ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
de Silva N, Hall A, 2010. Using the prevalence of individual species of intestinal nematode worms to estimate the combined prevalence of any species. PLoS Negl Trop Dis 4: e655.
-
2.
de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19: 547–551.
-
3.
Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, Savioli L, 2008. Controlling soil-transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Negl Trop Dis 2: e126.
-
4.
Harhay MO, Horton J, Olliaro PL, 2010. Epidemiology and control of human gastrointestinal parasites in children. Expert Rev Anti Infect Ther 8: 219–234.
-
5.
Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis JD, Mor V, McGarvey ST, 2005. Functional significance of low-intensity polyparasite helminth infections in anemia. J Infect Dis 192: 2160–2170.
-
6.
Mupfasoni D et al. 2009. Polyparasite helminth infections and their association to anemia and undernutrition in northern Rwanda. PLoS Negl Trop Dis 3: e517.
-
7.
WHO, 2015. The Global Prevalence of Anemia in 2011. Geneva, Switzerland: World Health Organization.
-
8.
Ulukanligil M, Seyrek A, 2004. Demographic and socio-economic factors affecting the physical development, hemoglobin and parasitic infection status of schoolchildren in Sanliurfa province, Turkey. Public Health 118: 151–158.
-
9.
Wani SA, Ahmad F, Zargar SA, Dar ZA, Dar PA, Tak H, Fomda BA, 2008. Soil-transmitted helminths in relation to hemoglobin status among school children of the Kashmir Valley. J Parasitol 94: 591–593.
-
10.
Koukounari A, Estambale BB, Njagi JK, Cundill B, Ajanga A, Crudder C, Otido J, Jukes MC, Clarke SE, Brooker S, 2008. Relationships between anemia and parasitic infections in Kenyan schoolchildren: a Bayesian hierarchical modelling approach. Int J Parasitol 38: 1663–1671.
-
11.
Sorensen WC, Cappello M, Bell D, Difedele LM, Brown MA, 2011. Poly-helminth infection in east Guatemalan school children. J Glob Infect Dis 3: 25–31.
-
12.
Ngui R, Lim YA, Chong Kin L, Sek Chuen C, Jaffar S, 2012. Association between anemia, iron deficiency anemia, neglected parasitic infections and socioeconomic factors in rural children of west Malaysia. PLoS Negl Trop Dis 6: e1550.
-
13.
Saboyá MI, Catalá L, Nicholls RS, Ault SK, 2013. Update on the mapping of prevalence and intensity of infection for soil-transmitted helminth infections in Latin America and the Caribbean: a call for action. PLoS Negl Trop Dis 7: e2419.
-
14.
Ash LR, Orihel TC, Savioli L, 1994. Bench Aids for the Diagnosis of Intestinal Parasites. Geneva, Switzerland: World Health Organization.
-
15.
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.
-
16.
Knight WB, Hiatt RA, Cline BL, Ritchie LS, 1976. A modification of the formol-ether concentration technique for increased sensitivity in detecting Schistosoma mansoni eggs. Am J Trop Med Hyg 25: 818–823.
-
17.
Montresor A, Crompton DWT, Hall A, Bundy DAP, 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level (WHO/CDS/SIP/98.1). Geneva, Switzerland: World Health Organization.
-
18.
WHO, 2003. Controlling Disease Due to Helminth Infections. Crompton DWT, Montresor A, Nesheim MC, Savioli L, eds. Geneva, Switzerland: World Health Organization, 248.
-
19.
Hotez PJ, Woc-Colburn L, Bottazzi ME, 2014. Neglected tropical diseases in central America and Panama: review of their prevalence, populations at risk and impact on regional development. Int J Parasitol 44: 597–603.
-
20.
Rosewell A, Robleto G, Rodríguez G, Barragne-Bigot P, Amador JJ, Aldighieri S, 2010. Soil-transmitted helminth infection and urbanization in 880 primary school children in Nicaragua, 2005. Trop Doct 40: 141–143.
-
21.
Muñoz-Antoli C, Pavón A, Marcilla A, Toledo R, Esteban JG, 2014. Prevalence and risk factors related to intestinal parasites among children in department of Rio San Juan, Nicaragua. Trans R Soc Trop Med Hyg 108: 774–782.
-
22.
Muñoz-Antoli C, Pavón A, Pérez P, Toledo R, Esteban JG, 2017. Soil-transmitted helminth infections in schoolchildren of Laguna de Perlas (Nicaragua). J Trop Pediatr 63: 124–134.
-
23.
Cavuoti D, Lancaster KR, 1992. Intestinal parasitism of children on Corn Island, Nicaragua. Pediatr Infect Dis J 11: 775–776.
-
24.
Mujica-Coopman MF, Brito A, López de Romaña D, Ríos-Castillo I, Coris H, Olivares M, 2015. Prevalence of anemia in Latin America and the Caribbean. Food Nutr Bull 36: S119–S128.
-
25.
Erismann S et al. 2017. Prevalence and risk factors of undernutrition among schoolchildren in the Plateau Central and Centre-Ouest regions of Burkina Faso. Infect Dis Poverty 6: 17.
-
26.
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: 744–750.
-
27.
Aini UN et al. 2007. Serum iron status in Orang Asli children living in endemic areas of soil-transmitted helminths. Asia Pac J Clin Nutr 16: 724–730.
-
28.
Mbuh JV, Nembu NE, 2013. Malnutrition and intestinal helminth infections in schoolchildren from Dibanda, Cameroon. J Helminthol 87: 46–51.
-
29.
Oberhelman RA, Guerrero ES, Fernandez ML, Silio M, Mercado D, Comiskey N, Ihenacho G, Mera R, 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.
-
30.
Robertson LJ, Crompton DW, Sanjur D, Nesheim MC, 1992. Haemoglobin concentrations and concomitant infections of hookworm and Trichuris trichiura in Panamanian primary schoolchildren. Trans R Soc Trop Med Hyg 86: 654–656.
-
31.
Brooker S, Peshu N, Warn PA, Mosobo M, Guyatt HL, Marsh K, Snow RW, 1999. The epidemiology of hookworm infection and its contribution to anemia among pre-school children on the Kenyan coast. Trans R Soc Trop Med Hyg 93: 240–246.
-
32.
Osazuwa F, Ayo OM, Imade P, 2011. A significant association between intestinal helminth infection and anemia burden in children in rural communities of Edo state, Nigeria. N Am J Med Sci 3: 30–34.
-
33.
Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Savioli L, 1997. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. Am J Clin Nutr 65: 153–159.
-
34.
Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L, 1998. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 68: 179–186.
-
35.
Al-Mekhlafi MS, Surin J, Atiya AS, Ariffin WA, Mahdy AK, Abdullah HC, 2008. Current prevalence and predictors of protein-energy malnutrition among schoolchildren in rural Peninsular Malaysia. Southeast Asian J Trop Med Public Health 39: 922–931.
-
36.
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521–1532.
-
37.
Sousa-Figueiredo JC, Basáñez MG, Mgeni AF, Khamis IS, Rollinson D, Stothard JR, 2008. A parasitological survey, in rural Zanzibar, of pre-school children and their mothers for urinary schistosomiasis, soil-transmitted helminthiases and malaria, with observations on the prevalence of anemia. Ann Trop Med Parasitol 102: 679–692.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 377 | 296 | 15 |
| Full Text Views | 767 | 9 | 0 |
| PDF Downloads | 361 | 5 | 0 |
Soil-Transmitted Helminth Infections and Anemia in Schoolchildren from Corn Island Archipelago (RAAS, Nicaragua)
Carla Muñoz-Antoli
Carla Muñoz-Antoli
Departamento Parasitología, Facultad Farmacia, Universidad Valencia, Burjassot, Valencia, España;
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Paloma Pérez
Paloma Pérez
Departamento Parasitología, Facultad Farmacia, Universidad Valencia, Burjassot, Valencia, España;
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Aleyda Pavón
Aleyda Pavón
Departamento Bioanálisis Clínico, Instituto Politécnico de la Salud (IPS-Polisal), Universidad Nacional Autónoma de Nicaragua, Managua, Nicaragua
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Rafael Toledo
Rafael Toledo
Departamento Parasitología, Facultad Farmacia, Universidad Valencia, Burjassot, Valencia, España;
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Jose-Guillermo Esteban
Jose-Guillermo Esteban
Departamento Parasitología, Facultad Farmacia, Universidad Valencia, Burjassot, Valencia, España;
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The prevalence and intensity of soil-transmitted helminth (STH) infections in schoolchildren from Corn Islands (Nicaragua) were examined to detect mono- or poly-STH infected children, measuring different intensity levels, and to elucidate measurably increased odds of being anemic. A total of 341 stool samples provided by 2- to 15-year-old children were examined using a concentration technique and a Kato–Katz slide. Intensity of infection was expressed as eggs per gram (epg) of feces to classify light, moderate, or heavy intensity infection. A finger-prick blood sample was obtained from each student in the field. Soil-transmitted helminth prevalence was 54.3%, with Trichuris trichiura as the most prevalent species (48.9%). The combination T. trichiura/Ascaris lumbricoides (12.6%) was the most common. When T. trichiura or A. lumbricoides appeared as a single infection, light or moderate intensity infections were seen, whereas when multiple species were identified, heavy infections were present. Anemia was detected in those with any kind of STH infection (42.7%), with statistically significant differences (P = 0.004) when compared with uninfected individuals (28.2%). Polyparasite infection with one parasite species at moderate intensity and the other parasite species at light intensity or absent was found to be a significant factor for the odds of being anemic (odds ratio = 2.07). The present study reveals a high level of STH transmission requiring a deworming control program in Corn Islands and pointing to the need of improving the education and sanitary conditions of the population to avoid environmental contamination and reinfection.
- Supplemental Materials (PDF 207 KB)
Author Notes
Financial support: This work was supported by Proyecto de Cooperación al Desarrollo del Vicerrectorado de Relaciones Internacionales y Cooperación from the Universitat de València-Estudi General (Valencia, Spain), by PROMETEO2014-083 Fase II from Conselleria d’Educació, Generalitat valenciana (Valencia, Spain), and by No. RD16/0027/0023, red de Investigación Cooperativa en Enfermedades Tropicales-RICET, IV National Program of I+D+I 2017-20121, ISCIII-Subdirección General de Redes y Centros de Investigación Cooperativa from the Ministerio de Sanidad y Consumo (Madrid, Spain).
Ethical approval: This study was performed in collaboration with IPS-Polisal, approved by the UNAN-Managua, and supervised by Centro Nacional de Diagnóstico y Referencia of the Nicaraguan Ministry of Health.
Authors’ addresses: Carla Muñoz-Antoli, Paloma Pérez, Rafael Toledo, and Jose-Guillermo Esteban, Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Burjassot, Valencia, Spain, E-mails: carla.munoz@uv.es, escobedo@alumni.uv.es, rafael.toledo@uv.es, and jguillermo.esteban@uv.es. Aleyda Pavón, Departamento Bionálisis Clínico, Instituto Politécnico de la Salud (IPS-Polisal), Universidad Nacional Autónoma de Nicaragua, Managua, Nicaragua, E-mail: aleydapr@yahoo.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
de Silva N, Hall A, 2010. Using the prevalence of individual species of intestinal nematode worms to estimate the combined prevalence of any species. PLoS Negl Trop Dis 4: e655.
-
2.
de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19: 547–551.
-
3.
Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, Savioli L, 2008. Controlling soil-transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Negl Trop Dis 2: e126.
-
4.
Harhay MO, Horton J, Olliaro PL, 2010. Epidemiology and control of human gastrointestinal parasites in children. Expert Rev Anti Infect Ther 8: 219–234.
-
5.
Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis JD, Mor V, McGarvey ST, 2005. Functional significance of low-intensity polyparasite helminth infections in anemia. J Infect Dis 192: 2160–2170.
-
6.
Mupfasoni D et al. 2009. Polyparasite helminth infections and their association to anemia and undernutrition in northern Rwanda. PLoS Negl Trop Dis 3: e517.
-
7.
WHO, 2015. The Global Prevalence of Anemia in 2011. Geneva, Switzerland: World Health Organization.
-
8.
Ulukanligil M, Seyrek A, 2004. Demographic and socio-economic factors affecting the physical development, hemoglobin and parasitic infection status of schoolchildren in Sanliurfa province, Turkey. Public Health 118: 151–158.
-
9.
Wani SA, Ahmad F, Zargar SA, Dar ZA, Dar PA, Tak H, Fomda BA, 2008. Soil-transmitted helminths in relation to hemoglobin status among school children of the Kashmir Valley. J Parasitol 94: 591–593.
-
10.
Koukounari A, Estambale BB, Njagi JK, Cundill B, Ajanga A, Crudder C, Otido J, Jukes MC, Clarke SE, Brooker S, 2008. Relationships between anemia and parasitic infections in Kenyan schoolchildren: a Bayesian hierarchical modelling approach. Int J Parasitol 38: 1663–1671.
-
11.
Sorensen WC, Cappello M, Bell D, Difedele LM, Brown MA, 2011. Poly-helminth infection in east Guatemalan school children. J Glob Infect Dis 3: 25–31.
-
12.
Ngui R, Lim YA, Chong Kin L, Sek Chuen C, Jaffar S, 2012. Association between anemia, iron deficiency anemia, neglected parasitic infections and socioeconomic factors in rural children of west Malaysia. PLoS Negl Trop Dis 6: e1550.
-
13.
Saboyá MI, Catalá L, Nicholls RS, Ault SK, 2013. Update on the mapping of prevalence and intensity of infection for soil-transmitted helminth infections in Latin America and the Caribbean: a call for action. PLoS Negl Trop Dis 7: e2419.
-
14.
Ash LR, Orihel TC, Savioli L, 1994. Bench Aids for the Diagnosis of Intestinal Parasites. Geneva, Switzerland: World Health Organization.
-
15.
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.
-
16.
Knight WB, Hiatt RA, Cline BL, Ritchie LS, 1976. A modification of the formol-ether concentration technique for increased sensitivity in detecting Schistosoma mansoni eggs. Am J Trop Med Hyg 25: 818–823.
-
17.
Montresor A, Crompton DWT, Hall A, Bundy DAP, 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level (WHO/CDS/SIP/98.1). Geneva, Switzerland: World Health Organization.
-
18.
WHO, 2003. Controlling Disease Due to Helminth Infections. Crompton DWT, Montresor A, Nesheim MC, Savioli L, eds. Geneva, Switzerland: World Health Organization, 248.
-
19.
Hotez PJ, Woc-Colburn L, Bottazzi ME, 2014. Neglected tropical diseases in central America and Panama: review of their prevalence, populations at risk and impact on regional development. Int J Parasitol 44: 597–603.
-
20.
Rosewell A, Robleto G, Rodríguez G, Barragne-Bigot P, Amador JJ, Aldighieri S, 2010. Soil-transmitted helminth infection and urbanization in 880 primary school children in Nicaragua, 2005. Trop Doct 40: 141–143.
-
21.
Muñoz-Antoli C, Pavón A, Marcilla A, Toledo R, Esteban JG, 2014. Prevalence and risk factors related to intestinal parasites among children in department of Rio San Juan, Nicaragua. Trans R Soc Trop Med Hyg 108: 774–782.
-
22.
Muñoz-Antoli C, Pavón A, Pérez P, Toledo R, Esteban JG, 2017. Soil-transmitted helminth infections in schoolchildren of Laguna de Perlas (Nicaragua). J Trop Pediatr 63: 124–134.
-
23.
Cavuoti D, Lancaster KR, 1992. Intestinal parasitism of children on Corn Island, Nicaragua. Pediatr Infect Dis J 11: 775–776.
-
24.
Mujica-Coopman MF, Brito A, López de Romaña D, Ríos-Castillo I, Coris H, Olivares M, 2015. Prevalence of anemia in Latin America and the Caribbean. Food Nutr Bull 36: S119–S128.
-
25.
Erismann S et al. 2017. Prevalence and risk factors of undernutrition among schoolchildren in the Plateau Central and Centre-Ouest regions of Burkina Faso. Infect Dis Poverty 6: 17.
-
26.
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: 744–750.
-
27.
Aini UN et al. 2007. Serum iron status in Orang Asli children living in endemic areas of soil-transmitted helminths. Asia Pac J Clin Nutr 16: 724–730.
-
28.
Mbuh JV, Nembu NE, 2013. Malnutrition and intestinal helminth infections in schoolchildren from Dibanda, Cameroon. J Helminthol 87: 46–51.
-
29.
Oberhelman RA, Guerrero ES, Fernandez ML, Silio M, Mercado D, Comiskey N, Ihenacho G, Mera R, 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.
-
30.
Robertson LJ, Crompton DW, Sanjur D, Nesheim MC, 1992. Haemoglobin concentrations and concomitant infections of hookworm and Trichuris trichiura in Panamanian primary schoolchildren. Trans R Soc Trop Med Hyg 86: 654–656.
-
31.
Brooker S, Peshu N, Warn PA, Mosobo M, Guyatt HL, Marsh K, Snow RW, 1999. The epidemiology of hookworm infection and its contribution to anemia among pre-school children on the Kenyan coast. Trans R Soc Trop Med Hyg 93: 240–246.
-
32.
Osazuwa F, Ayo OM, Imade P, 2011. A significant association between intestinal helminth infection and anemia burden in children in rural communities of Edo state, Nigeria. N Am J Med Sci 3: 30–34.
-
33.
Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Savioli L, 1997. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. Am J Clin Nutr 65: 153–159.
-
34.
Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L, 1998. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 68: 179–186.
-
35.
Al-Mekhlafi MS, Surin J, Atiya AS, Ariffin WA, Mahdy AK, Abdullah HC, 2008. Current prevalence and predictors of protein-energy malnutrition among schoolchildren in rural Peninsular Malaysia. Southeast Asian J Trop Med Public Health 39: 922–931.
-
36.
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 1521–1532.
-
37.
Sousa-Figueiredo JC, Basáñez MG, Mgeni AF, Khamis IS, Rollinson D, Stothard JR, 2008. A parasitological survey, in rural Zanzibar, of pre-school children and their mothers for urinary schistosomiasis, soil-transmitted helminthiases and malaria, with observations on the prevalence of anemia. Ann Trop Med Parasitol 102: 679–692.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 377 | 296 | 15 |
| Full Text Views | 767 | 9 | 0 |
| PDF Downloads | 361 | 5 | 0 |