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Heritability of human hookworm infection in Papua New Guinea

  • L. PH. BREITLING (a1), A. J. WILSON (a2), A. RAIKO (a3), M. LAGOG (a3), P. SIBA (a4), M.-A. SHAW (a1) and R. J. QUINNELL (a1)...


Hookworms infect approximately 740 million humans worldwide and are an important cause of morbidity. The present study examines the role of additive genetic effects in determining the intensity of hookworm infection in humans, and whether these effects vary according to the sex of the host. Parasitological and epidemiological data for a population of 704 subjects in Papua New Guinea were used in variance components analysis. The ‘narrow-sense’ heritability of hookworm infection was estimated as 0·15±0·04 (P<0·001), and remained significant when controlling for shared environmental (household) effects. Allowing the variance components to vary between the sexes of the human host consistently revealed larger additive genetic effects in females than in males, reflected by heritabilities of 0·18 in females and 0·08 in males in a conservative model. Household effects were also higher in females than males, although the overall household effect was not significant. The results indicate that additive genetic effects are an important determinant of the intensity of human hookworm infection in this population. However, despite similar mean and variance of intensity in each sex, the factors responsible for generating variation in intensity differ markedly between males and females.


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*Corresponding author: Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK. Tel: +44 113 3432824. Fax: +44 113 3432835. E-mail:


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Almasy, L. and Blangero, J. (1998). Multipoint quantitative trait linkage analysis in general pedigrees. American Journal of Human Genetics 62, 11981211.
Anderson, R. M. and Schad, G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812825.
Bethony, J., Loukas, A., Smout, M., Brooker, S., Mendez, S., Plieskatt, J., Goud, G., Bottazzi, M. E., Zhan, B., Wang, Y., Williamson, A., Lustigman, S., Correa-Oliveira, R., Xiao, S. and Hotez, P. J. (2005). Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB Journal 19, 17431745.
Bethony, J., Williams, J. T., Blangero, J., Kloos, H., Gazzinelli, A., Soares-Filho, B., Coelho, L., Alves-Fraga, L., Williams-Blangero, S., Loverde, P. T. and Correa-Oliveira, R. (2002). Additive host genetic factors influence fecal egg excretion rates during Schistosoma mansoni infection in a rural area in Brazil. American Journal of Tropical Medicine and Hygiene 67, 336343.
Bethony, J. M. and Quinnell, R. J. (2008). Genetic epidemiology of human schistosomiasis in Brazil. Acta Tropica (in the Press). doi:10.1016/j.actatropica.2007.11.008
Bishop, S. C., Bairden, K., McKellar, Q. A., Park, M. and Stear, M. J. (1996). Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with live weight in young lambs. Animal Science 63, 423428.
Bradley, M. and Chandiwana, S. K. (1990). Age-dependency in predisposition to hookworm infection in the Burma valley area of Zimbabwe. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 826828.
Brooker, S., Alexander, N., Geiger, S., Moyeed, R. A., Stander, J., Fleming, F., Hotez, P. J., Correa-Oliveira, R. and Bethony, J. (2006). Contrasting patterns in the small-scale heterogeneity of human helminth infections in urban and rural environments in Brazil. International Journal for Parasitology 36, 11431151.
Brooker, S., Bethony, J. and Hotez, P. J. (2004). Human hookworm infection in the 21st century. Advances in Parasitology 58, 197288.
Cho, H. S., Guo, G., Iritani, B. J. and Hallfors, D. D. (2006). Genetic contribution to suicidal behaviours and associated risk factors among adolescents in the US. Prevention Science 7, 303311.
Coltman, D. W., Pilkington, J., Kruuk, L. E. B., Wilson, K. and Pemberton, J. M. (2001). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55, 21162125.
de Silva, N. R., Brooker, S., Hotez, P. J., Montresor, A., Engels, D. and Savioli, L. (2003). Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19, 547551.
Ellis, M. K., Li, Y., Rong, Z., Chen, H. and McManus, D. P. (2006). Familial aggregation of human infection with Schistosoma japonicum in the Poyang Lake region, China. International Journal for Parasitology 36, 7177.
Gilmour, A. R., Gogel, B. J., Cullis, B. R., Welham, S. J. and Thompson, R. (2002). ASReml User Guide Release 1.0. VSN International Ltd, Hemel Hempstead, UK.
Haswell-Elkins, M. R., Elkins, D. B., Manjula, K., Michael, E. and Anderson, R. M. (1988). An investigation of hookworm infection and reinfection following mass anthelmintic treatment in the south Indian fishing community of Vairavankuppam. Parasitology 96, 565577.
Hill, R. B. (1926). The estimation of the number of hookworms harbored, by the use of the dilution egg count method. American Journal of Hygiene 6, 1941.
Horton, J. (2000). Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology 121, S113S132.
Hotez, P. J., Brooker, S., Bethony, J. M., Bottazzi, M. E., Loukas, A. and Xiao, S. (2004). Hookworm infection. New England Journal of Medicine 351, 799807.
King, C. H., Blanton, R. E., Muchiri, E. M., Ouma, J. H., Kariuki, H. C., Mungai, P., Magak, P., Kadzo, H., Ireri, E. and Koech, D. K. (2004). Low heritable component of risk for infection intensity and infection-associated disease in urinary schistosomiasis among Wadigo village populations in Coast Province, Kenya. American Journal of Tropical Medicine and Hygiene 70, 5762.
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247264.
Lange, K. and Boehnke, M. (1983). Extensions to pedigree analysis. IV. Covariance components models for multivariate traits. American Journal of Medical Genetics 14, 513524.
Lange, K., Westlake, J. and Spence, M. A. (1976). Extensions to pedigree analysis. III. Variance components by the scoring method. Annals of Human Genetics 39, 485491.
Ober, C., Pan, L., Phillips, N., Parry, R. and Kurina, L. M. (2006). Sex-specific genetic architecture of asthma-associated quantitative trait loci in a founder population. Current Allergy and Asthma Reports 6, 241246.
Pilia, G., Chen, W. M., Scuteri, A., Orru, M., Albai, G., Dei, M., Lai, S., Usala, G., Lai, M., Loi, P., Mameli, C., Vacca, L., Deiana, M., Olla, N., Masala, M., Cao, A., Najjar, S. S., Terracciano, A., Nedorezov, T., Sharov, A., Zonderman, A. B., Abecasis, G. R., Costa, P., Lakatta, E. and Schlessinger, D. (2006). Heritability of cardiovascular and personality traits in 6,148 Sardinians. PLoS Genetics 2, 12071223.
Pritchard, D. I., Quinnell, R. J., Slater, A. F., McKean, P. G., Dale, D. D., Raiko, A. and Keymer, A. E. (1990). Epidemiology and immunology of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory-secretory and cuticular collagen antigens. Parasitology 100, 317326.
Pritchard, D. I., Quinnell, R. J. and Walsh, E. A. (1995). Immunity in humans to Necator americanus: IgE, parasite weight and fecundity. Parasite Immunology 17, 7175.
Quinnell, R. J. (2003). Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33, 12191231.
Quinnell, R. J., Griffin, J., Nowell, M. A., Raiko, A. and Pritchard, D. I. (2001). Predisposition to hookworm infection in Papua New Guinea. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 139142.
Quinnell, R. J., Pritchard, D. I., Raiko, A., Brown, A. P. and Shaw, M. A. (2004). Immune responses in human necatoriasis: association between interleukin-5 responses and resistance to reinfection. Journal of Infectious Diseases 190, 430438.
Quinnell, R. J., Slater, A. F., Tighe, P., Walsh, E. A., Keymer, A. E. and Pritchard, D. I. (1993). Reinfection with hookworm after chemotherapy in Papua New Guinea. Parasitology 106, 379385.
R Development Core Team. (2006). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Saathoff, E., Olsen, A., Sharp, B., Kvalsvig, J. D., Appleton, C. C. and Kleinschmidt, I. (2005). Ecologic covariates of hookworm infection and reinfection in rural Kwazulu-natal/south Africa: a geographic information system-based study. American Journal of Tropical Medicine and Hygiene 72, 384391.
Schad, G. A. and Anderson, R. M. (1985). Predisposition to hookworm infection in humans. Science 228, 15371540.
Scurrah, K. J., Byrnes, G. B., Hopper, J. L. and Harrap, S. B. (2006). Sex differences in genetic and environmental determinants of pulse pressure. Genetic Epidemiology 30, 397408.
Smith, J. A., Wilson, K., Pilkington, J. G. and Pemberton, J. M. (1999). Heritable variation in resistance to gastro-intestinal nematodes in an unmanaged mammal population. Proceedings of the Royal Society of London, B 266, 12831290.
Sokal, R. R. and Rohlf, F. J. (1995). Biometry. W. H. Freeman and Company, New York, USA.
Stear, M. J., Bairden, K., Duncan, J. L., Holmes, P. H., McKellar, Q. A., Park, M., Strain, S., Murray, M., Bishop, S. C. and Gettinby, G. (1997). How hosts control worms. Nature, London 389, 27.
Stoll, N. R. (1924). Investigations on the control of hookworm disease. XXXIII. The significance of egg-count data in necator infestations. American Journal of Hygiene 4, 466500.
Stram, D. O. and Lee, J. W. (1994). Variance components testing in the longitudinal mixed effects model. Biometrics 50, 11711177.
Towne, B., Blangero, J. and Siervogel, R. M. (1993). Genotype by sex interaction in measures of lipids, lipoproteins, and apolipoproteins. Genetic Epidemiology 10, 611616.
Towne, B., Siervogel, R. M. and Blangero, J. (1997). Effects of genotype-by-sex interaction on quantitative trait linkage analysis. Genetic Epidemiology 14, 10531058.
Venables, W. N. and Ripley, B. D. (2002). Modern Applied Statistics with S. Springer, New York and London.
Weiss, L. A., Pan, L., Abney, M. and Ober, C. (2006). The sex-specific genetic architecture of quantitative traits in humans. Nature Genetics 38, 218222.
Williams-Blangero, S., Blangero, J. and Bradley, M. (1997). Quantitative genetic analysis of susceptibility to hookworm infection in a population from rural Zimbabwe. Human Biology 69, 201208.
Williams-Blangero, S., McGarvey, S. T., Subedi, J., Wiest, P. M., Upadhayay, R. P., Rai, D. R., Jha, B., Olds, G. R., Guanling, W. and Blangero, J. (2002). Genetic component to susceptibility to Trichuris trichiura: evidence from two Asian populations. Genetic Epidemiology 22, 254264.
Williams-Blangero, S., Subedi, J., Upadhayay, R. P., Manral, D. B., Rai, D. R., Jha, B., Robinson, E. S. and Blangero, J. (1999). Genetic analysis of susceptibility to infection with Ascaris lumbricoides. American Journal of Tropical Medicine and Hygiene 60, 921926.


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Heritability of human hookworm infection in Papua New Guinea

  • L. PH. BREITLING (a1), A. J. WILSON (a2), A. RAIKO (a3), M. LAGOG (a3), P. SIBA (a4), M.-A. SHAW (a1) and R. J. QUINNELL (a1)...


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