Objective
To identify the characteristics of anemia in children living at different geographical altitude in the Arequipa Region of Peru.

Methods
We did a descriptive and retrospective study. The population consisted of 106 499 children under five years of age living in the Arequipa Region at different geographical altitude and receiving care by the Ministry of Health of Arequipa. Of these, 32 454 had anemia (30.5%). Socio-demographic data related to age, province, and beneficiary of the Comprehensive Health System program, home visits, and growth and development were obtained, in addition to data regarding anemia such as frequency, hemoglobin, and severity.

Results
The results were categorized by the geographical altitude of origin of children under 0 to 59 months of age and hemoglobin levels according to geographical altitude. Of the sample studied, the frequency of anemia at different geographical altitudes of Arequipa in children under five for the 2017 to 2019 period was: 18.7% at 0 to 999 meters above sea level; 29.6% at 1000 to 1999 meters; 31.6% at 2000 to 2999 meters; 42.9% at 3000 to 3999 meters; and 54.4% at 4000 to 4999 meters. There was a higher prevalence of anemia when the geographic altitude correction factor was used.

Conclusions
A significant statistical relationship (p < 0.05) was observed between the corrected hemoglobin according to the World Health Organization parameters and the altitude at which children with anemia live: the higher the geographical altitude, the greater the anemia in children. Supplementation programs should be included during home visits and at the time of evaluation of children's growth and development.

Authors: Águeda Muñoz del Carpio-Toia[1], Ismael Cornejo-Roselló[2], Sandrino Rojas-Pauca[2], Giancarlo Alvarez-Cervantes[3], Julio César Bernabé-Ortiz[4], Ada Gallegos[5], Sively Mercado-Mamani[6], Alex Veliz-Burgos[7], Milena Toia-Larsen[4]

Affiliation:
[1] Vicerrectorado de Investigación, Escuela de Medicina Humana, Universidad Católica de Santa María, Arequipa, Perú
[2] Dirección Regional de Salud de Arequipa, Arequipa, Perú
[3] Vicerrectorado de Investigación, Universidad Católica de Santa María, Arequipa, Perú
[4] Escuela de Postgrado, Universidad Católica de Santa María, Arequipa, Perú
[5] Facultad de Educación, Universidad Nacional Mayor de San Marcos, Lima, Perú
[6] Escuela de Postgrado, Universidad Nacional del Altiplano, Puno, Perú
[7] Departamento de Ciencias Sociales, Universidad de Los Lagos, Osorno, Chile

E-mail: amunozde@ucsm.edu.pe

Author address:
[1] Calle Garcilazo de la Vega 108 segundo piso Umacollo
Arequipa, Perú
Código postal: 04001

Citation: Muñoz del Carpio-Toia A, Cornejo-Roselló I, Rojas-Pauca S, Alvarez-Cervantes G, Bernabé-Ortiz JC, Gallegos A, et al. Childhood anemia in populations residing at different geographical altitudes of Arequipa, Peru: A descriptive and retrospective study. Medwave 2020;20(7):e8004 doi: 10.5867/medwave.2020.07.8004

Submission date: 26/2/2020

Acceptance date: 19/7/2020

Publication date: 26/8/2020

Origin: Not commissioned.

Type of review: Externally peer-reviewed by three reviewers, double-blind.

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1. World Health Organization. Worldwide prevalence of anemia, 1993-2005: WHO global database on anemia. Geneva. WHO. 2008. [Internet] | Link |
2. Gonzales GF, Fano D, Vásquez-Velásquez C. Necesidades de investigación para el diagnóstico de anemia en poblaciones de altura. Revista peruana de medicina experimental y salud pública. 2017. 34: 699-708. | CrossRef |
3. World Health Organization. Iron Deficiency Anemia. Assessment, Prevention and Control. In A Guide for Progamme Managers. Geneva. WHO. 2001. [Internet] | Link |
4. Ministerio de Salud del Perú. Norma técnica - manejo terapéutico y preventivo de la anemia en niños, adolescentes, mujeres gestantes y puérperas. Ministerio de Salud del Perú. 2017. [Internet] | Link |
5. Gonzales GF, Alarcón-Yaquetto DE, Zevallos-Concha A. Human adaptation to life at high altitude. En Biochemistry of Oxidative Stress. Springer, Cham, 2016: 109-126.
6. Gassmann M, Mairbäurl H, Livshits L, Seide S, Hackbusch M, Malczyk M, et al. The increase in hemoglobin concentration with altitude varies among human populations. Ann N Y Acad Sci. 2019 Aug;1450(1):204-220. | CrossRef | PubMed |
7. Zavaleta N. Anemia infantil: retos y oportunidades al 2021. Rev. perú. med. exp. salud publica. 2017;34(4): 588-589. | CrossRef |
8. Stoltzfus RJ, Mullany L, Black RE. Iron deficiency anaemia. Comparative quantification of health risks: global and regional burden of disease attributable to selected major risk factors. 2004; 1:163-209.
9. Engle-Stone R, Aaron GJ, Huang J, Wirth JP, Namaste SM, Williams AM, et al. Predictors of anemia in preschool children: Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project. Am J Clin Nutr. 2017 Jul;106(Suppl 1):402S-415S. | CrossRef | PubMed |
10. Organización Mundial de la Salud. Concentraciones de hemoglobina para diagnosticar la anemia y evaluar su gravedad. Ginebra. OMS. 2011. [Internet] | Link |
11. Garrido-Salazar DI, Garrido-Salazar SM, Torres-Changoluisa T, Fuseau-Herrera M, Muyulema-Ruiz C, Palate-Nuñez P, et al. Prevalencia de anemia en niños de dos escuelas rurales a diferentes altitudes. Un estudio transversal. Acta PediatrMex. 2018: 39(4):289-298. [Internet] | Link |
12. San Miguel-Simbrón JL, Muñoz-Vera M, Urteaga-Mamani N, Espejo-Aliaga E. Deficiencia de hierro y anemia en escolares residentes de gran altitud: asociación con infección. Cuad. - Hosp. Clín. 2014; 55(2): 24-33. [internet] | Link |
13. Tariku EZ, Abebe GA, Melketsedik ZA, Gutema BT, Megersa ND, Sorrie MB, et al. Anemia and its associated factors among school-age children living in different climatic zones of Arba Minch Zuria District, Southern Ethiopia. BMC Hematol. 2019 Apr 23;19:6. | CrossRef | PubMed |
14. Wise PH, Meyers A. Poverty and Child Health. Pediatric Clinics of North America. 1988; 35 (6): 1169-1186. | CrossRef |
15. Séraphin MN, Xinguang C, Ayoya MA, Ngnie-Teta I, Boldon E, Mamadoultaibou A, et al. Childhood anemia in Rural Haiti: the potential role of community health workers. Glob Health Res Policy. 2017 Jan 23;2:3. | CrossRef | PubMed |
16. Goswmai S, Das KK. Socio-economic and demographic determinants of childhood anemia. J Pediatr (Rio J). 2015 Sep-Oct;91(5):471-7. | CrossRef | PubMed |
17. Da Fonseca CRB, Machado BL, Alquati L R, Couto MM, Matubara FN. Anemia and Nutritional Status of Preschool Children: Comparison between Two Childhood Education Centres in Botucatu City, Brazil. Epidemiology (Sunnyvale). 2016; 6(282): 2161-1165. [Internet] | Link |
18. Hurtado A, Merino C, Delgado E. Influence of anoxaemia on the hematopoietic activity. Arch. Int. Med. 1945;75: 284–323. [Internet] | Link |
19. Ward M, Milledge J, West J. High Altitude Medicine and Physiology. 3era edición. Great Britain. Arnold, a member of the hodder headline group. 2000. Capítulo 17: High Altitude Populations. p2002.
20. West J. The Atmosphere. High Altitude and Exploration of Human Adaptation. New York, USA: Marcel Dekker. 2001. p25-40.
21. Trompetero-González AC, Cristancho-Mejía E, Benavides-Pinzón WF, Serrato M, Landinéz M-P, Rojas J. Comportamiento de la concentración de hemoglobina, el hematocrito y la saturación de oxígeno en una población universitaria en Colombia a diferentes alturas. Nutrición Hospitalaria. 2015;32(5):2309-2318. | CrossRef |
22. Gonzales GF, Fano D, Vasquez-Velasquez C. Diagnosis of anemia in populations at high altitudes. Revista peruana de medicina experimental y salud pública. 2017;34(4):699-708. | CrossRef | PubMed |
23. Dang SN, Yan H, Wang XL. Study on the hemoglobin levels of children under the age of three years and the prevalence of anemia at high altitude in Tibet of China. Zhonghua Liu Xing Bing Xue Za Zhi. 2003 Dec;24(12):1108-11. | PubMed |
24. Accinelli RA, Leon-Abarca JA. Age and altitude of residence determine anemia prevalence in Peruvian 6 to 35 months old children. PLoS One. 2020 Jan 15;15(1):e0226846. | CrossRef | PubMed |
25. Cohen JH, Haas JD. Hemoglobin correction factors for estimating the prevalence of iron deficiency anemia in pregnant women residing at high altitudes in Bolivia. Rev Panam Salud Publica. 1999 Dec;6(6):392-9. | CrossRef | PubMed |
26. Dang SN, Yan H, Wang XL. Study on the hemoglobin levels of children under the age of three years and the prevalence of anemia at high altitude in Tibet of China. Zhonghua Liu Xing Bing Xue Za Zhi. 2001 Dec;24(12):1108-11.
27. Donahue Angel M, Berti P, Siekmans K, Tugirimana PL, Boy E. Prevalence of Iron Deficiency and Iron Deficiency Anemia in the Northern and Southern Provinces of Rwanda. Food Nutr Bull. 2017 Dec;38(4):554-563. | CrossRef | PubMed |
28. Barrera-Reyes PK, Tejero ME. Genetic variation influencing hemoglobin levels and risk for anemia across populations. Ann N Y Acad Sci. 2019 Aug;1450(1):32-46. | CrossRef | PubMed |
29. Muñoz del Carpio-Toia A, Dueñas-Ancco A, Sánchez-Rodríguez K, Begazo-Muñoz L. Adecuación cultural y capacitación acerca del proceso de consentimiento informado en proyecto sobre nutrición escolar en un pueblo indígena aymara de Perú. pers.bioét. 2017 Jan; 21( 1 ): 78-91. | CrossRef |
30. Muñoz del Carpio-Toia A. Ética de la investigación en poblaciones originarias. Casado M y Luna F. Cuestiones de bioética en y desde Latinoamérica. Civitas. Navarra. 2012.
31. Muñoz del Carpio-Toia A, Góngora-Cárdenas R, Góngora-Prado R, Ontiveros-Aparicio W, Cuba JA, Meza-Gómez P, et al. Use of an educational intervention with audiovisual material to improve knowledge and practices on metaxenic diseases in schoolchildren. Peru. 2019. [Internet] | Link |

World Health Organization. Worldwide prevalence of anemia, 1993-2005: WHO global database on anemia. Geneva. WHO. 2008. [Internet] | Link |

Gonzales GF, Fano D, Vásquez-Velásquez C. Necesidades de investigación para el diagnóstico de anemia en poblaciones de altura. Revista peruana de medicina experimental y salud pública. 2017. 34: 699-708. | CrossRef |

World Health Organization. Iron Deficiency Anemia. Assessment, Prevention and Control. In A Guide for Progamme Managers. Geneva. WHO. 2001. [Internet] | Link |

Ministerio de Salud del Perú. Norma técnica - manejo terapéutico y preventivo de la anemia en niños, adolescentes, mujeres gestantes y puérperas. Ministerio de Salud del Perú. 2017. [Internet] | Link |

Gonzales GF, Alarcón-Yaquetto DE, Zevallos-Concha A. Human adaptation to life at high altitude. En Biochemistry of Oxidative Stress. Springer, Cham, 2016: 109-126.

Gassmann M, Mairbäurl H, Livshits L, Seide S, Hackbusch M, Malczyk M, et al. The increase in hemoglobin concentration with altitude varies among human populations. Ann N Y Acad Sci. 2019 Aug;1450(1):204-220. | CrossRef | PubMed |

Zavaleta N. Anemia infantil: retos y oportunidades al 2021. Rev. perú. med. exp. salud publica. 2017;34(4): 588-589. | CrossRef |

Stoltzfus RJ, Mullany L, Black RE. Iron deficiency anaemia. Comparative quantification of health risks: global and regional burden of disease attributable to selected major risk factors. 2004; 1:163-209.

Engle-Stone R, Aaron GJ, Huang J, Wirth JP, Namaste SM, Williams AM, et al. Predictors of anemia in preschool children: Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project. Am J Clin Nutr. 2017 Jul;106(Suppl 1):402S-415S. | CrossRef | PubMed |

Organización Mundial de la Salud. Concentraciones de hemoglobina para diagnosticar la anemia y evaluar su gravedad. Ginebra. OMS. 2011. [Internet] | Link |

Garrido-Salazar DI, Garrido-Salazar SM, Torres-Changoluisa T, Fuseau-Herrera M, Muyulema-Ruiz C, Palate-Nuñez P, et al. Prevalencia de anemia en niños de dos escuelas rurales a diferentes altitudes. Un estudio transversal. Acta PediatrMex. 2018: 39(4):289-298. [Internet] | Link |

San Miguel-Simbrón JL, Muñoz-Vera M, Urteaga-Mamani N, Espejo-Aliaga E. Deficiencia de hierro y anemia en escolares residentes de gran altitud: asociación con infección. Cuad. - Hosp. Clín. 2014; 55(2): 24-33. [internet] | Link |

Tariku EZ, Abebe GA, Melketsedik ZA, Gutema BT, Megersa ND, Sorrie MB, et al. Anemia and its associated factors among school-age children living in different climatic zones of Arba Minch Zuria District, Southern Ethiopia. BMC Hematol. 2019 Apr 23;19:6. | CrossRef | PubMed |

Wise PH, Meyers A. Poverty and Child Health. Pediatric Clinics of North America. 1988; 35 (6): 1169-1186. | CrossRef |

Séraphin MN, Xinguang C, Ayoya MA, Ngnie-Teta I, Boldon E, Mamadoultaibou A, et al. Childhood anemia in Rural Haiti: the potential role of community health workers. Glob Health Res Policy. 2017 Jan 23;2:3. | CrossRef | PubMed |

Goswmai S, Das KK. Socio-economic and demographic determinants of childhood anemia. J Pediatr (Rio J). 2015 Sep-Oct;91(5):471-7. | CrossRef | PubMed |

Da Fonseca CRB, Machado BL, Alquati L R, Couto MM, Matubara FN. Anemia and Nutritional Status of Preschool Children: Comparison between Two Childhood Education Centres in Botucatu City, Brazil. Epidemiology (Sunnyvale). 2016; 6(282): 2161-1165. [Internet] | Link |

Hurtado A, Merino C, Delgado E. Influence of anoxaemia on the hematopoietic activity. Arch. Int. Med. 1945;75: 284–323. [Internet] | Link |

Ward M, Milledge J, West J. High Altitude Medicine and Physiology. 3era edición. Great Britain. Arnold, a member of the hodder headline group. 2000. Capítulo 17: High Altitude Populations. p2002.

West J. The Atmosphere. High Altitude and Exploration of Human Adaptation. New York, USA: Marcel Dekker. 2001. p25-40.

Trompetero-González AC, Cristancho-Mejía E, Benavides-Pinzón WF, Serrato M, Landinéz M-P, Rojas J. Comportamiento de la concentración de hemoglobina, el hematocrito y la saturación de oxígeno en una población universitaria en Colombia a diferentes alturas. Nutrición Hospitalaria. 2015;32(5):2309-2318. | CrossRef |

Gonzales GF, Fano D, Vasquez-Velasquez C. Diagnosis of anemia in populations at high altitudes. Revista peruana de medicina experimental y salud pública. 2017;34(4):699-708. | CrossRef | PubMed |

Dang SN, Yan H, Wang XL. Study on the hemoglobin levels of children under the age of three years and the prevalence of anemia at high altitude in Tibet of China. Zhonghua Liu Xing Bing Xue Za Zhi. 2003 Dec;24(12):1108-11. | PubMed |

Accinelli RA, Leon-Abarca JA. Age and altitude of residence determine anemia prevalence in Peruvian 6 to 35 months old children. PLoS One. 2020 Jan 15;15(1):e0226846. | CrossRef | PubMed |

Cohen JH, Haas JD. Hemoglobin correction factors for estimating the prevalence of iron deficiency anemia in pregnant women residing at high altitudes in Bolivia. Rev Panam Salud Publica. 1999 Dec;6(6):392-9. | CrossRef | PubMed |

Dang SN, Yan H, Wang XL. Study on the hemoglobin levels of children under the age of three years and the prevalence of anemia at high altitude in Tibet of China. Zhonghua Liu Xing Bing Xue Za Zhi. 2001 Dec;24(12):1108-11.

Donahue Angel M, Berti P, Siekmans K, Tugirimana PL, Boy E. Prevalence of Iron Deficiency and Iron Deficiency Anemia in the Northern and Southern Provinces of Rwanda. Food Nutr Bull. 2017 Dec;38(4):554-563. | CrossRef | PubMed |

Barrera-Reyes PK, Tejero ME. Genetic variation influencing hemoglobin levels and risk for anemia across populations. Ann N Y Acad Sci. 2019 Aug;1450(1):32-46. | CrossRef | PubMed |

Muñoz del Carpio-Toia A, Dueñas-Ancco A, Sánchez-Rodríguez K, Begazo-Muñoz L. Adecuación cultural y capacitación acerca del proceso de consentimiento informado en proyecto sobre nutrición escolar en un pueblo indígena aymara de Perú. pers.bioét. 2017 Jan; 21( 1 ): 78-91. | CrossRef |

Muñoz del Carpio-Toia A. Ética de la investigación en poblaciones originarias. Casado M y Luna F. Cuestiones de bioética en y desde Latinoamérica. Civitas. Navarra. 2012.

Muñoz del Carpio-Toia A, Góngora-Cárdenas R, Góngora-Prado R, Ontiveros-Aparicio W, Cuba JA, Meza-Gómez P, et al. Use of an educational intervention with audiovisual material to improve knowledge and practices on metaxenic diseases in schoolchildren. Peru. 2019. [Internet] | Link |