World Health Organization , 2011. Hemoglobin Concentrations for the Diagnosis of Anemia and Assessment of Severity. WHO/NMH/NHD/MNM/11.1. Geneva, Switzerland: World Health Organization. Available at: https://apps.who.int/iris/handle/10665/85839. Accessed July 15, 2023.
McLean E , Cogswell M , Egli I , Wojdyla D , de Benoist B , 2009. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr 12: 444–454.
Rosas-Jimenez C , Tercan E , Horstick O , Igboegwu E , Dambach P , Louis VR , Winkler V , Deckert A , 2022. Prevalence of anemia among Indigenous children in Latin America: A systematic review. Rev Saude Publica 56: 99.
Walter T , De Andraca I , Chadud P , Perales CG , 1989. Iron deficiency anemia: Adverse effects on infant psychomotor development. Pediatrics 84: 7–17.
Lozoff B , De Andraca I , Castillo M , Smith JB , Walter Y , Pino P , 2003. Behavioral and developmental effects of preventing iron-deficiency anemia in healthy full-term infants. Pediatrics 112: 846–854.
World Health Organization , 2023. Anemia. Available at: www.who.int/health-topics/anaemia#tab=tab_2. Accessed July 20, 2023.
Ellwanger JH , Ziliotto M , Kulmann-Leal B , Chies JAB , 2022. Iron deficiency and soil-transmitted helminth infection: Classic and neglected connections. Parasitol Res 121: 3381–3392.
Gujo AB , Kare AP , 2021. Prevalence of intestinal parasite infection and its association with anemia among children aged 6 to 59 months in Sidama National Regional State, southern Ethiopia. Clin Med Insights Pediatr 15: 11795565211029259.
Le HT , Brouwer ID , Verhoef H , Nguyen KC , Kok FJ , 2007. Anemia and intestinal parasite infection in school children in rural Vietnam. Asia Pac J Clin Nutr 16: 716–723.
Caravedo MA , Cabada MM , 2020. Human fascioliasis: Current epidemiological status and strategies for diagnosis, treatment, and control. Res Rep Trop Med 11: 149–158.
Lopez M , White AC Jr. , Cabada MM , 2012. Burden of Fasciola hepatica infection among children from Paucartambo in Cusco, Peru. Am J Trop Med Hyg 86: 481–485.
Reiner RC et al., 2019. Diseases, injuries, and risk factors in child and adolescent health, 1990 to 2017: Findings from the Global Burden of Diseases, Injuries, and Risk Factors 2017 Study. JAMA Pediatr 173: e190337.
Accinelli RA , Leon-Abarca JA , 2020. Age and altitude of residence determine anemia prevalence in Peruvian 6 to 35 months old children. PLoS One 15: e0226846.
Smith JL , Johnston P , Dearden KA , Eggett DL , Campbell AK , 2010. The Impact of Altitude and Diet on Anemia in School-Aged Children in Lago San Pablo, Ecuador. Available at: https://journals.sagepub.com/doi/pdf/10.1177/1941406410383013. Accessed September 14, 2023.
Al-Kassab-Cordova A , Mendez-Guerra C , Quevedo-Ramirez A , Espinoza R , Enriquez-Vera D , Robles-Valcarcel P , 2022. Rural and urban disparities in anemia among Peruvian children aged 6–59 months: A multivariate decomposition and spatial analysis. Rural Remote Health 22: 6936.
Instituto Nacional de Estadistica e Informatica , 2020. Mapa de Pobreza Monetaria Provincial y Distrital 2018. Gobierno del Peru, Lima. Available at: www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1718/Libro.pdf. Accessed July 10, 2023.
Instituto Nacional de Estadistica e Informatica , 2020. Peru: Estimaciones y Proyecciones de Poblacion por Departamento, Provincia y Distrito, 2018–2020: Boletín Especial N°26. Gobierno del Peru, Lima. Available at: www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1715/libro.pdf Accessed July 2, 2023.
Webb MC , Morales ML , Lopez M , Baca-Turpo B , Arque E , White AC Jr. , Cabada MM , 2021. Stunting in pre-school and school-age children in the Peruvian highlands and its association with Fasciola infection and demographic factors. PLoS Negl Trop Dis 15: e0009519.
Schreiner M , 2012. Simple Poverty Scorecard Poverty–Assessment Tool Peru. Available at: www.simplepovertyscorecard.com/PER_2010_ENG.pdf Accessed May 30, 2023.
Lopez M , Morales ML , Konana M , Hoyer P , Pineda-Reyes R , White AC Jr , Garcia HH , Lescano AG , Gotuzzo E , Cabada MM , 2016. Kato-Katz and Lumbreras rapid sedimentation test to evaluate helminth prevalence in the setting of a school-based deworming program. Pathog Glob Health 110: 130–134.
Garrido-Salazar DI , Garrido-Salazar SM , Vivas-Armas G , 2019. Anemia frequency in children living at Andean high altitude in Ecuador, Peru, and Bolivia. Acta Pediatr Mex 40: 305–317.
Berky AJ , Robie E , Ortiz EJ , Meyer JN , Hsu-Kim H , Pan WK , 2020. Evaluation of Peruvian government interventions to reduce childhood anemia. Ann Glob Health 86: 98.
Nestel P , 2002. Adjusting Hemoglobin Values in Program Surveys. The International Nutritional Anemia Consultative Group Steering Committee. Available at: pdf.usaid.gov/pdf_docs/PNACQ927.pdf. Accessed May 15, 2023.
Cabada MM , Goodrich MR , Graham B , Villanueva-Meyer PG , Deichsel EL , Lopez M , Arque E , White AC Jr. , 2015. Prevalence of intestinal helminths, anemia, and malnutrition in Paucartambo, Peru. Rev Panam Salud Publica 37: 69–75.
Lopez A , Cacoub P , Macdougall IC , Peyrin-Biroulet L , 2016. Iron deficiency anaemia. Lancet 387: 907–916.
Choque-Quispe BM , Alarcon-Yaquetto DE , Paredes-Ugarte W , Zaira A , Ochoa A , Gonzales GF , 2020. Is the prevalence of anemia in children living at high altitudes real? An observational study in Peru. Ann N Y Acad Sci 1473: 35–47.
Sharma AJ , Addo OY , Mei Z , Suchdev PS , 2019. Reexamination of hemoglobin adjustments to define anemia: Altitude and smoking. Ann N Y Acad Sci 1450: 190–203.
Muñoz-Antoli C , Pérez P , Pavón A , Toledo R , Esteban JG , 2018. Soil-transmitted helminth infections and anemia in schoolchildren from Corn Island Archipelago (RAAS, Nicaragua). Am J Trop Med Hyg 99: 1591–1597.
Gyorkos TW , Gilbert NL , Larocque R , Casapia M , Montresor A , 2012. Re-visiting Trichuris trichiura intensity thresholds based on anemia during pregnancy. PLoS Negl Trop Dis 6: e1783.
Sarma H , Wangdi K , Tariqujjaman M , Das R , Rahman M , Kelly M , Ahmed T , Gray DJ , 2021. The effects of deworming and multiple micronutrients on anaemia in preschool children in Bangladesh: Analysis of five cross-sectional surveys. Nutrients 14: 150.
Spinicci M et al., 2018. Hymenolepis nana: An emerging intestinal parasite associated with anemia in school children from the Bolivian Chaco. Am J Trop Med Hyg 99: 1598–1601.
Afridi MF , Farhat K , Ahmed Z , Ahmed H , Ali S , Qaisrani MN , 2021. Association between intestinal helminthic infections and anaemia status in preschool children in the district Skardu of Pakistan. J Pak Med Assoc 71: 2309–2312.
Larsen DA , Grisham T , Slawsky E , Narine L , 2017. An individual-level meta-analysis assessing the impact of community-level sanitation access on child stunting, anemia, and diarrhea: Evidence from DHS and MICS surveys. PLoS Negl Trop Dis 11: e0005591.
Tusting LS , Gething PW , Gibson HS , Greenwood B , Knudsen J , Lindsay SW , Bhatt S , 2020. Housing and child health in sub-Saharan Africa: A cross-sectional analysis. PLoS Med 17: e1003055.
Vilchez Barreto PM , Gamboa R , Santivañez S , O’Neal SE , Muro C , Lescano AG , Moyano L-M , Gonzálvez G , García HH ; The Cysticercosis Working Group in Perú , 2017. Prevalence, age profile, and associated risk factors for Hymenolepis nana infection in a large population-based study in Northern Peru. Am J Trop Med Hyg 97: 583–586.
Cabada MM , Morales ML , Lopez M , Reynolds ST , Vilchez EC , Lescano AG , Gotuzzo E , Garcia HH , White AC Jr. , 2016. Hymenolepis nana impact among children in the highlands of Cusco, Peru: An emerging neglected parasite infection. Am J Trop Med Hyg 95: 1031–1036.
Shimanda PP , Amukugo HJ , Norström F , 2020. Socioeconomic factors associated with anemia among children aged 6–59 months in Namibia. J Public Health Africa 11: 1131.
Cabada MM , Morales ML , Webb CM , Yang L , Bravenec CA , Lopez M , Bascope R , White AC , Gotuzzo E , 2018. Socioeconomic factors associated with Fasciola hepatica infection among children from 26 communities of the Cusco region of Peru. Am J Trop Med Hyg 99: 1180–1185.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1935 | 1935 | 76 |
Full Text Views | 208 | 208 | 22 |
PDF Downloads | 74 | 74 | 2 |
Anemia is a complex condition associated with diet, chronic infections, and blood loss. Children living at high altitudes have higher absolute hemoglobin levels due to hypoxemia. However, they are exposed to repeated infections and dietary limitations. We conducted a cross-sectional study to identify factors affecting the hemoglobin concentration in children living in high-altitude rural communities in the Anta province of Peru. All children 3–16 years of age attending public schools were invited to participate. We enrolled children 3–16 years old in schools and visited their homes to collect demographic, socioeconomic, medical history, and anthropometric data. Children provided blood and stool samples for complete blood counts, iron status markers, and helminth infection testing. Among the 2,000 children enrolled, the mean age was 9.9 (±3.4) years, 1,004 (50.2%) were female, and the median residence altitude was 3,398 (interquartile range 3,35–3,497) meters. The mean hemoglobin level was 15 (±1.15) mg/dL; 320 (16%) had anemia as defined by WHO. Children with anemia were more likely to have lower serum iron levels (odds ratio [OR] 2.8 [95% CI 2.2–3.6], P <0.001) and serum transferrin saturation (OR 2.8 [95% CI 2–3.9], P <0.001). Younger age (OR 0.85 [95% CI 0.82–0.89], P <0.001), stunting (OR 0.68 [95% CI 0.59–0.79], P <0.001), education of the mother (OR 0.94 [95% CI 0.91–0.98], P <0.005), and low eosinophils (OR 0.49 [95% CI 0.26–0.9], P = 0.022) were associated with anemia. Helminth infections were not associated with anemia. Anemia among children at high altitude is multifactorial, but iron deficiency is a contributing factor. Further studies are needed to evaluate iron status and anemia in children living at high altitudes.
Financial support: This study was supported by the
Disclosure: The contents of this manuscript are solely the responsibility of the authors and do not necessarily represent the official views of the National Institute for Allergy and Infectious Diseases.
Authors’ addresses: Maria A. Caravedo, Melinda Tanabe, and A. Clinton White Jr., Division of Infectious Diseases, Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, E-mails: macarave@utmb.edu, mbtanabe@utmb.edu, and acwhite@utmb.edu. Maria Luisa Morales and Martha Lopez, Sede Cusco – Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Cusco, Peru, E-mails: malu.morales.fernandez@gmail.com and martlop2000@gmail.com. Miguel M. Cabada, Division of Infectious Diseases, Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, and Sede Cusco – Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Cusco, Peru, E-mail: micabada@utmb.edu.
World Health Organization , 2011. Hemoglobin Concentrations for the Diagnosis of Anemia and Assessment of Severity. WHO/NMH/NHD/MNM/11.1. Geneva, Switzerland: World Health Organization. Available at: https://apps.who.int/iris/handle/10665/85839. Accessed July 15, 2023.
McLean E , Cogswell M , Egli I , Wojdyla D , de Benoist B , 2009. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr 12: 444–454.
Rosas-Jimenez C , Tercan E , Horstick O , Igboegwu E , Dambach P , Louis VR , Winkler V , Deckert A , 2022. Prevalence of anemia among Indigenous children in Latin America: A systematic review. Rev Saude Publica 56: 99.
Walter T , De Andraca I , Chadud P , Perales CG , 1989. Iron deficiency anemia: Adverse effects on infant psychomotor development. Pediatrics 84: 7–17.
Lozoff B , De Andraca I , Castillo M , Smith JB , Walter Y , Pino P , 2003. Behavioral and developmental effects of preventing iron-deficiency anemia in healthy full-term infants. Pediatrics 112: 846–854.
World Health Organization , 2023. Anemia. Available at: www.who.int/health-topics/anaemia#tab=tab_2. Accessed July 20, 2023.
Ellwanger JH , Ziliotto M , Kulmann-Leal B , Chies JAB , 2022. Iron deficiency and soil-transmitted helminth infection: Classic and neglected connections. Parasitol Res 121: 3381–3392.
Gujo AB , Kare AP , 2021. Prevalence of intestinal parasite infection and its association with anemia among children aged 6 to 59 months in Sidama National Regional State, southern Ethiopia. Clin Med Insights Pediatr 15: 11795565211029259.
Le HT , Brouwer ID , Verhoef H , Nguyen KC , Kok FJ , 2007. Anemia and intestinal parasite infection in school children in rural Vietnam. Asia Pac J Clin Nutr 16: 716–723.
Caravedo MA , Cabada MM , 2020. Human fascioliasis: Current epidemiological status and strategies for diagnosis, treatment, and control. Res Rep Trop Med 11: 149–158.
Lopez M , White AC Jr. , Cabada MM , 2012. Burden of Fasciola hepatica infection among children from Paucartambo in Cusco, Peru. Am J Trop Med Hyg 86: 481–485.
Reiner RC et al., 2019. Diseases, injuries, and risk factors in child and adolescent health, 1990 to 2017: Findings from the Global Burden of Diseases, Injuries, and Risk Factors 2017 Study. JAMA Pediatr 173: e190337.
Accinelli RA , Leon-Abarca JA , 2020. Age and altitude of residence determine anemia prevalence in Peruvian 6 to 35 months old children. PLoS One 15: e0226846.
Smith JL , Johnston P , Dearden KA , Eggett DL , Campbell AK , 2010. The Impact of Altitude and Diet on Anemia in School-Aged Children in Lago San Pablo, Ecuador. Available at: https://journals.sagepub.com/doi/pdf/10.1177/1941406410383013. Accessed September 14, 2023.
Al-Kassab-Cordova A , Mendez-Guerra C , Quevedo-Ramirez A , Espinoza R , Enriquez-Vera D , Robles-Valcarcel P , 2022. Rural and urban disparities in anemia among Peruvian children aged 6–59 months: A multivariate decomposition and spatial analysis. Rural Remote Health 22: 6936.
Instituto Nacional de Estadistica e Informatica , 2020. Mapa de Pobreza Monetaria Provincial y Distrital 2018. Gobierno del Peru, Lima. Available at: www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1718/Libro.pdf. Accessed July 10, 2023.
Instituto Nacional de Estadistica e Informatica , 2020. Peru: Estimaciones y Proyecciones de Poblacion por Departamento, Provincia y Distrito, 2018–2020: Boletín Especial N°26. Gobierno del Peru, Lima. Available at: www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1715/libro.pdf Accessed July 2, 2023.
Webb MC , Morales ML , Lopez M , Baca-Turpo B , Arque E , White AC Jr. , Cabada MM , 2021. Stunting in pre-school and school-age children in the Peruvian highlands and its association with Fasciola infection and demographic factors. PLoS Negl Trop Dis 15: e0009519.
Schreiner M , 2012. Simple Poverty Scorecard Poverty–Assessment Tool Peru. Available at: www.simplepovertyscorecard.com/PER_2010_ENG.pdf Accessed May 30, 2023.
Lopez M , Morales ML , Konana M , Hoyer P , Pineda-Reyes R , White AC Jr , Garcia HH , Lescano AG , Gotuzzo E , Cabada MM , 2016. Kato-Katz and Lumbreras rapid sedimentation test to evaluate helminth prevalence in the setting of a school-based deworming program. Pathog Glob Health 110: 130–134.
Garrido-Salazar DI , Garrido-Salazar SM , Vivas-Armas G , 2019. Anemia frequency in children living at Andean high altitude in Ecuador, Peru, and Bolivia. Acta Pediatr Mex 40: 305–317.
Berky AJ , Robie E , Ortiz EJ , Meyer JN , Hsu-Kim H , Pan WK , 2020. Evaluation of Peruvian government interventions to reduce childhood anemia. Ann Glob Health 86: 98.
Nestel P , 2002. Adjusting Hemoglobin Values in Program Surveys. The International Nutritional Anemia Consultative Group Steering Committee. Available at: pdf.usaid.gov/pdf_docs/PNACQ927.pdf. Accessed May 15, 2023.
Cabada MM , Goodrich MR , Graham B , Villanueva-Meyer PG , Deichsel EL , Lopez M , Arque E , White AC Jr. , 2015. Prevalence of intestinal helminths, anemia, and malnutrition in Paucartambo, Peru. Rev Panam Salud Publica 37: 69–75.
Lopez A , Cacoub P , Macdougall IC , Peyrin-Biroulet L , 2016. Iron deficiency anaemia. Lancet 387: 907–916.
Choque-Quispe BM , Alarcon-Yaquetto DE , Paredes-Ugarte W , Zaira A , Ochoa A , Gonzales GF , 2020. Is the prevalence of anemia in children living at high altitudes real? An observational study in Peru. Ann N Y Acad Sci 1473: 35–47.
Sharma AJ , Addo OY , Mei Z , Suchdev PS , 2019. Reexamination of hemoglobin adjustments to define anemia: Altitude and smoking. Ann N Y Acad Sci 1450: 190–203.
Muñoz-Antoli C , Pérez P , Pavón A , Toledo R , Esteban JG , 2018. Soil-transmitted helminth infections and anemia in schoolchildren from Corn Island Archipelago (RAAS, Nicaragua). Am J Trop Med Hyg 99: 1591–1597.
Gyorkos TW , Gilbert NL , Larocque R , Casapia M , Montresor A , 2012. Re-visiting Trichuris trichiura intensity thresholds based on anemia during pregnancy. PLoS Negl Trop Dis 6: e1783.
Sarma H , Wangdi K , Tariqujjaman M , Das R , Rahman M , Kelly M , Ahmed T , Gray DJ , 2021. The effects of deworming and multiple micronutrients on anaemia in preschool children in Bangladesh: Analysis of five cross-sectional surveys. Nutrients 14: 150.
Spinicci M et al., 2018. Hymenolepis nana: An emerging intestinal parasite associated with anemia in school children from the Bolivian Chaco. Am J Trop Med Hyg 99: 1598–1601.
Afridi MF , Farhat K , Ahmed Z , Ahmed H , Ali S , Qaisrani MN , 2021. Association between intestinal helminthic infections and anaemia status in preschool children in the district Skardu of Pakistan. J Pak Med Assoc 71: 2309–2312.
Larsen DA , Grisham T , Slawsky E , Narine L , 2017. An individual-level meta-analysis assessing the impact of community-level sanitation access on child stunting, anemia, and diarrhea: Evidence from DHS and MICS surveys. PLoS Negl Trop Dis 11: e0005591.
Tusting LS , Gething PW , Gibson HS , Greenwood B , Knudsen J , Lindsay SW , Bhatt S , 2020. Housing and child health in sub-Saharan Africa: A cross-sectional analysis. PLoS Med 17: e1003055.
Vilchez Barreto PM , Gamboa R , Santivañez S , O’Neal SE , Muro C , Lescano AG , Moyano L-M , Gonzálvez G , García HH ; The Cysticercosis Working Group in Perú , 2017. Prevalence, age profile, and associated risk factors for Hymenolepis nana infection in a large population-based study in Northern Peru. Am J Trop Med Hyg 97: 583–586.
Cabada MM , Morales ML , Lopez M , Reynolds ST , Vilchez EC , Lescano AG , Gotuzzo E , Garcia HH , White AC Jr. , 2016. Hymenolepis nana impact among children in the highlands of Cusco, Peru: An emerging neglected parasite infection. Am J Trop Med Hyg 95: 1031–1036.
Shimanda PP , Amukugo HJ , Norström F , 2020. Socioeconomic factors associated with anemia among children aged 6–59 months in Namibia. J Public Health Africa 11: 1131.
Cabada MM , Morales ML , Webb CM , Yang L , Bravenec CA , Lopez M , Bascope R , White AC , Gotuzzo E , 2018. Socioeconomic factors associated with Fasciola hepatica infection among children from 26 communities of the Cusco region of Peru. Am J Trop Med Hyg 99: 1180–1185.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1935 | 1935 | 76 |
Full Text Views | 208 | 208 | 22 |
PDF Downloads | 74 | 74 | 2 |