Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: Evidence of Trichomonadidae infections

Julie Rushmore; Andrew B Allison; Erin E Edwards; Ujwal Bagal; Sonia Altizer; Mike R Cranfield; Travis C Glenn; Hsi Liu; Antoine Mudakikwa; Lawrence Mugisha; Martin N Muller; Rebecca M Stumpf; Melissa Emery Thompson; Richard Wrangham; Michael J Yabsley

doi:10.1002/ajp.22442

Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: Evidence of Trichomonadidae infections

Am J Primatol. 2015 Oct;77(10):1075-85. doi: 10.1002/ajp.22442. Epub 2015 Jun 26.

Authors

Julie Rushmore^{1

2}, Andrew B Allison³, Erin E Edwards², Ujwal Bagal⁴, Sonia Altizer¹, Mike R Cranfield^{5

6}, Travis C Glenn⁷, Hsi Liu⁸, Antoine Mudakikwa⁹, Lawrence Mugisha^{10

11}, Martin N Muller¹², Rebecca M Stumpf¹³, Melissa Emery Thompson, Richard Wrangham¹⁴, Michael J Yabsley¹⁵

Affiliations

¹ Odum School of Ecology, The University of Georgia, Athens, Georgia.
² College of Veterinary Medicine, The University of Georgia, Athens, Georgia.
³ Baker Institute for Animal Health, Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, New York.
⁴ Institute of Bioinformatics, The University of Georgia, Athens, Georgia.
⁵ Gorilla Doctors, Wildlife Health Center, University of California Davis, Davis, California.
⁶ The Department of Molecular and Pathobiology, Johns Hopkins School of Medicine, Baltimore, Maryland.
⁷ Department of Environmental Health Science, The University of Georgia, Athens, Georgia.
⁸ National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control, Athens, Georgia.
⁹ Rwanda Development Board, Department of Tourism and Conservation, Kigali, Rwanda.
¹⁰ Conservation and Ecosystem Health Alliance (CEHA), Kampala, Uganda.
¹¹ College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda.
¹² Department of Anthropology, University of New Mexico, Albuquerque, New Mexico.
¹³ Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, Illinois.
¹⁴ Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts.
¹⁵ Warnell School of Forestry and Natural Resources, The University of Georgia and the Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, The University of Georgia, Athens, Georgia.

PMID: 26119266
DOI: 10.1002/ajp.22442

Abstract

Sexually transmitted diseases (STDs) can persist endemically, are known to cause sterility and infant mortality in humans, and could have similar impacts in wildlife populations. African apes (i.e., chimpanzees, bonobos, and to a lesser extent gorillas) show multi-male mating behavior that could offer opportunities for STD transmission, yet little is known about the prevalence and impact of STDs in this endangered primate group. We used serology and PCR-based detection methods to screen biological samples from wild and orphaned eastern chimpanzees and gorillas (N = 172 individuals, including adults, and juveniles) for four classes of pathogens that either commonly cause human STDs or were previously detected in captive apes: trichomonads, Chlamydia spp., Treponema pallidum (syphilis and yaws), and papillomaviruses. Based on results from prior modeling and comparative research, we expected STD prevalence to be highest in females versus males and in sexually mature versus immature individuals. All samples were negative for Chlamydia, Treponema pallidum, and papillomaviruses; however, a high percentage of wild chimpanzee urine and fecal samples showed evidence of trichomonads (protozoa). Analysis revealed that females were more likely than males to have positive urine-but not fecal-samples; however, there was no evidence of age (sexual maturity) differences in infection status. Sequence analysis of chimpanzee trichomonad samples revealed a close relationship to previously described trichomonads within the genus Tetratrichomonas. Phylogenetic comparisons to archived sequences from multiple vertebrate hosts suggests that many of the chimpanzee parasites from our study are likely transmitted via fecal-oral contact, but the transmission of some Tetratrichomonas sequence-types remains unknown and could include sexual contact. Our work emphasizes that only a fraction of infectious agents affecting wild apes are presently known to science, and that further work on great ape STDs could offer insights for the management of endangered great apes and for understanding human STD origins.

Keywords: Chlamydia spp.; Gorilla beringei; Pan troglodytes; Tetratrichomonas spp; Treponema pallidum; papillomavirus.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Chlamydia / isolation & purification*
Feces / parasitology
Female
Gorilla gorilla
Male
Pan troglodytes
Papillomaviridae / isolation & purification*
Prevalence
Primate Diseases / microbiology
Primate Diseases / parasitology*
Primate Diseases / virology
Protozoan Infections, Animal
Sex Factors
Sexually Transmitted Diseases / veterinary*
Treponema pallidum / isolation & purification*
Trichomonadida / isolation & purification*
Urine / parasitology