Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-29T12:04:01.173Z Has data issue: false hasContentIssue false
  • English
  • Français

Rates and intensity of re-infection with human helminths after treatment and the influence of individual, household, and environmental factors in a Brazilian community

Published online by Cambridge University Press:  08 August 2011

BONNIE CUNDILL ,
NEAL ALEXANDER ,
JEFF M. BETHONY ,
DAVID DIEMERT ,
RACHEL L. PULLAN  and
SIMON BROOKER
BONNIE CUNDILL*
Affiliation:
London School of Hygiene and Tropical Medicine, London, UK
NEAL ALEXANDER
Affiliation:
London School of Hygiene and Tropical Medicine, London, UK The George Washington University, Washington D.C., USA
JEFF M. BETHONY
Affiliation:
The George Washington University, Washington D.C., USA Centro de Pesquisas René Rachou (FIOCRUZ), Belo Horizonte, Minas Gerais, Brazil
DAVID DIEMERT
Affiliation:
The George Washington University, Washington D.C., USA Sabin Vaccine Institute, Washington D.C., USA
RACHEL L. PULLAN
Affiliation:
London School of Hygiene and Tropical Medicine, London, UK
SIMON BROOKER
Affiliation:
London School of Hygiene and Tropical Medicine, London, UK Kenya Medical Research Institute – Wellcome Trust Research Programme, Nairobi, Kenya
*
*Corresponding author: Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK. Tel: +44 207 927 2111. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study quantifies the rate and intensity of re-infection with human hookworm and Schistosoma mansoni infection 12 months following successful treatment, and investigates the influence of socio-economic, geographical and environmental factors. A longitudinal study of 642 individuals aged over 5 years was conducted in Minas Gerais State, Brazil from June 2004 to March 2006. Risk factors were assessed using interval censored regression for the rate and negative binomial regression for intensity. The crude rate and intensity of hookworm re-infection was 0·21 per year (95% confidence interval (CI) 0·15–0·29) and 70·9 epg (95% CI 47·2–106·6). For S. mansoni the rate was 0·06 per year (95% CI 0·03–0·10) and intensity 6·51 epg (95% CI 3·82–11·11). Rate and intensity of re-infection with hookworm were highest among males and positively associated with previous infection status, absence of a toilet and house structure. Rate and intensity of S. mansoni re-infection were associated with previous infection status as well as geographical, environmental and socio-economic factors. The implications of findings for the design of anti-helminth vaccine trials are discussed.

Keywords

Necator americanushookwormSchistosoma mansonirisk factorsre-infectionnegative binomial
Type
Research Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1406 - 1416
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albonico, M., Smith, P. G., Ercole, E., Hall, A., Chwaya, H. M., Alawi, K. S. and Savioli, L. (1995). Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or albendazole in a highly endemic area. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 538–541.Google Scholar
Alexander, N., Cundill, B., Sabatelli, L., Bethony, J. M., Diemert, D., Hotez, P., Smith, P. G., Rodrigues, L. C. and Brooker, S. (2011). Selection and quantification of infection endpoints for trials of vaccines against intestinal helminths. Vaccine. doi:10.1016/j.vaccine.2011.03.026.Google Scholar
Anderson, R. M. (1993). Modern Parasitology, 2nd Edn. Blackwell, Oxford, UK.Google Scholar
Anderson, R. M. and Medley, G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629–660.Google Scholar
Baker, M. C., Mathieu, E., Fleming, F. M., Deming, M., King, J. D., Garba, A., Koroma, J. B., Bockarie, M., Kabore, A., Sankara, D. P. and Molyneux, D. H. (2010). Mapping, monitoring, and surveillance of neglected tropical diseases: towards a policy framework. Lancet 375, 231–238. doi:10.1016/S0140-6736(09)61458-6.Google Scholar
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, 1143–1151. doi:10.1016/j.ijpara.2006.05.009.Google Scholar
Brooker, S., Jardim-Botelho, A., Quinnell, R. J., Geiger, S. M., Caldas, I. R., Fleming, F., Hotez, P. J., Correa-Oliveira, R., Rodrigues, L. C. and Bethony, J. M. (2007). Age-related changes in hookworm infection, anaemia and iron deficiency in an area of high Necator americanus hookworm transmission in south-eastern Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 146–154.Google Scholar
Bundy, D. A., Cooper, E. S., Thompson, D. E., Didier, J. M. and Simmons, I. (1988). Effect of age and initial infection intensity on the rate of reinfection with Trichuris trichiura after treatment. Parasitology 97, 469–476.Google Scholar
Bundy, D. A. and Medley, G. F. (1992). Immuno-epidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden. Parasitology 104 (Suppl.), S105–S119. doi:10.1017/S0031182000075284.Google Scholar
Collett (2003 a). Modelling Binary Data, 2nd Edn. Chapman and Hall, London, UK.Google Scholar
Collett (2003 b). Modelling Survival Data in Medical Research, 2nd Edn. CRC Press, Boca Raton, FL, USA.Google Scholar
Diemert, D. J., Bethony, J. M. and Hotez, P. J. (2008). Hookworm vaccines. Clinical Infectious Diseases 46, 282–288. doi:10.1086/524070.Google Scholar
Filmer, D. and Pritchett, L. H. (2001). Estimating wealth effects without expenditure data – or tears: an application to educational enrollments in states of India. Demography 38, 115–132. doi:10.1353/dem.2001.0003.Google Scholar
Fleming, F. M., Brooker, S., Geiger, S. M., Caldas, 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. Tropical Medicine and International Health 11, 56–64. doi:10.1111/j.1365-3156.2005.01541.x.Google Scholar
Geiger, S. M., Caldas, I. R., Mc Glone, B. E., Campi-Azevedo, A. C., De Oliveira, L. M., Brooker, S., Diemert, D., Correa-Oliveira, R. and Bethony, J. M. (2007). Stage-specific immune responses in human Necator americanus infection. Parasite Immunology 29, 347–358. doi:10.1111/j.1365-3024.2007.00950.x.Google Scholar
Haswell-Elkins, M. R., Elkins, D. B. and Anderson, R. M. (1987). Evidence for predisposition in humans to infection with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community. Parasitology 95, 323–337.Google Scholar
Henry, F. J. (1988). Reinfection with Ascaris lumbricoides after chemotherapy: a comparative study in three villages with varying sanitation. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 460–464.Google Scholar
Hesham Al-Mekhlafi, M., Surin, J., Atiya, A. S., Ariffin, W. A., Mohammed Mahdy, A. K. and Che Abdullah, H. (2008). Pattern and predictors of soil-transmitted helminth reinfection among aboriginal schoolchildren in rural Peninsular Malaysia. Acta Tropica 107, 200–204. doi:10.1016/j.actatropica.2008.05.022.Google Scholar
Hilbe, J. M. (2007). Negative Binomial Regression, Cambridge University Press, Cambridge, UK.Google Scholar
Holland, C. V. (2009). Predisposition to ascariasis: patterns, mechanisms and implications. Parasitology 136, 1537–1547. doi:10.1017/S0031182009005952.Google Scholar
Hotez, P. J., Bethony, J. M., Diemert, D. J., Pearson, M. and Loukas, A. (2010). Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nature Reviews Microbiology 8, 814–826. doi:10.1038/nrmicro2438.Google Scholar
Jardim-Botelho, A., Brooker, S., Geiger, S. M., Fleming, F., Souza Lopes, A. C., Diemert, D. J., Correa-Oliveira, R. and Bethony, J. M. (2008). Age patterns in undernutrition and helminth infection in a rural area of Brazil: associations with ascariasis and hookworm. Tropical Medicine and International Health 13, 458–467. doi:10.1111/j.1365–3156.2008.02022.x.Google Scholar
Kabatereine, N. B., Vennervald, B. J., Ouma, J. H., Kemijumbi, J., Butterworth, A. E., Dunne, D. W. and Fulford, A. J. (1999). Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118, 101–105.Google Scholar
Loukas, A., Bethony, J., Brooker, S. and Hotez, P. (2006). Hookworm vaccines: past, present, and future. Lancet Infectious Diseases 6, 733–741. doi:10.1016/S1473-3099(06)70630-2.Google Scholar
Narain, K., Medhi, G. K., Rajguru, S. K. and Mahanta, J. (2004). Cure and reinfection patterns of geohelminthic infections after treatment in communities inhabiting the tropical rainforest of Assam, India. Southeast Asian Journal of Tropical Medicine and Public Health 35, 512–517.Google Scholar
Olsen, A., Nawiri, J. and Friis, H. (2000). The impact of iron supplementation on reinfection with intestinal helminths and Schistosoma mansoni in western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 493–499.Google Scholar
Olsen, A., Thiong'o, F. W., Ouma, J. H., Mwaniki, D., Magnussen, P., Michaelsen, K. F., Friis, H. and Geissler, P. W. (2003). Effects of multimicronutrient supplementation on helminth reinfection: a randomized, controlled trial in Kenyan schoolchildren. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 109–114.Google Scholar
Pullan, R., Bethony, J., Geiger, S., Cundill, B., Correa-Oliveira, R., Quinnell, R. J. and Brooker, S. (2008). Human helminth co-infection: analysis of spatial patterns and risk factors in a Brazilian community. PLoS Neglected Tropical Diseases 2, e352. doi:10.1371/journal.pntd.0000352.Google Scholar
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, 139–142.Google Scholar
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, 379–385.Google Scholar
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, 384–391.Google Scholar
Tingley, G. A., Butterworth, A. E., Anderson, R. M., Kariuki, H. C., Koech, D., Mugambi, M., Ouma, J. H., Arap Siongok, T. K. and Sturrock, R. F. (1988). Predisposition of humans to infection with Schistosoma mansoni: evidence from the reinfection of individuals following chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 448–452.Google Scholar
Victora, C. G., Huttly, S. R., Fuchs, S. C. and Olinto, M. T. (1997). The role of conceptual frameworks in epidemiological analysis: a hierarchical approach. International Journal of Epidemiology 26, 224–227.Google Scholar
Wu, Z. D., Lu, Z. Y. and Yu, X. B. (2005). Development of a vaccine against Schistosoma japonicum in China: a review. Acta Tropica 96, 106–116. doi:10.1016/j.actatropica.2005.08.005.Google Scholar