• Users Online: 683
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 


 
 
Table of Contents
RESEARCH ARTICLE
Year : 2018  |  Volume : 55  |  Issue : 2  |  Page : 116-121

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


1 Department of Microbiology, Immunology and Parasitology, School of Medicine; Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Ethiopia
2 Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Ethiopia

Date of Submission12-Aug-2017
Date of Acceptance10-May-2018
Date of Web Publication1-Oct-2018

Correspondence Address:
Tadesse Kebede
Department of Microbiology, Immunology and Parasitology, School of Medicine, Addis Ababa University
Ethiopia
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.242558

Rights and Permissions
  Abstract 

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.

Keywords: Baboon; Chlorocebus aethiops; Ethiopia; human; nonhuman primates; Papio anubis; Schistosoma mansoni; vervet


How to cite this article:
Kebede T, Negash Y, Erko B. Schistosoma mansoni infection in human and nonhuman primates in selected areas of Oromia Regional State, Ethiopia. J Vector Borne Dis 2018;55:116-21

How to cite this URL:
Kebede T, Negash Y, Erko B. Schistosoma mansoni infection in human and nonhuman primates in selected areas of Oromia Regional State, Ethiopia. J Vector Borne Dis [serial online] 2018 [cited 2018 Oct 21];55:116-21. Available from: http://www.jvbd.org/text.asp?2018/55/2/116/242558




  Introduction Top


Schistosomiasis is the most important human helminth infection in terms of morbidity and mortality, affecting >250 million people in 76 countries[1],[2]. It is estimated that 97% of all cases of schistosomiasis occur in Africa[3]. More than 800 million people are at risk of acquiring the infection that accounts for 300,000 deaths per year. Annually, it leads to 4.5 million disability-adjusted life year losses[4] resulting due to anaemia, pain, diarrhoea, exercise intolerance, and under nutrition from chronic infection[2],[5],[6]. The highest prevalence estimates and infection intensities of schistosomiasis are usually found in school-age children, adolescents and young adults, as well as in infants and preschool children[7], because of the high frequency of time spent swimming or bathing in water containing infectious cercariae. These groups are known to suffer from the highest morbidity and mortality[8].

In Ethiopia, it is estimated that >30 million people are at risk of infection, while four million people are already infected with schistosomes[5], but the figure underestimate the present status. Schistosoma mansoni in Ethiopia has been reported to infect nonhuman primates (NHPs) including baboons (Papio anubis)[9],[10] and monkeys (Cercopithecus aethiops)[9]. It occupies a very large geographical range and can utilize a variety of definitive mammalian hosts, but is tightly tied to a specific range of intermediate snail hosts, planorbids of the genus Biomphalaria[11]. Although, human plays important role in maintaining the life cycle of S. mansoni, there are a number of studies showing that other mammals also act as source of infection[12],[13]. With close geographical and genetic proximity of many NHP species to humans and given sufficient epidemiological opportunity, they can become infected with S. mansoni, potentially exhibiting similar clinical signs and symptoms[14], and sometimes act as fully competent definitive hosts[15]. It remains unclear whether NHPs are playing an important role as zoonotic reservoirs for human infection in Ethiopia. However, previously it was considered that Schistosomiasis mansoni is a zoonosis with human as the main definitive host[16]. The objective of this study was, therefore, to determine the prevalence of S. mansoni in human and NHP hosts in selected endemic areas of Ethiopia.


  Material & Methods Top


Study area

The study sites were Ziway (Bochesa village), Bishan Gari [Kime area (around Burka Dita forest reserve)], and Finchaa Sugar Estate area (Camp 7) located in Oromia Regional State. The areas are known to be inhabited by human and NHPs and share the same resources.

Bochesa village is located around Lake Ziway about 160 km south of Addis Ababa at an altitude of 1642 m above sea level (masl). The people in the village use the lake water for irrigation, fishing and other domestic activities. Similarly, numerous vervet monkeys range in the environment and share the same water source with humans. Kime is situated 235 km south of Addis Ababa on the eastern shores of Lake Langano. It is situated at about 1600 masl. There were two troops of free-ranging baboons with overlapping territories in Bishan Gari and Burka Dita forest reserve areas, in close proximity to human habitation. The baboons range freely over human peridomestic habitats. The study area has been described in detail elsewhere[10]. Finchaa (Camp 7) is located in the Finchaa Sugar Factory about 350 km west of Addis Ababa at an altitude of about 1567 masl. The area is stretched in most part of the Finchaa River Valley[17] state farm with an irrigation system, which could create favorable conditions for transmission of Schistosoma, associated agro-industrial activities and high population influx. Some free ranging vervets and baboons were also present in the forest, surrounding the sugar plantation.

Study population

The study was conducted in three S. mansoni endemic foci from human and two species of nonhuman primates, P. anubis (baboon) and Ch. aethiops (vervet) from September 2015 to June 2016.

Study design, sample size determination and sampling technique

Cross-sectional surveys of human communities were conducted using purposive sampling technique in geographically overlapped population with nonhuman primates, and study subjects were enrolled voluntarily. The sample size was calculated using prevalence of S. mansoni in NHPs on the study sites using Daniel’s formula [n = Z2P(1–P)/d2], where n is the sample size, Z is statistic for level of confidence (1.96), P is expected prevalence or proportion, and d is precision (0.05). For nonhuman primates, using reported prevalence[10] of 12% , the sample size for the whole endemic site of Ethiopia was 162 (i.e. 54 samples per study site).

Stool sample collection and examination

Small plastic sheets were provided to human study subjects and a stool specimen was collected. The collected samples were quantitatively examined using Kato-Katz method of 41.7 mg template[18],[19] for intestinal parasites. The intensity of infection was classified into light infection [1–99 eggs per gram of stool (EPG)], moderate infection (100–399 EPG) and heavy infection (≥400 EPG) in S. mansoni positive samples and the EPG was determined[20] by multiplying the number of eggs counted by a factor of 24. Fresh faecal droppings from NHPs were collected early in the morning as they defecated and while the NHPs were in the trees where they passed the night[21]. Microscopic examination was carried out to determine the prevalence of intestinal parasites. Collection of samples from baboons from Kime was made once but from Finchaa it was made in two different days. Collection of samples from vervets in Bochesa was made once from different localities in two different times. During collection, much care was taken to pick only distinct droppings so that each dropping would represent a single baboon or vervet sample.

Data analysis

Data was double entered in Microsoft Office Excel version 2010, and analyzed with Stata Statistical Software, Release 11, StataCorp LP. The statistical significance was tested using the chi-square test at α = 0.05.

Ethical statement

Ethical clearance was obtained from Institutional Review Board (IRB) of Aklilu Lemma Institute of Pathobiology, Addis Ababa University (Ref. No.: ALI-PB/994/2005/13) and National Research Ethics Review Committees of Federal Republic of Ethiopia, Ministry of Science and Technology (Ref. No.: 3.10/434/106). All ethical issues were strictly handled according to the International Ethical Guidelines for Biomedical Research. Informed verbal consent was obtained from all adults. For children younger than 18, informed verbal consent was obtained from their parents and the children also gave their assent. All study subjects found positive for S. mansoni and other intestinal helminth were treated with praziquantel at a dose of 40 mg/kg body weight and albendazole (400 mg), respectively.


  Results Top


In total, 911 individuals; 283 from Bochesa, 318 from Kime, and 310 from Finchaa study sites voluntarily provided stool samples for intestinal parasites examination, in which 56.2% were males with a mean age of 17.9 yr (Range: 3–70 yr, SD + 13.9). The sample size and the corresponding distribution of age and sex across the different study sites are summarized in [Table 1].
Table 1: Sociodemographic characteristics of study subjects by study sites, 2016

Click here to view


The overall prevalence of helminthiasis among the study population was 42.4% (386/911). The prevalence of soil transmitted helminth infection (A. lumbricoides, hookworm, and T. trichiura) was 13.4% (122/911). The most predominant parasite in human was S. mansoni (210/911, 23.1%) followed by A. lumbricoides (79/911, 8.7%), hookworms (53/911, 5.8%), T. trichiura (44/911, 4.8%), Taenia species (20/911, 2.2%), E. vermicularis (19/911, 2.1%) and H. nana (29/911, 3.2%) [Figure 1]. Double and triple helminthic infections were found in 6.4% (58/911) and 0.4% (4/911) cases, respectively.
Figure 1: Proportion of helminthic infections among the study sites during 2016.

Click here to view


The prevalence of S. mansoni infection among the study participants in Bochesa, Kime and Finchaa was 23.7, 14.5, and 31.3%, respectively. In all the study sites, males were more likely to be infected with S. mansoni2 = 21.1, df = 1, p < 0.001), with prevalence of 30.3, 20.6, and 33.1%, in Bochesa, Kime and Finchaa, respectively. There was variation in the prevalence of infection in males and females among the study sites with χ2 = 17.1, df = 1,p < 0.001 in Bochesa; χ2 = 7.2, df = 1,p = 0.007 in Kime; and χ2 = 0.64, df = 1, p = 0.423 in Finchaa.

Statistically, significant differences were observed in parasitic infection between different age groups at Bochesa and Finchaa with χ2 = 12, df = 3,p < 0.001; and χ2 = 18.9, df = 3,p < 0.001, respectively. However, there was no statistically significant difference in parasitic infection between age groups in Kime. There was statistically significant difference in parasitic infection between sexes in Bochesa (χ2 = 17.1, df = 1, p < 0.001) and Kime (χ2 = 7.2, df = 1,p < 0.001).

Of the 210 egg-positive study participants, 141 (67.1%) had light, 41 (19.5%) moderate and 28 (13.3%) had heavy infections. There was no statistically significant difference in intensity of infection between sexes/genders and age group.

In general, for the whole study population the prevalence of schistosomiasis was significantly higher among lower age groups (χ2 = 13.6,p < 0.05) [Table 2] as observed in Bochesa and Finchaa populations (χ2 = 12, p < 0.05) and (χ2 = 18.9, p < 0.05), respectively. However, the prevalence of schistosomiasis was not significantly different for Kime (χ2 = 2.4, p > 0.05) in the lower age group. Moreover, it appeared that infection was higher in males compared to females as there was significant association at Bochesa and Kime.
Table 2: Prevalence of Schistosoma mansoni infection among study subjects by sex, age, age group, and study sites in 2016

Click here to view


The prevalence of different intestinal helminth infections were determined in NHPs in the three localities. In total 106 NHP droppings were collected (37 from Bochesa vervet monkeys, 58 from Kime baboons and 11 from Finchaa baboons). Out of 37 faecal samples collected from vervet monkeys, 8 (21.6%) samples were positive for S. mansoni and 5 (13.5%) for T. trichiura. Similarly, out of 58 faecal samples collected from baboons from Kime, 30 (51.7%) samples were positive for S. mansoni, 7 (12.1%) for T. trichiura, and 8 (13.8%) were positive for Strongyloides spp. From Finchaa (around Camp 7) 11 faecal samples were collected and 5 (45.5%) of the samples were positive for S. mansoni.


  Discussion Top


The objective of this study was to determine the prevalence of S. mansoni infection in human and NHPs living in close proximities to villages in selected endemic areas of Ethiopia and to show the role of NHPs in local transmission and maintenance of S. mansoni infection. The prevalence of S. mansoni infection in Finchaa Sugar Plantation (Camp 7) was 31.3%. This result was higher than that reported by Erko et al[22] in a study carried out in Wondo Genet (26%) and lower than reported (37%) recently by Dufera et al[17]. This variation could be due to the difference in the study populations, seasonal population migration and application of intermittent control measures such as endod application.

Although more males than females were found infected in the present study in comparison to earlier studies, the difference in prevalence of schistosomiasis between males (33.1%) and females (28.9%) in Finchaa was not statistically significant. This is in agreement with the earlier reports from other parts of the country[23],[24]. On the other hand, the difference in prevalence of schistosomiasis in males (30.5%) was higher than in females (7.3%) in Bochesa. More males (20.6%) than females (9.9%) were also infected in Kime with statistically significant difference, in agreement with the previous report of Dufera et al[17] and Erko et al[22].

Similarly, the results are also in agreement with another study[25] wherein the S. mansoni infection among males and females was 38.4 and 27.3%, respectively. However, the result in Bochesa and Kime are in disagreement with the earlier report of 13.6% in males and 10.5% in females[23]. The reasons might be due to implementation of school-based deworming control activities, lower sample size in current study population particularly in Bochesa and similarities in outdoor activities of both sexes. However, the result is not statistically significant though the data supports that males are more exposed than females.

There was a general tendency for S. mansoni infection rate to increase with age, both in terms of prevalence and intensity of infection. The highest prevalence was observed in the 15–17 yr age group, which is in agreement with earlier reports in different parts of Ethiopia[23], [26],[27],[28],[29]. Such rise in infection with age may correspond with intense human water contact activities. Particularly in Bochesa, the prevalence of schistosomiasis was high in the age group of 11–18 yr and this could be due to the fact that young adults are exposed to water bodies during fishing.

WHO[20] categorizes communities in schistosomiasis endemic areas as low, moderate, and high risk communities for the respective prevalence of <10, 10–50, and >50%, respectively. In the present study, since S. mansoni prevalence was 23.7% for Bochesa, 14.5% for Kime and 31.3% for Finchaa, the communities can be categorized as moderate risk.

In this study, natural infection in Ch. aethiops (vervet monkeys) with S. mansoni and T. trichiura species were detected from faecal examination. This confirms the reports by Teklemariam et al[30] in which the prevalence was as high as 20% in the vervet monkeys from the same area. A number of other studies from different parts of the world have also demonstrated various intestinal parasites of zoonotic importance in non-human primates[31],[32],[33],[34].

Although indepth studies have not been conducted on helminth infections involving vervet monkeys, however, few studies conducted suggested that they harbor rich helminth fauna. Some of the helminth species identified from various populations in Africa include Streptopharagus spp, Trichuris trichiuria, Primasubulura spp, Spirurina fam. gen. sp, Dicrocoeliidae spp, Physaloptera spp, Necator spp, Oesophagostomum spp and Strongyloides spp[21], [35],[36].

In the present study, faecal examination revealed natural infection in baboons (P. anubis) with S. mansoni, Trichuris trichiuria, and Strongyloides spp. Earlier studies in the Rift Valley areas of Ethiopia have also demonstrated the occurrence of natural infection of S. mansoni and other parasites in NHPs, particularly in P. anubis[9],[10],[37]. Reports from other countries have also shown that baboons have naturally been infected with schistosomes and other helminth parasite including Oesophagostomum, Trichostrongylus, Trichuris, Strongyloides, Ternidens, Abbreviata, Molineus, Streptopharagus, and Physaloptera[32],[35],[36],[38],[39].

Among trematode parasites, S. mansoni is the most common in baboons of Africa, and of public health importance because they are responsible for zoonosis[10],[21],[32],[34]. Several aspects of helminthic infections (prevalence, infection intensity, parasite diversity, and transmission patterns) in baboons have been a subject of many empirical studies[21],[32],[34] which have demonstrated that the epidemiology of helminth infections vary among populations and habitats. For instance, there is divergence in infection patterns in populations dwelling in forested habitats compared to those in savannah[40].

In General, the present study confirms that NHPs play an important role in disease epidemiology of S. mansoni in Ethiopia. In many rural parts and recreational areas of Ethiopia, there is a close interaction between wild primates, especially baboons and vervets and humans. In other areas with similar ecological settings where schistosomiasis is endemic and in particular, where currently water-based development projects are escalating, there is a need to assess the occurrence of natural schistosome infections in wild animals. It is also important to monitor the epidemiology of schistosomiasis in areas with similar ecological settings, that are free of schistosomiasis to avoid the risk of re-establishment of schistosomiasis. Whatever the reason, the involvement of free ranging wild animals such as monkeys and baboons in the transmission cycle of schistosomiasis has very important epidemiological implication in that it complicates control and eventually elimination programmes.

The potential role that NHPs play in transmission of the parasite is now being acknowledged. However, there exists a serious lack of epidemiological data on S. mansoni infection in NHPs in particular and other animals in general, and hence their actual role in transmission, upon which any appropriate and sustainable surveillance, prevention and control strategies must be based, remains unknown[41]. In such areas control programs must take reservoir hosts into consideration because infection source in the reservoirs alone would suffice to maintain transmission of the disease in the presence of intermediate hosts, snail. The persistence of the focus of infection to both human and NHPs requires new strategies, such as supplementation of chemotherapy with snail control.


  Conclusion Top


This study provides insights into the epidemiology of S. mansoni in human and nonhuman primates in Ethiopia, a crucial information for the control of schistosomiasis. Reservoir hosts could perpetuate snail infections and favour renewed transmission to humans during and after termination of control programme unless reservoir hosts are considered in these programmes. In order to identify new schistosomiasis transmission foci in Ethiopia, there is a need to extend schistosomiasis mapping to ensure that the areas inhabited by NHPs are covered. Given potentially vast population size of NHP in Ethiopia their impact on S. mansoni transmission needs further study. Sustainable control of schistosomiasis requires an integrated, intersectorial approach that must go beyond current deworming program. Public health and wildlife professional should work together to develop a better disease control strategy. Complementary prevention strategies including snail control, health education, safe water and adequate sanitary facilities provision should simultaneously be implemented in order to interrupt transmission of the disease.

Conflicts of interest

The authors declare that no conflict of interests exist.


  Acknowledgements Top


The authors would like to extend their gratitude to Mr. Nega Nigusie and Mrs. Baysasu G/medhin of Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Ethiopia for their technical assistance.



 
  References Top

1.
Hu W, Brindley PJ, McManus DP, Feng Z, Han ZG. Schistosome transcriptomes: New insights into the parasite and schistosomiasis. Trends Mol Med 2004; 10(5): 217–25.  Back to cited text no. 1
    
2.
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: Systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 2006; 6(7): 411–25.  Back to cited text no. 2
    
3.
Stothard JR, Chitsulo L, Kristensen TK, Utzinger J. Control of schistosomiasis in sub-Saharan Africa: Progress made, new opportunities and remaining challenges. Parasitology 2009; 136(13): 1665–75.  Back to cited text no. 3
    
4.
Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, et al. Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: A systematic analysis for the global burden of disease study 2010. Lancet 2012; 380(9859): 2163–96.  Back to cited text no. 4
    
5.
Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Trop 2000; 77(1): 41–51.  Back to cited text no. 5
    
6.
Chitsulo L, Loverde P, Engels D. Schistosomiasis. Nat Rev Microbiol 2004; 2(1): 12–3.  Back to cited text no. 6
    
7.
Standley CJ, Kabatereine NB, Lange CN, Lwambo NJ, Stothard JR. Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria. Parasitology 2010; 137(13): 1937–49.  Back to cited text no. 7
    
8.
Hotez PJ, Kamath A. Neglected tropical diseases in sub-saharan Africa: Review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis 2009; 3(8): e412.  Back to cited text no. 8
    
9.
Fuller GK, Lemma A, Haile T. Schistosomiasis in man and monkeys in Omo National Park, southwest Ethiopia. Trans R Soc Trop Med Hyg 1979; 73(1): 121–2.  Back to cited text no. 9
    
10.
Erko B, Gebre-Michael T, Balcha F, Gundersen SG. Implication of Papio anubis in the transmission of intestinal schistosomiasis in three new foci in Kime area, Ethiopia. Parasitol Int 2001; 50(4): 259–66.  Back to cited text no. 10
    
11.
Webster BL, Webster JP, Gouvras AN, Garba A, Lamine MS, Diaw OT, et al. DNA ‘barcoding’ of Schistosoma mansoni across sub-Saharan Africa supports substantial within locality diversity and geographical separation of genotypes. Acta Trop 2013; 128(2): 250–60.  Back to cited text no. 11
    
12.
Modena CM, dos Santos Lima W, Coelho PM. Wild and domesticated animals as reservoirs of Schistosomiasis mansoni in Brazil. Acta Trop 2008; 108(2–3): 242–4.  Back to cited text no. 12
    
13.
Agola LE, Steinauer ML, Mburu DN, Mungai BN, Mwangi IN, Magoma GN, et al. Genetic diversity and population structure of Schistosoma mansoni within human infrapopulations in Mwea, central Kenya assessed by microsatellite markers. Acta Trop 2009; 111(3): 219–25.  Back to cited text no. 13
    
14.
Standley C, Dobson A, Stothard J. Out of animals and back again: Schistosomiasis as a zoonosis in Africa. In: Rokni MB, editor. Schistosomiasis. London (UK): IntechOpen Ltd. 2012; p. 209–30.  Back to cited text no. 14
    
15.
Standley CJ, Mugisha L, Dobson AP, Stothard JR. Zoonotic schistosomiasis in non-human primates: Past, present and future activities at the human-wildlife interface in Africa. J Helminthol 2012; 86(2): 131–40.  Back to cited text no. 15
    
16.
Nelson GS. Schistosome infections as zoonoses in Africa. Trans R Soc Trop Med Hyg 1960; 54: 301–24.  Back to cited text no. 16
    
17.
Dufera M, Petros B, Erko B, Berhe N, Gundersen S. G. Schistosoma mansoni infection in Finchaa sugar estate: Public health problem assessment based on clinical records and parasitological surveys, western Ethiopia. Sci Technol Arts Res J 2014; 3(2): 155–61.  Back to cited text no. 17
    
18.
Bench aids for the diagnosis of intestinal parasites. Geneva: World Health Organization 1994. Available from: http://www. who.int/iris/handle/10665/37323 (Accessed on December 8, 2015).  Back to cited text no. 18
    
19.
Feldmeier H, Poggensee G. Diagnostic techniques in schistosomiasis control. A review. Acta Trop 1993; 52(4): 205–20.  Back to cited text no. 19
    
20.
Prevention and control of schistosomiasis and soil-transmitted helminthiasis: Report of a WHO expert committee. Geneva: World Health Organization 2002. Available from: http://www. who.int/iris/handle/10665/42588 (Accessed on November 10, 2015).  Back to cited text no. 20
    
21.
Legesse M, Erko B. Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Trop 2004; 90(3): 231–6.  Back to cited text no. 21
    
22.
Erko B, Medihin G, Balcha F, Raje S. Evaluation of pilot control trial of intestinal schistosomiasis in Finchaa sugar estate, Ethiopia. Ethiop Med J 2003; 41: 141–50.  Back to cited text no. 22
    
23.
Mitiku H, Legesse M, Teklemariam Z, Erko B. Transmission of Schistosoma mansoni in Tikur Wuha area, southern Ethiopia. Ethiop J Health Dev 2010; 24(3): 180–4.  Back to cited text no. 23
    
24.
Aemero M, Boissier J, Climent D, Mone H, Mouahid G, Berhe N, et al. Genetic diversity, multiplicity of infection and population structure of Schistosoma mansoni isolates from human hosts in Ethiopia. BMC Genet 2015; 16: 137.  Back to cited text no. 24
    
25.
Erko B, Medhin G, Berhe N, Abebe F, Gebre-Michael T, Gundersen SG. Epidemiological studies on intestinal schistosomiasis in Wondo Genet, southern Ethiopia. Ethiop Med J 2002; 40(1): 29–39.  Back to cited text no. 25
    
26.
Erko B, Tedla S, Petros B. Transmission of intestinal schistosomiasis in Bahir Dar, northwest Ethiopia. Ethiop Med J 1991; 29(4): 199–211.  Back to cited text no. 26
    
27.
Woldemichael T, Kebede A. Newly identified endemic areas of Schistosomiasis mansoni in Tigray, northern Ethiopia. Ethiop Med J 1996; 34(2): 73–82.  Back to cited text no. 27
    
28.
Assefa T, Woldemmicale T, Dejene A. Intestinal parasitism among students in three localities in South Wello, Ethiopia. Ethiop J Health Dev 1998; 12: 231–5.  Back to cited text no. 28
    
29.
Merid Y, Hegazy M, Mekete G, Tekle Mariam S. Intestinal helmintic infection among children at Lake Awassa area, south Ethiopia. Ethiop J Health Dev 2001; 15: 31–7.  Back to cited text no. 29
    
30.
Teklemariam D, Legesse M, Degarege A, Liang S, Erko B. Schistosoma mansoni and other intestinal parasitic infections in schoolchildren and vervet monkeys in Lake Ziway area, Ethiopia. BMC Res Notes 2018; 11(1): 3248–2.  Back to cited text no. 30
    
31.
Ghandour AM, Zahid NZ, Banaja AA, Kamal KB, Bouq AI. Zoonotic intestinal parasites of hamadryas baboons Papio hamadryas in the western and northern regions of Saudi Arabia. J Trop Med Hyg 1995; 98(6): 431–9.  Back to cited text no. 31
    
32.
Munene E, Otsyula M, Mbaabu DA, Mutahi WT, Muriuki SM, Muchemi GM. Helminth and protozoan gastrointestinal tract parasites in captive and wild-trapped African non-human primates. Vet Parasitol 1998; 78(3): 195–201.  Back to cited text no. 32
    
33.
Muriuki SM, Murugu RK, Munene E, Karere GM, Chai DC. Some gastro-intestinal parasites of zoonotic (public health) importance commonly observed in old world non-human primates in Kenya. Acta Trop 1998; 71(1): 73–82.  Back to cited text no. 33
    
34.
Murray S, Stem C, Boudreau B, Goodall J. Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park. J Zoo Wildl Med 2000; 31(2): 176–8  Back to cited text no. 34
    
35.
Gillespie RT, Greiner CE, Chapman AC. Gastrointestinal parasites of the Guenons of western Uganda. J Parasitol 2004; 90(6): 1356–60.  Back to cited text no. 35
    
36.
Kooriyama T, Hasegawa H, Shimozuru M, Tsubota T, Nishida T, Iwaki T. Parasitology of five primates in Mahale Mountains National Park, Tanzania. Primates 2012; 53(4): 365–75.  Back to cited text no. 36
    
37.
Fuller GK, Lemma A, Haile T. Schistosomiasis in Omo National Park of southwest Ethiopia. Am J Trop Med Hyg 1979; 28(3): 526–30.  Back to cited text no. 37
    
38.
Muller-Graf CD, Collins DA, Woolhouse ME. Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 1996; 112 (pt V): 489–97.  Back to cited text no. 38
    
39.
Hahn N, Proulx D, Muruthi P, Alberts S, Altmann J. Gastrointestinal parasites in free-ranging Kenyan baboons (Papio cynocephalus and P. anubis). Int J Primatol 2003; 24(2): 271–9.  Back to cited text no. 39
    
40.
Bezjian M, Gillespie RT, Chapman AC, Greiner CE. Coprologic evidence of gastrointestinal helminths of forest baboons, Papio anubis, in Kibale National Park, Uganda. J Wildl Dis 2008; 44(4): 878–87.  Back to cited text no. 40
    
41.
Hagan P, Gryseels B. Schistosomiasis research and the European community. Trop Geogr Med 1994; 46(4): 259–68.  Back to cited text no. 41
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2]



 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
Material & M...
Results
Discussion
Conclusion
Acknowledgements
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed72    
    Printed0    
    Emailed0    
    PDF Downloaded31    
    Comments [Add]    

Recommend this journal