1921
Volume 96, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

Soil-transmitted helminths (STHs) infect over one billion people worldwide. There is concern that chronic infection with STHs among school-aged children may detrimentally affect their development, including their health, cognition, and education. However, two recent Cochrane reviews examining the impact of deworming drugs for STH on nutrition, hemoglobin, and school performance found that randomized controlled trials (RCTs) in the literature provide an insufficient evidence base to draw reliable conclusions. This study uses a cluster-RCT to add to existing evidence by assessing the impact of a deworming intervention on nutrition, cognition, and school performance among schoolchildren in rural China. The intervention, implemented by local health practitioners in a setting with a baseline infection prevalence of 41.9% (95% confidence interval [CI] = 39.8%, 43.9%) and infection intensity of 599.5 eggs per gram of feces among positive-tested schoolchildren (95% CI = 473.2, 725.8), consisted of distributing a 400-mg dose of albendazole accompanied with educational training about STH infection, treatment, and prevention. The intervention was conducted twice over the course of the study—at baseline in May 2013 and later in November 2013. We found that the deworming intervention reduced both infection prevalence and infection intensity, but these declines in infection were not accompanied by an impact on outcomes of nutrition, cognition, or school performance. Our interpretation is that the impact of deworming was attenuated by the light infection intensity in our sample population. Evidence from future RCTs is needed to assess the effect of deworming on key outcomes in areas with moderate and severe worm infections.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.16-0354
2017-06-07
2018-08-20
Loading full text...

Full text loading...

/deliver/fulltext/14761645/96/6/1478.html?itemId=/content/journals/10.4269/ajtmh.16-0354&mimeType=html&fmt=ahah

References

  1. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J, , 2008. Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 13111321.[Crossref]
  2. Pullan RL, Brooker SJ, , 2012. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors 5: 81.[Crossref]
  3. Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, Hatz CF, , 2012. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly 142: 13727.
  4. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, , 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 15211532.[Crossref]
  5. Hall A, Hewitt G, Tuffrey V, , 2008. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr 4: 118236.[Crossref]
  6. Suchdev PS, Davis SM, Bartoces M, Ruth LJ, Worrell CM, Kanyi H, Odero K, Wiegand RE, Njenga SM, Montgomery JM, Fox LM, , 2014. Soil-transmitted helminth infection and nutritional status among urban slum children in Kenya. Am J Trop Med Hyg 90: 299305.[Crossref]
  7. Ezeamama AE, Friedman JF, Acosta LP, Bellinger DC, Langdon GC, Manalo DL, Olveda RM, Kurtis JD, McGarvey ST, , 2005. Helminth infection and cognitive impairment among Filipino children. Am J Trop Med Hyg 72: 540548.
  8. Liu C, Luo R, Yi H, Zhang L, Li S, Bai Y, Medina A, Rozelle S, Smith S, Wang G, Wang J, , 2015. Soil-transmitted helminths in southwestern China: a cross-sectional study of links to cognitive ability, nutrition, and school performance among children. PLoS Negl Trop Dis 9: e0003877.[Crossref]
  9. Miguel E, Kremer M, , 2004. Worms: identifying impacts on education and health in the presence of treatment externalities. Econometrica 72: 159217.[Crossref]
  10. Vercruysse J, Behnke JM, Albonico M, Ame SM, Angebault C, Bethony JM, Engels D, Guillard B, Nguyen TV, Kang G, Kattula D, Kotze AC, McCarthy JS, Mekonnen Z, Montresor A, Periago MV, Sumo L, Tchuenté LA, Dang TC, Zeynudin A, Levecke B, , 2011. Assessment of the anthelmintic efficacy of albendazole in school children in seven countries where soil-transmitted helminths are endemic. PLoS Negl Trop Dis 5: e948.[Crossref]
  11. Keiser J, Utzinger J, , 2008. Efficacy of current drugs against soil-transmitted helminth infections. JAMA 299: 19371948.[Crossref]
  12. Taylor-Robinson DC, Maayan N, Soares-Weiser K, Donegan S, Garner P, , 2012. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin and school performance (Review). Cochrane Database Syst Rev 11: CD000371.
  13. Ebenezer R, Gunawardena K, Kumarendran B, Pathmeswaran A, Jukes MCH, Drake LJ, de Silva N, , 2013. Cluster-randomised trial of the impact of school-based deworming and iron supplementation on the cognitive abilities of schoolchildren in Sri Lanka's plantation sector. Trop Med Int Health 8: 942951.[Crossref]
  14. Yap P, Wu F-W, Du Z-W, Hattendorf J, Chen R, Jiang JY, Kriemler S, Krauth SJ, Zhou XN, Utzinger J, Steinmann P, , 2014. Effect of deworming on physical fitness of school-aged children in Yunnan, China: a double-blind, randomized, placebo-controlled trial. PLoS Negl Trop Dis 8: e2983.[Crossref]
  15. Awasthi S, Peto R, Read S, Richards SM, Pande V, Bundy D, DEVTA (Deworming and Enhanced Vitamin A) Team; , 2013. Population deworming every 6 months with albendazole in 1 million pre-school children in north India: DEVTA, a cluster-randomised trial. Lancet 381: 14781486.[Crossref]
  16. Vicotra CG, Black RE, Boerma JT, Bryce J, , 2011. Measuring impact in the Millennium Development Goal era and beyond: a new approach to large-scale effectiveness evaluations. Lancet 377: 8595.[Crossref]
  17. Gartlehner G, Hansen RA, Nissman D, Lohr KN, Carey TS, , 2006. Criteria for Distinguishing Effectiveness from Efficacy Trials in Systematic Reviews. Rockville, MD: Agency for Healthcare Research and Quality (US).
  18. Aiken AM, Davey C, Hargreaves JR, Hayes RJ, , 2015. Re-analysis of health and educational impacts of a school-based deworming programme in western Kenya: a pure replication. Int J Epidemiol 44: 15721580.[Crossref]
  19. Davey C, Aiken AM, Hayes RJ, Hargreaves JR, , 2015. Re-analysis of health and educational impacts of a school-based deworming programme in western Kenya: a statistical replication of a cluster quasi-randomized stepped-wedge trial. Int J Epidemiol 44: 15811592.[Crossref]
  20. Hicks JH, Kremer M, Miguel E, , 2015. The case for mass treatment of intestinal helminths in endemic areas. PLoS Negl Trop Dis 9: e0004214.[Crossref]
  21. Hicks JH, Kremer M, Miguel E, , 2015. Commentary: deworming externalities and schooling impacts in Kenya: a comment on Aiken et al. (2015) and Davey et al. (2015). Int J Epidemiol 44: 15931596.[Crossref]
  22. Humphreys M, , 2015. What Has Been Learned from the Deworming Replications: A Nonpartisan View. Available at: http://www.macartan.nyc/comments/worms2/. Accessed November 25, 2016.
  23. Ozier O, , 2014. Exploiting Externalities to Estimate the Long-Run Effect of Early Childhood Deworming. Policy Research Working Paper 7052. Washington, DC: The World Bank.[Crossref]
  24. Baird S, Hicks JH, Kremer M, Miguel E, , 2016. Worms at work: long-run impacts of a child health investment. Q J Econ 2016: 16371680.
  25. Wang X, Zhang L, Luo R, Wang G, Chen Y, Medina A, Eggleston K, Rozelle S, Smith DS, , 2012. Soil-transmitted helminth infections and correlated risk factors in preschool and school-aged children in rural southwest China. PLoS One 7: e45939.[Crossref]
  26. Zhou H, Ohtsuka R, He Y, Yuan L, Yamauchi T, Sleigh AC, , 2005. Impact of parasitic infections and dietary intake on child growth in the schistosomiasis-endemic Dongting Lake region, China. Am J Trop Med Hyg 72: 534539.
  27. Guizhou Provincial Bureau of Statistics, 2012. Guizhou Statistical Yearbook 2011. Beijing, China: China Statistics Press.
  28. Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P, Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P, , 2006. Chapter 24: Helminth infections: soil-transmitted helminth infections and schistosomiasis. eds. Disease Control Priorities in Developing Countries, 2nd edition. Washington, DC: The World Bank.[Crossref]
  29. Moore Ryan T, , 2012. Block Tools: Blocking, Assignment, and Diagnosing Interference in Randomized Experiments. Technical Report.
  30. Ash LR, Orihel TC, Savioli L, Sin MA, Montresor A, Renganathan E, , 1998. Training Manual on Diagnosis of Intestinal Parasites. Geneva, Switzerland: World Health Organization.
  31. World Health Organization, 2011. Helminth Control for School-Age Children. Geneva, Switzerland: World Health Organization.
  32. de Onis M, Blossner M, Borghi E, Morris R, Fronglio EA, , 2004. Methodology for estimating regional and global trends in child malnutrition. Int J Epidemiol 33: 12601270.[Crossref]
  33. Wechsler D, , 2008. Wechsler Intelligence Scale for Children Fourth Edition (WISC-IV) Administration and Scoring Manual (Chinese version). Zhuhai, China: King-may Psychological Assessment Ltd.
  34. Nokes C, Grantham-McGregor SM, Sawyer AW, Cooper ES, Bundy DA, , 1992. Parasitic helminthic infection and cognitive function in school children. Proc R Soc Lond B Biol Sci 247: 7781.[Crossref]
  35. Jardim-Botelho A, Raff S, De Ávila Rodrigues R, Hoffman HJ, Diemert DJ, Corrêa-Oliveira R, Bethony JM, Gazzinelli MF, , 2008. Hookworm, Ascaris lumbricoides infection and polyparasitism associated with poor cognitive performance in Brazilian schoolchildren. Trop Med Int Health 13: 9941004.[Crossref]
  36. Mullis IV, Martin MO, Gonzalez EJ, Chrostowski SJ, , 2004. TIMSS 2003 International Mathematics Report: Findings from IEA's Trends in International Mathematics and Science Study at the Fourth and Eighth Grades. Boston, MA: International Association for the Evaluation of Educational Achievement, TIMSS, and PIRLS International Study Center, Lynch School of Education, Boston College.
  37. Ministry of Health, 2010. Technical Guidelines for Soil-Transmitted Helminth Disease Control (2010 Version) [in Chinese]. Beijing, China.
  38. World Health Organization, 2001. Iron Deficiency Anemia: Assessment, Prevention and Control, A Guide for Programme Managers. Geneva, Switzerland: World Health Organization.
  39. World Health Organization, 2009. WHO AnthroPlus for Personal Computers Manual: Software for Assessing Growth of the World's Children and Adolescents. Available at: http://www.who.int/growthref/tools/en/.
  40. Centers for Disease Control and Prevention (CDC), 2014. A SAS Program for the 2000 CDC Growth Charts (Ages 0 to < 20 Years). Available at: http://www.cdc.gov/nccdphp/dnpao/growthcharts/resources/sas.htm.
  41. Bruhn M, McKenzie D, , 2009. In pursuit of balance: randomization in practice in development field experiments. Am Econ J Appl Econ 1: 200232.[Crossref]
  42. Greevy R, Lu B, Silber JH, Rosenbaum P, , 2004. Optimal multivariate matching before randomization. Biostat 5: 263275.[Crossref]
  43. Shang Y, , 2011. Burden of Diseases on Soil-Transmitted Helminth Infections among School-Age Children in China [in Chinese]. Doctoral Thesis, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, China.
  44. Angrist JD, Imbens GW, Rubin DB, , 1996. Identification of causal effects using instrumental variables. J Am Stat Assoc 91: 444455.[Crossref]
  45. World Health Organization, 2011. Helminth Control in School-Age Children: A Guide for Managers of Control Programmes, 2nd edition. Geneva, Switzerland: World Health Organization.
  46. Holland CV, , 2009. Predisposition to ascariasis: patterns, mechanisms and implications. Parasitology 136: 15371547.[Crossref]
  47. Jia T-W, Melville S, Utzinger J, King CH, Zhou X-N, , 2012. Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis 6: e1621.[Crossref]
  48. Cabrera BD, , 1984. Reinfection and infection rates of ascariasis in relation to seasonal variation in the Philippines. Southeast Asian J Trop Med Public Health 15: 394401.
  49. Pan CT, Ritchie LS, Hunter GW, 3rd, 1954. Reinfection and seasonal fluctuations of Ascaris lumbricoides among a group of children in an area where night soil is used. J Parasitol 40: 603608.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.16-0354
Loading
/content/journals/10.4269/ajtmh.16-0354
Loading

Data & Media loading...

Supplementary Data

Supplemental Appendix

  • Received : 03 May 2016
  • Accepted : 05 Dec 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error