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Skeletal evidence of probable treponemal infection in free-ranging African apes

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Abstract

The prevalence and patterning of inflammatory lesions of the skeleton were investigated in samples of chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) curated at the Powell-Cotton Museum, Birchington, UK. One hundred and two chimpanzees (42 adults and 60 subadults) and 126 gorillas (50 adults and 76 subadults) comprise the samples. Twenty per cent of chimpanzees and 14% of gorillas were affected with a disseminated inflammatory skeletal condition caused by infection. The lesions appear to have originated as localized patches of new bone deposition on the surface of long bones and to have progressed to infection of the bone cortex and marrow. Although female prevalence of involvement exceeds that of males in both species, the differences are not statistically significant. The age distribution of affected animals indicates that the disease began in some animals as early as 2 yr of age. Given the skeletal and demographic prevalence and patterning of the lesions as well as the ecology and behavior of these animals, the most likely diagnosis of the condition is a yaws-like treponemal infection.

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References

  • Al-Doory, Y. 1972. Intermediate mycoses. In:Pathology of Simian Primates, Part II: Infectious and Parasitic Diseases,Fiennes,R. N. T.-W. (ed.) Karger, Basel, pp. 214–223.

    Google Scholar 

  • Anemone, R. L.;Mooney, M. P.;Siegel, M. I. 1996. Longitudinal study of dental development in chimpanzees of known chronological age: implications for understanding the age at death of Plio-Pleistocene hominids.Amer. J. Phys. Anthropol., 99: 119–133.

    Article  CAS  Google Scholar 

  • Anemone, R. L.;Watts, E. S.;Swindler, D. S. 1991. Dental development of known-age chimpanzees,Pan troglodytes (Primates, Pongidae).Amer. J. Phys. Anthropol., 86: 229–241.

    Article  Google Scholar 

  • Aufderheide, A. C.;Rodriguez-Martin, C. 1998.The Cambridge Encyclopedia of Human Paleopathology, Cambridge Univ. Press, Cambridge.

    Google Scholar 

  • Baker, B. J.;Armelagos, G. J. 1988. The origin and antiquity of syphilis.Cur. Anthropol., 29: 703–737.

    Article  CAS  Google Scholar 

  • Barker, M. J. M.;Herbert, R. T. 1972. Diseases of the skeleton. In:Pathology of Simian Primates, Part I: General Pathology,Fiennes,R. N. T.-W. (ed.), Karger, Basel, pp. 433–519.

    Google Scholar 

  • Bramblett, C. 1967. Pathology in the Darajani baboon.Amer. J. Phys. Anthropol., 21: 331–340.

    Article  Google Scholar 

  • Buikstra, J. E. 1975. Healed fractures inMacaca mulatta: age, sex, and symmetry.Folia Primatol., 23: 140–148.

    PubMed  CAS  Google Scholar 

  • Chulay, J. D. 1990. Treponema species (yaws, pinta, bejel). In:Principles and Practice of Infectious Diseases (3rd ed.),Mandell, G. L.;Douglas, R. G. Jr.;Bennett, J. E. (eds.), Churchill Livingstone, New York, pp. 1808–1812.

    Google Scholar 

  • Cockburn, A. 1963. The treponematoses. In:The Evolution and Eradication of Infectious Disease,Cockburn,A. (ed.) Johns Hopkins, Baltimore, pp. 152–174.

    Google Scholar 

  • Cockburn, A. (ed.). 1967. The evolution of human infectious diseases. In:Infectious Diseases: Their Evolution and Eradication, CC Thomas, Springfield, pp. 84–107.

    Google Scholar 

  • Cousins, D. 1972. Diseases and injuries in wild and captive gorillas.Int. Zoo Yrbk., 12: 211–218.

    Google Scholar 

  • Dean, M. C.;Jones, M. E.;Pilley, J. R. 1992. The natural history of tooth wear, continuous eruption and periodontal disease in wild shot great apes.J. Human Evol., 22: 23–39.

    Article  Google Scholar 

  • Degusta, D.;Milton, K. 1998. Skeletal pathologies in a population ofAloutta palliata: behavioral, ecological, and evolutionary implications.Int. J. Primatol., 19: 615–650.

    Article  Google Scholar 

  • Derousseau, C. J. 1988.Osteoarthritis in Rhesus Monkeys and Gibbons: A Locomotor Model of Joint Degeneration, Vol. 25: Contributions to Primatology. Karger, Basel.

    Google Scholar 

  • Deturckheim, G.;Merz, E. 1984. Breeding Barbary macaques in outdoor open enclosures. In:The Barbary Macaque: A Case Study in Conservation,Fa,J. E. (ed.), Plenum, New York, pp. 241–261.

    Google Scholar 

  • Dittus, W. P. J.;Ratnayeke, S. M. 1989. Individual and social behavior responses to injury in wild toque macaque (Macaca sinica).Int. J. Primatol., 10: 215–234.

    Google Scholar 

  • Donham, K. J.;Leininger, J. R. 1977. Spontaneous leprosy-like lesions in a chimpanzee.,J. Infect. Dis., 136: 132–136.

    PubMed  CAS  Google Scholar 

  • Engelkens, H. J. H.;Judanarso, J.;Oranje, A. P.;Vuzevski, V. D.;Niemel, P. L. A.;Van Der Sluis, J. J.;Stolz, E. 1991. Endemic treponematoses.Int. J. Dermatol., 30: 77–83.

    PubMed  CAS  Google Scholar 

  • Fa, J. E. (ed.). 1984. Structure and dynamics of the Barbary macaque population in Gibraltar., In:The Barbary Macaque: A Case Study in Conservation, Plenum, New York, pp. 263–306.

    Google Scholar 

  • Fiennes, R. N. T.-W. 1967.Zoonoses of Primates. Cornell, Ithaca.

    Google Scholar 

  • Fossey, D. 1983.Gorillas in the Mist. Houghton Mifflin, Boston.

    Google Scholar 

  • Fribourg-Blanc, A. 1972. Treponema. In:Pathology of Simian Primates, Vol. 2,Fiennes,R. N. T.-W. (ed.), Karger, Basel, pp. 255–262.

    Google Scholar 

  • Gao, F.;Bailes, E.;Robertson, D. L.;Chen, Y.;Rodenburg, C. M.;Michael, S. F.;Cummins, L. B.;Arthur, L. O.;Peeters, M.;Shaw, G. M.;Sharp, P. M.;Hahn, B. H. 1999. Origin of hiv-1 in the chimpanzeePan troglodytes troglodytes.Nature, 397: 436–441.

    Article  PubMed  CAS  Google Scholar 

  • Geddes, H. 1955.Gorilla. Andrew Melrose, London.

    Google Scholar 

  • Goodall, J. 1986.The Chimpanzees of Gombe. Harvard Univ. Press, Cambridge, Massachusetts.

    Google Scholar 

  • Guatelli-Steinberg, D.;Lukacs, J. R. 1998. Preferential expression of linear enamel hypoplasia on the sectorial premolars of rhesus monkeys (Macaca mulatta).Amer. J. Phys. Anthropol., 107: 179–186.

    Article  CAS  Google Scholar 

  • Hackett, C. J. 1963. On the origin of the human treponematoses (pinta, yaws, endemic syphilis, and venereal syphilis).Bull. World Health Org., 29: 7–41.

    PubMed  CAS  Google Scholar 

  • Hoeprich, P. D. 1994. Nonsyphilitic treponematoses. In:Infectious Diseases (5th ed.),Hoeprich, P. D.;Jordan, M. C.;Ronald, A. R. (eds.), Lippincott, Philadelphia, pp. 1018–1028.

    Google Scholar 

  • Holland, W. J. 1924. Account of a skeleton of a gorilla remarkable because showing recovery from gunshot wounds.Ann. Carnegie Mus., 15: 293–298.

    Google Scholar 

  • Hudson, E. H. 1964. Treponematosis and African slavery.Br. J. Vener. Dis., 40: 43–51.

    PubMed  CAS  Google Scholar 

  • Jurmain R. 1989. Trauma, degenerative disease, and other pathologies among the Gombe chimpanzees.Amer. J. Phys. Anthropol., 80: 229–237.

    Article  CAS  Google Scholar 

  • Jurmain, R. 1997. Skeletal evidence of trauma in African apes, with special reference to the Gombe chimpanzees.Primates, 38: 1–14.

    Article  Google Scholar 

  • Jurmain, R.; Kilgore, L. 1994. Pathological conditions of the skeleton in free ranging pongids: evolutionary implications. Provisional report submitted to the L. S. B. Leakey Foundation, March, 1994.

  • Kerley, E. R. 1966. Skeletal age changes in the chimpanzee.Tulane Studies Zool., 13: 71–82.

    Google Scholar 

  • Kilgore, L. 1989. Dental pathologies in ten free-ranging chimpanzees from Gombe National Park, Tanzania.Amer. J. Phys. Anthropol., 80: 219–227.

    Article  CAS  Google Scholar 

  • Koff, A. B.;Rosen, T. 1993. Nonvenereal treponematoses: yaws, endemic syphilis, and pinta.J. Amer. Acad. Dermatol., 29: 519–535.

    Article  CAS  Google Scholar 

  • Long, J. C.;Merbs, C. F. 1981. Coccidioidomycosis: a primate model. In:Prehistoric Tuberculosis in the Americas,Buikstra,J. E. (ed.), Northwestern Univ. Archaeol. Prog., Evanston, Sci. Papers No. 5, pp. 69–83.

    Google Scholar 

  • Lovell, N. C. 1990a.Illness and Injury in Great Apes: A Skeletal Analysis. Smithsonian Inst, Washington.

    Google Scholar 

  • Lovell, N. C. 1990b. Skeletal and dental pathology of free-ranging mountain gorillas.Amer. J. Phys. Anthropol., 81: 399–412.

    Article  CAS  Google Scholar 

  • Lovell, N. C. 1991. An evolutionary framework for assessing illness and injury in nonhuman primates.Yrbk. Phys. Anthropol., 34: 117–155.

    Article  Google Scholar 

  • Manz, H. J.;Buck, A. A. 1997. Yaws, bejel, and pinta. In:Pathology of Infectious Diseases, Vol. 1,Connor,D. H.;Chandler,F. W.;Schwartz,D. A.;Manz,H. J.;Lack,E. E. (eds.), Appleton & Lange, Stamford, pp. 911–916.

    Google Scholar 

  • Morbeck, M. E.;Zihlman, A. L.;Sumner, D. R. Jr.; Galloway, A. 1991. Poliomyelitis and skeletal asymmetry in Gombe chimpanzees.Primates, 32: 77–91.

    Article  Google Scholar 

  • Murray, J. 1998.Cultural Atlas of Africa (revised ed.). Andromeda, Oxford.

    Google Scholar 

  • Musher, D. M. 1992. Treponemes: microbiology. In:Infectious Diseases,Gorbach,S. L.;Barlett,S. G.;Blacklow,N. R. (eds.), Saunders, Philadelphia, pp. 1596–1599.

    Google Scholar 

  • Nathan, H.;Haas, N. 1966. On the presence of cribra orbitalia in apes and monkeys.Amer. J. Phys. Anthropol., 24: 351–360.

    Article  CAS  Google Scholar 

  • Nerlich, A. G.;Parsche, F.;Von Den Driesch, A.;Löhrs, U. 1993. Osteopathological findings in mummified babbons from ancient Egypt.Int. J. Osteoarchaeol., 3: 189–198.

    Article  Google Scholar 

  • Noordhoek, G. T.;Van Embden, J. D. A. 1991. Yaws, an endemic treponematosis reconsidered in the HIV era,Eur. J. Clin. Micro. Infect. Dis., 10: 4–5.

    Article  CAS  Google Scholar 

  • Ortner, D. J. 1992. Livingstone's “alternative hypothesis.”Paleopathol. News, 79: 5–6.

    Google Scholar 

  • Ortner, D. J.;Putschar, W. G. J. 1981.Identification of Pathological Conditions in Human Skeletal Remains: Contributions to Anthropology 28. Smithsonian Inst., Washington.

    Google Scholar 

  • Perine, P. L.;Hopkins, D. R.;St. John R. K.;Niemel, P. L. A.;Causse G.;Antal, G. M. 1984.Handbook of Endemic Treponematoses: Yaws, Endemic Syphilis and Pinta. World Health Org., Geneva.

    Google Scholar 

  • Powell, M. L. 1988.Status and Health in Prehistory: A Case Study of the Moundville Chiefdom. Smithsonian Inst., Washington.

    Google Scholar 

  • Powell, M. L. 1992. Health and disease in the late prehistoric south-east. In:Disease and Demography in the Americas,Verano,J.;Ubelaker,D. H. (eds.), Smithsonian Inst., Washington, pp. 41–53.

    Google Scholar 

  • Randall, F. E. 1943. The skeletal and dental development and variability of the gorilla (continued).Human Biol., 15: 307–337.

    Google Scholar 

  • Randall, F. E. 1944. The skeletal and dental development and variability of the gorilla (concluded).Human Biol., 16: 23–76.

    Google Scholar 

  • Rankin, J. D.; Mcdiarmid, A. 1968. Mycobacterial infections in free-ranging wild animals. In:Diseases in Free-living Wild Animals,Mcdiarmid, A. (eds.)Symp. Zool. Soc. Lond., 24: 119–131.

  • Reeder, M. M.;Palmer, P. E. S. (eds.). 1981. Yaws and endemic (non venereal) syphilis. In:The Radiology of Tropical Diseases with Epidemiological, Pathological, and Clinical Correlation, Williams & Wilkins, Baltimore, pp. 749–764.

    Google Scholar 

  • Resnick, D.;Niwayama, G. (eds.) 1988. Osteomyelitis, septic arthritis, and soft tissue infection: the organisms. In:Diagnosis of Bone and Joint Disorders, Vol. 4 (2nd ed.), Saunders, Philadelphia, pp. 2647–2754.

    Google Scholar 

  • Rollet, E. 1891. Maladies osseuses des grands singes.C. R. Acad. Sci. (Paris), ser. 1: 1476–1478.

    Google Scholar 

  • Rothschild, B. M. 1989. On the antiquity of treponemal infection.Med. Hypotheses, 28: 181–184.

    Article  PubMed  CAS  Google Scholar 

  • Rothschild, B. M.;Woods, R. J. 1989. Spondyloarthropathy in gorillas.Semin Arthritis Rheum., 18: 267–276.

    Article  PubMed  CAS  Google Scholar 

  • Rothschild, B. M.;Woods, R. J. 1991. Reactive erosive arthritis in chimpanzees.Amer. J. Primatol., 25: 49–56.

    Article  Google Scholar 

  • Roy, A. D.;Cameron, H. M. 1972. Rhinophycomycomycosis entomophthorae occurring in a chimpanzee in the wild in East Africa.Amer. J. Trop. Med., 21: 234–237.

    PubMed  CAS  Google Scholar 

  • Schmidt, R. E. 1978. Systemic pathology of chimpanzees.J. Med. Primatol., 7: 274–318.

    Google Scholar 

  • Schultz, A. 1939. Notes on diseases and healed fractures of wild apes and their bearing on the antiquity of pathological conditions in man.Bull. Hist. Med., 7: 571–582.

    Google Scholar 

  • Schultz, A. 1956. The occurrence and frequency of pathological and teratological conditions and of twinning among non-human primates.Primatologia, 1: 965–1014.

    Google Scholar 

  • Simonds, P. E. 1965. The bonnet macaques in South India., In:Primate Behavior: Field Studies of Monkeys and Apes,DeVore,I. (ed.), Holt, Reinhart & Winston, New York, pp. 175–196.

    Google Scholar 

  • Skinner, M. F. 1986. Enamel hypoplasia in sympatric chimpanzee and gorilla.Human Evol., 1: 289–312.

    Article  Google Scholar 

  • Skinner, M. F. 1999. Treponemal disease in west African nonhuman primates. Paper presented at the annual meeting of the Paleopathology Assoc., Columbus.

  • Smith, G. H.;Grummett, T. L.;Brandt, K. L. 1994. Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories.Yrbk. Phys. Anthropol., 37: 177–231.

    Article  Google Scholar 

  • Stamm, L. V.;Greene, S. R.;Bergen, H. L.;Hardham, J. M.;Barnes, N. Y. 1998. Identification and sequence analysis ofTreponema pallidum tprJ, a member of a polymorphic multigene family.FEMS Microbiol. Lett., 169: 155–163.

    Article  PubMed  CAS  Google Scholar 

  • Steinbock, R. T. 1976.Paleopathological Diagnosis and Interpretation. C. C. Thomas, Springfield.

    Google Scholar 

  • Stoner, K. E. 1995. Dental pathology inPongo satyrus borneensis.Amer. J. Phys. Anthropol., 98: 307–321.

    Article  CAS  Google Scholar 

  • Sumner, D. R.;Morbeck, M. E.;Lobick, J. J. 1989. Apparent age-related bone loss among adult female Gombe chimpanzees.Amer. J. Phys. Anthropol., 79: 225–246.

    Article  CAS  Google Scholar 

  • Vanthournout, I.;Quinet, B.;Neuenschwander, S. 1991. Pediatric yaws osteoperiostitis.Ped. Radiol., 21: 303.

    Article  CAS  Google Scholar 

  • Wallis, W. D. 1934. A gorilla skull with abnormal denture.Amer. Naturalist, 68: 179–183.

    Article  Google Scholar 

  • Watts, E. S. 1986. Skeletal development. In:Comparative Primate Biology, Vol. 3: Reproduction and Development, Dukelow, W. R.; Erwin, J. (eds.) Alan R. Liss, New York, pp. 415–439.

    Google Scholar 

  • Weiss, R. A.;Wrangham, R. W. 1999. FromPan to Pandemic.Nature, 397: 385–386.

    Article  PubMed  CAS  Google Scholar 

  • Whittet, H. B.;Quiney, R. E. 1988J. Laryngol. Otol., 102: 1147–1149.

    PubMed  CAS  Google Scholar 

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Lovell, N.C., Jurmain, R. & Kilgore, L. Skeletal evidence of probable treponemal infection in free-ranging African apes. Primates 41, 275–290 (2000). https://doi.org/10.1007/BF02557597

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