Water, Sanitation, Hygiene, and Soil-Transmitted Helminth Infection: A Systematic Review and Meta-Analysis

PLoS Medicine

Volumn 11, Issue 3, 2014, Pages

  Strunz, Eric C ^a   Addiss, David G ^a   Stocks, Meredith E ^b   Ogden, Stephanie ^a,b,c   Utzinger, Jürg ^d,e   Freeman, Matthew C ^b  

^a Children Without Worms   (United States)

^b EMORY UNIVERSITY   (United States)

^c International Trachoma Initiative   (United States)

^d SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^e UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

SOAP; WATER;

ANCYLOSTOMIASIS; ARTICLE; ASCARIASIS; ECOSYSTEM MONITORING; ENVIRONMENTAL EXPOSURE; HAND WASHING; HEALTH CARE QUALITY; HELMINTHIASIS; HOOKWORM INFECTION; HUMAN; HYGIENE; INFECTION CONTROL; INFECTION RISK; META ANALYSIS; NONHUMAN; PREVALENCE; SANITATION; STRONGYLOIDIASIS; SYSTEMATIC REVIEW; TRICHURIASIS;

ADOLESCENT; ADULT; ANIMALS; CHILD; CHILD, PRESCHOOL; HAND DISINFECTION; HUMANS; HYGIENE; INFANT; INFANT, NEWBORN; NEMATODA; NEMATODE INFECTIONS; SANITATION; SOIL;

EID: 84898949931     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.1001620     Document Type: Article

References (180)

1. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, et al. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521-1532.
2. Murray CJ, Vos T, Lozano R, Naghavi M, Flaxman AD, et al. (2013) Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380: 2197-2223.
3. Brooker S, (2010) Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers - A review. Int J Parasitol 40: 1137-1144.
4. Chan MS, (1997) The global burden of intestinal nematode infections - fifty years on. Parasitol Today 13: 438-443.
5. Utzinger J, Raso G, Brooker S, De Savigny D, Tanner M, et al. (2009) Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology 136: 1859-1874.
6. 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.
7. Bartram J, Cairncross S, (2010) Hygiene, sanitation, and water: forgotten foundations of health. PLoS Med 7: e1000367.
8. WHO (2006) Preventive chemotherapy in human helminthiasis. Geneva: World Health Organization. 71 p.
9. Hong ST, Chai JY, Choi MH, Huh S, Rim HJ, et al. (2006) A successful experience of soil-transmitted helminth control in the Republic of Korea. Korean J Parasitol 44: 177-185.
10. Kobayashi A, Hara T, Kajima J, (2006) Historical aspects for the control of soil-transmitted helminthiases. Parasitol Int 55 Suppl: S289-291.
11. Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, et al. (2005) Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis 5: 42-52.
12. Clasen T, Roberts I, Rabie T, Schmidt W, Cairncross S, (2006) Interventions to improve water quality for preventing diarrhoea. Cochrane Database Syst Rev pp. CD004794.
13. Arnold B, Arana B, Mäusezahl D, Hubbard A, Colford JM Jr, (2009) Evaluation of a pre-existing, 3-year household water treatment and handwashing intervention in rural Guatemala. Int J Epidemiol 38: 1651-1661.
14. Cairncross S, Hunt C, Boisson S, Bostoen K, Curtis V, et al. (2010) Water, sanitation and hygiene for the prevention of diarrhoea. Int J Epidemiol 39 Suppl 1: i193-i205.
15. Clasen TF, Bostoen K, Schmidt W-P, Boisson S, Fung ICH, et al. (2010) Interventions to improve disposal of human excreta for preventing diarrhoea. Cochrane Database Syst Rev pp. CD007180.
16. Graf J, Zebaze Togouet S, Kemka N, Niyitegeka D, Meierhofer R, et al. (2010) Health gains from solar water disinfection (SODIS): evaluation of a water quality intervention in Yaoundé, Cameroon. J Water Health 8: 779-796.
17. Hunter PR, Ramírez Toro GI, Minnigh HA, (2010) Impact on diarrhoeal illness of a community educational intervention to improve drinking water quality in rural communities in Puerto Rico. BMC Public Health 10: 219.
18. Freeman MC, Clasen T, (2011) Assessing the impact of a school-based safe water intervention on household adoption of point-of-use water treatment practices in southern India. Am J Trop Med Hyg 84: 370-378.
19. Greene LE, Freeman MC, Akoko D, Saboori S, Moe C, et al. (2012) Impact of a school-based hygiene promotion and sanitation intervention on pupil hand contamination in Western Kenya: a cluster randomized trial. Am J Trop Med Hyg 87: 385-393.
20. Gruber JS, Reygadas F, Arnold BF, Ray I, Nelson K, et al. (2013) A stepped wedge, cluster-randomized trial of a household UV-disinfection and safe storage drinking water intervention in rural Baja California Sur, Mexico. Am J Trop Med Hyg 89: 238-245.
21. The PLoS Medicine Editors (2009) Clean water should be recognized as a human right. PLoS Med 6: e1000102.
22. Pink R, (2012) Child rights, right to water and sanitation, and human security. Health Hum Rights 14: E78-E87.
23. Luh J, Baum R, Bartram J, (2013) Equity in water and sanitation: developing an index to measure progressive realization of the human right. Int J Hyg Environ Health 216: 662-671.
24. Emerson P, Kollmann M, MacArthur C, Bush S, Haddad D, (2012) SAFE strategy for blinding trachoma addresses sanitation, the other half of MDG7. Lancet 380: 27-28.
25. Esrey SA, Potash JB, Roberts L, Shiff C, (1991) Effects of improved water supply and sanitation on ascariasis, diarrhoea, dracunculiasis, hookworm infection, schistosomiasis, and trachoma. Bull World Health Organ 69: 609-621.
26. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, et al. (2012) Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med 9: e1001162.
27. Freeman MC, Clasen T, Brooker S, Akoko D, Rheingans R, (2013) The impact of a school-based hygiene, water quality and sanitation intervention on soil-transmitted helminth re-infection: a cluster-randomized trial. Am J Trop Med Hyg 89: 875-883.
28. Freeman MC, Ogden S, Jacobson J, Abbott D, Addiss DG, et al. (2013) Integration of water, sanitation, and hygiene for the prevention and control of neglected tropical diseases: a rationale for inter-sectoral collaboration. PLoS Negl Trop Dis 7: e2439.
29. van Hest R, Grant A, Abubakar I, (2011) Quality assessment of capture-recapture studies in resource-limited countries. Trop Med Int Health 16: 1019-1041.
30. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, et al. (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283: 2008-2012.
31. Moher D, Liberati A, Tetzlaff J, Altman DG, (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6: e1000097.
32. Asaolu SO, Ofoezie IE, (2003) The role of health education and sanitation in the control of helminth infections. Acta Trop 86: 283-294.
33. Ram PK, Halder AK, Granger SP, Jones T, Hall P, et al. (2010) Is structured observation a valid technique to measure handwashing behavior? Use of acceleration sensors embedded in soap to assess reactivity to structured observation. Am J Trop Med Hyg 83: 1070.
34. WHO (2006) Core Questions on Drinking-Water and Sanitation for Household Surveys: World Health Organization. 24 p.
35. WHO, UNICEF (2012) Progress on sanitation and drinking-water 2012 update. Geneva; New York: World Health Organization; Unicef.
36. DerSimonian R, Laird N, (1986) Meta-analysis in clinical trials. Control Clin Trials 7: 177-188.
37. Reeves B, Deeks J, Higgins J, Wells G (2008) Chapter 13: Including non-randomized studies. Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions. 1st edition. Chichester (UK); Hoboken (New Jersey): Wiley. pp. 672.
38. Kawai K, Saathoff E, Antelman G, Msamanga G, Fawzi WW, (2009) Geophagy (soil-eating) in relation to anemia and helminth infection among HIV-infected pregnant women in Tanzania. Am J Trop Med Hyg 80: 36-43.
39. Guyatt GH, Oxman AD, Schünemann HJ, Tugwell P, Knottnerus A, (2011) GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology. J Clin Epidemiol 64: 380-382.
40. Balshem H, Helfand M, Schünemann HJ, Oxman AD, Kunz R, et al. (2011) GRADE guidelines: 3. Rating the quality of evidence. J Clin Epidemiol 64: 401-406.
41. Guyatt GH, Oxman AD, Vist G, Kunz R, Brozek J, et al. (2011) GRADE guidelines: 4. Rating the quality of evidence-study limitations (risk of bias). J Clin Epidemiol 64: 407-415.
42. Higgins JP, Green S (2008) Cochrane handbook for systematic reviews of interventions: Wiley Online Library.
43. Downs SH, Black N, (1998) The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health 52: 377-384.
44. Wells G, Shea B, O'Connell D, Peterson J, Welch V, et al. (2008) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
45. Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, et al. (2011) GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol 64: 383-394.
46. Deeks J, Higgins J, Altman D (2008) Chapter 9: Analysing data and undertaking meta-analyses. Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions. 1st edition. Chichester (UK); Hoboken (New Jersey): Wiley. pp. 672.
47. Higgins JP, Thompson SG, (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21: 1539-1558.
48. Egger M, Davey Smith G, Schneider M, Minder C, (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629-634.
49. Davies HTO, Crombie IK, Tavakoli M, (1998) When can odds ratios mislead? BMJ 316: 989-991.
50. Manun'Ebo M, Cousens S, Haggerty P, Kalengaie M, Ashworth A, et al. (1997) Measuring hygiene practices: a comparison of questionnaires with direct observations in rural Zaire. Trop Med Int Health 2: 1015-1021.
51. Curtis V, Cousens S, Mertens T, Traore E, Kanki B, et al. (1993) Structured observations of hygiene behaviours in Burkina Faso: validity, variability, and utility. Bull World Health Organ 71: 23-32.
52. Jenner EA, Fletcher BC, Watson P, Jones FA, Miller L, et al. (2006) Discrepancy between self-reported and observed hand hygiene behaviour in healthcare professionals. J Hosp Infect 63: 418-422.
53. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, et al. (2012) Soil transmitted helminths and schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. Parasitol Int 61: 101-106.
54. Curtale F, Pezzotti P, Sharbini AL, Al Maadat H, Ingrosso P, et al. (1998) Knowledge, perceptions and behaviour of mothers toward intestinal helminths in Upper Egypt: Implications for control. Health Policy Plan 13: 423-432.
55. Quihui L, Valencia ME, Crompton DW, Phillips S, Hagan P, et al. (2006) Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in Mexican rural schoolchildren. Vet Immunol Immunopathol 114: 135-148.
56. Nematian J, Nematian E, Gholamrezanezhad A, Asgari AA, (2004) Prevalence of intestinal parasitic infections and their relation with socio-economic factors and hygienic habits in Tehran primary school students. Acta Trop 92: 179-186.
57. Carneiro FF, Cifuentes E, Tellez-Rojo MM, Romieu I, (2002) The risk of Ascaris lumbricoides infection in children as an environmental health indicator to guide preventive activities in Caparao and Alto Caparao, Brazil. Rev Saude Publica 36: 69-74.
58. Alyousefi NA, Mahdy MAK, Mahmud R, Lim YAL, (2011) Factors associated with high prevalence of intestinal protozoan infections among patients in Sana'a city, Yemen. PLoS ONE 6: e22044.
59. Ruiz Lopes FM, Goncalves DD, Dos Reis CR, Bregano RM, Filho FA, et al. (2006) Occurrence of enteroparasitosis in schoolchildren of the municipal district of Jataizinho, State of Parana, Brazil. Acta Scientiarum- Health Sciences 28: 107-111.
60. Alaofe H, Zee J, Dossa R, O'Brien HT, (2008) Intestinal parasitic infections in adolescent girls from two boarding schools in southern Benin. Trans R Soc Trop Med Hyg 102: 653-661.
61. Chirdan OO, Akosu JT, Adah SO, (2010) Intestinal parasites in children attending day care centers in Jos, Central Nigeria. Niger J Med 19: 219-222.
62. Escobedo AA, Canete R, Nunez FA, (2008) Prevalence, risk factors and clinical features associated with intestinal parasitic infections in children from San Juan y Martinez, Pinar del Rio, Cuba. West Indian Med J 57: 377-382.
63. Krause RJ, Koski KG, Scott ME, (2012) Evidence that multisector food security intervention program in rural panama reduces hookworm infection in preschool children. Am J Trop Med Hyg 87: 341.
64. Worrell CM, Davis SM, Wiegand RE, Lopez G, Cosmas L, et al. (2012) Water- and sanitation-related risk factors for soil-transmitted helminth infection in urban school- and preschool-aged children in Kibera, Nairobi. Am J Trop Med Hyg 87: 380-381.
65. Chongsuvivatwong V, Pas-Ong S, McNeil D, Geater A, Duerawee M, (1996) Predictors for the risk of hookworm infection: experience from endemic villages in southern Thailand. Trans R Soc Trop Med Hyg 90: 630-633.
66. Nasr NA, Al-Mekhlafi HM, Ahmed A, Roslan MA, Bulgiba A, (2013) Towards an effective control programme of soil-transmitted helminth infections among Orang Asli in rural Malaysia. Part 1: prevalence and associated key factors. Parasit Vectors 6: 27.
67. Cundill B, Alexander N, Bethony JM, Diemert D, Pullan RL, et al. (2011) Rates and intensity of re-infection with human helminths after treatment and the influence of individual, household, and environmental factors in a Brazilian community. Parasitology 138: 1406-1416.
68. Kounnavong S, Vonglokham M, Houamboun K, Odermatt P, Boupha B, (2011) Soil-transmitted helminth infections and risk factors in preschool children in southern rural Lao People's Democratic Republic. Trans R Soc Trop Med Hyg 105: 160-166.
69. Quintero K, Duran C, Duri D, Medina F, Garcia J, et al. (2012) Household social determinants of ascariasis and trichuriasis in North Central Venezuela. International Health 4: 103-110.
70. Belyhun Y, Medhin G, Amberbir A, Erko B, Hanlon C, et al. (2010) Prevalence and risk factors for soil-transmitted helminth infection in mothers and their infants in Butajira, Ethiopia: a population based study. BMC Public Health 10: 21.
71. Matthys B, Tschannen AB, Tian-Bi NT, Comoe H, Diabate S, et al. (2007) Risk factors for Schistosoma mansoni and hookworm in urban farming communities in western Cote d'Ivoire. Trop Med Int Health 12: 709-723.
72. Hall A, Conway DJ, Anwar KS, Rahman ML, (1994) Strongyloides stercoralis in an urban slum community in Bangladesh: factors independently associated with infection. Trans R Soc Trop Med Hyg 88: 527-530.
73. Hughes RG, Sharp DS, Hughes MC, Akau'ola S, Heinsbroek P, et al. (2004) Environmental influences on helminthiasis and nutritional status among Pacific schoolchildren. Int J Environ Health Res 14: 163-177.
74. Worrell C, Davis S, Wiegand R, Lopez G, Odero K, et al. (2013) Water, sanitation, and hygiene-related risk factors for soil-transmitted helminth infection in urban school- and pre-school-aged children in Kibera, Nairobi 2013; ASTMH 61st Annual Meeting; 11-15 November 2013, Atlanta.
75. Xu LQ, Xiao DH, Zhou CH, Zhang XQ, Lan SG, et al. (2001) [On cleanliness of hands in diminution of Ascaris lumbricoides infection in children]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi [Chinese journal of parasitology & parasitic diseases] 19: 294-297.
76. Bieri FA, Gray DJ, Williams GM, Raso G, Li YS, et al. (2013) Health-education package to prevent worm infections in Chinese schoolchildren. N Engl J Med 368: 1603-1612.
77. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M, (2013) Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis 7: e2397.
78. Balen J, Raso G, Li YS, Zhao ZY, Yuan LP, et al. (2011) Risk factors for helminth infections in a rural and a peri-urban setting of the Dongting Lake area, People's Republic of China. Int J Parasitol 41: 1165-1173.
79. Steinmann P, Usubalieva J, Imanalieva C, Minbaeva G, Stefiuk K, et al. (2010) Rapid appraisal of human intestinal helminth infections among schoolchildren in Osh oblast, Kyrgyzstan. Acta Trop 116: 178-184.
80. Hohmann H, Panzer S, Phimpachan C, Southivong C, Schelp FP, (2001) Relationship of intestinal parasites to the environment and to behavioral factors in children in the Bolikhamxay Province of Lao PDR. Southeast Asian J Trop Med Public Health 32: 4-13.
81. Nishiura H, Imai H, Nakao H, Tsukino H, Changazi MA, et al. (2002) Ascaris lumbricoides among children in rural communities in the Northern Area, Pakistan: prevalence, intensity, and associated socio-cultural and behavioral risk factors. Acta Trop 83: 223-231.
82. Young SL, Dave G, Farag TH, Said MA, Khatib MR, et al. (2007) Geophagia is not associated with Trichuris or hookworm transmission in Zanzibar, Tanzania. Trans R Soc Trop Med Hyg 101: 766-772.
83. Nwaneri DU, Ibadin MO, Ofovwe GE, Sadoh AE, (2012) Intestinal helminthiasis in children with chronic neurological disorders in Benin City, Nigeria: intensity and behavioral risk factors. World J Pediatr 10.1007/s12519-012-0394-9.
84. Narain K, Rajguru SK, Mahanta J, (2000) Prevalence of Trichuris trichiura in relation to socio-economic & behavioural determinants of exposure to infection in rural Assam. Indian J Med Res 112: 140-146.
85. Alvarado BE, Vasquez LR, (2006) [Social determinants, feeding practices and nutritional consequences of intestinal parasitism in young children]. Biomedica 26: 82-94.
86. Dumba R, Kaddu JB, Wabwire-Mangen F, (2013) Design and implementation of participatory hygiene and sanitation transformation (PHAST) as a strategy to control soil-transmitted helminth infections in Luweero, Uganda. Afr Health Sci 13: 512-517.
87. Khieu V, Schar F, Marti H, Sayasone S, Duong S, et al. (2013) Diagnosis, treatment and risk factors of Strongyloides stercoralis in schoolchildren in Cambodia. PLoS Negl Trop Dis 7: e2035.
88. Yori PP, Kosek M, Gilman RH, Cordova J, Bern C, et al. (2005) Seroepidemiology of strongyloidiasis in the Peruvian Amazon. Cad Saude Publica 21: 1778-1784.
89. Knopp S, Stothard JR, Rollinson D, Mohammed KA, Khamis IS, et al. (2013) From morbidity control to transmission control: time to change tactics against helminths on Unguja Island, Zanzibar. Acta Trop 128: 412-422.
90. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M, (2013) Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis 7: e2397.
91. Hall A, Hewitt G, Tuffrey V, de Silva N, (2008) A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr 4 Suppl 1: 118-236.
92. Chipeta MG, Ngwira B, Kazembe LN, (2013) Analysis of Schistosomiasis haematobium infection prevalence and intensity in Chikhwawa, Malawi: an application of a two part model. PLoS Negl Trop Dis 7: e2131.
93. Nodtvedt A, Dohoo I, Sanchez J, Conboy G, DesCjteaux L, et al. (2002) The use of negative binomial modelling in a longitudinal study of gastrointestinal parasite burdens in Canadian dairy cows. Canadian journal of veterinary research = Revue canadienne de recherche veterinaire 66: 249-257.
94. Vounatsou P, Raso G, Tanner M, N'Goran E K, Utzinger J, (2009) Bayesian geostatistical modelling for mapping schistosomiasis transmission. Parasitology 136: 1695-1705.
95. Wang X, Hunter PR, (2010) A systematic review and meta-analysis of the association between self-reported diarrheal disease and distance from home to water source. Am J Trop Med Hyg 83: 582-584.
96. Pickering AJ, Davis J, (2012) Freshwater availability and water fetching distance affect child health in sub-saharan Africa. Environ Sci Technol 46: 2391-2397.
97. Wordemann M, Polman K, Menocal Heredia LT, Diaz RJ, Madurga AM, et al. (2006) Prevalence and risk factors of intestinal parasites in Cuban children. Trop Med Int Health 11: 1813-1820.
98. Johnston RB, Halder AK, Huda TMN, Akhter S, Huque MR, et al. (2009) Monitoring impacts of WASH interventions: The case of SHEWAB; 18-22 May 2009; United Nations Conference Centre, Addis Ababa, Ethiopia. Loughborough University of Technology. pp. 352-359.
99. Dumba R, Kaddu JB, Wabwire Mangen F, (2008) Intestinal helminths in Luweero district, Uganda. Afr Health Sci 8: 90-96.
100. Harbord RM, Egger M, Sterne JA, (2006) A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 25: 3443-3457.
101. 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. Cochrane Database Syst Rev 11: CD000371.
102. Awasthi S, Peto R, Read S, Richards SM, Pande V, et al. (2013) Population deworming every 6 months with albendazole in 1 million pre-school children in north India: DEVTA, a cluster-randomised trial. Lancet 381: 1478-1486.
103. Anderson RM, Truscott JE, Pullan RL, Brooker SJ, Hollingsworth TD, (2013) How effective is school-based deworming for the community-wide control of soil-transmitted helminths? PLoS Negl Trop Dis 7: e2027.
104. Addiss DG, (2013) Epidemiologic models, key logs, and realizing the promise of WHA 54.19. PLoS Negl Trop Dis 7: e2092.
105. Montresor A, Gabrielli AF, Engels D, Daumerie D, Savioli L, (2013) Has the NTD community neglected evidence-based policy? PLOS NTDs 2013 expert commentary of the viewpoint by Nagpal S, Sinclair D, Garner P. PLoS Negl Trop Dis 7: e2299.
106. Nagpal S, Sinclair D, Garner P, (2013) Has the NTD community neglected evidence-based policy? PLoS Negl Trop Dis 7: e2238.
107. Spiegel JM, Dharamsi S, Wasan KM, Yassi A, Singer B, et al. (2010) Which new approaches to tackling neglected tropical diseases show promise? PLoS Med 7: e1000255.
108. Clasen T, Boisson S, Routray P, Cumming O, Jenkins M, et al. (2012) The effect of improved rural sanitation on diarrhoea and helminth infection: design of a cluster-randomized trial in Orissa, India. Emer Themes Epidemiol 9: 7.
109. Nakagawa J, Ehrenberg JP, Nealon J, Furst T, Aratchige P, et al. (2013) Towards effective prevention and control of helminth neglected tropical diseases in the Western Pacific Region through multi-disease and multi-sectoral interventions. Acta Trop In press.
110. Singer BH, de Castro MC, (2007) Bridges to sustainable tropical health. Proc Natl Acad Sci U S A 104: 16038-16043.
111. Ahmed A, Al-Mekhlafi HM, Choy SH, Ithoi I, Al-Adhroey AH, et al. (2011) The burden of moderate-to-heavy soil-transmitted helminth infections among rural malaysian aborigines: an urgent need for an integrated control programme. Parasit Vectors 4: 242.
112. Wang X, Zhang L, Luo R, Wang G, Chen Y, et al. (2012) Soil-transmitted helminth infections and correlated risk factors in preschool and school-aged children in rural southwest China. PLoS ONE 7: e45939.
113. Aimpun P, Hshieh P, (2004) Survey for intestinal parasites in Belize, Central America. Southeast Asian J Trop Med Public Health 35: 506-511.
114. Roy E, Hasan KZ, Haque R, Fazlul Haque AKM, Siddique AK, et al. (2011) Patterns and risk factors for helminthiasis in rural children aged under 2 in Bangladesh. SAJCH South African Journal of Child Health 5: 78-84.
115. Pham-Duc P, Nguyen-Viet H, Hattendorf J, Zinsstag J, Phung-Dac C, et al. (2013) Ascaris lumbricoides and Trichuris trichiura infections associated with wastewater and human excreta use in agriculture in Vietnam. Parasitol Int 62: 172-180.
116. Ivan E, Crowther NJ, Mutimura E, Osuwat LO, Janssen S, et al. (2013) Helminthic infections rates and malaria in HIV-infected pregnant women on anti-retroviral therapy in Rwanda. PLoS Negl Trop Dis 7: e2380.
117. Morales-Espinoza EM, Sanchez-Perez HJ, Garcia-Gil Mdel M, Vargas-Morales G, Mendez-Sanchez JD, et al. (2003) Intestinal parasites in children, in highly deprived areas in the border region of Chiapas, Mexico. Salud Publica Mex 45: 379-388.
118. Traub RJ, Robertson ID, Irwin P, Mencke N, Andrew Thompson RC, (2004) The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Trop Med Int Health 9: 688-701.
119. Fonseca EO, Teixeira MG, Barreto ML, Carmo EH, Costa Mda C, (2010) [Prevalence and factors associated with geohelminth infections in children living in municipalities with low HDI in North and Northeast Brazil]. Cad Saude Publica 26: 143-152.
120. Stothard JR, Imison E, French MD, Sousa-Figueiredo JC, Khamis IS, et al. (2008) Soil-transmitted helminthiasis among mothers and their pre-school children on Unguja Island, Zanzibar with emphasis upon ascariasis. Parasitology 135: 1447-1455.
121. Do TT, Molbak K, Phung DC, Dalsgaard A, (2007) Helminth infections among people using wastewater and human excreta in peri-urban agriculture and aquaculture in Hanoi, Vietnam. Trop Med Int Health 12 Suppl 2: 82-90.
122. Hidayah NI, Teoh ST, Hillman E, (1997) Socio-environmental predictors of soil-transmitted helminthiasis in a rural community in Malaysia. Southeast Asian J Trop Med Public Health 28: 811-815.
123. Asaolu SO, Ofoezie IE, Odumuyiwa PA, Sowemimo OA, Ogunniyi TA, (2002) Effect of water supply and sanitation on the prevalence and intensity of Ascaris lumbricoides among pre-school-age children in Ajebandele and Ifewara, Osun State, Nigeria. Trans R Soc Trop Med Hyg 96: 600-604.
124. Corrales LF, Izurieta R, Moe CL, (2006) Association between intestinal parasitic infections and type of sanitation system in rural El Salvador. Trop Med Int Health 11: 1821-1831.
125. Knopp S, Stothard JR, Rollinson D, Mohammed KA, Khamis IS, et al. (2011) From morbidity control to transmission control: time to change tactics against helminths on Unguja Island, Zanzibar. PLoS Genet 7: e1001384.
126. Schmidlin T, Hurlimann E, Silue KD, Yapi RB, Houngbedji C, et al. (2013) Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Cote d'Ivoire. PLoS ONE 8: e65722.
127. Mahmud MA, Spigt M, Bezabih AM, Pavon IL, Dinant GJ, et al. (2013) Risk factors for intestinal parasitosis, anaemia, and malnutrition among school children in Ethiopia. Pathog Glob Health 107: 58-65.
128. Mihrshahi S, Casey GJ, Montresor A, Phuc TQ, Thach DTC, et al. (2009) The effectiveness of 4 monthly albendazole treatment in the reduction of soil-transmitted helminth infections in women of reproductive age in Viet Nam. Int J Parasitol 39: 1037-1043.
129. Parajuli RP, Umezaki M, Watanabe C, (2009) Behavioral and nutritional factors and geohelminth infection among two ethnic groups in the Terai region, Nepal. Am J Hum Biol 21: 98-104.
130. Gunawardena GS, Karunaweera ND, Ismail MM, (2004) Socio-economic and behavioural factors affecting the prevalence of Ascaris infection in a low-country tea plantation in Sri Lanka. Ann Trop Med Parasitol 98: 615-621.
131. Balen J, Raso G, Li YS, Zhao ZY, Yuan LP, et al. (2011) Risk factors for helminth infections in a rural and a peri-urban setting of the Dongting Lake area, People's Republic of China. Int J Parasitol 41: 1165-1173.
132. Humphries D, Mosites E, Otchere J, Twum WA, Woo L, et al. (2011) Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. Am J Trop Med Hyg 84: 792-800.
133. Jiraanankul V, Aphijirawat W, Mungthin M, Khositnithikul R, Rangsin R, et al. (2011) Incidence and risk factors of hookworm infection in a rural community of central Thailand. Am J Trop Med Hyg 84: 594-598.
134. Phiri K, Whitty CJ, Graham SM, Ssembatya-Lule G, (2000) Urban/rural differences in prevalence and risk factors for intestinal helminth infection in southern Malawi. Folia Parasitol (Praha) 47: 111-117.
135. Rücker G, Schwarzer G, Carpenter J, (2008) Arcsine test for publication bias in meta-analyses with binary outcomes. Stat Med 27: 746-763.
136. Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L, (2006) Comparison of two methods to detect publication bias in meta-analysis. JAMA 295: 676-680.
137. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, et al. (2011) Soil transmitted helminths and schistosoma mansoni infections among school children in zarima town, northwest Ethiopia. BMC Infect Dis 11.
138. Al-Mekhlafi MS, Atiya AS, Lim YA, Mahdy AK, Ariffin WA, et al. (2007) An unceasing problem: soil-transmitted helminthiases in rural Malaysian communities. Southeast Asian J Trop Med Public Health 38: 998-1007.
139. Al-Mekhlafi HM, Surin J, Atiya AS, Ariffin WA, Mohammed Mahdy AK, et al. (2008) Pattern and predictors of soil-transmitted helminth reinfection among aboriginal schoolchildren in rural Peninsular Malaysia. Acta Trop 107: 200-204.
140. Amahmid O, Bouhoum K, (2005) Assessment of the health hazards associated with wastewater reuse: transmission of geohelminthic infections (Marrakech, Morocco). Ann Agric Environ Med 12: 35-38.
141. Awasthi S, Verma T, Kotecha P, Venkatesh V, Joshi V, et al. (2008) Prevalence and risk factors associated with worm infestation in pre-school children (6-23 months) in selected blocks of Uttar Pradesh and Jharkhand, India. Indian J Med Sci 62: 484-491.
142. Barreto ML, Genser B, Strina A, Teixeira MG, Assis AMO, et al. (2010) Impact of a citywide sanitation program in Northeast Brazil on intestinal parasites infection in young children. Environ Health Perspect 118: 1637-1642.
143. Basualdo JA, Cordoba MA, de Luca MM, Ciarmela ML, Pezzani BC, et al. (2007) Intestinal parasitoses and environmental factors in a rural population of Argentina, 2002-2003. Bull Soc Pathol Exot 100: 174-175.
144. Belo S, Rompao H, Goncalves L, Gracio MA, (2005) Prevalence, behavioural and social factors associated with Schistosoma intercalatum and geohelminth infections in Sao Tome and Principe. Parassitologia 47: 227-231.
145. Carneiro FF, Cifuentes E, Tellez-Rojo MM, Romieu I, (2002) The risk of Ascaris lumbricoides infection in children as an environmental health indicator to guide preventive activities in Caparao and Alto Caparao, Brazil. Bull World Health Organ 80: 40-46.
146. Ellis MK, Raso G, Li YS, Rong Z, Chen HG, et al. (2007) Familial aggregation of human susceptibility to co- and multiple helminth infections in a population from the Poyang Lake region, China. Int J Parasitol 37: 1153-1161.
147. Ensink JH, van der Hoek W, Mukhtar M, Tahir Z, Amerasinghe FP, (2005) High risk of hookworm infection among wastewater farmers in Pakistan. Proc Natl Acad Sci U S A 102: 12449-12454.
148. Farook MU, Sudharmini S, Remadevi S, Vijayakumar K, (2002) Intestinal helminthic infestations among tribal populations of Kottoor and Achankovil areas in Kerala (India). J Commun Dis 34: 171-178.
149. Ferreira MU, Ferreira CD, Monteiro CA, (2000) Secular trends in child intestinal parasitic diseases in S. Paulo city, Brazil (1984-1996). Rev Saude Publica 34: 73-82.
150. Geissler PW, Mwaniki D, Thiong'o F, Friis H, (1998) Geophagy as a risk factor for geohelminth infections: A longitudinal study of Kenyan primary schoolchildren. Trans R Soc Trop Med Hyg 92: 7-11.
151. Glickman LT, Camara AO, Glickman NW, McCabe GP, (1999) Nematode intestinal parasites of children in rural Guinea, Africa: prevalence and relationship to geophagia. Int J Epidemiol 28: 169-174.
152. Gunawardena GS, Karunaweera ND, Ismail MM, (2005) Effects of climatic, socio-economic and behavioural factors on the transmission of hookworm (Necator americanus) on two low-country plantations in Sri Lanka. Ann Trop Med Parasitol 99: 601-609.
153. Gunawardena K, Kumarendran B, Ebenezer R, Gunasingha MS, Pathmeswaran A, et al. (2011) Soil-transmitted helminth infections among plantation sector schoolchildren in Sri Lanka: prevalence after ten years of preventive chemotherapy. PLoS Negl Trop Dis 5: e1341.
154. Guo-Fei W, Ying-Dan C, Chang-Hai Z, Ting-Jun Z, (2011) [Analysis of influencing factors of Trichuris trichiura infection in demonstration plots of comprehensive control of parasitic diseases]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi [Chinese journal of schistosomiasis control] 23: 495-500.
155. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M, (2011) Exploring determinants of hookworm infection in peruvian schoolchildren using a gender analysis. Am J Epidemiol 173: S224.
156. Habbari K, Tifnouti A, Bitton G, Mandil A, (2001) Geohelminthic infections associated with raw wastewater reuse for agricultural purposes in Beni-Mellal, Morocco. J Parasitol 87: 169-172.
157. Halpenny CM, Paller C, Koski KG, Valdes VE, Scott ME, (2013) Regional, household and individual factors that influence soil transmitted helminth reinfection dynamics in preschool children from rural indigenous Panama. PLoS Negl Trop Dis 7: e2070.
158. Henry FJ, (1988) Reinfection with Ascaris lumbricoides after chemotherapy: a comparative study in three villages with varying sanitation. Ann Parasitol Hum Comp 63: 448-454.
159. Huat LB, Mitra AK, Noor Jamil NI, Dam PC, Jan Mohamed HJ, et al. (2012) Prevalence and risk factors of intestinal helminth infection among rural Malay children. Journal of Global Infectious Diseases 4: 10-14.
160. Koura GK, Briand V, Massougbodji A, Cot M, Garcia A, (2011) Prevalence and risk factors for soil-transmitted helminth infection in beninese women during pregnancy. Am J Epidemiol 173: S225.
161. Lee VJ, Ong A, Lee NG, Lee WT, Fong KL, et al. (2007) Hookworm infections in Singaporean soldiers after jungle training in Brunei Darussalam. Vet Parasitol 150: 128-138 Epub 2007 Oct 2024.
162. Luoba AI, Geissler PW, Estambale B, Ouma JH, Alusala D, et al. (2005) Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya. Trop Med Int Health 10: 220-227.
163. Moraes LR, Cancio JA, Cairncross S, (2004) Impact of drainage and sewerage on intestinal nematode infections in poor urban areas in Salvador, Brazil. Trans R Soc Trop Med Hyg 98: 197-204.
164. Moraes LRS, (2007) Household solid waste bagging and collection and their health implications for children living in outlying urban settlements in Salvador, Bahia State, Brazil. Cad Saude Publica 23: S643-S649.
165. Nguyen PH, Nguyen KC, Nguyen TD, Le MB, Bern C, et al. (2006) Intestinal helminth infections among reproductive age women in Vietnam: prevalence, co-infection and risk factors. Southeast Asian J Trop Med Public Health 37: 865-874.
166. Norhayati M, Oothuman P, Fatmah MS, (1999) Some risk factors of Ascaris and Trichuris infection in Malaysian aborigine (Orang Asli) children. Med J Malaysia 54: 96-101.
167. Olsen A, Samuelsen H, Onyango-Ouma W, (2001) A study of risk factors for intestinal helminth infections using epidemiological and anthropological approaches. J Biosoc Sci 33: 569-584.
168. Ortiz Valencia LI, Drumond Fortes BDPM, De Andrade Medronho R, (2005) Spatial Ascariasis risk estimation using socioeconomic variables. Int J Environ Health Res 15: 411-424.
169. Riess H, Clowes P, Kroidl I, Kowuor DO, Nsojo A, et al. (2013) Hookworm infection and environmental factors in mbeya region, Tanzania: a cross-sectional, population-based study. PLoS Negl Trop Dis 7: e2408.
170. Rísquez PA, Márquez TMD, Quintero PGdC, Ramírez DJP, Requena JG, et al. (2010) Condiciones higiénico-sanitarias como factores de riesgo para las parasitosis intestinales en una comunidad rural venezolana. Rev Fac Med (Caracas) 33: 151-158.
171. Saathoff E, Olsen A, Kvalsvig JD, Geissler WP, (2002) Geophagy and its association with geohelminth infection in rural schoolchildren from northern KwaZulu-Natal, South Africa. Trans R Soc Trop Med Hyg 96: 485-490.
172. Scolari C, Torti C, Beltrame A, Matteelli A, Castelli F, et al. (2000) Prevalence and distribution of soil-transmitted helminth (STH) infections in urban and indigenous schoolchildren in Ortigueira, State of Parana, Brasil: implications for control. Rev Inst Med Trop Sao Paulo 42: 115-117.
173. Sherkhonov T, Yap P, Mammadov S, Sayfuddin K, Martinez P, et al. (2013) National intestinal helminth survey among schoolchildren in Tajikistan: prevalences, risk factors and perceptions. Acta Trop 126: 93-98.
174. Soares Magalhaes RJ, Barnett AG, Clements ACA, (2011) Geographical analysis of the role of water supply and sanitation in the risk of helminth infections of children in West Africa. Proc Natl Acad Sci U S A 108: 20084-20089.
175. Steenhard NR, Ornbjerg N, Molbak K, (2009) Concurrent infections and socioeconomic determinants of geohelminth infection: a community study of schoolchildren in periurban Guinea-Bissau. Trans R Soc Trop Med Hyg 103: 839-845.
176. Teixeira JC, Heller L, (2004) Fatores ambientais associados às helmintoses intestinais em áreas de assentamento subnormal, Juiz de Fora, MG. Eng sanit ambient 9: 301-305.
177. Trang DT, van der Hoek W, Cam PD, Vinh KT, Hoa NV, et al. (2006) Low risk for helminth infection in wastewater-fed rice cultivation in Vietnam. East Mediterr Health J 12: 137-143.
178. Ugbomoiko US, Dalumo V, Ofoezie IE, Obiezue RNN, (2009) Socio-environmental factors and ascariasis infection among school-aged children in Ilobu, Osun State, Nigeria. Trans R Soc Trop Med Hyg 103: 223-228.
179. Walker M, Hall A, Basanez MG, (2011) Individual predisposition, household clustering and risk factors for human infection with Ascaris lumbricoides: new epidemiological insights. PLoS Negl Trop Dis 5: e1047.
180. Yajima A, Jouquet P, Do TD, Dang TC, Tran CD, et al. (2009) High latrine coverage is not reducing the prevalence of soil-transmitted helminthiasis in Hoa Binh province, Vietnam. Parasitol Res 104: 321-328.