The role of helminthes in human evolution implications for global health in the 21st century

Medicine and Evolution: Current Applications, Future Prospects

Volumn , Issue , 2008, Pages 153-180

  Hurtado, A Magdalena ^a   Frey, M Anderson ^b   Hurtado, Inés ^a   Hill, Kim ^a   Baker, Jack ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85019425556     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (107)

1. Grove, D. 1990. A history of human helminthology. Wallingford, UK: CAB International.
2. University of Cambridge, Department of Pathology. 2007. Helminth infections of man. http://www.path.cam.ac.uk/schisto/General_Parasitology/Hm.helminths.html. Accessed 18 Feb 2008.
3. Minchella, D. J. 1985. Host life history variation in response to parasitism. Parasitology 90:205-16.
4. Poulin, R., Morand, S., and Skorping, A. 2000. Evolutionary biology of host-parasite relationships: Theory meets reality. New York: Elsevier.
5. Barrett, R., Kuzawa, C., McDade, T., and Armelagos, G. J. 1998. Emerging and re-emerging infectious diseases: The third epidemiologic transition. Ann. Rev. Anthropol. 27:247-71.
6. Hill, K., Hurtado, A. M., and Walker, R. S. 2007. High adult mortality among Hiwi hunter-gatherers: Implications for human evolution. J. Hum. Evol. 52:443-54.
7. Hill, K., and Hurtado, A. M. 1996. Ache life history: The ecology and demography of a foraging people. New York: Aldine Press.
8. http://www.pubmed.org.
9. Hurtado, A. M., Lambourne, C. A., James, P., Hill, K., Cheman, K., and Baca, K. 2005. Human rights, biomedical science, and infectious diseases among South American indigenous groups. Annu. Rev. Anthropol. 34:639-65.
10. Centers for Disease Control and Prevention. 2007. Parasites of the intestinal tract. Atlanta, GA: Infectious Disease Department. http://www.dpd.cdc.gov/DPDx/HTML/Para_Health.htm. Accessed 18 Feb 2008.
11. Goncalves, M. L., Araujo, A., and Ferreira, L. F. 2003. Human intestinal parasites in the past: New findings and a review. Mem. Inst. Oswaldo Cruz 98:103-18.
12. Hoberg, E. P., Alkire, N. L., de Queiroz, A., and Jones, A. 2001. Out of Africa: Origins of the Taenia tapeworm in humans. Proc. R. Soc. B 268:781-87.
13. Hotez, P. J., Brooker, S., Bethony, J. M., Bottazzi, M. E., Loukas, A., and Xiao, S. 2004. Hookworm infection. N. Engl. J. Med. 351:799-807.
14. Matthews, B. E. 2005. An introduction to parasitology. Cambridge: Cambridge University Press.
15. Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D., and Hotez, P. J. 2006. Soil-transmitted helminth infections: Ascariasis, trichuriasis, and hookworm. Lancet 367:1521-32.
16. Murray, S., Stem, C., Boudreau, B., and Goodall, J. 2000. Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park. J. Zool. Wild Med. 31:176-78.
17. Michaud, C., Tantalean, M., Ique, C., Montoya, E., and Gozalo, A. 2003. A survey for helminth parasites in feral New World non-human primate populations and its comparison with parasitological data from man in the region. J. Med. Primatol. 32:341-45.
18. Gillespie, T. R., Chapman, C. A., and Greiner, E. C. 2005. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J. Appl. Ecol. 42:699-707.
19. Bouchet, F., Baffier, D., Girard, M., Morel, P. H., Paicheler, J. C., and David, F. 1996. Paleoparasitology in a Pleistocene context: Initial observations in the Grande Grotte at Arcy-sur-Cure. C.R. Acad. Sci. Ser. 319:147-51.
20. Evans, A. C., Markus, M. B., Mason, R. J., and Steel, R. 1996. Late stone-age coprolite reveals evidence of prehistoric parasitism. SAMJ 86:846-49.
21. Ferreira, L. F., Araujo, A., Confalonieri, U., Chame, M., and Ribeiro Filho, B. 1987. The finding of hookworm eggs in human coprolites from 7230 ± 80 years BP, from Piaui, Brazil. An. Acad. Bras. Cienc. 59:280-81.
22. Fry, G. F., and Hall, H. J. 1969. Parasitological examination of prehistoric human coprolites from Utah. Proc. Utah Acad. Sci. Art. Lett. 46 (Part 2):102-5.
23. Hall, H. J. 1976. Untitled notes. Paleopathol. News 13:9.
24. Dommelier-Espejo, S. 2001. Contribution a l’etude paleoparasitologique des sites Neolithiques en environnement lacustre dans les domaines Jurassien et Peri-alpin. Thesis, Universite de Reims.
25. Roever-Bonnet, H., Rijpstra, C., van Renesse, M. A., and Peen, C. H. 1979. Helminth eggs and gregarines from coprolites from the excavations at Swifterbant. Helinium 19:7-12.
26. Aspock, H., Auer, H., and Picher, O. 1996. Trichuris trichiura eggs in the neolithic glacier mummy from the Alps. Parasitol. Today 12:255-56.
27. Ferreira, L. F., Araujo, A., and Confalonieri, U. 1982. Untitled note. Paleopathol. News 38:5.
28. Jones, A. K., and Nicholson, C. 1988. Recent finds of Trichuris and Ascaris ova from Britain. Paleopathol. News 62:5-6.
29. Patrucco, R., Tello, R., and Bonavia, D. 1983. Parasitological studies of coprolites of pre-Hispanic Peruvian populations. Curr. Anthropol. 24:393-94.
30. Iniguez, A. M., Reinhard, K., Goncalves, M. L., Ferreira, L. F., Araujo, A., and Vicente, A. C. 2006. SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites. Int. J. Parasitol. 36:1419-25.
31. Udonsi, J. K., and Ogan, V. N. 1993. Assesment of the effectiveness of primary health care interventions in the control of three intestinal nematode infections in rural communities. Pub. Health 107:53-60.
32. Ferreira, C. S., Ferreira, M. U., and Nogueira, M. R. 1994. The prevalence of infection by intestinal parasites in an urban slum in Sao Paulo, Brazil. J. Trop. Med. Hyg. 97:121-27.
33. Kobayashi, J., Hasegawa, H., Forli, A. A., Nishimura, N. F., Yamanaka, A., Shimabukuro, T., and Sato, Y. 1995. Prevalence of intestinal parasitic infection in five farms in Holambra, Sao Paulo, Brazil. Rev. Inst. Med. Trop. Sao Paulo 37:13-18.
34. Hopkins, R. M., Gracey, M. S., Hobbs, R. P., Spargo, R. M., Yates, M., and Thompson, R. C. 1997. The prevalence of hookworm infection, iron deficiency and anaemia in an aboriginal community in north-west Australia. Med. J. Aust. 166:241-44.
35. Stoltzfus, R. L., Chwaya, H. M., Tielsch, J. M., Schilze, K. J., Albonico, M., and Savioli, L. 1997. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: The importance of hookworms. Am. J. Clin. Nutr. 65:153-59.
36. Labiano-Abello, N., Canese, J., Velazquez, M. E., Hawdow, J. M., Wilson, M. L., and Hotez, P. J. 1999. Epidemiology of hookworm infection in Itagua, Paraguay: A cross sectional study. Mem. Inst. Oswaldo Cruz 94:583-86.
37. Chacin-Bonilla, L., and Sanchez-Chavez, Y. 2000. Intestinal parasitic infections, with a special emphasis on cryptosporidiosis, in Amerindians from western Venezuela. Am. J. Trop. Med. Hyg. 62:347-52.
38. Scolari, C., Torti, C., Beltrame, A., Matteelli, A., Castelli, F., Gulletta, M., Ribas, M., Morana, S., and Urbani, C. 2000. Prevalence and distribution of soil-transmitted helminth (STH) infections in urban and indigenous schoolchildren in Ortigueira, state of Parana, Brasil: Implications for control. Trop. Med. Int. Health 5:302-7.
39. Andrade, C., Alava, T., Palacio, I. A., Poggio, P. D., Jamoletti, C., Gulletta, M., and Montresor, A. 2001. Prevalence and intensity of soil-transmitted helminthiasis in the city of Portoviejo (Ecuador). Mem. Inst. Oswaldo Cruz 96:1075-79.
40. Flores, A., Esteban, J. G., Angles, R., and Mas-Coma, S. 2001. Soil-transmitted helminth infections at a very high altitude in Bolivia. Trans. R. Soc. Trop. Med. Hyg. 95:272-77.
41. Carme, B., Motard, A., Bau, P., Day, C., Aznar, C., and Moreau, B. 2002. Intestinal parasitoses among Wayampi Indians from French Guiana. Parasite 9:167-74.
42. Taranto, N. J., Cajal, S. P., De Marzi, M. C., Fernandez, M. M., Frank, F. M., Bru, A. M., Minvielle, M. C., Basualdo, J. A., and Malchiodi, E. L. 2003. Clinical status and parasitic infection in a Wichi Aboriginal community in Salta, Argentina. Trans. R. Soc. Trop. Med. Hyg. 97:554-58.
43. De Quadros, R. M., Marques, S., Arruda, A. A., Delfes, P. S., and Medeiros, I. A. 2004. Intestinal parasites in nursery schools of Lages, southern Brazil. Rev. Soc. Bras. Med. Trop. 37(5).
44. Araujo, C. F., and Fernandez, C. L. 2005. Prevalence of intestinal parasitosis in the city of Eirunepe, Amazon. Rev. Soc. Bras. Med. Trop. 38(1).
45. Tanner, S. N. 2005. A population in transition: Health, cultural change, and intestinal parasitism among the Tsimane’ of lowland Bolivia. Unpublished dissertation, University of Michigan.
46. Fleming, F. M., Brooker, S., Geiger, S. M., Calda, I. R., Correa-Oliveira, R., Hotez, P. J., and Bethony, J. M. 2006. Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Top. Med. Int. Health 11:56-64.
47. Ferrari, J. O., Ferreira, M. U., Camargo, L. M. A., and Ferreira, C. S. 1992. Intestinal parasites among Karitiana Indians from Rondonia State, Brazil. Rev. Inst. Med. Trop. Sao Paulo 34:223-25.
48. Ferreira, M. R., Souza, W., Perez, E. P., Lapa, T., Carvalho, A. B., Furtado, A., Coutinho, H. B., and Wakelin, D. 1998. Intestinal helminthiasis and anemia in youngsters from Matriz da Luz, district of Sao Lourenco da Mata, state of Pernambuco, Brazil. Mem. Inst. Oswaldo Cruz 93:289-93.
49. Anderson, R. M., and May, R. M. 1991. Infectious diseases of humans: Dynamics and control. Oxford: Oxford University Press.
50. Hagan, P., Blumenthal, U. J., Dunn, D., Simpson, A. J., and Wilkins, H. A. 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349:243.
51. Rihet, P., Demeure, C. E., Bourgois, A., Prata, A., and Dessein, A. J. 1991. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur. J. Immunol. 21:2679.
52. Dunne, D. W., Butterworth, A. E., Fulford, A. J., Kariuki, H. C., Langley, J. G., Ouma, J. H., Capron, A., Pierce, R. J., and Sturrock, R. F. 1992. Immunity after treatment of human schistosomiasis: Association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur. J. Immunol. 22:1483.
53. Ackerman, S. J. 1993. Characterization and function of eosinophil granule proteins. In Eosinophils: Biological and clinical aspects, ed. S. Mkino and T. Fukuda, 33-71. Boca Raton, FL: CRC Press.
54. Hurtado, A. M., Hurtado, I., and Hill, K. 2004. Public health and adaptive immunity among natives of South America. In Lost paradises and the ethics of research and publication, ed. F. M. Salzano and A. M. Hurtado, 164-90. New York: Oxford University Press.
55. McDade, T. W. 2005. The ecologies of human immune function. Annu. Rev. Anthropol. 34:495-521.
56. Lisse, I. M., Aaby, P., Whittle, H., Jensen, H., Engelmann, M., and Christensen, L. B. 1997. T-lymphocyte subsets in West African children: Impact of age, sex, season. J. Pediatr. 130:77-85.
57. Witt, C. S., and Alpers, M. P. 1991. Lymphocyte subsets in Eastern Highlanders of Papua New Guinea. PNG Med. J. 34:98-103.
58. Muehlenbein, M. P., Bribiescas, R. G. 2005. Testosterone-mediated immune functions and male life histories. Am. J. Hum. Biol. 17:527-558.
59. Long, C. L. 1977. Energy balance and carbohydrate metabolism in infection and sepsis. Am. J. Clin. Nutr. 30:1301-10.
60. Moret, Y., and Schmid-Hempel, P. 2000. Survival for immunity: The price of immune system activation for bumblebee workers. Science 290:1166-68.
61. Lee, K. P., Cory, J. S., Wilson, K., Raubenheimer, D., and Simpson, S. J. 2006. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. B 273:823-29.
62. DiPiro, J. T., Hamilton, R. G., Howdieshell, T. R., Adkinson, N. F., and Mansberg, A. R. 1992. Total IgE in plasma is elevated after traumatic injury and is associated with sepsis syndrome. Ann. Surg. 215:460-66.
63. Crouser, E. D., and Dorinsky, P. M. 1996. Metabolic consequences of sepsis: Correlation with altered intracellular calcium homeostasis. Clin. Chest Med. 17:249-61.
64. Michie, H. R. 1996. Metabolism of sepsis and multiple organ failure. World J. Surg. 20:460-64.
65. Chiolero, R., Revelly, J. P., and Tappy, L. 1997. Energy metabolism in sepsis and injury. Nutrition 13:45-51.
66. Patiño, J. F., de Pimiento, S. E., Vergara, A., Savino, P., Rodriguez, M., and Escallón, J. 1999. Hypocaloric support in the critically ill. World J. Surg. 23:553-59.
67. Tredget, E. E., and Yu, Y. M. 1992. The metabolic effects of thermal injury. World J. Surg. 16:68-79.
68. Roe, C., and Kinney, J. 1965. The caloric equivalent of fever: Influence of major trauma. Ann. Surg. 161:140-48.
69. Cooper, A. L., Horan, M. A., Little, R. A., and Rothwell, N. J. 1992. Metabolic and febrile responses to typhoid vaccine in humans: Effect of B-adrenergie blockage. J. Appl. Physiol. 72:2322-28.
70. Kreymann, G., Grosser, S., Buggisch, P., Gottschall, C., Matthaei, S., and Greten, H. 1993. Oxygen consumption and resting metabolic rate in sepsis, sepsis syndrome and septic shock. Crit. Care Med. 21:1012-19.
71. Christe, P. 2002. Intraseasonal variation in immune defence, body mass, and hematocrit in adult house martins Delichon urbica. J. Avian Biol. 33:321-25.
72. Shell-Duncan, B., and Wood, J. W. 1997. The evaluation of delayed-type hypersensitivity responsiveness and nutritional status as predictors of gastro-intestinal and acute respiratory infection: A prospective field study among traditional nomadic Kenyan children. J. Trop. Pediatr. 43:25-32.
73. Ulvestad, E. 2007. Defending Life: The Nature of Host-Parasite Relations. The Netherlands: Springer.
74. Biolo, G., Toigo, G., Ciocchi, B., Situlin, R., Iscra, F., Gullo, A., and Guarnieri, G. 1997. Metabolic response to injury and sepsis: Changes in protein metabolism. Nutrition 13:52-57.
75. Hobler, S. C., Williams, A. B., Fischer, J. E., and Hasselgren, P. O. 1998. IGF-I stimulates protein synthesis but does not inhibit protein breakdown in muscle from septic rats. Am. J. Physiol. Reg. Integ. Comp. Physiol. 274:R571-76.
76. Scrimshaw, N. S. 1991. Effect of infection on nutrient requirements. J. Parent. Enter. Nutr. 15:589-600.
77. Nelson, R. J., and Demas, G. E. 1996. Seasonal changes in immune function. Q. Rev. Biol. 71:511-48.
78. Zuk, M., and Stoehr, A. M. 2002. Immune defense and host life history. Am. Nat. 160:S9-22.
79. Soler, J. J., de Neve, L., Perez-Contreras, T., Soler, M., and Sorci, G. 2003. Tradeoff between immunocompetence and growth in magpies: An experimental study. Proc. Biol. Sci. 270:241-48.
80. Roy, B. A., and Kirchner, J. W. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51-63.
81. Lekander, M. 2002. Ecological immunology: The role of the immune system in psychology and neuroscience. Eur. Psychol. 7:98-115.
82. Steen, R. G., Emudianughe, T., Hunte, M., Glass, J., Wu, S., Xiong, X., and Reddick, W. E. 2005. Brain volume in pediatric patients with sickle cell disease: Evidence of volumetric growth delay? Am. J. Neuroradiol. 26:455-62.
83. Amat, J. A., Aguilera, E., and Visser, G. H. 2007. Energetic and developmental costs of mounting an immune response in greenfinches (Carduelis chloris). Ecol. Res. 22:282-87.
84. Fair, J. M., and Myers, O. B. 2002. The ecological and physiological costs of lead shot and immunological challenge to developing western bluebirds. Ecotoxicology 11:199-208.
85. Fair, J. M., and Ricklefs, R. E. 2002. Physiological, growth, and immune responses of Japanese quail chicks to the multiple stressors of immunological challenge and lead shot. Arch. Environ. Cont. Toxicol. 42:77-87.
86. Sanz, J. J., Moreno, J., Merino, S., and Tomas, G. 2004. A trade-off between two resource demanding functions: Post-nuptial moult and immunity during reproduction in male pied flycatchers. J. Anim. Ecol. 73:441-47.
87. Whitaker, S., and Fair, J. 2002. The costs of immunological challenge to developing mountain chickadees, Poecile gambeli, in the wild. Oikos 99:161-65.
88. Panter-Brick, C., Lunn, P. G., Baker, R., and Todd, A. 2000. Elevated acute-phase protein in stunted Nepali children reporting low morbidity: Different rural and urban profiles. Br. J. Nutr. 85:1-8.
89. Hurtado A. M., Hill, K., Kaplan, H., and Lancaster, J. 2001. The epidemiology of infectious diseases among South American Indians. Curr. Anthropol. 42:425-32.
90. Hurtado, A. M., Hill, K. R., and Hurtado, I. 2001. The compromised health of South American Indians: The need for study under ethical rules. Interciencia 26:166-70.
91. Nacher, M., Singhasivanon, P., Yimsamran, S., Manibunyong, W., Thanyavanich, N., Wuthisen, P., and Looareesuwan, S. 2002. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J. Parasitol. 88:55-58.
92. Bentwich, Z., Kalinkovich, A., Weisman, Z., Borkow, G., Beyers, N., and Beyers, A. D. 1999. Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunol. Today 20:485-87.
93. Christensen, N. O., Nansen, P., Fagbemi, B. O., and Monrad, J. 1987. Heterologous antagonistic and synergistic interactions between helminthes and between helminthes and protozoans in concurrent experimental infection of mammalian hosts. Parasitol. Res. 73:387-410.
94. Long, K. Z., Nanthakumar, N. 2004. Energetic and nutritional regulation of the adaptive immune response and trade-offs in ecological immunology. Am. J. Hum. Biol. 16: 499-507.
95. Ribeiro, D. 1971. The Americas and Civilization. London: Allen and Unwin.
96. Bentwich, Z., Kalinkovich, A., Weisman, Z., Borkowa, G., Beyers, N., Beyers, A. D. 1999. Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunol. Today 20: 485-487.
97. Hurtado, A. M., Hill, K. R., Rosenblatt, W., Scharmen, T. 2003. Longitudinal study of tuberculosis outcomes among immunologically naïve Ache natives of Paraguay. Am. J. Phys. Anthropol. 121:134-150.
98. Hill, K., Boesch, C., Goodall, J., Pusey, A., Williams, J., and Wrangham, R. 2001. Mortality rates among wild chimpanzees. J. Hum. Evol. 40:437-50.
99. Montenegro, R.A., and Stephens, C. 2006. Indigenous health in Latin America and the Caribbean. Lancet 367:1859-69.
100. Ewald, P. 1996. Evolution of infectious disease. Oxford: Oxford University Press.
101. Stearns, S.C. 1998. Evolution in health and disease. Oxford: Oxford University Press.
102. Hurtado, A. M., Arenas de Hurtado, I., Hill, K., and Rodriguez, S. 1997. The evolutionary ecology of chronic allergic conditions: The Hiwi of Venezuela. Hum. Nat. 8:51-75.
103. Hurtado, A. M., Hurtado, I., Sapien, R., and Hill, K. 1999. The evolutionary ecology of childhood asthma. In Evolutionary medicine, ed. W. Trevathan, J. McKenna, and E.O. Smith, 101-34. Oxford: Oxford University Press.
104. Wickelgren, I. 2004. Immunotherapy: can worms tame the immune system? Science 305: 170-171.
105. Graham, A. L., Allen, J. E., and Read, A. F. 2005. Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst. 36:373-97.
106. Gluckman, P. D., Cutfield, W., Hofman, P., and Hanson, M. A. 2005. The fetal, neonatal, and infant environments-The long-term consequences for disease risk. Early Hum. Dev. 81:51-59.
107. Morley, R. 2006. Fetal origins of adult disease. Semin. Fetal Neonatal Med. 11:73-78.