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

Primates

Volumn 41, Issue 3, 2000, Pages 275-290

  Lovell, Nancy C ^a   Jurmain, Robert ^b   Kilgore, Lynn ^c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b SAN JOSE STATE UNIVERSITY   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Chimpanzee; Gorilla; Paleopathology; Yaws

Indexed keywords

EID: 0012698963     PISSN: 00328332     EISSN: 16107365     Source Type: Journal    
DOI: 10.1007/BF02557597     Document Type: Article

References (79)

1. 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.
2. 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. DOI: 10.1002/(SICI)1096-8644(199601)99:1<119::AID-AJPA7>3.0.CO;2-W
3. 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. DOI: 10.1002/ajpa.1330860211
4. Aufderheide, A. C.;Rodriguez-Martin, C. 1998.The Cambridge Encyclopedia of Human Paleopathology, Cambridge Univ. Press, Cambridge.
5. Baker, B. J.;Armelagos, G. J. 1988. The origin and antiquity of syphilis.Cur. Anthropol., 29: 703–737. DOI: 10.1086/203691
6. 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.
7. Bramblett, C. 1967. Pathology in the Darajani baboon.Amer. J. Phys. Anthropol., 21: 331–340. DOI: 10.1002/ajpa.1330260308
8. Buikstra, J. E. 1975. Healed fractures inMacaca mulatta: age, sex, and symmetry.Folia Primatol., 23: 140–148.
9. 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.
10. Cockburn, A. 1963. The treponematoses. In:The Evolution and Eradication of Infectious Disease,Cockburn,A. (ed.) Johns Hopkins, Baltimore, pp. 152–174.
11. Cockburn, A. (ed.). 1967. The evolution of human infectious diseases. In:Infectious Diseases: Their Evolution and Eradication, CC Thomas, Springfield, pp. 84–107.
12. Cousins, D. 1972. Diseases and injuries in wild and captive gorillas.Int. Zoo Yrbk., 12: 211–218.
13. 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. DOI: 10.1016/0047-2484(92)90027-7
14. Degusta, D.;Milton, K. 1998. Skeletal pathologies in a population ofAloutta palliata: behavioral, ecological, and evolutionary implications.Int. J. Primatol., 19: 615–650. DOI: 10.1023/A:1020372825031
15. Derousseau, C. J. 1988.Osteoarthritis in Rhesus Monkeys and Gibbons: A Locomotor Model of Joint Degeneration, Vol. 25: Contributions to Primatology. Karger, Basel.
16. 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.
17. 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.
18. Donham, K. J.;Leininger, J. R. 1977. Spontaneous leprosy-like lesions in a chimpanzee.,J. Infect. Dis., 136: 132–136.
19. 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.
20. 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.
21. Fiennes, R. N. T.-W. 1967.Zoonoses of Primates. Cornell, Ithaca.
22. Fossey, D. 1983.Gorillas in the Mist. Houghton Mifflin, Boston.
23. Fribourg-Blanc, A. 1972. Treponema. In:Pathology of Simian Primates, Vol. 2,Fiennes,R. N. T.-W. (ed.), Karger, Basel, pp. 255–262.
24. 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. DOI: 10.1038/17130
25. Geddes, H. 1955.Gorilla. Andrew Melrose, London.
26. Goodall, J. 1986.The Chimpanzees of Gombe. Harvard Univ. Press, Cambridge, Massachusetts.
27. 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. DOI: 10.1002/(SICI)1096-8644(199810)107:2<179::AID-AJPA4>3.0.CO;2-Q
28. 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.
29. 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.
30. Holland, W. J. 1924. Account of a skeleton of a gorilla remarkable because showing recovery from gunshot wounds.Ann. Carnegie Mus., 15: 293–298.
31. Hudson, E. H. 1964. Treponematosis and African slavery.Br. J. Vener. Dis., 40: 43–51.
32. Jurmain R. 1989. Trauma, degenerative disease, and other pathologies among the Gombe chimpanzees.Amer. J. Phys. Anthropol., 80: 229–237. DOI: 10.1002/ajpa.1330800211
33. Jurmain, R. 1997. Skeletal evidence of trauma in African apes, with special reference to the Gombe chimpanzees.Primates, 38: 1–14. DOI: 10.1007/BF02385918
34. 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.
35. Kerley, E. R. 1966. Skeletal age changes in the chimpanzee.Tulane Studies Zool., 13: 71–82.
36. Kilgore, L. 1989. Dental pathologies in ten free-ranging chimpanzees from Gombe National Park, Tanzania.Amer. J. Phys. Anthropol., 80: 219–227. DOI: 10.1002/ajpa.1330800210
37. Koff, A. B.;Rosen, T. 1993. Nonvenereal treponematoses: yaws, endemic syphilis, and pinta.J. Amer. Acad. Dermatol., 29: 519–535. DOI: 10.1016/0190-9622(93)70217-H
38. 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.
39. Lovell, N. C. 1990a.Illness and Injury in Great Apes: A Skeletal Analysis. Smithsonian Inst, Washington.
40. Lovell, N. C. 1990b. Skeletal and dental pathology of free-ranging mountain gorillas.Amer. J. Phys. Anthropol., 81: 399–412. DOI: 10.1002/ajpa.1330810309
41. Lovell, N. C. 1991. An evolutionary framework for assessing illness and injury in nonhuman primates.Yrbk. Phys. Anthropol., 34: 117–155. DOI: 10.1002/ajpa.1330340608
42. 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.
43. Morbeck, M. E.;Zihlman, A. L.;Sumner, D. R. Jr.; Galloway, A. 1991. Poliomyelitis and skeletal asymmetry in Gombe chimpanzees.Primates, 32: 77–91. DOI: 10.1007/BF02381602
44. Murray, J. 1998.Cultural Atlas of Africa (revised ed.). Andromeda, Oxford.
45. Musher, D. M. 1992. Treponemes: microbiology. In:Infectious Diseases,Gorbach,S. L.;Barlett,S. G.;Blacklow,N. R. (eds.), Saunders, Philadelphia, pp. 1596–1599.
46. Nathan, H.;Haas, N. 1966. On the presence of cribra orbitalia in apes and monkeys.Amer. J. Phys. Anthropol., 24: 351–360. DOI: 10.1002/ajpa.1330240307
47. 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. DOI: 10.1002/oa.1390030305
48. 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. DOI: 10.1007/BF01967089
49. Ortner, D. J. 1992. Livingstone's “alternative hypothesis.”Paleopathol. News, 79: 5–6.
50. Ortner, D. J.;Putschar, W. G. J. 1981.Identification of Pathological Conditions in Human Skeletal Remains: Contributions to Anthropology 28. Smithsonian Inst., Washington.
51. 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.
52. Powell, M. L. 1988.Status and Health in Prehistory: A Case Study of the Moundville Chiefdom. Smithsonian Inst., Washington.
53. 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.
54. Randall, F. E. 1943. The skeletal and dental development and variability of the gorilla (continued).Human Biol., 15: 307–337.
55. Randall, F. E. 1944. The skeletal and dental development and variability of the gorilla (concluded).Human Biol., 16: 23–76.
56. 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.
57. 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.
58. 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.
59. Rollet, E. 1891. Maladies osseuses des grands singes.C. R. Acad. Sci. (Paris), ser. 1: 1476–1478.
60. Rothschild, B. M. 1989. On the antiquity of treponemal infection.Med. Hypotheses, 28: 181–184. DOI: 10.1016/0306-9877(89)90049-2
61. Rothschild, B. M.;Woods, R. J. 1989. Spondyloarthropathy in gorillas.Semin Arthritis Rheum., 18: 267–276. DOI: 10.1016/0049-0172(89)90048-6
62. Rothschild, B. M.;Woods, R. J. 1991. Reactive erosive arthritis in chimpanzees.Amer. J. Primatol., 25: 49–56. DOI: 10.1002/ajp.1350250105
63. 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.
64. Schmidt, R. E. 1978. Systemic pathology of chimpanzees.J. Med. Primatol., 7: 274–318.
65. 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.
66. Schultz, A. 1956. The occurrence and frequency of pathological and teratological conditions and of twinning among non-human primates.Primatologia, 1: 965–1014.
67. 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.
68. Skinner, M. F. 1986. Enamel hypoplasia in sympatric chimpanzee and gorilla.Human Evol., 1: 289–312. DOI: 10.1007/BF02436704
69. Skinner, M. F. 1999. Treponemal disease in west African nonhuman primates. Paper presented at the annual meeting of the Paleopathology Assoc., Columbus.
70. 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. DOI: 10.1002/ajpa.1330370608
71. 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. DOI: 10.1111/j.1574-6968.1998.tb13312.x
72. Steinbock, R. T. 1976.Paleopathological Diagnosis and Interpretation. C. C. Thomas, Springfield.
73. Stoner, K. E. 1995. Dental pathology inPongo satyrus borneensis.Amer. J. Phys. Anthropol., 98: 307–321. DOI: 10.1002/ajpa.1330980305
74. 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. DOI: 10.1002/ajpa.1330790210
75. Vanthournout, I.;Quinet, B.;Neuenschwander, S. 1991. Pediatric yaws osteoperiostitis.Ped. Radiol., 21: 303. DOI: 10.1007/BF02018632
76. Wallis, W. D. 1934. A gorilla skull with abnormal denture.Amer. Naturalist, 68: 179–183. DOI: 10.1086/280536
77. 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.
78. Weiss, R. A.;Wrangham, R. W. 1999. FromPan to Pandemic.Nature, 397: 385–386. DOI: 10.1038/17008
79. Whittet, H. B.;Quiney, R. E. 1988J. Laryngol. Otol., 102: 1147–1149.