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Haemoprotozoan Parasites of Non-Human Primates in Kenya: Studies on Prevalence and Characterization of Haemoprotozoan Parasites of Wild-Caught Baboons, African Green Monkeys and Syke's Monkeys
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Comparative Medicine.
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis reports on cross-sectional surveys aimed at detecting and characterizing haemoprotozoan parasites infecting wild free-ranging non human primates (NHPs) in Kenya, East Africa. Blood samples from olive baboons (Papio cynocephalus anubis), vervet monkeys or African green monkeys (AGMs, Chlorocebus aethiops) and Syke's monkeys (Cercopithecus mitis) from five provinces of Kenya were analyzed. The haemoprotozoan parasites survey was performed with microscopic evaluation of blood smears, serological techniques and molecular tools.

Blood specimens and serum samples from 121 NHPs were tested for the presence of Trypanosoma brucei (Study I). Indirect antibody enzyme-linked immunosorbent assay (Ab-ELISA) detected titers of anti-T. brucei antibodies in 19% (23/121) of the sera sampled. Subsequent field-oriented latex agglutination test (LAT) detected presence of T. brucei antigens in 16% (19/121) of the sera. However, there were no active infections detected on fixed blood smears, or wet blood films. Of the 378 NHPs sera samples tested for Leishmania major exposure using Ab-ELISA, 66% had detectable anti-L. major antibodies (study II). Western blot (WB) assay detected anti-L. major antibodies in sera from 46% (175/378) of the NHPs samples. Specific proliferation of peripheral blood mononuclear cells to L. major antigen was demonstrated in 23% (17/57) of AGMs samples. Haemoprotozoan parasites, Entopolypoides macaci and Hepatocystis kochi were detected by microscopic evaluation of Giemsa-stained blood smears from 179 NHPs (study III). The prevalence rate of E. macaci was 43% in African green monkeys, 35% in Syke’s monkeys and 33% in baboons. H. kochi infection rate was 18% in African green monkeys, 23% in baboons and 25% in Syke’s monkeys. Subsequent indirect immunofluorescent antibody test (IFAT) supported the morphologic appearance of E. macaci observed by microscopy. Molecular tools were used to detect and identify haemoprotozoan parasites in wild free-ranging NHPs (study IV). Nested polymerase chain reaction (PCR) targeting Babesia β-tubulin gene detected a 22% (27/125) B. microti infections in free-ranging NHPs in Kenya. PCR also detected 22% mixed infections by Hepatocystis and Entopolypoides, 12% Hepatocystis and Babesia and 7% Entopolypoides and Babesia (study V). Phylogenetic analysis inferred from mitochondrial cytochrome b (Cyt-b) gene confirmed the presence of Hepatocystis kochi whereas analysis of 18SS rRNA gene confirmed presence of two piroplasms, Babesia sp. and Entopolypoides macaci.

In conclusion, epidemiological results from sero-prevalence studies provide strong circumstantial evidence that some species of Kenyan NHPs are naturally exposed to L. major and T. brucei infections and could be potential reservoir hosts for these haemoparasites. Molecular diagnosis revealed the occurrence of mixed parasite infections and confirmed the circulation of Babesia and Entopolypoides species in the same populations of Kenyan NHPs.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2011. , 52 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 663
Keyword [en]
haemoprotozoan parasites, nonhuman primates, Kenya
National Category
Microbiology in the medical area
Research subject
Comparative Medicine
Identifiers
URN: urn:nbn:se:uu:diva-150467ISBN: 978-91-554-8049-3OAI: oai:DiVA.org:uu-150467DiVA: diva2:407540
Public defence
2011-05-10, Room B41, Uppsala Biomedicinska Centrum, Uppsala, 10:00 (English)
Opponent
Available from: 2011-04-19 Created: 2011-03-30 Last updated: 2011-05-05Bibliographically approved
List of papers
1. Sero-epizootiologic survey of Trypanosoma brucei in Kenyan nonhuman primates
Open this publication in new window or tab >>Sero-epizootiologic survey of Trypanosoma brucei in Kenyan nonhuman primates
2002 (English)In: Journal of zoo and wildlife medicine, ISSN 1042-7260, ISSN ISSN 1042-7260, Vol. 33, no 4, 337-341 p.Article in journal (Refereed) Published
Keyword
nonhuman primates, Trypanosoma brucei, Kenya
National Category
Microbiology in the medical area
Research subject
Comparative Medicine
Identifiers
urn:nbn:se:uu:diva-150264 (URN)
Available from: 2011-03-28 Created: 2011-03-28 Last updated: 2011-05-05
2. Prevalence of antibodies and cell mediated immune responce against Leishmania major in feral non-human primates from Kenya
Open this publication in new window or tab >>Prevalence of antibodies and cell mediated immune responce against Leishmania major in feral non-human primates from Kenya
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2009 (English)In: Acta Tropica, ISSN 0001-706X, E-ISSN 1873-6254, Vol. 109, no 2, 136-140 p.Article in journal (Refereed) Published
Abstract [en]

In Kenya, Leishmania major is responsible for human cutaneous leishmaniasis (CL). Natural infection with L. major of a vervet monkey and experimental susceptibility of some nonhuman primates (NHPs) from Kenya has been established. However, there has been no comprehensive study of the prevalence of zoonotic CL in Kenya. And also, no investigation has been done to assess whether NHPs could be potential reservoir hosts of L. major even when the involvement of reservoir animals is obligatory in transmission of this parasite. To achieve this, wild caught Chlorocebus aethiops (Vervet monkeys n=213), Papio cynocephalus anubis (olive baboons n=101) and Cercopithecus mitis (Syke's monkeys n=64) from five geographical locations in Kenya were screened for antibodies against L. major using enzyme linked immunosorbent assay (ELISA) and Western blot (WB) analysis. From the population of C. aethiops (n=213) captured, 57 were used in lymphocyte proliferation assay. ELISA revealed a high prevalence of leishmaniasis sero conversion in olive baboons 78/101 (77.2%), vervet monkeys 129/213 (60.6%) and Sykes' monkeys 43/64 (67.2%). WB detected anti-L. major antibodies in 48.5% (49/101) of the baboons, 48% (102/213) of vervet monkeys and 37.5% (24/64) of Sykes' monkey sera. Specific proliferation of peripheral blood mononuclear cells to L. major antigen was demonstrated in 17 of the 57 (29.8%) vervet monkeys. In conclusion, the results of serological assays provide strong circumstantial evidence that CL is prevalent in five Provinces of Kenya and that Kenyan NHPs could be could be a potential reservoir hosts of L. major.

Keyword
Nonhuman primates, Leishmaniasis, seroprevalence, Kenya
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-105020 (URN)10.1016/j.actatropica.2008.09.020 (DOI)000262737200008 ()18983806 (PubMedID)
Available from: 2009-05-31 Created: 2009-05-31 Last updated: 2011-05-05Bibliographically approved
3. Enzootic simian piroplasm(Entopolypoides macaci) in wild-caught Kenyan non-human primates.
Open this publication in new window or tab >>Enzootic simian piroplasm(Entopolypoides macaci) in wild-caught Kenyan non-human primates.
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2008 (English)In: Journal of medical primatology, ISSN 0047-2565, Vol. 37, no 6, 329-336 p.Article in journal (Refereed) Published
Abstract [en]

BACKGROUND

Three species of non-human primates comprising African green monkeys (AGMs), (Cercopithecus aethiops, n = 89), Syke's monkeys (Cercopithecus mitis, n = 60) and olive baboons (Papio cynocephalus anubis, n = 30), were screened for Entopolypoides macaci.

METHODS

Observation of blood smears prepared from these animals revealed E. macaci infection rate of 42.7% in AGMs, 35% in Syke's monkeys and 33.3% in baboons.

RESULTS

Gender infection rate was 38.2% in females and 29% in males. Statistically, there was no significant difference in infection rates between the monkey species and sexes (P > 0.05). Subsequent indirect immuno fluorescent antibody test supported the morphological appearance of E. macaci observed by microscopy. Sera from infected animals reacted positively (1:625) with E. macaci antigen, but not to Babesia bigemina or B. bovis antigen at 1:125 titer.

CONCLUSION

This study has revealed high prevalence of E. macaci infection in all three widely distributed Kenyan non-human primates. With the continued use of these animals as models for human parasitic diseases, the presence of this highly enzootic parasite should be noted.

Keyword
C. mitis, Cercopithecus aethiops, Entopolypoides macaci, Kenya, Papio cynocephalus anubis, prevalence
Identifiers
urn:nbn:se:uu:diva-105008 (URN)10.1111/j.1600-0684.2008.00294.x (DOI)18507704 (PubMedID)
Available from: 2009-05-31 Created: 2009-05-31 Last updated: 2011-05-05Bibliographically approved
4. Prevalence of Babesia microti in free-ranging Baboons and African Green Monkeys
Open this publication in new window or tab >>Prevalence of Babesia microti in free-ranging Baboons and African Green Monkeys
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2011 (English)In: Journal of Parasitology, ISSN 0022-3395, Vol. 97, no 1, 63-67 p.Article in journal (Refereed) Published
Abstract [en]

Babesia microti-like parasites have been reported to infect captive non-human primates (NHPs). However, studies on the prevalence of Babesia spp. in free-ranging NHPs are lacking. This investigation aimed at determining the prevalence of B. microti in wild-caught Kenyan NHPs. In total, 125 animals were studied, including 65 olive baboons (Papio cynocephalus anubis) and 60 African green monkeys ([AGMs] Chlorocebus aethiops). Nested polymerase chain reaction targeting Babesia β-tubulin genes was used to diagnose infection prevalence. Results indicated a prevalence of 22% (27/125) B. microti infection in free-ranging NHPs in Kenya. There was no statistically significant difference in B. microti infection prevalence between baboons and AGMs or male and female animals. This is the first report of the presence and prevalence of B. microti in free-ranging Kenyan NHPs.

Keyword
Babesia microti
National Category
Microbiology in the medical area
Research subject
Comparative Medicine
Identifiers
urn:nbn:se:uu:diva-150261 (URN)10.1645/GE-2391.1 (DOI)21348608 (PubMedID)
Available from: 2011-03-28 Created: 2011-03-28 Last updated: 2013-03-12Bibliographically approved
5. Detection and molecular characterization of haemoprotozoan parasites of wild-caught nonhuman primates in Kenya
Open this publication in new window or tab >>Detection and molecular characterization of haemoprotozoan parasites of wild-caught nonhuman primates in Kenya
(English)Manuscript (preprint) (Other academic)
Keyword
haemoprotozoan parasites, nonhuman primates, PCR, Kenya
National Category
Microbiology in the medical area
Research subject
Comparative Medicine
Identifiers
urn:nbn:se:uu:diva-150441 (URN)
Available from: 2011-03-30 Created: 2011-03-30 Last updated: 2011-05-05Bibliographically approved

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