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Volume 25, Number 11—November 2019
Research Letter

Endemicity of Yaws and Seroprevalence of Treponema pallidum Antibodies in Nonhuman Primates, Kenya

Dawn M. ZimmermanComments to Author , Emily H. Hardgrove, Michael E. von Fricken, Joseph Kamau, Daniel Chai, Samson Mutura, Velma Kivali, Fatima Hussein, Peris Ambala, Andrea Surmat, Joseph G. Maina, and Sascha Knauf
Author affiliations: Smithsonian Conservation Biology Institute, Washington DC, USA (D.M. Zimmerman, E.H. Hardgrove, M.E. von Fricken); George Mason University, Fairfax, Virginia, USA (D.M. Zimmerman, M.E. von Fricken); Virginia Polytechnic Institute and State University, Blacksburg, Virginia, USA (E.H. Hardgrove); Institute of Primate Research, Nairobi, Kenya (J. Kamau, D. Chai, S. Mutura, F. Hussein, P. Ambala); International Livestock Research Institute, Nairobi (V. Kivali); Mpala Research Centre and Wildlife Foundation, Nanyuki, Kenya (A. Surmat); Kenya Wildlife Service, Nairobi (J.G. Maina); German Primate Center, Goettingen, Germany (S. Knauf)

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Abstract

Human yaws has historically been endemic to Kenya, but current epidemiologic data are lacking. We report seroprevalence for Treponema pallidum antibodies in olive baboons (Papio anubis) and vervet monkeys (Chlorocebus pygerythrus) in Laikipia County, Kenya. Our results suggest endemicity of the yaws bacterium in monkeys, posing a possible zoonotic threat to humans.

Yaws is a disease caused by the bacterium Treponema pallidum subsp. pertenue, which is believed to be an exclusively human pathogen (1). However, this bacterium has recently been identified in African nonhuman primates (NHPs) (2), raising concerns about a possible zoonotic reservoir for human infection. Kenya is 1 of 76 countries that the World Health Organization categorizes as previously endemic for yaws, but no current data support its presence or absence (http://apps.who.int/gho/data/node.main.NTDYAWSEND). However, sustainable yaws eradication will rely on information about transmission dynamics and potential links between human and NHP T. pallidum strains (3).

In the early 1960s, Fribourg-Blanc and Mollaret tested 150 serum samples from wild-caught baboons (Papio sp.) from Guinea and Kenya (4). Although 72 (65%) of 111 serum samples from Guinea were positive for T. pallidum antibodies, none of the samples from Kenya were positive. In subsequent years, an additional 276 serum samples from baboons in Kenya supported the absence of T. pallidum infection. However, a more recent study of baboon samples collected during 1977–1994 in Kenya reported serologic evidence of T. pallidum infection in Nanyuki, Laikipia County (prevalence 57.5%) (5). For our study, we hypothesized that 39 years after the first samples were positive for antibodies against T. pallidum in Nanyuki (5), infection is still present in the NHP population.

All animal protocols were approved by the Kenya Wildlife Service (permit #4004), the Institute of Primate Research Scientific and Ethics Review Committee, and the Smithsonian Institution Animal Use and Care Committee. In October 2016, we sampled 65 olive baboons (Papio anubis) and 2 vervet monkeys (Chlorocebus pygerythrus) at sites surrounding the Mpala Research Centre in Laikipia County, Kenya. We performed a preliminary serologic screening by using the immunochromatographic Dual Path Platform (DPP) HIV-Syphilis Assay (Chembio Diagnostic Systems, Inc., http://chembio.com) according to the manufacturer guidelines. This syphilis (T. pallidum) assay is a useful screening tool because antibodies against Treponema subspecies are cross-reactive (6). We tested 67 samples with the DPP assay; 49 were positive and 18 negative.

However, because this test is not certified for use with NHPs, we subsequently confirmed results by using the T. pallidum Particle Agglutination Assay (TPPA) (SERODIA TPPA, https://www.fujirebio-us.com), which has been validated for use in baboons (7). Of the 52 samples tested with the TPPA assay, there were 33 positive, 6 negative, and 13 inconclusive results. Inconclusive TPPA results indicate nonspecific antibodies reacting with nonsensitized particles. Because of limited sample material, we were unable to perform repeated testing with a preabsorption step to remove all nonspecific binding antibodies (as described in the assay manual) and therefore excluded the inconclusive TPPA results from our analysis.

If we defined seropositive monkeys as those with positive results for the TPPA or DPP, 1 of 2 vervet monkeys and 53 (85.5%) of 62 baboons were seropositive. Male baboons (90.4%, 38/42) had a relative seropositivity risk ratio of 1.3 (95% CI 0.984–1.858) when compared with female baboons (72.2%, 13/18); however, this difference was not significant (p = 0.111 by Fisher exact test). If we included age, in addition to sex, in the analysis, adult male and female baboons both showed 100% seropositivity (21/21 and 10/10, respectively). Subadult males and females also showed seropositivity of 100% (6/6 and 1/1, respectively). Juveniles had a combined seropositivity of 61.1%: a total of 81.8% (9/11) of males and 28.6% (2/7) of females were seropositive. Infants had the lowest seroprevalence rate (50%, 2/4) (Table).

None of the tested NHPs had overt clinical signs of infection, such as skin lesions, which might have contained T. pallidum DNA. However, several other studies found that NHPs are frequently seropositive for T. pallidum antibodies without clinical lesions (5,8,9). Because wild NHPs are not treated and bacterial clearance is unlikely, the absence of lesions presumably corresponds to the latency stage of infection, which is also a key characteristic of human treponematoses (10). Future molecular investigations should include nontreponemal tests to further support the assumption that animals are in the latency stage and should target the DNA of the pathogen, which would enable comparison of T. pallidum strains of NHP origin from Kenya with those infecting NHPs in neighboring countries and possibly humans. In Tanzania, a country that has a similar history of previous yaws endemicity in humans and lacks current prevalence data, clinical lesions have been documented in olive baboons, vervet monkeys, yellow baboons, and blue monkeys, in addition to widespread seroprevalence in NHPs closely matching previous human infection geographic distribution (9).

Our results suggest that evidence of Treponema exposure in NHPs continues to be present in Laikipia County almost 4 decades after it was first detected. Our data provide further evidence that, in East Africa, T. pallidum infection is endemic to NHPs and that multiple NHP taxa contain antibodies indicating latent infection. Providing reliable information on the epidemiology of treponematoses in humans and NHPs has major programmatic implications for yaws eradication. Under a One Health approach, we call for additional yaws surveillance in communities in Kenya, especially in regions where NHPs and humans coexist.

Dr. Zimmerman is director of wildlife health and associate program director for the Smithsonian Conservation Biology Institute’s Global Health Program, Washington, DC, and country lead for the US Agency for International Development Emerging Pandemic Threats PREDICT program in Kenya. Her primary research interests include applying a One Health approach to the conservation of critically endangered wildlife species and the mitigation of emerging infectious diseases at the wildlife–human interface.

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Acknowledgments

We thank the Kenya Wildlife Service and Mpala Research Centre for assistance during this study.

This study was supported by the US Agency for International Development Emerging Pandemic Threats PREDICT Project (cooperative agreement mo. GHN-A-OO-09-00010-00) and the German Research Foundation (grant DFG KN 1097/3-1 to S.K.).

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References

  1. Marks  M, Lebari  D, Solomon  AW, Higgins  SP. Yaws. Int J STD AIDS. 2015;26:696703. DOIPubMed
  2. Knauf  S, Gogarten  JF, Schuenemann  VJ, De Nys  HM, Düx  A, Strouhal  M, et al. Nonhuman primates across sub-Saharan Africa are infected with the yaws bacterium Treponema pallidum subsp. pertenue. Emerg Microbes Infect. 2018;7:157. DOIPubMed
  3. Bodimeade  C, Marks  M, Mabey  D. Neglected tropical diseases: elimination and eradication. Clin Med (Lond). 2019;19:15760. DOIPubMed
  4. Fribourg-Blanc  A, Mollaret  HH. Natural treponematosis of the African primate. Primates Med. 1969;3:11321.PubMed
  5. Harper  KN, Fyumagwa  RD, Hoare  R, Wambura  PN, Coppenhaver  DH, Sapolsky  RM, et al. Treponema pallidum infection in the wild baboons of East Africa: distribution and genetic characterization of the strains responsible. PLoS One. 2012;7:e50882. DOIPubMed
  6. Chi  KH, Danavall  D, Taleo  F, Pillay  A, Ye  T, Nachamkin  E, et al. Molecular differentiation of Treponema pallidum subspecies in skin ulceration clinically suspected as yaws in Vanuatu using real-time multiplex PCR and serological methods. Am J Trop Med Hyg. 2015;92:1348. DOIPubMed
  7. Knauf  S, Dahlmann  F, Batamuzi  EK, Frischmann  S, Liu  H. Validation of serological tests for the detection of antibodies against Treponema pallidum in nonhuman primates. PLoS Negl Trop Dis. 2015;9:e0003637. DOIPubMed
  8. Knauf  S, Batamuzi  EK, Mlengeya  T, Kilewo  M, Lejora  IA, Nordhoff  M, et al. Treponema infection associated with genital ulceration in wild baboons. Vet Pathol. 2012;49:292303. DOIPubMed
  9. Chuma  IS, Batamuzi  EK, Collins  DA, Fyumagwa  RD, Hallmaier-Wacker  LK, Kazwala  RR, et al. Widespread Treponema pallidum infection in nonhuman primates, Tanzania. Emerg Infect Dis. 2018;24:10029. DOIPubMed
  10. Marks  M, Mitjà  O, Solomon  AW, Asiedu  KB, Mabey  DC. Yaws. Br Med Bull. 2015;113:91100. DOIPubMed

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Table

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Cite This Article

DOI: 10.3201/eid2511.190716

Original Publication Date: 10/3/2019

Table of Contents – Volume 25, Number 11—November 2019

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Dawn M. Zimmerman, Smithsonian Conservation Biology Institute, National Zoological Park, 3001 Connecticut Ave NW, Washington DC 20008, USA:

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Page created: October 15, 2019
Page updated: October 15, 2019
Page reviewed: October 15, 2019
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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