1921
Volume 84, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

In areas endemic for schistosomiasis having limited healthcare, targeted drug treatment of school-age children is recommended for control of -associated morbidity. However, optimal timing, number, and frequency of treatments are not established. Because longitudinal studies of long-term impact of treatment are few, for current policy considerations we performed quantitative simulation (based on calibrated modeling of -associated disease formation) to project the impact of different school-age treatment regimens. Using published efficacy data from targeted programs, combined with age-specific risk for growth retardation and reinfection, we examined the likely impact of different strategies for morbidity prevention. Results suggest the need for early, repeated treatment through primary school years to optimally prevent the disabling sequelae of stunting and undernutrition. Dynamics of infection/reinfection during childhood and adolescence, combined with early treatment effects against reversible infection-associated morbidities, create a need for aggressive retreatment of preadolescents to achieve optimal suppression of morbidity where drug-based control is used.

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2011-05-05
2017-11-21
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References

  1. Chitsulo L, Engels D, Montresor A, Savioli L, , 2000. The global status of schistosomiasis and its control. Acta Trop 77: 4151.[Crossref]
  2. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, , 2006. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411425.[Crossref]
  3. King CH, Mahmoud AA, , 1989. Drugs five years later: praziquantel. Ann Intern Med 110: 290296.[Crossref]
  4. Fenwick A, , 2006. New initiatives against Africa's worms. Trans R Soc Trop Med Hyg 100: 200207.[Crossref]
  5. Molyneux DH, Hotez PJ, Fenwick A, , 2005. “Rapid-impact interventions”: how a policy of integrated control for Africa's neglected tropical diseases could benefit the poor. PLoS Med 2: e336.[Crossref]
  6. Satayathum SA, Muchiri EM, Ouma JH, Whalen CC, King CH, , 2006. Factors affecting infection or reinfection with Schistosoma haematobium in coastal Kenya: survival analysis during a nine-year, school-based treatment program. Am J Trop Med Hyg 75: 8392.
  7. King CH, , 2007. Lifting the burden of schistosomiasis-defining elements of infection-associated disease and the benefits of antiparasite treatment. J Infect Dis 196: 653655.[Crossref]
  8. King CH, Sturrock RF, Kariuki HC, Hamburger J, , 2006. Transmission control for schistosomiasis—why it matters now. Trends Parasitol 22: 575582.[Crossref]
  9. King CH, Mahmoud AA, , 2001. Epidemiology of schistosomiasis: determinants of transmission of infection. , ed. Schistosomiasis. London, UK: Imperial College Press, 115132.[Crossref]
  10. Smith JH, Christie JD, , 1986. The pathobiology of Schistosoma haematobium infection in humans. Hum Pathol 17: 333345.[Crossref]
  11. Richter J, Correia Dacal AR, Vergetti Siqueira JG, Poggensee G, Mannsmann U, Deelder A, Feldmeier H, , 1998. Sonographic prediction of variceal bleeding in patients with liver fibrosis due to Schistosoma mansoni . Trop Med Int Health 3: 728735.[Crossref]
  12. van der Werf MJ, de Vlas SJ, Brooker S, Looman CWN, Nagelkerke NJD, Habbema JDF, Engels D, , 2003. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86: 125139.[Crossref]
  13. Koukounari A, Gabrielli AF, Toure S, Bosque-Oliva E, Zhang Y, Sellin B, Donnelly CA, Fenwick A, Webster JP, , 2007. Schistosoma haematobium infection and morbidity before and after large-scale administration of praziquantel in Burkina Faso. J Infect Dis 196: 659669.[Crossref]
  14. Olveda RM, Mahmoud AA, , 2001. Disease in schistosomiasis japonica. , ed. Schistosomiasis. London: Imperial College Press, 361390.[Crossref]
  15. King CH, Dickman K, Tisch DJ, , 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 15611569.[Crossref]
  16. Friedman JF, Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Wu H, Olveda RM, McGarvey ST, Kurtis JD, , 2005. Relationship between Schistosoma japonicum and nutritional status among children and young adults in Leyte, the Philippines. Am J Trop Med Hyg 72: 527533.
  17. King CH, Dangerfield-Cha M, , 2008. The unacknowledged impact of chronic schistosomiasis. Chronic Illn 4: 6579.[Crossref]
  18. 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.
  19. Nokes C, McGarvey ST, Shiue L, Wu G, Wu H, Bundy DA, Olds GR, , 1999. Evidence for an improvement in cognitive function following treatment of Schistosoma japonicum infection in Chinese primary schoolchildren. Am J Trop Med Hyg 60: 556565.
  20. King CH, , 2010. Parasites and poverty: the case of schistosomiasis. Acta Trop 113: 95104.[Crossref]
  21. 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.[Crossref]
  22. WHO, 2006. Preventive Chemotherapy in Human Helminthiasis: Coordinated Use of Anthelminthic Drugs in Control Interventions: A Manual for Health Professionals and Programme Managers. Geneva, Switzerland: World Health Organization.
  23. Medley GF, Bundy DAP, , 1996. Dynamic modeling of epidemiologic patterns of schistosomiasis morbidity. Am J Trop Med Hyg 55: 149158.
  24. Chan MS, Guyatt HL, Bundy DA, Booth M, Fulford AJ, Medley GF, , 1995. The development of an age structured model for schistosomiasis transmission dynamics and control and its validation for Schistosoma mansoni . Epidemiol Infect 115: 325344.[Crossref]
  25. Gurarie D, King CH, , 2005. Heterogeneous model of schistosomiasis transmission and long-term control: the combined influence of spatial variation and age-dependent factors on optimal allocation of drug therapy. Parasitology 130: 4965.[Crossref]
  26. Gurarie D, King CH, Wang X, , 2010. A new approach to modelling schistosomiasis transmission based on stratified worm burden. Parasitology 137: 19511965.[Crossref]
  27. Stephenson LS, Latham MC, Kurz KM, Kinoti SN, , 1989. Single dose metrifonate or praziquantel treatment in Kenyan children. II. Effects on growth in relation to Schistosoma haematobium and hookworm egg counts. Am J Trop Med Hyg 41: 445453.
  28. Stephenson LS, Latham MC, Kurz KM, Kinoti SN, Oduori ML, Crompton DW, , 1985. Relationships of Schistosoma haematobium, hookworm and malarial infections and metrifonate treatment to growth of Kenyan school children. Am J Trop Med Hyg 34: 11091118.
  29. Parraga IM, Assis AM, Prado MS, Barreto ML, Reis MG, King CH, Blanton RE, , 1996. Gender differences in growth of school-aged children with schistosomiasis and geohelminth infection. Am J Trop Med Hyg 55: 150156.
  30. de Onis M, Garza C, Onyango AW, Borghi E, , 2007. Comparison of the WHO child growth standards and the CDC 2000 growth charts. J Nutr 137: 144148.
  31. Olds GR, King CH, Hewlett J, Olveda R, Wu G, Ouma JH, Peters PA, McGarvey S, Koech D, Liu CY, Aligui G, Gachihi G, Kombe Y, Parraga I, Ramirez B, Whalen C, Horton RJ, Reeve P, , 1999. Double-blind placebo controlled study of concurrent administration of albendazole and praziquantel in school children with schistosomiasis and geohelminths. J Infect Dis 179: 9961003.[Crossref]
  32. Blanton RE, Salam EA, Ehsan A, King CH, Goddard KA, , 2005. Schistosomal hepatic fibrosis and the interferon gamma receptor: a linkage analysis using single-nucleotide polymorphic markers. Eur J Hum Genet 13: 660668.[Crossref]
  33. Dessein AJ, Hillaire D, Elwali NE, Marquet S, Mohamed-Ali Q, Mirghani A, Henri S, Abdelhameed AA, Saeed OK, Magzoub MM, Abel L, , 1999. Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene. Am J Hum Genet 65: 709721.[Crossref]
  34. Koukounari A, Fenwick A, Whawell S, Kabatereine NB, Kazibwe F, Tukahebwa EM, Stothard JR, Donnelly CA, Webster JP, , 2006. Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. Am J Trop Med Hyg 75: 278286.
  35. Leenstra T, Acosta LP, Langdon GC, Manalo DL, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, , 2006. Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines. Am J Clin Nutr 83: 371379.
  36. Klumpp RK, Webbe G, , 1987. Focal, seasonal and behavioural patterns of infection and transmission of Schistosoma haematobium in a farming village at the Volta Lake, Ghana. J Trop Med Hyg 90: 265281.
  37. Kloos H, Fulford AJ, Butterworth AE, Sturrock RF, Ouma JH, Kariuki HC, Thiongo FW, Dalton PR, Klumpp RK, , 1997. Spatial patterns of human water contact and Schistosoma mansoni transmission and infection in four rural areas in Machakos District, Kenya. Soc Sci Med 44: 949968.[Crossref]
  38. Kvalsvig JD, Schutte CH, , 1986. The role of human water contact patterns in the transmission of schistosomiasis in an informal settlement near a major industrial area. Ann Trop Med Parasitol 80: 1326.[Crossref]
  39. Hagan P, Blumenthal UJ, Chaudri M, Greenwood BM, Hayes RJ, Hodgson I, Kelly C, Knight M, Simpson AJ, Smithers SR, Wilkins HA, , 1987. Resistance to reinfection with Schistosoma haematobium in Gambian children: analysis of their immune responses. Trans R Soc Trop Med Hyg 81: 938946.[Crossref]
  40. Etard JF, Audibert M, Dabo A, , 1995. Age-acquired resistance and predisposition to reinfection with Schistosoma haematobium after treatment with praziquantel in Mali. Am J Trop Med Hyg 52: 549558.
  41. Kurtis JD, Friedman JF, Leenstra T, Langdon GC, Wu HW, Manalo DL, Su L, Jiz M, Jarilla B, Pablo AO, McGarvey ST, Olveda RM, Acosta LP, , 2006. Pubertal development predicts resistance to infection and reinfection with Schistosoma japonicum . Clin Infect Dis 42: 16921698.[Crossref]
  42. Naus CW, Kimani G, Ouma JH, Fulford AJ, Webster M, van Dam GJ, Deelder AM, Butterworth AE, Dunne DW, , 1999. Development of antibody isotype responses to Schistosoma mansoni in an immunologically naive immigrant population: influence of infection duration, infection intensity, and host age. Infect Immun 67: 34443451.
  43. Olveda RM, Daniel BL, Ramirez BD, Aligui GD, Acosta LP, Fevidal P, Tiu E, de Veyra F, Peters PA, Romulo R, Domingo E, Wiest PM, Olds GR, , 1996. Schistosomiasis japonica in the Philippines: the long-term impact of population-based chemotherapy on infection, transmission, and morbidity. J Infect Dis 174: 163172.[Crossref]
  44. Boersma B, Wit JM, , 1997. Catch-up growth. Endocr Rev 18: 646661.[Crossref]
  45. Coutinho HM, Acosta LP, McGarvey ST, Jarilla B, Jiz M, Pablo A, Su L, Manalo DL, Olveda RM, Kurtis JD, Friedman JF, , 2006. Nutritional status improves after treatment of Schistosoma japonicum-infected children and adolescents. J Nutr 136: 183188.
  46. Coutinho HM, McGarvey ST, Acosta LP, Manalo DL, Langdon GC, Leenstra T, Kanzaria HK, Solomon J, Wu H, Olveda RM, Kurtis JD, Friedman JF, , 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J Infect Dis 192: 528536.[Crossref]
  47. Wilson RA, van Dam GJ, Kariuki TM, Farah IO, Deelder AM, Coulson PS, , 2006. The detection limits for estimates of infection intensity in schistosomiasis mansoni established by a study in non-human primates. Int J Parasitol 36: 12411244.[Crossref]
  48. WHO, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Tech Rep Ser 912: 157.
  49. Assis AM, Barreto ML, Prado MS, Reis MG, Parraga IM, Blanton RE, , 1998. Schistosoma mansoni infection and nutritional status in schoolchildren: a randomized, double-blind trial in northeastern Brazil. Am J Clin Nutr 68: 12471253.
  50. Kirigia JM, , 1997. Economic evaluation in schistosomiasis: using the delphi technique to assess effectiveness. Acta Trop 64: 175190.[Crossref]
  51. Bustinduy AL, King CH, Fratamico PM, Smith JL, Brogden KA, , 2009. Parasitic helminths. , eds. Post-Infectious Sequelae and Long-Term Consequences of Infectious Diseases. Washington, DC: American Society for Microbiology Press, 291329.[Crossref]
  52. Warren KS, , 1982. Selective primary health care: strategies for control of disease in the developing world. I. Schistosomiasis. Rev Infect Dis 4: 715726.[Crossref]
  53. Beasley NM, Tomkins AM, Hall A, Kihamia CM, Lorri W, Nduma B, Issae W, Nokes C, Bundy DA, , 1999. The impact of population level deworming on the haemoglobin levels of schoolchildren in Tanga, Tanzania. Trop Med Int Health 4: 744750.[Crossref]
  54. Leenstra T, Coutinho HM, Acosta LP, Langdon GC, Su L, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, , 2006. Schistosoma japonicum reinfection after praziquantel treatment causes anemia associated with inflammation. Infect Immun 74: 63986407.[Crossref]
  55. Kjetland EF, Ndhlovu PD, Kurewa EN, Midzi N, Gomo E, Mduluza T, Friis H, Gundersen SG, , 2008. Prevention of gynecologic contact bleeding and genital sandy patches by childhood anti-schistosomal treatment. Am J Trop Med Hyg 79: 7983.
  56. Ouma JH, King CH, Muchiri EM, Mungai P, Koech DK, Ireri E, Magak P, Kadzo H, , 2005. Late benefits 10–18 years after drug therapy for infection with Schistosoma haematobium in Kwale District, Coast Province, Kenya. Am J Trop Med Hyg 73: 359364.
  57. Coutinho HM, Leenstra T, Acosta LP, Olveda RM, McGarvey ST, Friedman JF, Kurtis JD, , 2007. Higher serum concentrations of DHEAS predict improved nutritional status in helminth-infected children, adolescents, and young adults in Leyte, the Philippines. J Nutr 137: 433439.
  58. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL, , 2002. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 11 May: 1190.
  59. de Onis M, Habicht JP, , 1996. Anthropometric reference data for international use: recommendations from a World Health Organization Expert Committee. Am J Clin Nutr 64: 650658.
  60. WHO, 2006. Assessment of differences in linear growth among populations in the WHO Multicentre Growth Reference Study. Acta Paediatr Suppl 450: 5665.
  61. Woolhouse ME, Watts CH, Chandiwana SK, , 1991. Heterogeneities in transmission rates and the epidemiology of schistosome infection. Proc R Soc Lond B Biol Sci 245: 109114.[Crossref]
  62. Kvalsvig JD, , 1986. The effects of schistosomiasis haematobium on the activity of school children. J Trop Med Hyg 89: 8590.
  63. Gryseels B, , 1989. The relevance of schistosomiasis for public health. Trop Med Parasitol 40: 134142.
  64. Tanner M, , 1989. Evaluation of public health impact of schistosomiasis. Trop Med Parasitol 40: 143148.
  65. Warren KS, Mahmoud AA, , 1976. Targeted mass treatment: a new approach to the control of schistosomiasis. Trans Assoc Am Physicians 89: 195204.
  66. Mott KE, Murray CJ, Lopez A, Mathers CD, , 2004. Schistosomiasis. , eds. The Global Epidemiology of Infectious Diseases. Geneva, Switzerland: World Health Organization.
  67. de Lima e Costa MF, Leite ML, Rocha RS, de Almeida Magalhaes MH, Katz N, , 1988. Anthropometric measures in relation to schistosomiasis mansoni and socioeconomic variables. Int J Epidemiol 17: 880886.[Crossref]
  68. McGarvey ST, Wu G, Zhang S, Wang Y, Peters P, Olds GR, Wiest PM, , 1993. Child growth, nutritional status, and schistosomiasis japonica in Jiangxi, People's Republic of China. Am J Trop Med Hyg 48: 547553.
  69. Blas BL, Lipayon IL, Tormis LC, Portillo LA, Hayashi M, Matsuda H, , 2006. An attempt to study the economic loss arising from Schistosoma japonicum infection and the benefits derived from treatment. Southeast Asian J Trop Med Public Health 37: 2632.
  70. Strauss J, Thomas D, , 1998. Health, nutrition, and economic development. J Econ Lit 36: 766817.
  71. Florencio TT, Ferreira HS, Cavalcante JC, Assuncao ML, Sawaya AL, , 2008. Short stature and food habits as determining factors for the low productivity of sugarcane laborers in the State of Alagoas, north-eastern Brazil. Arch Latinoam Nutr 58: 3339.
  72. Coly AN, Milet J, Diallo A, Ndiaye T, Benefice E, Simondon F, Wade S, Simondon KB, , 2006. Preschool stunting, adolescent migration, catch-up growth, and adult height in young Senegalese men and women of rural origin. J Nutr 136: 24122420.
  73. Lwambo NJ, Brooker S, Siza JE, Bundy DA, Guyatt H, , 2000. Age patterns in stunting and anaemia in African schoolchildren: a cross-sectional study in Tanzania. Eur J Clin Nutr 54: 3640.[Crossref]
  74. Coutinho HM, Leenstra T, Acosta LP, Su L, Jarilla B, Jiz MA, Langdon GC, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, , 2006. Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. Am J Trop Med Hyg 75: 720726.
  75. Golden MH, , 1994. Is complete catch-up possible for stunted malnourished children? Eur J Clin Nutr 48 (Suppl 1): S5870; discussion S71.
  76. Stothard JR, Gabrielli AF, , 2007. Schistosomiasis in African infants and preschool children: to treat or not to treat? Trends Parasitol 23: 8386.[Crossref]
  77. Carabin H, Marshall CM, Joseph L, Riley S, Olveda R, McGarvey ST, , 2005. Estimating the intensity of infection with Schistosoma japonicum in villagers of Leyte, Philippines. Part I: a Bayesian cumulative logit model. The Schistosomiasis Transmission & Ecology Project (STEP). Am J Trop Med Hyg 72: 745753.
  78. de Vlas SJ, Gryseels B, , 1992. Underestimation of Schistosoma mansoni prevalences. Parasitol Today 8: 274277.[Crossref]
  79. Savioli L, Hatz C, Dixon H, Kisumku UM, Mott KE, , 1990. Control of morbidity due to Schistosoma haematobium on Pemba Island: egg excretion and hematuria as indicators of infection. Am J Trop Med Hyg 43: 289295.
  80. Shane HL, Verani JR, Abudho B, Montgomery SP, Blackstock AJ, Mwinzi PN, Butler SE, Karanja DM, Secor WE, , 2011. Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in western Kenya. PLoS Negl Trop Dis 5: e591.[Crossref]
  81. Stothard JR, Sousa-Figuereido JC, Betson M, Adriko M, Arinaitwe M, Rowell C, Besiyge F, Kabatereine NB, , 2011. Schistosoma mansoni infections in young children: when are schistosome antigens in urine, eggs in stool and antibodies to eggs first detectable? PLoS Negl Trop Dis 5: e938.[Crossref]
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Supplementary Data

Supplemental appendix

  • Received : 12 Nov 2010
  • Accepted : 24 Jan 2011

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