Effect of sanitation on soil-transmitted helminth infection: Systematic review and meta-analysis

PLoS Medicine

Volumn 9, Issue 1, 2012, Pages

  Ziegelbauer, Kathrin ^a,b   Speich, Benjamin ^a,b   Mäusezahl, Daniel ^a,b   Bos, Robert ^c   Keiser, Jennifer ^a,b   Utzinger, Jürg ^a,b  

^a SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c WORLD HEALTH ORGANIZATION   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ASCARIS LUMBRICOIDES; DATA BASE; EMBASE; FECES; HEALTH EDUCATION; HELMINTHIASIS; HOOKWORM; HOUSEHOLD; HUMAN; INFECTION PREVENTION; INFORMATION PROCESSING; MEDLINE; PARASITE TRANSMISSION; QUALITY CONTROL; REVIEW; RISK REDUCTION; SANITATION; SOIL TRANSMITTED HELMINTH INFECTION; SYSTEMATIC REVIEW; TRICHURIS; URINE; WASTE DISPOSAL; WEB OF SCIENCE; WORLD HEALTH ORGANIZATION; ANIMAL; ASCARIASIS; DISEASE TRANSMISSION; HOOKWORM INFECTION; META ANALYSIS; NEMATODE; NEMATODIASIS; PARASITOLOGY; PHYSIOLOGY; SOIL; TRICHURIASIS;

ANCYLOSTOMATOIDEA; ANIMALS; ASCARIASIS; ASCARIS LUMBRICOIDES; HOOKWORM INFECTIONS; HUMANS; NEMATODA; NEMATODE INFECTIONS; SANITATION; SOIL; TRICHURIASIS; TRICHURIS;

EID: 84856472304     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.1001162     Document Type: Review

References (96)

1. Horton J, (2003) Human gastrointestinal helminth infections: are they now neglected diseases? Trends Parasitol 19: 527-531.
2. Utzinger J, Keiser J, (2004) Schistosomiasis and soil-transmitted helminthiasis: common drugs for treatment and control. Expert Opin Pharmacother 5: 263-285.
3. 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.
4. 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.
5. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, et al. (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 1311-1321.
6. Horton J, (2003) Global anthelmintic chemotherapy programs: learning from history. Trends Parasitol 19: 405-409.
7. Utzinger J, Bergquist R, Olveda R, Zhou XN, (2010) Important helminth infections in Southeast Asia: diversity, potential for control and prospects for elimination. Adv Parasitol 72: 1-30.
8. Chan MS, (1997) The global burden of intestinal nematode infections-fifty years on. Parasitol Today 13: 438-443.
9. World Health Organization (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Tech Rep Ser 912: 1-57.
10. Hotez PJ, Molyneux DH, Fenwick A, Ottesen E, Ehrlich Sachs S, et al. (2006) Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Med 3: e102 doi:10.1371/journal.pmed.0030102.
11. Brooker S, Clements ACA, Bundy DAP, (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62: 221-261.
12. King CH, Bertino AM, (2008) Asymmetries of poverty: why global burden of disease valuations underestimate the burden of neglected tropical diseases. PLoS Negl Trop Dis 2: e209 doi:10.1371/journal.pntd.0000209.
13. World Health Organization (2006) Preventive chemotherapy in human helminthiasis: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers Geneva World Health Organization.
14. Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Ehrlich Sachs S, et al. (2007) Control of neglected tropical diseases. N Engl J Med 357: 1018-1027.
15. Singer BH, Castro MC, (2007) Bridges to sustainable tropical health. Proc Natl Acad Sci U S A 104: 16038-16043.
16. 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.
17. 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 doi:10.1371/journal.pmed.1000255.
18. Bartram J, Cairncross S, (2010) Hygiene, sanitation, and water: forgotten foundations of health. PLoS Med 7: e1000367 doi:10.1371/journal.pmed.1000367.
19. Mara D, Lane J, Scott B, Trouba D, (2010) Sanitation and health. PLoS Med 7: e1000363 doi:10.1371/journal.pmed.1000363.
20. Cort WW, Schapiro L, Stoll NR, (1929) A study of reinfection after treatment with hookworm and Ascaris in two villages in Panama. Am J Epidemiol 10: 614-625.
21. Khalil M, (1931) The pail closet as an efficient means of controlling human helminth infection as observed in Tura Prison, Egypt, with a discussion on the source of Ascaris infection. Ann Trop Med Parasitol 25: 35-54.
22. Stiles CW, (1939) Early history, in part esoteric, of the hookworm (uncinariasis) campaign in our southern United States. J Parasitol 25: 283-308.
23. Wang LD, Guo JG, Wu XH, Chen HG, Wang TP, et al. (2009) China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Trop Med Int Health 14: 1475-1483.
24. Schad GA, Rozeboom LE, (1976) Integrated control of helminths in human populations. Ann Rev Ecol Syst 7: 393-420.
25. Utzinger J, Bergquist R, Xiao SH, Singer BH, Tanner M, (2003) Sustainable schistosomiasis control-the way forward. Lancet 362: 1932-1934.
26. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, et al. (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283: 2008-2012.
27. 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.
28. Asaolu SO, Ofoezie IE, (2003) The role of health education and sanitation in the control of helminth infections. Acta Trop 86: 283-294.
29. Clasen TF, Bostoen K, Schmidt WP, Boisson S, Fung IC, et al. (2010) Interventions to improve disposal of human excreta for preventing diarrhoea. Cochrane Database Syst Rev 2010: CD007180.
30. Atkins D, Best D, Briss PA, Eccles M, Falck-Ytter Y, et al. (2004) Grading quality of evidence and strength of recommendations. BMJ 328: 1490.
31. Sterne JA, Egger M, Smith GD, (2001) Systematic reviews in health care: investigating and dealing with publication and other biases in meta-analysis. BMJ 323: 101-105.
32. DerSimonian R, Laird N, (1986) Meta-analysis in clinical trials. Control Clin Trials 7: 177-188.
33. 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.
34. Ensink JHJ, van der Hoek W, Mukhtar M, Tahir Z, Amerasinghe FP, (2005) High risk of hookworm infection among wastewater farmers in Pakistan. Trans R Soc Trop Med Hyg 99: 809-818.
35. 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.
36. 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.
37. 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.
38. Sun YD, Ma XY, Wang YS, Yang ZP, Xu FN, (2003) [Study on influence of improved latrine on intestinal parasite infections in rural populations.] Chin J Dis Control Prev 7: 326-328.
39. Toma A, Miyagi I, Kamimura K, Tokuyama Y, Hasegawa H, et al. (1999) Questionnaire survey and prevalence of intestinal helminthic infections in Barru, Sulawesi, Indonesia. Southeast Asian J Trop Med Public Health 30: 68-77.
40. 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.
41. 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.
42. 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. Trans R Soc Trop Med Hyg 103: 237-241.
43. Raja'a YA, Sulaiman SM, Mubarak JS, El-Bakri MM, Al-Adimi WH, et al. (2001) Some aspects in the control of schistosomosis and soil-transmitted helminthosis in Yemeni children. Saudi Med J 22: 428-432.
44. Trang DT, Molbak K, Cam PD, 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: 82-90.
45. 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. J Water Health 4: 321-331.
46. Erlanger TE, Sayasone S, Krieger GR, Kaul S, Sananikhom P, et al. (2008) Baseline health situation of communities affected by the Nam Theun 2 hydroelectric project in central Lao PDR and indicators for monitoring. Int J Environ Health Res 18: 223-242.
47. 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.
48. 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.
49. Stephenson LS, Crompton DWT, Latham MC, Arnold SE, Jansen AAJ, (1983) Evaluation of a four year project to control Ascaris infection in children in two Kenyan villages. J Trop Pediatr 29: 175-184.
50. Kightlinger LK, Seed JR, Kightlinger MB, (1998) Ascaris lumbricoides intensity in relation to environmental, socioeconomic, and behavioral determinants of exposure to infection in children from southeast Madagascar. J Parasitol 84: 480-484.
51. 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.
52. 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.
53. 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.
54. Jombo GT, Egah DZ, Akosu JT, (2007) Intestinal parasitism, potable water availability and methods of sewage disposal in three communities in Benue state, Nigeria: a survey. Ann Afr Med 6: 17-21.
55. 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 Côte d'Ivoire. Trop Med Int Health 12: 709-723.
56. 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.
57. Ugbomoiko US, Dalumo V, Ofoezie IE, Obiezue RN, (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.
58. Knopp S, Mohammed KA, Stothard JR, Khamis IS, Rollinson D, et al. (2010) Patterns and risk factors of helminthiasis and anemia in a rural and a peri-urban community in Zanzibar, in the context of helminth control programs. PLoS Negl Trop Dis 4: e681 doi:10.1371/journal.pntd.0000681.
59. Ilechukwu GC, Ilechukwu CG, Ozumba AN, Ojinnaka NC, Ibe BC, et al. (2010) Some behavioural risk factors for intestinal helminthiasis in nursery and primary school children in Enugu, south eastern Nigeria. Niger J Clin Pract 13: 288-293.
60. Holland CV, Taren DL, Crompton DWT, Nesheim MC, Sanjur D, et al. (1988) Intestinal helminthiases in relation to the socioeconomic environment of Panamanian children. Soc Sci Med 26: 209-213.
61. 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.
62. Wördemann M, Polman K, Diaz RJ, Heredia LTM, Madurga AMC, et al. (2006) The challenge of diagnosing atopic diseases: outcomes in Cuban children depend on definition and methodology. Allergy 61: 1125-1131.
63. Morales-Espinoza EM, Sanchez-Perez HJ, Garcia-Gil MDM, 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.
64. 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. Rev Inst Med Trop São Paulo 49: 251-255.
65. de Souza EA, da Silva-Nunes M, Malafronte RS, Muniz PT, Cardoso MA, et al. (2007) Prevalence and spatial distribution of intestinal parasitic infections in a rural Amazonian settlement, Acre State, Brazil. Cad Saude Publica 23: 427-434.
66. Torres P, Otth L, Montefusco A, Wilson G, Ramirez C, et al. (1997) [Infection by intestinal protozoa and helminths in schoolchildren from riverside sectors, with different fecal contamination levels, of Valdivia River, Chile.] Bol Chil Parasitol 52: 3-11.
67. Hagel I, Lynch NR, Perez M, Di Prisco MC, Lopez R, et al. (1993) Relationship between the degree of poverty and the IgE response to Ascaris infection in slum children. Trans R Soc Trop Med Hyg 87: 16-18.
68. Gloor RF, Breyley ER, Martinez IG, (1970) Hookworm infection in a rural Kentucky county. Am J Trop Med Hyg 19: 1007-1009.
69. 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.
70. Scott JA, Barlow CH, (1938) Limitations to the control of helminth parasites in Egypt by means of treatment and sanitation. Am J Epidemiol 27: 619-648.
71. Otto GF, Spindler LA, (1930) Effect of partial sanitation on infestation with intestinal parasites in southwest Virginia. South Med J 23: 556-559.
72. Schliessmann DJ, Atchley FO, Wilcomb MJ Jr, Welch SF, (1958) Relation of environmental factors to the occurrence of enteric diseases in areas of eastern Kentucky. Public Health Monogr 54: 1-33.
73. Katz N, Chaves A, Pellegrino J, (1972) A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop São Paulo 14: 397-400.
74. Hunter PR, MacDonald AM, Carter RC, (2010) Water supply and health. PLoS Med 7: e1000361 doi:10.1371/journal.pmed.1000361.
75. Cairncross S, Bartram J, Cumming O, Brocklehurst C, (2010) Hygiene, sanitation, and water: what needs to be done? PLoS Med 7: e1000365 doi:10.1371/journal.pmed.1000365.
76. United Nations (2010) MDG monitor: tracking the millennium development goals. Available: http://www.mdgmonitor.org/goal7.cfm. Accessed 18 August 2010.
77. Anonymous (2010) Water and sanitation become human rights, albeit turbidly. Lancet 376: 390.
78. Arfaa F, Sahba GH, Farahmandian I, Jalali H, (1977) Evaluation of the effect of different methods of control of soil-transmitted helminths in Khuzestan, southwest Iran. Am J Trop Med Hyg 26: 230-233.
79. Boot M, Cairncross S, (1993) Actions speak: the study of hygiene behaviour in water and sanitation projects The Hague IRC International Water and Sanitation Centre.
80. 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.
81. Cairncross S, (1987) Low-cost sanitation technology for the control of intestinal helminths. Parasitol Today 3: 94-98.
82. World Health Organization, United Nations Children's Fund (2010) Progress on sanitation and drinking water: 2010 update Geneva World Health Organization.
83. Stürchler D, Stahel E, Saladin K, Saladin B, (1980) Intestinal parasitoses in eight Liberian settlements: prevalences and community anthelminthic chemotherapy. Tropenmed Parasitol 31: 87-93.
84. Cairncross S, Blumenthal U, Kolsky P, Moraes L, Tayeh A, (1996) The public and domestic domains in the transmission of disease. Trop Med Int Health 1: 27-34.
85. Okun DA, (1988) The value of water supply and sanitation in development: an assessment. Am J Public Health 78: 1463-1467.
86. Grimes DA, Schulz KF, (2002) An overview of clinical research: the lay of the land. Lancet 359: 57-61.
87. 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.
88. 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.
89. Keiser J, Singer BH, Utzinger J, (2005) Reducing the burden of malaria in different eco-epidemiological settings with environmental management: a systematic review. Lancet Infect Dis 5: 695-708.
90. Norman G, Pedley S, Takkouche B, (2010) Effects of sewerage on diarrhoea and enteric infections: a systematic review and meta-analysis. Lancet Infect Dis 10: 536-544.
91. Hartinger SM, Lanata CF, Hattendorf J, Gil AI, Verastegui H, et al. (2011) A community randomised controlled trial evaluating a home-based environmental intervention package of improved stoves, solar water disinfection and kitchen sinks in rural Peru: rationale, trial design and baseline findings. Contemp Clin Trials 32: 864-873.
92. Waddington H, Snilstveit B, White H, Fewtrell L, (2009) Water, sanitation and hygiene interventions to combat childhood diarrhoea in developing countries London International Initiative for Impact Evaluation.
93. Arnold BF, Colford JM Jr, (2007) Treating water with chlorine at point-of-use to improve water quality and reduce child diarrhea in developing countries: a systematic review and meta-analysis. Am J Trop Med Hyg 76: 354-364.
94. Strina A, Cairncross S, Barreto ML, Larrea C, Prado MS, (2003) Childhood diarrhea and observed hygiene behavior in Salvador, Brazil. Am J Epidemiol 157: 1032-1038.
95. Burton MJ, Holland MJ, Makalo P, Aryee EA, Sillah A, et al. (2010) Profound and sustained reduction in Chlamydia trachomatis in The Gambia: a five-year longitudinal study of trachoma endemic communities. PLoS Negl Trop Dis 4: e835 doi:10.1371/journal.pntd.0000835.
96. Brocklehurst C, Bartram J, (2010) Swimming upstream: why sanitation, hygiene and water are so important to mothers and their daughters. Bull World Health Organ 88: 482.