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Deworming and Development: Asking the Right Questions, Asking the Questions Right

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Deworming and Development: Asking the Right Questions, Asking the Questions Right
  Viewpoint Deworming and Development: Asking the RightQuestions, Asking the Questions Right Donald A. P. Bundy 1 * , Michael Kremer 2 , Hoyt Bleakley 3 , Matthew C. H. Jukes 4 , Edward Miguel 5 1 Human Development Network, World Bank, Washington, D.C., United States of America,  2 Department of Economics, Harvard University, Cambridge, Massachusetts,United States of America,  3 Graduate School of Business, University of Chicago, Illinois, United States of America,  4 Graduate School of Education, Harvard University,Cambridge, Massachusetts, United States of America,  5 Center of Evaluation for Global Action, University of California, Berkeley, California, United States of America Two billion people are infected withintestinal worms [1]. In many areas, themajority of schoolchildren are infected,and the World Health Organization(WHO) has called for school-based massdeworming. The key area for debate is notwhether deworming medicine works—infact, the medical literature finds thattreatment is highly effective [2], and thusthe standard of care calls for treating anypatient known to harbor an infection. Asthe authors of the Cochrane systematicreview point out, a critical issue inevaluating current soil-transmitted hel-minth policies is whether the benefits of deworming exceed the costs or whether itwould be more prudent to use the moneyfor other purposes [3].While in general we think the Cochraneapproach is very valuable, we argue belowthat many of the underlying studies of deworming suffer from three critical meth-odological problems: treatment externalitiesin dynamic infection systems, inadequatemeasurement of cognitive outcomes andschool attendance, and sampleattrition. Wethen argue that the currently availableevidence from studies that address theseissues is consistent with the consensus viewexpressed by other reviews and by policy-makers that deworming is a very cost-effective way to increase school participa-tion and has a high benefit to cost ratio. Treatment Externalities Most of the studies included in DavidTaylor-Robinson and colleagues’ system-atic review do not adequately address thepopulation dynamics of helminth infec-tion. These studies follow standard prac-tice in clinical trials and consider untreat-ed people as a control group. Butgeohelminth transmission is a dynamicprocess, and both theoretical and commu-nity studies have shown that treatment of some individuals leads to a reduction intransmission in the community as a whole[4,5]. Thus, in a trial randomized at thelevel of the individual, the expecteddifference between treatment and controlchildren within the same area will be lessthan the actual treatment effect. If, forexample, school attendance increases by 8percentage points among treated childrenand by 4 percentage points among theuntreated due to externalities, the estimat-ed impact using this technique will only be4 percentage points, rather than the trueeffect of 8 percentage points. Theseconcerns are not merely hypothetical: astudy in Kenya found large health andeducational spillovers to untreated stu-dents within treated schools and even tostudents in nearby schools [6]. In light of this finding, the primary focus of a reviewshould be studies that use a cluster designand correct standard errors for intra-cluster correlation [6–8], if indeed thepurpose of such a review is to evaluate thedesirability of mass deworming as a policy.The three studies cited which used thisapproach, some of which were excludedfrom the Cochrane review, did findpositive effects of deworming. Measuring Cognitive Outcomesand School Attendance The summary of the Cochrane review [3]published in this issue of   PLoS Neglected Tropical Diseases   focuses on biomedical out-comes while only touching on cognitive andeducational issues in a single paragraph.Measuring the impact of a healthintervention on cognitive outcomes re-quires careful consideration based on anunderstanding of the nature of cognitivedevelopment, and at least three issues needto be addressed [9]. First, impairedcognition rarely results from a single cause[10]. Worm infections are likely to affectchildren’s cognitive development different-ly according to their levels of poverty,psychosocial stimulation, and generalhealth status. Reporting of these otherenvironmental risk factors is essential forinterpreting studies on cognitive impacts, yet such reporting is rarely used as aninclusion criterion in systematic reviews.Second, the cumulative and interacting impacts of multiple threats to cognitivedevelopment typically means a range of functions could be affected, requiring acomprehensive battery of cognitive assess-ments. However, Taylor-Robinson andcolleagues did not give the design of thesecognitive assessments the same weight asother methodological considerations whenselecting studies for their systematic re- view. Finally, recovery of cognitive im-pairments may depend on remedial edu-cation or psychosocial stimulation inaddition to treatment of the diseaseleading to the impairment [11]. Conse-quently, null results with cognitive out-comes are difficult to interpret unless trialdesigns address the above issues.When measuring the quantity of school-ing, it is also critical to directly verifyattendance through independent checkson site rather than relying on reporteddata, which is often influenced by incen-tives for teachers to exaggerate enrollmentand attendance to increase funding. Onestudy found large discrepancies betweenschool attendance measured by registers versus spot checks in a sample of Kenyanprimary schools, with average attendanceover 10 percentage points higher in the Citation:  Bundy DAP, Kremer M, Bleakley H, Jukes MCH, Miguel E (2009) Deworming and Development: Askingthe Right Questions, Asking the Questions Right. PLoS Negl Trop Dis 3(1): e362. doi:10.1371/ journal.pntd.0000362 Editor:  Gavin Yamey,  PLoS Neglected Tropical Diseases , United States of America Published  January 27, 2009 Copyright:    2009 Bundy et al. This is an open-access article distributed under the terms of the CreativeCommons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,provided the srcinal author and source are credited. Funding:  The authors received no specific funding to write this article. Competing Interests:  The authors declare that no competing interests exist.* E-mail: 1 January 2009 | Volume 3 | Issue 1 | e362  school registers data [6]. The two trialsincluded in the review reported negativefindings on attendance [12,13], but bothrelied on such secondary data. Sample Attrition The impact of deworming on schoolparticipation creates its own methodolog-ical problem of sample attrition, whichwas not adequately addressed in thestudies that were included in the Cochranereview [3]. For example, one includedstudy reports test score data for 89% of students in the treatment group but only59% in the comparison group [14]. If fewer test scores are available for pupils inthe comparison group because academi-cally marginal pupils are more likely to beabsent, then the true impact of deworming will be underestimated. This attrition biasmight also explain why another studyfound no effect of deworming on primaryschool attendance after excluding allperiods of extended school absence, per-haps the very effect they were seeking todetect [13]. Evidence on Health andEducation Even without addressing the concernsabout treatment externalities, the Co-chrane systematic review found that‘‘[w]eight gain after one dose of anthel-minth drugs became just significant, andwith confidence intervals that includepotentially important weight gain values’’[3]. This is despite the notorious difficultyof detecting change in growth in school-age children. Another recent systematicreview found that deworming shows asmall effect on anemia where worminfection is common [15], and anotherconcludes that ‘‘all (included) studiesshowed a benefit [of deworming] formaternal and child health’’ [16]. A large school-based study addressing the above methodological issues foundthat treatment reduced absence by 7percentage points, amounting to a 25percent decline in total absence [6]. (Notethat contrary to the claim in the Cochranesystematic review, the results in [6] are notconfounded by uncontrolled use of praz-iquantel. The school participation benefitsof deworming are similarly large andstatistically significant in the study subre-gion, consisting of 58 primary schools,where schistosomiasis was largely absentand where the protocol thus called forpraziquantel not to be provided.) Costs and Benefits From an economic policy perspective,the merits of deworming depend mainlyon whether its long-term impact onearnings exceeds its cost. Deworming costspennies per dose, or about US$0.25 perchild per year with delivery costs, so gainsof a mere fraction of a percent in incomewould provide a very high benefit to costratio. Studies designed to pick up sucheffect sizes would have to be large andlong-lived, perhaps prohibitively so in thesetting of a randomized controlled trial.Fortunately, history provides a naturalexperiment—the Rockefeller-sponsoredcampaign against hookworm in the UnitedStates South in the 1910s. Census dataand difference-in-difference analysis havebeen used to examine the interaction effectof the pre-campaign prevalence of hook-worm in different parts of the South withthe timing of a mass deworming program[17]. The study found large gains inliteracy, school attendance, and subse-quent income among cohorts offereddeworming as children, implying thatpersistent hookworm infection in child-hood depressed eventual educational at-tainment by 2.1 years and adult income by40%. The findings imply that wormsaccounted for 22% of the large 1900income gap between the US South andNorth. Based on the estimated rate of return to education in Kenya, deworming is likely to increase the net present value of wages by over US$30 per treated individ-ual, creating a benefit to cost ratio of over100. Even if these estimates from Kenyaand the US South [17] overstate theeconomic returns by an order of magni-tude, the benefit to cost ratio would behighly favorable. Conclusions Existing evidence indicates that massschool-based deworming is extraordinarilycost-effective once health, educational,and economic outcomes are all taken intoaccount, and it is thus unsurprising that aseries of studies from the 1993 WorldDevelopment Report [18] to the recentCopenhagen Consensus [19] argue thattreatment of the most prevalent worminfections is a very high return investment. A review by the Abdul Latif JameelPoverty Action Lab at the MassachusettsInstitute of Technology found that de-worming was by far the most cost-effectiveway to increase primary school participa-tion [20]. These analyses depend in parton the impact of deworming on thebiomedical outcomes that are the focusof the Cochrane systematic review [3], butthey also depend on the implications forthe future development of the individualand society. Future income is a centralmeasure of this development. Becausethere is strong evidence that obtaining more education leads to higher adultincome, the effect of deworming on schoolparticipation should be central to anyreasonable policy analysis.We believe that future iterations of theCochrane review that address the threemethodological issues described above andinclude more detailed coverage of otherhealth and non-health outcomes would besignificant contributions for both thebiomedical and social science literatures.We agree with Taylor-Robinson andcolleagues that more trials would be valuable but we also believe that, basedon the current evidence, policymakerswho have to make decisions today shouldtreat those infected with soil-transmittedhelminths. References 1. De Silva NR, Brooker S, Hotez PJ, Montresor A,Engels D, et al. (2003) Soil-transmitted helminthinfections: updating the global picture. TrendsParasitol 19: 547–551.2. Awasthi S, Bundy DAP, Savioli L (2003)Helminthic infections. BMJ 19: 885–888.3. Taylor-Robinson D, Jones A, Garner P (2007)Deworming drugs for treating soil-transmittedintestinal worms in children: effects on growth andschool performance. Cochrane Database of Sys-tematicReviews2007,Issue4.Art.No. CD000371.doi:10.1002/14651858.CD000371.pub31.4. Anderson RM, May RM (1991) Infectious diseasesof humans. New York: Oxford University Press.5. Bundy DAP, Wong MS, Lewis LL, Horton J(1990) Control of geohelminths by delivery of targeted chemotherapy through schools. Trans RSoc Trop Med Hyg 84: 115–120.6. Miguel E, Kremer M (2004) Worms: identifying impacts on education and health in the presence of treatmentexternalities.Econometrica72: 159–217.7. Stoltzfus RJ, Chwaya HM, Tielsch JM,Schultze KJ, Albonico M, et al. (1997) Epidemi-ology of iron deficiency anemia in Zanzibarischoolchildren: the importance of hookworms. Am J Clin Nutr 65: 153–159.8. Awasthi S, Peto R, Pande VK, Fletcher RH,Read S, et al. (2008) Effects of deworming onmalnourished preschool children in India: anopen-labelled, cluster-randomized trial. PLoSNegl Trop Dis 2: e223. doi:10.1371/journal.pntd.0000223.9. Jukes MCH, Drake LJ, Bundy DAP (2007) Schoolhealth, nutrition, and education for all: leveling the playing field. Wallingford (United Kingdom):Cabi Publishing.10. Sameroff AJ, Fiese BH (2000) Transactionalregulation: the develomental ecology of earlyintervention. In Shonkoff JP, Meisels SJ, eds.Handbook of early childhood intervention. 2ndedition. New York: Cambridge University Press.pp 135–159. 2 January 2009 | Volume 3 | Issue 1 | e362  11. Walker SP, Grantham-McGregor SM,Powell CA, Chang SM (2000) Effects of growthrestriction in early childhood on growth, IQ, andcognition at age 11 to 12 years and the benefits of nutritional supplementation and psychosocialstimulation. J Pediatr 137: 36–41.12. Simeon DT, Grantham-McGregor SM,Callender JE, Wong MS (1995) Treatment of Trichuris trichiura infections improves growth,spelling scores, and school attendance in somechildren. J Nutr 125: 1875–1883.13. Watkins WE, Cruz JR, Pollitt E (1996) The effectsof deworming on indicators of school perfor-mance in Guatamala. Trans R Soc Trop MedHyg 90: 156–161.14. Nokes C, Grantham-McGregor SM, Sawyer AW,Cooper ES, Robinson BA, et al. (1992) Moderate-to-heavy infection of Trichuris trichiura affectcognitive function in Jamaican school children.Parisitology 104: 539–547.15. Gulani A, Nagpal J, Osmond C, Sachdev HPS(2007) Effect of administration of intestinalantihelminthic drugs on haemoglobin: systematicreview of randomised controlled trials. BMJ 334:1095.16. Brooker S, Hotez PJ, Bundy DAP (2008)Hookworm-related anaemia among pregnantwomen: a systematic review. PLoS Negl TropDis 2: e291. doi:10.1371/journal.pntd.0000291.17. Bleakley H (2007) Disease and development:evidence from hookworm eradication in the American South. Q J Econ 122: 73–117.18. World Bank (1993) Investing in health. WorldBank development report. Washington (D.C.):The World Bank.19. Copenhagen Consensus Center (2008) Copenha-gen Consensus 2008. Available: Accessed 27 Decem-ber 2008.20. Abdul Latif Jameel Poverty Action Lab (2005)Education: meeting the Millenium Developmentgoals. Fighting poverty: what works? Issue 1. Available: Accessed 27December 2008. 3 January 2009 | Volume 3 | Issue 1 | e362
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