Regional, Household and Individual Factors that Influence Soil Transmitted Helminth Reinfection Dynamics in Preschool Children from Rural Indigenous Panamá

PLoS Neglected Tropical Diseases

Volumn 7, Issue 2, 2013, Pages

  Halpenny, Carli M ^a   Paller, Claire ^a   Koski, Kristine G ^a   Valdés, Victoria E ^b   Scott, Marilyn E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSIDAD DE PANAMÁ   (Panama)

Author keywords

[No Author keywords available]

Indexed keywords

ALBENDAZOLE;

ARTICLE; ASCARIS LUMBRICOIDES; CHILD; CLUSTER ANALYSIS; COMPARATIVE STUDY; CORRELATION ANALYSIS; DISEASE TRANSMISSION; EXPOSURE; FECES; FEMALE; HELMINTHIASIS; HOOKWORM; HOST SUSCEPTIBILITY; HOUSEHOLD; HUMAN; MAJOR CLINICAL STUDY; MALE; PANAMA; PRESCHOOL CHILD; PREVALENCE; REINFECTION; RISK FACTOR; SCORING SYSTEM; SINGLE DRUG DOSE; SOIL; TRICHURIS TRICHIURA;

EID: 84874775156     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002070     Document Type: Article

References (73)

1. Chan MS, (1997) The global burden of intestinal nematode infections- Fifty years on. Parasitol Today 13: 438-443.
2. Berkman DS, Lescano AG, Gilman RH, Lopez S, Black MM, (2002) Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359: 564-571.
3. Oberhelman RA, Guerrero ES, Fernandez ML, Silio M, Mercado D, et al. (1998) Correlations between intestinal parasitosis, physical growth, and psychomotor development among infants and children from rural Nicaragua. Am J Trop Med Hyg 58: 470-475.
4. Stephenson LS, Crompton DWT, Latham MC, Schulpen TWJ, Nesheim MC, et al. (1980) Relationships between Ascaris infection and growth of malnourished preschool children in Kenya. Am J Clin Nutr 33: 1165-1172.
5. Stephenson LS, Latham MC, Ottesen EA, (2000) Malnutrition and parasitic helminth infections. Parasitology 121: S23-S38.
6. WHO (2006) Preventative chemotherapy in human helminthiasis- Coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: World Health Organization. 74 p.
7. Montresor A, Crompton DW, Gyorkos T, Savioli L (2002) Helminth control in school-age children: A guide for managers of control programmes. Geneva: World Health Organization. 78 p.
8. Anderson RM, May RM, (1982) Population dynamics of human helminth infections: Control by chemotherapy. Nature 297: 557-563.
9. Bundy DAP, Wong MS, Lewis LL, Horton J, (1990) Control of geohelminths by delivery of targeted chemotherapy through schools. Trans R Soc Trop Med Hyg 84: 115-120.
10. Koski KG, Scott ME, (2001) Gastrointestinal nematodes, nutrition and immunity: Breaking the negative spiral. Annu Rev Nutr 21: 297-321.
11. Holland CV, (2009) Predisposition to Ascariasis: Patterns, mechanisms and implications. Parasitology 136: 1537-1547.
12. Jia T-W, S M, Utzinger J, King C, Zhou XN, (2012) Soil-transmitted helminth reinfection after drug treatment: A systematic review and meta-analysis. PLoS Neglect Trop Dis 6: e1621.
13. Williams-Blangero S, VandeBerg JL, Subedi J, Jha B, Corrêa-Oliveira R, et al. (2008) Localization of multiple quantitative trait loci influencing susceptibility to infection with Ascaris lumbricoides. J Infect Dis 197: 66-71.
14. Hagel I, Lynch NR, Di Prisco MC, Pérez M, Sánchez JE, et al. (1999) Helminthic infection and anthropometric indicators in children from a tropical slum: Ascaris reinfection after anthelmintic treatment. J Trop Pediatr 45: 215-220.
15. Saldiva SRM, Carvalho HB, Castilho VP, Struchiner CJ, Massad E, (2002) Malnutrition and susceptibility to enteroparasites: Reinfection rates after mass chemotherapy. Paediatr Perinat Epidemiol 16: 166-171.
16. Hesham Al-Mekhlafi M, 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.
17. 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.
18. 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.
19. Bartram J, Cairncross S, (2010) Hygiene, sanitation, and water: forgotten foundations of health. PLoS Med 7: e1000367.
20. 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.
21. Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RCA, (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.
22. 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.
23. Pullan RL, Bethony JM, Geiger SM, Cundill B, Correa-Oliveira R, et al. (2008) Human helminth co-infection: Analysis of spatial patterns and risk factors in a Brazilian community. PLoS Neglect Trop Dis 2: e352.
24. De Souza EA, Da Silva-Nunes M, Dos Santos Malafronte R, 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.
25. Naish S, McCarthy J, Williams GM, (2004) Prevalence, intensity and risk factors for soil-transmitted helminth infection in a South Indian fishing village. Acta Trop 91: 177-187.
26. 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.
27. Forrester JE, Scott ME, Bundy DAP, Golden MHN, (1988) Clustering of Ascaris lumbricoides and Trichuris trichiura infections within households. Trans R Soc Trop Med Hyg 82: 282-288.
28. Chan L, Bundy DAP, Kan SP, (1994) Aggregation and predisposition to Ascaris lumbricoides and Trichuris trichiura at the familial level. Trans R Soc Trop Med Hyg 88: 46-48.
29. Brooker S, Kabatereine NB, Tukahebwa EM, Kazibwe F, (2004) Spatial analysis of the distribution of intestinal nematode infections in Uganda. Epidemiol Infect 132: 1065-1071.
30. Koroma JB, Peterson J, Gbakima AA, Nylander FE, Sahr F, et al. (2010) Geographical distribution of intestinal schistosomiasis and soil-transmitted helminthiasis and preventive chemotherapy strategies in Sierra Leone. PLoS Neglect Trop Dis 4: e891.
31. Raso G, Vounatsou P, Gosoniu L, Tanner M, Goran E, et al. (2006) Risk factors and spatial patterns of hookworm infection among schoolchildren in a rural area of western Cote d'Ivoire. Int J Parasitol 36: 201-210.
32. Saathoff E, Olsen A, Kvalsvig JD, Appleton CC, Sharp B, et al. (2005) Ecological covariates of Ascaris lumbricoides infection in schoolchildren from rural KwaZulu-Natal, South Africa. Trop Med Int Health 10: 412-422.
33. Knopp S, Mohammed KA, Khamis IS, Mgeni AF, Stothard JR, et al. (2008) Spatial distribution of soil-transmitted helminths, including Strongyloides stercoralis, among children in Zanzibar. Geospat Health 3: 47-56.
34. Steinmann P, Zhou X-N, Li Y-L, Li H-J, Chen S-R, et al. (2007) Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Trop 104: 38-51.
35. 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. Acta Trop pp. 10.1016/j.actatropica.2011.1004.1010.
36. Pullan RL, Kabatereine NB, Quinnell RJ, Brooker S, (2010) Spatial and genetic epidemiology of hookworm in a rural community in Uganda. PLoS Neglect Trop Dis 4: e713.
37. 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.
38. Walker M, Hall A, Basáñez MG, (2011) Individual predisposition, household clustering and risk factors for human infection with Ascaris lumbricoides: New epidemiological insights. PLoS Neglect Trop Dis 5: e1047.
39. Ministerio de Economía y Finanzas (2010) La Distribución del Ingreso en Los Hogares de Panamá:Encuesta de Niveles de Vida 2008. Panamá: Ministerio de Economía y Finanzas. 34 p.
40. Halpenny CM, Koski KG, Valdés VE, Scott ME, (2012) Prediction of child health by household density and asset-based indices in impoverished Indigenous villages in rural Panamá. Am J Trop Med Hyg 86: 280-291.
41. Hotez PJ, De Silva N, Brooker S, Bethony J (2003) Soil transmitted helminth infections: The nature, causes and burden of the condition, Working Paper No. 3, Disease Control Priorities Project. Bethesda, Maryland: Fogarty International Center, National Institutes of Health.
42. Montresor A, Crompton DW, Bundy D, Hall A, Savioli L (1998) Guidelines for the evaluation of soil transmitted helminthiasis and schistosomiasis at community level. Geneva: WHO. 49 p.
43. Cringoli G, (2006) FLOTAC, a novel apparatus for a multivalent faecal egg count technique. Parassitologia 48: 381-384.
44. Forrester JE, Scott ME, Bundy DAP, Golden MHN, (1990) Predisposition of individuals and families in Mexico to heavy infection with Ascaris lumbricoides and Trichuris trichiura. Trans R Soc Trop Med Hyg 84: 272-276.
45. Kightlinger LK, Seed JR, Kightlinger MB, (1995) The epidemiology of Ascaris lumbricoides, Trichuris trichiura, and hookworm in children in the Ranomafana rainforest, Madagascar. J Parasitol 81: 159-169.
46. Payne L, Koski KG, Ortega-Barria E, Scott ME, (2007) Benefit of vitamin A supplementation on Ascaris re-infection is less evident in stunted children. J Nutr 137: 1455-1459.
47. WHO Multicentre Growth Reference Study Group (2006) WHO Child Growth Standards: Methods and development: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Geneva: WHO.
48. Kuldorff M, Nagarwalla N, (1995) Spatial disease clusters: detection and inference. Stat Med 14: 799-819.
49. Kuldorff M, (2011) SaTScan v9.0: Software for the spatial and space-time scan statistics. Information Management Services, Inc http://www.satscan.org.
50. Sacko M, De Clercq D, Behnke JM, Gilbert FS, Dorny P, et al. (1999) Comparison of the efficacy of mebendazole, albendazole and pyrantel in treatment of human hookworm infections in the Southern Region of Mali, West Africa. Trans R Soc Trop Med Hyg 93: 195-203.
51. Anderson RM, May RM (1991) Infectious diseases of Humans: Dynamics and Control. Oxford: Oxford University Press. 757 p.
52. Bundy DAP, Thompson DE, Cooper ES, Golden MHN, Anderson RM, (1985) Population dynamics and chemotherapeutic control of Trichuris trichiura infection of children in Jamaica and St. Lucia. Trans R Soc Trop Med Hyg 79: 759-764.
53. Gunawardena GSA, Karunaweera ND, Ismail MM, (2004) Wet-days: Are they better indicators of Ascaris infection levels? J Helminthol 78: 305-310.
54. Nwosu ABC, Anya AO, (1980) Seasonality in human hookworm infection in an endemic area of Nigeria, and its relationship to rainfall. Tropenmed Parasitol 31: 201-208.
55. Gabrielli AF, Montresor A, Chitsulo L, Engels D, Savioli L, (2011) Preventive chemotherapy in human helminthiasis: Theoretical and operational aspects. Trans R Soc Trop Med Hyg 105: 683-693.
56. Albonico M, Stoltzfus RJ, Savioli L, Chwaya HM, D'Harcourt E, et al. (1999) A controlled evaluation of two school based anthelminthic chemotherapy regimens on intensity of intestinal helminth infections. Int J Epidemiol 28: 591-596.
57. Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, et al. (2008) Controlling soil-transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Neglect Trop Dis 2: e126.
58. Keiser J, Utzinger J, (2008) Efficacy of current drugs against soil-transmitted helminth infections: Systematic review and meta-analysis. J Am Med Ass 299: 1937-1948.
59. Bennett A, Guyatt H, (2000) Reducing intestinal nematode infection: Efficacy of albendazole and mebendazole. Parasitol Today 16: 71-74.
60. Vercruysse J, Behnke JM, Albonico M, Ame SM, Angebault C, et al. (2011) Assessment of the anthelmintic efficacy of albendazole in school children in seven countries where soil-transmitted helminths are endemic. PLoS Neglect Trop Dis 5: e948.
61. Diawara A, Drake LJ, Suswillo RR, Kihara J, Bundy DAP, et al. (2009) Assays to detect β-tubulin codon 200 polymorphism in Trichuris trichiura and Ascaris lumbricoides. PLoS Neglect Trop Dis 3: e397.
62. Matthys B, Tschannen AB, Tian-Bi NT, Comoé H, Diabaté 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.
63. Stothard JR, French MD, Khamis IS, Basáñez MG, Rollinson D, (2009) The epidemiology and control of urinary schistosomiasis and soil-transmitted helminthiasis in schoolchildren on Unguja Island, Zanzibar. Trans R Soc Trop Med Hyg 103: 1031-1044.
64. Quinnell RJ, Pullan RL, Breitling LP, Geiger SM, Cundill B, et al. (2010) Genetic and household determinants of predisposition to human hookworm infectionin a Brazilian community. J Infect Dis 202: 954-961.
65. Quinnell RJ, (2003) Genetics of susceptibility to human helminth infection. Int J Parasitol 33: 1219-1231.
66. Stephenson LS, Latham MC, Adams EJ, Kinoti SN, Pertet A, (1993) Weight gain of Kenyan school children infected with hookworm, Trichuris trichiura and Ascaris lumbricoides is improved following once- or twice- yearly treatment with albendazole. J Nutr 123: 656-665.
67. Hlaing T, Toe T, Saw T, Kyin ML, Lwin M, (1991) A controlled chemotherapeutic intervention trial on the relationship between Ascaris lumbricoides infection and malnutrition in children. Trans R Soc Trop Med Hyg 85: 523-528.
68. Bundy DAP, Cooper ES, Thompson DE, Didier JM, Simmons I, (1987) Epidemiology and population dynamics of Ascaris lumbricoides and Trichuris trichuria infection in the same community. Trans R Soc Trop Med Hyg 81: 987-993.
69. LeVine RA, Rowe ML, (2009) Maternal literacy and child health in less-developed countries: evidence, processes, and limitations. J Dev Behav Pediatr 30: 340-349.
70. Knopp S, Glinz D, Rinaldi L, Mohammed KA, N'Goran EK, et al. (2009) FLOTAC: A promising technique for detecting helminth eggs in human faeces. Trans R Soc Trop Med Hyg 103: 1190-1194.
71. Utzinger J, Rinaldi L, Lohourignon LK, Rohner F, Zimmermann MB, et al. (2008) FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg 102: 84-90.
72. Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, et al. (2010) Comparing diagnostic accuracy of Kato-Katz, Koga Agar Plate, Ether-Concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Neglect Trop Dis 4: e754.
73. Knopp S, Speich B, Hattendorf J, Rinaldi L, Mohammed KA, et al. (2011) Diagnostic accuracy of Kato-Katz and FLOTAC for assessing anthelmintic drug efficacy. PLoS Neglect Trop Dis 5: e1036.