates including baboons, colobus, and cercopithecid monkeys. In five chimpanzees, there was no evidence of any significant underlying disease aside from oesophagostomiasis to explain the thin condition or diarrhea. All five of these chimpanzees had moderate to numerous parasitic nodules. In general, nodules were more numerous in older chimpanzees. Three of four chimpanzees with the highest average Oesophagostomum egg counts in feces collected during the year prior to their death had numerous parasitic nodules at necropsy. In contrast, the four chimpanzees with the lowest egg counts had only moderate numbers of nodules. No association (P = 0.74) was noted between frequency of diarrhea in the year prior to death and the number of nodules noted at necropsy. Nodules were also present in all baboons examined documenting pathology associated with Oesophagostomum infection in wild baboons. In contrast, no lesions were noted in colobus or cercopithecid monkeys, although it is uncertain if they are infected as no fecal studies have been completed in these species to date at Gombe. Sequence of DNA isolated from nodules in chimpanzees matched (99%) Oesophagostomum stephanostomum. Further research is needed to identify the types of Oesophagostomum causing lesions in baboons and to determine if baboons suffer from these infections. Am. J. Primatol. 80:e22572, 2018. © 2016 Wiley Periodicals, Inc.

Schistosoma mansoni infection in human and nonhuman primates in selected areas of Oromia Regional State, Ethiopia.

BACKGROUND & OBJECTIVES: The transmission of schistosomiasis, caused by trematodes of the genus Schistosoma, relies on freshwater snails that act as an intermediate host while human and other mammalian act as the definitive hosts. Many non-human primates (NHPs) such as Chlorocebus aethiops (vervet) and Papio anubis (baboon) are reported to be infected with Schistosoma mansoni in Ethiopia, but the role they play in parasite maintenance and transmission is still not clear. The objective of this study was, therefore, to determine the prevalence of S. mansoni infection in human and NHPs living in close proximities to villages in selected endemic areas of Ethiopia. METHODS: In this cross-sectional study, stool specimens were collected from 911 humans, and fresh faecal droppings from 106 NHPs from Bochesa (Ziway), Bishan Gari (Kime) and Finchaa (Camp 7) endemic localities in Oromia Regional State, and examined for S. mansoni and other helminth infections using Kato-Katz method for human participants and direct microscopic examination for NHPs. RESULTS: The prevalence of helminthiasis among the human study population was 42.4% (386/911), and for soil-transmitted helminth infections (A. lumbricoides, hookworms, and T. trichiura) it was 13.4% (122/911). In humans S. mansoni was the predominant parasite, 23.1% (210/911) followed by A. lumbricoides, 8.7% (79/911); hookworms, 5.8% (53/911); T. trichiura, 4.8% (44/911); Taenia species, 2.2% (20/911); E. vermicularis, 2.1% (19/911); and H. nana, 3.2% (29/911). NHPs were found positive for Trichuris species and Strongyloides species besides S. mansoni. INTERPRETATION & CONCLUSION: NHPs might play a significant role in local transmission and maintenance of S. mansoni infection even in the absence of human hosts. This calls for supplementation of chemotherapy for schistosomiasis along with measures such as snail control to interrupt transmission of the disease from humans to NHPs, and vice-versa.

Differences between chimpanzee and baboon gastrointestinal parasite communities.

Cross-species infection among humans, chimpanzees (Pan troglodytes) and baboons (Papio spp.) is potentially a significant public health issue in Africa, and of concern in the conservation of P. troglodytes. However, to date, no statistical comparisons have been made between the prevalence, richness and composition of parasite communities in sympatric populations of baboons and P. troglodytes. We compared parasite communities in sympatric P. troglodytes and Papio papio living in a wilderness site, in the Republic of Senegal, West Africa. We asked whether, in the absence of humans, there are significant differences between these hosts in their interactions with gastrointestinal parasites. We tested whether host, location, or time of collection accounted for variation in prevalence, richness and community composition, and compared prevalence across six studies. We concluded that, despite being closely related, there are significant differences between these two hosts with respect to their parasite communities. At our study site, prevalence of Balantidium, Trichuris and Watsonius was higher in P. papio. Papio papio harboured more parasites per host, and we found evidence of a positive association between Trichuris and Balantidium in P. troglodytes but not P. papio.

Use of an Sm-p80-based therapeutic vaccine to kill established adult schistosome parasites in chronically infected baboons.

No vaccines are available for human use for any parasitic infections, including the helminthic disease schistosomiasis. Sm-p80, the large subunit of Schistosoma mansoni calpain, is a leading antigen candidate for a schistosomiasis vaccine. Prophylactic and antifecundity efficacies of Sm-p80 have been tested using a variety of vaccine approaches in both rodent and nonhuman primate models. However, the therapeutic efficacy of a Sm-p80-based vaccine had not been determined. In this study, we evaluated the therapeutic efficacy of Sm-p80 by using 2 different strategies and 3 Sm-p80-based vaccine formulations in baboons. Vaccine formulations were able to decrease established adult worms by 10%-36%, reduce retention of eggs in tissues by 10%-57%, and decrease egg excretion in feces by 13%-33%, compared with control formulations. Marked differences were observed in B and T cell immune correlates between vaccinated and control animals. This is the first report of killing of established adult schistosome worms by a vaccine. In addition to distinct prophylactic efficacy of Sm-p80, this study adds to the evidence that Sm-p80 is a potentially important antigen with both substantial prophylactic and therapeutic efficacies. These data reinforce that Sm-p80 should be moved forward along the path toward human clinical trials.

Hydrodynamic gene delivery of baboon trypanosome lytic factor eliminates both animal and human-infective African trypanosomes.

Several species of African trypanosomes cause fatal disease in livestock, but most cannot infect humans due to innate trypanosome lytic factors (TLFs). Human TLFs are pore forming high-density lipoprotein (HDL) particles that contain apolipoprotein L-I (apoL-I) the trypanolytic component, and haptoglobin-related protein (Hpr), which binds free hemoglobin (Hb) in blood and facilitates the uptake of TLF via a trypanosome haptoglobin-hemoglobin receptor. The human-infective Trypanosoma brucei rhodesiense escapes lysis by TLF by expression of serum resistance-associated (SRA) protein, which binds and neutralizes apoL-I. Unlike humans, baboons are not susceptible to infection by T. b. rhodesiense due to previously unidentified serum factors. Here, we show that baboons have a TLF complex that contains orthologs of Hpr and apoL-I and that full-length baboon apoL-I confers trypanolytic activity to mice and when expressed together with baboon Hpr and human apoA-I, provides protection against both animal infective and the human-infective T. brucei rhodesiense in vivo. We further define two critical lysines near the C terminus of baboon apoL-1 that are necessary and sufficient to prevent binding to SRA and thereby confer resistance to human-infective trypanosomes. These findings form the basis for the creation of TLF transgenic livestock that would be resistant to animal and human-infective trypanosomes, which would result in the reduction of disease and the zoonotic transmission of human infective trypanosomes.

Gastrointestinal parasites of baboons (Papio papio) in Niokolo-Koba National Park, Senegal.

Background: Primates can harbor parasites that could be pathogenic or not for humans and primates themselves. It is necessary to know the parasitological situation of the primates that are under surveillance in the park. Aim: To estimate the prevalence and diversity of gastrointestinal parasites, including zoonotic potential parasites, in baboons in the Niokolo-Koba National Park located in Senegal. Method: Fecal samples (n = 50) from two groups of baboons (A and B) were collected in October 2019. The samples were processed using the flotation technique and the modified Ritchie method. Slides were examined microscopically and the parasite identification was based on morphology, color, and parasite content. Results: A total of seven nematodes (Strongyloides sp., Trichirus sp., Ancylostoma sp., Mammo monogamus, Enterobius sp., Strongyloides stercoralis, Strongyle digestif), one cestode (Bertiella sp.), and one trematode (Fasciolopsis sp.) were identified. The overall prevalence was 78%, while the prevalence of poly-infected samples was 49%. The parasite with zoonotic potential, S. stercoralis, was identified in group B samples. Trichuris sp., which is common and pathogenic to humans and primates, was present with prevalence of 52% and of 32% in groups A and B, respectively. Conclusion: These results suggest that baboons are infested with zoonotic parasites and this situation could expose people working in this park to infection. Contact between humans and these baboons or their feces could expose them to infection with zoonotic parasites.

Cyclospora papionis, Cryptosporidium hominis, and human-pathogenic Enterocytozoon bieneusi in captive baboons in Kenya.

Cyclospora papionis, Cryptosporidium hominis, and Enterocytozoon bieneusi were detected in 42 (17.9%), 6 (2.6%), and 29 (12.3%) of 235 newly captured baboons in Kenya, respectively. Most C. hominis subtypes and E. bieneusi genotypes found have been detected in humans in the area, suggesting that cross-species transmission of cryptosporidiosis and microsporidiosis is possible.

Circulating Anodic Antigen (CAA): A Highly Sensitive Diagnostic Biomarker to Detect Active Schistosoma Infections-Improvement and Use during SCORE.

The Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) was funded in 2008 to conduct research that would support country schistosomiasis control programs. As schistosomiasis prevalence decreases in many places and elimination is increasingly within reach, a sensitive and specific test to detect infection with Schistosoma mansoni and Schistosoma haematobium has become a pressing need. After obtaining broad input, SCORE supported Leiden University Medical Center (LUMC) to modify the serum-based antigen assay for use with urine, simplify the assay, and improve its sensitivity. The urine assay eventually contributed to several of the larger SCORE studies. For example, in Zanzibar, we demonstrated that urine filtration, the standard parasite egg detection diagnostic test for S. haematobium, greatly underestimated prevalence in low-prevalence settings. In Burundi and Rwanda, the circulating anodic antigen (CAA) assay provided critical information about the limitations of the stool-based Kato-Katz parasite egg-detection assay for S. mansoni in low-prevalence settings. Other SCORE-supported CAA work demonstrated that frozen, banked urine specimens yielded similar results to fresh ones; pooling of specimens may be a useful, cost-effective approach for surveillance in some settings; and the assay can be performed in local laboratories equipped with adequate centrifuge capacity. These improvements in the assay continue to be of use to researchers around the world. However, additional work will be needed if widespread dissemination of the CAA assay is to occur, for example, by building capacity in places besides LUMC and commercialization of the assay. Here, we review the evolution of the CAA assay format during the SCORE period with emphasis on urine-based applications.

Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya.

BACKGROUND: Gastrointestinal parasites are neglected infections, yet they cause significant burden to animal and human health globally. To date, most studies of gastrointestinal parasites focus on host-parasite systems that involve either a single parasite or a host species. However, when hosts share habitat and resources, they may also cross-transmit generalist gastrointestinal parasites. Here we explore multi-host-parasite interactions in a single ecosystem to understand the infection patterns, especially those linked to livestock-wildlife interfaces and zoonotic risk. METHODS: We used both coprological methods (flotation and sedimentation; N = 1,138 fecal samples) and molecular identification techniques (rDNA and mtDNA; N = 18 larvae) to identify gastrointestinal parasites in nine sympatric host species (cattle, sheep, goats, wildebeest, Grant's gazelles, Thomson's gazelles, impala, vervet monkeys and baboons) in the Amboseli ecosystem, Kenya. RESULTS: We found that the host community harbored a diverse community of gastrointestinal helminths, including 22 species and/or morphotypes that were heterogeneously distributed across the hosts. Six zoonotic gastrointestinal helminths were identified: Trichuris spp., Trichostrongylus colubriformis, Enterobius spp. Oesophagostomum bifurcum, Strongyloides stercoralis and Strongyloides fuelleborni. The dominant parasite was Trichuris spp, whose ova occurred in two morphological types. Baboons were co-infected with Strongyloides fuelleborni and S. stercoralis. CONCLUSIONS: We found that the interface zone shared by wild ungulates, livestock and non-human primates is rich in diversity of gastrointestinal helminths, of which some are extensively shared across the host species. Closely related host species were most likely to be infected by the same parasite species. Several parasites showed genetic sub-structuring according to either geography or host species. Of significance and contrary to expectation, we found that livestock had a higher parasite richness than wild bovids, which is a health risk for both conservation and livestock production. The zoonotic parasites are of public health risk, especially to pastoralist communities living in areas contiguous to wildlife areas. These results expand information on the epidemiology of these parasites and highlights potential zoonotic risk in East African savanna habitats.

Antibodies elicited by the secretions from schistosome cercariae and eggs are predominantly against glycan epitopes.

The glycoproteins secreted by Schistosoma mansoni cercariae and eggs play a key role in parasite transmission to and from the mammalian host. We used secreted preparations from these two life cycle stages to characterize the reactivity of sera from baboons exposed to normal and/or attenuated cercariae, in comparison with somatic antigen preparations and defined glycan epitopes. Periodate treatment of native antigens revealed that responses to the two secreted preparations were overwhelmingly directed against glycans rather than peptides. Considerable immunological cross-reactivity between glycans in the two preparations was inferred from a comparison of sera from infected-only and vaccinated-only animals, predominantly exposed to egg and cercarial secretions, respectively. In contrast, when somatic antigen preparations derived from adult worms or eggs were used to probe sera, a stronger antipeptide response was seen that accounted for up to 66% of maximum reactivity. Probing of sera with defined glycan structures confirmed the time course of responses and the presence of cross-reactive epitopes. In spite of the intense antiglycan response elicited in mice by administration of live eggs, no protection against a cercarial challenge was observed. Our data further support the hypothesis that antiglycan responses are a smokescreen with negligible protective potential.

Schistosoma mansoni: anti-SMw32 proteinase response in vaccinated and challenged baboons.

Antibodies to a cysteinyl proteinase of the trematode Schistosoma mansoni have been detected in serum from infected mice and humans. We have evaluated antiproteinase responses in infected baboons and in baboons vaccinated with irradiated, cryopreserved schistosomules prior to challenge. Prechallenge sera and normal, uninfected control sera were nonreactive by ELISA and immunoblots. Serum antibodies were first detectable by ELISA at two months post-challenge in both challenged (C) and vaccinated-challenged (V-C) baboons (serum dilution 1:200). By four months post-challenge, ELISA absorbance values for subgroup C baboons were significantly higher than for V-C counterparts. The immunoblot technique provided a more sensitive means of detecting antibody early in the infection. One month post-challenge, 7 of 12 C and V-C sera (diluted 1:100) contained measurable anti-proteinase antibody. By month two, 12 of 12 were immunoblot-positive. Baboons vaccinated but not challenged (subgroup V) remained negative. The presence of the anti-proteinase antibody appears to be a sensitive and early marker for infection by S. mansoni.

Use of polymerase chain reaction for accurate follow-up of Loa loa experimental infection in Mandrillus sphinx.

Mandrills (Mandrillus sphinx) experimentally infected with human Loa loa usually remain microfilaremic for a long period of time. Nevertheless some control their microfilaremia while still harboring adults worms, and therefore become occult-infected. A nested polymerase chain reaction (PCR) assay, targeted on the repeat 3 region of the gene coding for the L. loa 15-kD protein (15r3-PCR), has been evaluated in mandrills infected with third-stage larvae (L3) of L. loa. The results of this assay were negative during the prepatency period (4 months after inoculation), but became positive when microfilariae appeared in the blood, and remained positive in all mandrills, even in those that became amicrofilaremic. These results show that the positivity of the 15r3-PCR assay is linked to the appearance of microfilariae in peripheral blood and demonstrated that L. loa-specific DNA can be detected in blood from occult-infected mandrills.

Loa loa: development to the infective stage in an American deerfly, Chrysops atlanticus.

Chrysops atlanticus, an American species of deerfly collected along the Mississippi Gulf Coast, will support the development of the microfilaria of human Loa loa to the infective stage. Development takes place in the fat body of the fly and requires 9 to 10 days of development and pattern of morphogenesis of the parasite in C. atlanticus is virtually identical to that described in natural African vectors. Chrysops atlanticus will support the development of large numbers of L. loa to the infective stage without apparent ill effects. Two uninfected patas nonkeys each were given 75 third-stage larvae obtained from experimentally infected C. atlanticus. Both animals developed patent infections in approximately 5 months, clearly demonstrating that the entire life cycle of Loa loa can be maintained in the laboratory outside endemic areas.

Loa loa: experimental infection in two species of African primates.

Four species of primates, baboon (Papio anubis), patas monkeys (Erythrocebus patas), green monkey (Cercopithecus aethiops) and chimpanzee (Pan troglodytes) were inoculated with third-stage larvae of a human strain of Loa loa from Cameroon, West African. The baboon and patas monkeys developed patent infections after 135 to 148 days; the green monkeys and chimpanzee did not. In each animal which became patent, microfilaremia rose rapidly to high levels. In the baboon, but not in the patas monkeys, there was a suppression of microfilaremia during the 4th month of patency. After splenectomy, microfilariae reappeared in the peripheral blood in large numbers. In both baboon and patas monkeys, the microfilariae of Loa loa maintain the diurnal periodicity so characteristic of their behavior in man.

Schistosome migration in primates: a study in the olive baboon (Papio anubis).

The migration of isotopically labelled schistosomula of Schistosoma mansoni from the skin to the hepatic portal system of baboons was tracked by autoradiography of compressed organ preparations. Passage of schistosomula from skin to lungs was rapid between days 2 and 5, 72% of applied parasites being detected in the lungs at the latter time. There was an equally rapid migration from lungs to liver, 60% of the adult worm burden having arrived by day 9. Perfusion data indicated a final maturation of not less than 78%. No evidence was found to support or refute a systemic phase of migration. Thus, in comparison to rodents, schistosome migration in baboons appears to be faster and more successful, possibly because the lungs do not represent a significant obstacle to migration.

Survival of Loa loa following transplantation from drills (Mandrillus leucophaeus) into jirds (Meriones unguiculatus): parasitology and pathology.

Two drills infected with Loa loa maintained a microfilaraemia for four and a half years ranging from less than 1 mf/100 microliters to 1150 mf/100 microliters. No significant tissue reactions to the adult worms were seen at autopsy. Adult worms were transplanted into the peritoneal cavities of naive jirds when a persistent microfilaraemia first developed by 17 days. Retransplantation of adult worms into naive jirds produced a microfilaraemia and microfilariae in the peritoneal cavities of three out of five animals. These three animals were all negative for circulating parasites by eight and a half months. The tissue reactions to the worms in the jirds are described, including a granulomatous response surrounding adults and a myositis involving microfilariae.

Immunization of baboons with attenuated schistosomula of Schistosoma haematobium: levels of protection induced by immunization with larvae irradiated with 20 and 60 krad.

We have shown previously that baboons (Papio anubis) develop high levels (greater than 80%) of protection against challenge infection following immunization with Schistosoma haematobium cercariae irradiated with 20 krad. In the present study baboons were immunized with schistosomula irradiated with either 20 krad or 60 krad, with variations in the timing and number of larvae comprising each vaccination. Baboons immunized 2 or 3 times with schistosomula irradiated with 20 krad were significantly more protected (85-90%) against challenge infection than baboons similarly immunized with larvae receiving 60 krad (56-50% protection). Baboons immunized with schistosomula irradiated with 20 krad were better protected against challenge infection at 8 weeks after immunization than at 28 weeks after immunization. Protection was manifest by a reduction in worm numbers, tissue and excreta egg counts, gross pathology and, to a lesser extent, by stability of body weight and haematological indices following challenge. Enzyme-linked immunosorbent assay (ELISA) results of selected baboon sera showed few differences related to irradiation dose alone, but titres were higher in baboons receiving booster immunizations, and there was a significant correlation between titres immediately preceding challenge and the degree of resistance. Examination of responses to individual schistosomular surface antigens by immunoprecipitation and sodium dodecyl sulphate-polyacrylamide gel electrophoresis showed no correlation between the pattern of antigens recognized and resistance status. As with the ELISA assay, an anamnestic response was detected after vaccination, while the amount of antibody present declined markedly with increasing time after individual immunizations.

Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia.

A total of 59 faecal samples from ranging Papio anubis (baboons) and another 41 from Cercopithecus aethiops (vervet) from the Rift Valley areas of Ethiopia were microscopically examined to determine the prevalence and species of major gastro-intestinal parasites of zoonotic importance. Faecal smears were prepared from fresh faecal samples, stained using modified Ziehl-Neelsen method and microscopically examined. About 3 gm of the dropping was also preserved separately in clean and properly labelled containers containing 10% formalin. The specimens were microscopically examined after formalin-ether concentration for ova, larvae, cysts and oocyst of intestinal parasites. The results of microscopic examination of faecal samples of baboons demonstrated the presence of Trichuris sp. (27.1%), Strongyloides sp. (37.3%), Trichostrongylus sp. (8.5%), Oesophagostomum sp. (10.2%), Schistosoma mansoni (20.3%), Entamoeba coli (83.1%), Entamoeba histolytica/dispar (16.9%), Blastocystis hominis (3.3%), Cyclospora sp. (13.3%) and Cryptosporidium sp. (11.9%). Likewise, the results of microscopic examination of faecal samples of vervets demonstrated the presence of Trichuris sp. (36.6%), Oesophagostomum sp. (4.9%), E. coli (61.0%), E. histolytica/dispar (24.4%), B. hominis (34.2%), Cyclospora sp. (22.0%) and Cryptosporidium sp. (29.3%). The presence of parasitic protozoa and helminths in baboons and vervets in the study areas is a high risk to human welfare because these non-human primates use the same water sources as humans and range freely in human habitats. An implication of such parasitic infection for the control programme is discussed.