Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 4, Number 2—June 1998
Perspective

Wild Primate Populations in Emerging Infectious Disease Research: The Missing Link?

Nathan D. Wolfe*, Ananias A. Escalante†, William B. Karesh‡, Annelisa Kilbourn‡, Andrew Spielman*, and Altaf A. Lal†
Author affiliations: *Harvard School of Public Health, Boston, Massachusetts, USA; †Centers for Disease Control and Prevention, U.S. Public Health Service, Chamblee, Georgia, USA; ‡Wildlife Health Sciences, Wildlife Conservation Society, Bronx, New York, USA.

Main Article

Figure 2

Relationships between primate and human parasites: Malaria phylogeny based on the circumsporozoite protein gene. The alignment does not include the central repeat region. P. falciparum (Pfa), P. vivax (Pvi), and P. malariae (Pma) are from humans; P. cynomolgi (Pcy), P. simiovale (Pso), and P. knowlesi (Pkn) are from macaques; P. simium (Psi) and P. brasilianum (Pbr) are from New World monkeys; P. reichenowi (Pre) is from chimpanzees; P. gallinacium (Pga) is from birds; and P. berghei (Pbe) and P

Figure 2. Relationships between primate and human parasites: Malaria phylogeny based on the circumsporozoite protein gene. The alignment does not include the central repeat region. P. falciparum (Pfa), P. vivax (Pvi), and P. malariae (Pma) are from humans; P. cynomolgi (Pcy), P. simiovale (Pso), and P. knowlesi (Pkn) are from macaques; P. simium (Psi) and P. brasilianum (Pbr) are from New World monkeys; P. reichenowi (Pre) is from chimpanzees; P. gallinacium (Pga) is from birds; and P. berghei (Pbe) and P. yoelii (Pyo) are from rodents. The numbers in the names indicate different isolates as described in (30). The sequence of P. gallinacium was reported by (31). The numbers on the branches are bootstrap % based on 500 pseudoreplications. The tree was estimated by the neighbor-joining method with the Tajima and Nei distance (32).

Main Article

References
  1. Ruch  TC. Diseases of laboratory primates. Philadelphia: W.B. Saunders Company; 1959.
  2. Brack  M. Agents transmissible from simians to man. Berlin: Springer-Verlag; 1987.
  3. Morse  SS. Emerging viruses. In: Morse SS, editor. Emerging viruses. New York: Oxford University Press, Inc.; 1993.
  4. Levins  R, Awerbuch  T, Brinkmann  U, Eckardt  I, Epstein  P, Makhoul  N, The emergence of new diseases. Am Sci. 1994;82:52–60.
  5. Wilson  ME, Levins  R, Spielman  A. Disease in evolution: global changes and emergence of infectious diseases. Ann N Y Acad Sci. 1994;:740.
  6. Mutombo  M, Arita  I, Jezek  Z. Human monkeypox transmitted by a chimpanzee in a tropical rain-forest area of Zaire. Lancet. 1983;34:735–7. DOIGoogle Scholar
  7. Eidson  M, Tierney  LA, Rollag  OJ, Becker  T, Brown  T, Hull  HF. Feline plague in New Mexico: risk factors and transmission to humans. Am J Public Health. 1988;78:1333–5. DOIPubMedGoogle Scholar
  8. Douglas  JD, Soike  KF, Raynor  J. The incidence of poliovirus in chimpanzees (Pan troglodytes). Lab Anim Care. 1970;20:265–8.PubMedGoogle Scholar
  9. Morell  V. Chimpanzee outbreak heats up search for Ebola origin. Science. 1995;268:974–5. DOIPubMedGoogle Scholar
  10. Meyers  WM, Gormus  BJ, Walsh  GP, Baskin  B, Hubbard  GB. Naturally acquired and experimental leprosy in nonhuman primates. Am J Trop Med Hyg. 1991;44:24–7.PubMedGoogle Scholar
  11. McCallum  H, Dobson  A. Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol. 1995;10:190–4. DOIGoogle Scholar
  12. Coatney  GR, Collins  WE, Warren  M, Contacos  PG. The primate malarias. Bethesda: U.S. Department of Health, Education, and Welfare; 1971.
  13. Beverley-Burton  M, Crichton  VF. Attempted experimental cross infections with mammalian guinea-worms, Drancunculus spp. (Nematoda: Dracunculoidea). Am J Trop Med Hyg. 1976;25:704–8.PubMedGoogle Scholar
  14. Fuller  GK, Lemma  A, Haile  T. Schistosomiasis in Omo National Park of Southwest Ethiopia. Am J Trop Med Hyg. 1979;28:526–30.PubMedGoogle Scholar
  15. Shah  KV. A review of the circumstances and consequences of simian virus SV40 contamination of human vaccines. Symposium on Continuous Cell Lines as Substrates for Biologicals. Developments in biological standardization, Vol. 70; 1989.
  16. Khabbaz  RF, Heneine  W, George  JR, Parekh  B, Rowe  T, Woods  T, Brief report: infection of a laboratory worker with simian immunodeficiency virus. N Engl J Med. 1994;330:172–7. DOIPubMedGoogle Scholar
  17. Michler  RE. Xenotransplantation: risks, clinical potential, and future prospects. Emerg Infect Dis. 1996;2:64–70. DOIPubMedGoogle Scholar
  18. Berkelman  RL, Pinner  RW, Hughes  JM. Addressing emerging microbial threats in the United States. JAMA. 1996;275:315–7. DOIPubMedGoogle Scholar
  19. Lederberg  J, Shope  RE, Oaks  SC. Emerging infections: microbial threats to health in the United States. Washington: National Academy Press; 1992.
  20. LeDuc  JW. World Health Organization strategy for emerging infectious diseases. JAMA. 1996;275:318–20. DOIPubMedGoogle Scholar
  21. Meslin  FX. Surveillance and control of emerging zoonoses. World Health Stat Q. 1992;45:200–7.PubMedGoogle Scholar
  22. Holmes  ED, Nee  S, Rambaut  A, Garnett  GP, Harvey  PH. Revealing the history of infectious disease epidemics through phylogenetic trees. Philos Trans R Soc Lond B Biol Sci. 1995;349:33–40. DOIPubMedGoogle Scholar
  23. Kalter  SS, Heberling  RL, Cooke  AW, Barry  JD, Tian  PY, Northam  WJ. Viral infections of non-human primates. Lab Anim Sci. 1997;47:461–7.PubMedGoogle Scholar
  24. Myers  G, MacInnes  K, Korber  B. The emergence of simian/human immunodeficiency viruses. AIDS Res Hum Retroviruses. 1992;8:373–86. DOIPubMedGoogle Scholar
  25. Peeters  M, Fransen  K, Delaporte  E, Van Den Haesevelde  M, Gershy-Damet  GM, Kestens  L, Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. AIDS. 1992;6:447–51.PubMedGoogle Scholar
  26. Huet  TR, Cheynier  A, Meyerhans  A, Roelants  G, Wain-Hobson  S. Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature. 1990;345:356–459. DOIPubMedGoogle Scholar
  27. Mindell  DP. Positive selection and rates of evolution in immunodeficiency viruses from humans and chimpanzees. Proc Natl Acad Sci U S A. 1996;93:3284–8. DOIPubMedGoogle Scholar
  28. Liu  HF, Goubau  P, Van Brussel  M, Van Laethem  K, Chen  YC, Desmyter  J, The three human T-lymphotropic virus type I subtypes arose from three geographically distinct simian reservoirs. J Gen Virol. 1996;77:359–68. DOIPubMedGoogle Scholar
  29. Collins  WE. Major animal models in malaria research: simian. In: Wernsdorfer WH, editor. Malaria: principles and practice of malariology. Edinburgh: Churchill Livingstone; 1988.
  30. Escalante  AA, Barrio  E, Ayala  FJ. Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Mol Biol Evol. 1995;12:616–26.PubMedGoogle Scholar
  31. McCutchan  TF, Kissinger  JC, Touray  MG, Rogers  MJ, Li  J, Sullivan  M, Comparison of circumsporozoite proteins from avian and mammalian malaria: biological and phylogenetic implications. Proc Natl Acad Sci U S A. 1996;93:11889–94. DOIPubMedGoogle Scholar
  32. Tajima  F, Nei  M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984;1:269–85.PubMedGoogle Scholar
  33. Qari  SH, Shi  YP, Pieniazek  NJ, Collins  WE, Lal  AA. Phylogenetic relationship among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum. Mol Phylogenet Evol. 1996;6:157–65. DOIPubMedGoogle Scholar
  34. Waters  AP, Higgins  DG, McCutchan  TF. Evolutionary relatedness of some primate models of Plasmodium. Mol Biol Evol. 1993;10:914–23.PubMedGoogle Scholar
  35. Escalante  AA, Ayala  FJ. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci U S A. 1994;91:11373–7. DOIPubMedGoogle Scholar
  36. Qari  SH, Shi  YP, Povoa  MM, Alpers  MP, Deloron  P, Murphy  GS, Global occurrence of Plasmodium vivax-like human malaria parasite. J Infect Dis. 1993;168:1485–9.PubMedGoogle Scholar
  37. Desrosiers  RC. HIV-1 origins: a finger on the missing link. Nature. 1990;345:288–9. DOIPubMedGoogle Scholar
  38. Peeters  M, Janssens  W, Fransen  K, Brandful  J, Heyndrickx  L, Koffi  K, Isolation of simian immunodeficiency viruses from two sooty mangabeys in Côte d'Ivoire: virological and genetic characterization and relationship to other HIV type 2 and SIVsm/mac strains. AIDS Res Hum Retroviruses. 1994;10:1289–94. DOIPubMedGoogle Scholar
  39. Brooks  DR, McLennan  DA. Parascript: parasites and the language of evolution. Washington: Smithsonian Institution Press; 1993.
  40. Gouteux  JP, Noireau  F. The host preferences of Chrysops silacea and C. dimidiata. Diptera: Tabanidae in an endemic area of Loa loa in the Congo. Ann Trop Med Parasitol. 1989;83:167–72.PubMedGoogle Scholar
  41. Peters  W, Garnham  PCC, Rajapaksa  N, Cheong  WH, Cadigan  FC. Malaria of the Orangutan in Borneo. Philos Trans R Soc Lond B Biol Sci. 1976;275:439–82. DOIPubMedGoogle Scholar
  42. Suleman  MA, Johnson  BJ, Tarara  R, Sayer  PD, Ochieng  DM, Muli  JM, An outbreak of poliomyelitis caused by poliovirus type I in captive black and white colobus monkeys (Colobus abyssinicus kikuyuensis) in Kenya. Trans R Soc Trop Med Hyg. 1984;78:665–9. DOIPubMedGoogle Scholar
  43. Goodall  J. Population dynamics during a 15 year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania. Z Tierpsychol. 1983;61:1–60.
  44. Mak  JW, Cheong  WH, Yen  PK, Lim  PK, Chan  WC. Studies on the epidemiology of subperiodic Brugia malayi in Malaysia: problems in its control. Acta Trop. 1982;39:237–45.PubMedGoogle Scholar
  45. Rolland  RM, Hausfater  G, Marshall  B, Levy  SB. Antibiotic-resistant bacteria in wild primates: increased prevalence in baboons feeding on human refuse. Appl Environ Microbiol. 1985;49:791–4.PubMedGoogle Scholar
  46. Turner  IM. Species loss in fragments of tropical rain forest: a review of the evidence. J Appl Ecol. 1996;33:200–9. DOIGoogle Scholar
  47. Wilson  ME. Travel and the emergence of infectious diseases. Emerg Infect Dis. 1995;1:39–46. DOIPubMedGoogle Scholar
  48. Grenfell  BT, Dobson  AP, eds. Ecology of infectious diseases in natural populations. Cambridge: Cambridge University Press; 1995.
  49. Fleagle  JG, Reed  KE. Comparing primate communities: a multivariate approach. J Hum Evol. 1996;30:489–510. DOIGoogle Scholar
  50. Davies  CR, Ayres  JM, Dye  C, Deane  LM. Malaria infection rate of Amazonian primates increases with body weight and group size. Funct Ecol. 1991;5:655–62. DOIGoogle Scholar
  51. Freeland  WJ. Pathogens and the evolution of primate sociality. Biotropica. 1976;8:12–24. DOIGoogle Scholar
  52. Loehle  C. Social barriers to pathogen transmission in wild animal populations. Ecology. 1995;76:326–35. DOIGoogle Scholar
  53. Le Guenno  B, Formentry  P, Wyers  M, Gounon  P, Walker  F, Boesch  C. Isolation and partial characterization of a new strain of Ebola virus. Lancet. 1995;345:1271–444. DOIPubMedGoogle Scholar
  54. World Health Organization. Outbreak of Ebola haemorrhagic fever in Gabon officially declared over. Wkly Epidemiol Rec. 1996;71:125–6.
  55. Jezek  Z, Arita  I, Mutombo  M, Dunn  C, Nakano  JH, Szczeniowski  M. Four generations of probable person-to-person transmission of human monkeypox. Am J Epidemiol. 1986;123:1004–12.PubMedGoogle Scholar
  56. Fenner  SS. Human monkeypox, a newly discovered human virus disease. In: Morse SS, editor. Emerging viruses. New York: Oxford University Press, Inc.; 1993. p. 176-183.
  57. Palmer  AE. Herpesvirus simiae: historical perspective. J Med Primatol. 1987;16:99–130.PubMedGoogle Scholar
  58. Schrag  SJ, Wiener  P. Emerging infectious disease: what are the relative roles of ecology and evolution? Trends Ecol Evol. 1995;10:319–24. DOIGoogle Scholar
  59. Karesh  WB, Cook  RA. Applications of veterinary medicine to in situ conservation efforts. Oryx. 1995;29:244–52. DOIGoogle Scholar
  60. Hafner  MS, Page  RDM. Molecular phylogenies and host-parasite cospeciation: gophers and lice as a model system. Philos Trans R Soc Lond B Biol Sci. 1995;349:77–83. DOIPubMedGoogle Scholar
  61. Freeland  WJ. Primate social groups as biological islands. Ecology. 1979;60:719–28. DOIGoogle Scholar
  62. Jin  MJ, Rogers  J, Phillips-Conroy  JE, Allan  JS, Desrosiers  RC, Shaw  GM, Infection of a yellow baboon with simian immunodeficiency virus from African green monkeys: evidence for cross-species transmission in the wild. J Virol. 1994;68:8454–60.PubMedGoogle Scholar
  63. Jolly  CJ, Phillips-Conroy  JE, Turner  TR, Broussard  S, Allan  JS. SIV-agm incidence over two decades in a natural population of Ethiopian grivet monkeys (Cercopithecus aethiops aethiops). J Med Primatol. 1996;25:78–83.PubMedGoogle Scholar
  64. Rodriguez del Valle  M, Quakyi  IA, Amuesi  J, Quaye  JT, Nkrumah  FK, Taylor  DW. Detection of antigens and antibodies in the urine of humans with Plasmodium falciparum malaria. J Clin Microbiol. 1991;29:1236–42.PubMedGoogle Scholar
  65. Karesh  WB, Smith  F, Frazier-Taylor  H. A remote method for obtaining skin biopsy samples. Conserv Biol. 1987;1:261–2. DOIGoogle Scholar
  66. Centers for Disease Control and Prevention. Tuberculosis in imported nonhuman primatesUnited States, June 1990-May 1993. MMWR Morb Mortal Wkly Rep. 1993;42:572–6.PubMedGoogle Scholar
  67. Tarara  R, Suleman  MA, Sapolsky  R, Wabomba  MJ, Else  JG. Tuberculosis in wild olive baboons, Papio cynocephalus anubis (Lesson), in Kenya. J Wildl Dis. 1985;21:137–40.PubMedGoogle Scholar
  68. Clayton  DH, Wolfe  ND. The adaptive significance of self-medication. Trends Ecol Evol. 1995;8:60–3. DOIGoogle Scholar
  69. Robles  M, Aregullin  M, West  J, Rodriguez  E. Recent studies on the zoopharmacognosy, pharmacology and neurotoxicology of sesquiterpene lactones. Planta Med. 1995;61:199–203. DOIPubMedGoogle Scholar
  70. Hill  AV, Yates  SN, Allsopp  CE, Gupta  S, Gilbert  SC, Lalvani  A, Human leukocyte antigens and natural selection by malaria. Philos Trans R Soc Lond B Biol Sci. 1994;346:379–85. DOIPubMedGoogle Scholar
  71. Skolnick  AA. Newfound genetic defect hints at clues for developing novel antimalarial agents. JAMA. 1993;269:1765. DOIPubMedGoogle Scholar
  72. Stephenson  J. Findings on host resistance genes for infectious diseases are pointing the way to drugs, vaccines. JAMA. 1996;275:1464–5. DOIPubMedGoogle Scholar

Main Article

Page created: December 14, 2010
Page updated: December 14, 2010
Page reviewed: December 14, 2010
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.
file_external