Age and altitude of residence determine anemia prevalence in Peruvian 6 to 35 months old children

Autoři: Roberto Alfonso Accinelli aff001;  Juan Alonso Leon-Abarca aff001
Působiště autorů: Instituto de Investigaciones de la Altura, Universidad Peruana Cayetano Heredia, Lima, Perú aff001;  Facultad de Medicina Alberto Hurtado, Universidad Peruana Cayetano Heredia, Lima, Perú aff002;  Hospital Cayetano Heredia, Lima, Perú aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article



A Demographic and Family Health Survey (ENDES, for Encuesta Demográfica y de Salud Familiar in Spanish) is carried out annually in Peru. Based on it, the anemia prevalence was 43.6% in 2016 and 43.8% in 2017 using the WHO cutoff value of 11 g/dL and the altitude-correction equation.


To assess factors contributing to anemia and to determine its prevalence in Peruvian children 6 to 35 months old.


We used the MEASURE DHS-based ENDES survey to obtain representative data for11364 children from 6 to 35 months old on hemoglobin and health determinants. To evaluate normal hemoglobin levels, we used the original WHO criterion of the 5th percentile in children without chronic malnutrition and then applied it to the overall population. Relationships between hemoglobin and altitude levels, usage of cleaning methods to sanitize water safe to drink, usage of solid fuels and poverty status were tested using methodology for complex survey data. Percentile curves were made for altitude intervals by plotting hemoglobin compared to age. The new anemia rates are presented in graphs by Peruvian political regions according to the degree of public health significance.


Hemoglobin increased as age and altitude of residence increased. Using the 5th percentile, anemia prevalence was 7.3% in 2016 and 2017. Children from low altitudes had higher anemia prevalence (8.5%) than those from high altitudes (1.2%, p<0.0001). In the rainforest area of Peru, anemia prevalence was highest (13.5%), while in the highlands it was lowest (3.3%, p<0.0001). With access to safe drinking water and without chronic malnutrition, anemia rates could be reduced in the rainforest by 45% and 33%, respectively.


Anemia prevalence in Peruvian children from 6 to 35 months old was 7.3% in 2016 and 2017.

Klíčová slova:

anémia – Fuels – Hemoglobin – Children – Iron deficiency anemia – Malnutrition – Rainforests – Water resources


1. World Health Organization. Iron deficiency anemia: Report of a study group. Wld Hlth Org techn Rep Ser. 1959;(182):4.

2. WHO Scientific Group on Nutritional Anaemias, World Health Organization. Nutritional anaemias: report of a WHO scientific group [‎meeting held in Geneva from 13 to 17 March 1967]‎. World Health Organ Tech Rep Ser. 1968;405. 4975372

3. Din ZU, Pervez L, Amir A, Abbas M, Khan I, Iqbal Z, et al. Parasitic infections, malnutrition and anemia among preschool children living in rural areas of Peshawar, Pakistan. Nutr Hosp. 2018 Oct 5;35(5):1145–52. doi: 10.20960/nh.1685 30307299

4. Kawo KN, Asfaw ZG, Yohannes N. Multilevel Analysis of Determinants of Anemia Prevalence among Children Aged 6–59 Months in Ethiopia: Classical and Bayesian Approach. Anemia. Jun 3;2018:3087354. doi: 10.1155/2018/3087354 29973986

5. Monge MC. La enfermedad de los Andes (Síndromes eritrémicos). Anales de la Facultad de Medicina. 1928; 14:1–314.

6. Hurtado A, Merino C, Delgado E. Influence of anoxemia on the hemopoietic activity. Arch Intern Med. 1945;75(5):284–323.

7. Centers for Disease Control and Prevention. Criteria for anemia in children and childbearing-aged women. MMWR Morb Mortal Wkly Rep 1989;38:400–4. 2542755

8. Centers for Disease Control and Prevention. Recommendations to prevent and Control Iron Deficiency in the United States. MMWR 1998; 47(No. RR-3): p13.

9. Lozoff B, Beard J, Connor J, Barbara F, Georgieff M, Schallert T. Long-lasting neural and behavioral effects of iron deficiency in infancy. Nutr Rev. 2006 May;64(5 Pt 2):S34–43; discussion S72-91.

10. Ministerio de Salud. Guía técnica: Guía de práctica clínica para el diagnóstico y tratamiento de la anemia por deficiencia de hierro en niñas, niños y adolescentes en establecimientos de salud del primer nivel de atención. Lima, Perú: MINSA; 2016.

11. The World Bank. World development indicators: Peru, GDP (currrent US$) [Internet]. Available from:

12. Instituto Nacional de Estadística e Informática. Informe Perú: Indicadores de Resultados de los Programas Presupuestales, 2013–2018 –Primer Semestre. Lima, Perú. July 2018.

13. Cook JD, Boy E, Flowers C, Daroca M del C. The influence of high-altitude living on body iron. Blood. 2005 Aug 15;106(4):1441–6. doi: 10.1182/blood-2004-12-4782 15870179

14. Munares-García O, Gómez-Guizado G. Niveles de hemoglobina y anemia en gestantes adolescentes atendidas en establecimientos del Ministerio de Salud del Perú, 2009–2012. Rev Peru Med Exp Salud Publica. 2014;31(3):501–8 25418649

15. Ministerio de Economía y Finanzas. Informe de cumplimiento de metas de indicadores priorizados del convenio de apoyo presupuestario al programa articulado nutricional-EUROPAN Tramo variable año 2011. Lima, Perú:MEF;2012.

16. Gonzales GF. [The cutoff point of hemoglobin to define maternal anemia in altitude should not be corrected]. [Article in Spanish]. Rev Peru Med Exp Salud Publica. 2015 Jan-Mar;32(1):198. 26102130

17. Gonzales GF, Rubín de Celis V, Begazo J, Del Rosario Hinojosa M, Yucra S, Zevallos-Concha A, et al. Correcting the cut-off point of hemoglobin at high altitude favors misclassification of anemia, erythrocytosis and excessive erythrocytosis. Am J Hematol. 2018 Jan;93(1):E12–E16. doi: 10.1002/ajh.24932 28983947

18. Gonzales GF, Fano D, Vásquez-Velásquez C. [Diagnosis of anemia in populations at high altitudes]. Rev Peru Med Exp Salud Publica. 2017 Oct-Dec;34(4):699–708. doi: 10.17843/rpmesp.2017.344.3208 29364423

19. Sarna K, Gebremedin A, Brittenham GM, Beall CM. WHO hemoglobin thresholds for altitude increase the prevalence of anemia among Ethiopian highlanders. Am J Hematol. 2018 Sep;93(9):E229–E231. doi: 10.1002/ajh.25194 30040139

20. Instituto Nacional de Estadística e Informática. Encuesta Demográfica y de Salud Familiar—ENDES 2017. Lima, Perú:INEI;2018.

21. United Nations International Children's Emergency Fund, United Nations University, World Health Organization. Iron deficiency anaemia: assessment, prevention, and control: a guide for programme managers. Geneva, Switzerland:WHO;2001.

22. Earl R, Woteki CE, ed. by. Iron deficiency anemia: recommended guidelines for the prevention, detection, and management among U.S. children and women of childbearing age. Food and Nutrition Board, Institute of Medicine. Washington DC: National Academy Press. 1993.

23. Crawford JE, Amaru R, Song J, Julian CG, Racimo F, Cheng JY et al. Natural Selection on Genes Related to Cardiovascular Health in High-Altitude Adapted Andeans. Am J Hum Genet. 2017 Nov 2; 101(5):752–67. doi: 10.1016/j.ajhg.2017.09.023 29100088

24. Croft TN, Marshall AMJ, Allen CK, Arnold F, Assaf S, Balian S, et al. Guide to DHS Statistics. Rockville, Maryland, USA: 338 ICF. 2018.

25. Centers for Disease Control. Enhanced Pediatric Nutrition Surveillance System User’s Manual. Division of Nutrition, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Public Health Service, US Department of Health and Human Services, Atlanta, GA, 1994.

26. World Health Organization. The global prevalence of anemia in 2011. Geneva: World Health Organization. 2015.

27. Waterlow JC. Classification and definition of protein-calorie malnutrition. Br Med J. 1972 Sep 2;3(5826):566–9. doi: 10.1136/bmj.3.5826.566 4627051

28. Waterlow JC, Buzina R, Keller W, Lane JM, Nichaman MZ, Tanner JM. The presentation and use of height and weight data for comparing the nutritional status of groups of children under the age of 10 years. Bull World Health Organ. 1977;55(4):489–98. 304391

29. World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. Wld Hlth Org techn Rep Ser. 1995;(854).

30. Rutstein SO, Johnson K. The DHS Wealth Index.DHS Comparative Reports Nº 6 Calverton, Maryland: ORC Macro. 2004.

31. Department of the Army. Military Mountaineering. Field Manual No.3-97.61. Mountain living. Washington, DC. 2002.

32. US department of transportation. Aircraft Operations at Altitudes Above 25,000 Feet Mean Sea Level or Mach Numbers Greater Than .75. Advisory Circular 61-107B. 2013.

33. Harrell FE, Davis CE. A new distribution-free quantile estimator. Biometrika. 1982;69: 635–640

34. De Benoist B, McLean E, Cogswell M, ed. by. Worldwide prevalence of anaemia 1993-2005.WHO global database on anaemia. Ginebra, Switzerland:WHO; 2008.

35. Dallman PR, Yip R, Johnson C. Prevalence and causes of anemia in the United States, 1976 to 1980. Am J Clin Nutr 1984; 39:437–45. doi: 10.1093/ajcn/39.3.437 6695843

36. World Health Organization, Centers for Disease Control and prevention. Assessing the iron status of populations: Report of a Joint World Health Organization/Centers for Disease Control and Prevention Technical Consultation on the Assessment of Iron Status at the Population Level. Geneva, Switzerland. 2007.

37. Yip R, Johnson C, Dallman PR. Age-related changes in laboratory values used in the diagnosis of anemia and iron deficiency. Am J Clin Nutr 1984;39:427–36. 6695842

38. Donahue AM, 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. doi: 10.1177/0379572117723134 28826251

39. Kumar T, Taneja S, Sachdev HPS, Refsum H, Yajnik CS, Bhandari N, et al. Supplementation of vitamin B12 or folic acid on hemoglobin concentration in children 6–36 months of age: A randomized placebo controlled trial. Clin Nutr. 2017 Aug;36(4):986–91. doi: 10.1016/j.clnu.2016.07.002 27486122

40. Natvig K. Studies on hemoglobin values in Norway. V. Hemoglobin concentration and hematocrit in men aged 15–21 years. Acta Med Scand. 1966;180(5):613–20. 5923383

41. Kilpatrick GS, Hardisty RM. The prevalence of anaemia in the community. A survey of a random sample of the population. Br Med J. 1961;1(5228):778–82. doi: 10.1136/bmj.1.5228.778 13830948

42. De Leeuw NK, Lowenstein L, Hsieh YS. Iron deficiency and hydremia in normal pregnancy. Medicine (Baltimore), 1966, 45:291–315.

43. Sturgeon P. Studies of iron requirements in infants. III. Influence of supplemental iron during normal pregnancy on mother and infant. A The mother. Br J Haematol. 1959; 5(1):31–44. doi: 10.1111/j.1365-2141.1959.tb04011.x 13628927

44. National Institute of Statistics of Rwanda (NISR) [Rwanda], Ministry of Health (MOH) [Rwanda], and ICF International. Rwanda Demographic and Health Survey 2014–15. Rockville, Maryland, USA:NISR, MOH, and ICF International. 2015.

45. Chowdhury SD, Ghosh T. Undernutrition in Santal children: a biochemical and hematological study. Homo. 2013 Jun;64(3):215–27. doi: 10.1016/j.jchb.2013.03.006 23587130

46. Nguyen PH, Scott S, Avula R, Tran LM, Menon P. Trends and drivers of change in the prevalence of anaemia among 1 million women and children in India, 2006 to 2016. BMJ Glob Health. 2018 Oct 19;3(5):e001010. doi: 10.1136/bmjgh-2018-001010 30397516

47. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet. 2007; 370(9586):511–520. doi: 10.1016/S0140-6736(07)61235-5 17693180

48. Accinelli RA, Leon-Abarca JA. Solid fuel use is associated with anemia in children. Environ Res. 2017;158:431–5. doi: 10.1016/j.envres.2017.06.032 28689034

49. Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK, et al. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J. Clin. Invest. 2004;113(9): 1271–6. doi: 10.1172/JCI20945 15124018

50. Rishi G, Wallace DF, Subramaniam VN. Hepcidin: regulation of the master iron regulator. Biosci Rep. 2015 Mar 31;35(3). pii: e00192. doi: 10.1042/BSR20150014 26182354

51. Ocas-Córdova S, Tapia V, Gonzales GF. Hemoglobin concentration in children at different altitudes in Peru: proposal for [hb] correction for altitude to diagnose anemia and polycythemia. High Alt Med Biol. 2018 Dec;19(4):398–403. doi: 10.1089/ham.2018.0032 30251888

52. Jelkmann W. Erythropoietin: structure, control of production, and function. Physiol Rev. 1992 Apr;72(2):449–89. doi: 10.1152/physrev.1992.72.2.449 1557429

53. Digicaylioglu M, Lipton SA. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature. 2001 Aug 9;412(6847):641–7. doi: 10.1038/35088074 11493922

54. Grimm C, Wenzel A, Groszer M, Mayser H, Seeliger M, Samardzija M, et al. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med. 2002 Jul;8(7):718–24. doi: 10.1038/nm723 12068288

55. Ratcliffe PJ. HIF-1 and HIF-2: working alone or together in hypoxia?. J Clin Invest. 2007 Apr;117(4):862–5 doi: 10.1172/JCI31750 17404612

56. Daugas E, Cande C, Kroemer G. Erythrocytes: Death of a mummy. Cell Death Differ. 2001 Dec;8(12):1131–3. doi: 10.1038/sj.cdd.4400953 11753560

57. Koury MJ, Bondurant MC. Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science. 1990 Apr 20;248(4953):378–81. doi: 10.1126/science.2326648 2326648

58. Adamson JW. The relationship of erythropoietin and iron metabolism to red blood cell production in humans. Semin Oncol. 1994 Apr;21(2 Suppl 3):9–15.

59. Kimura T, Sonoda Y, Iwai N, Satoh M, Yamaguchi-Tsukio M, Izui T, et al. Proliferation and cell death of embryonic primitive erythrocytes. Exp Hematol. 2000 Jun;28(6):635–41. doi: 10.1016/s0301-472x(00)00156-9 10880749

60. Orkin SH, Weiss MJ. Apoptosis. Cutting red-cell production. Nature. 1999;401(6752): 433, 435–6. doi: 10.1038/46699 10519540

61. Polenakovic M, Sikole A. Is erythropoietin a survival factor for red blood cells?. J Am Soc Nephrol. 1996 Aug;7(8):1178–82. 8866410

62. Tang F, Feng L, Li R, Wang W, Liu H, Yang Q, et al. Inhibition of Suicidal Erythrocyte Death by Chronic Hypoxia. High Alt Med Biol. 2019 Jun;20(2):112–9. doi: 10.1089/ham.2017.0159 30192653

63. World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva, Switzerland: World Health Organization. 2011.

64. Koller O. The clinical significance of hemodilution during pregnancy. Obstetrical and Gynecological Survey, 1982,37:649–52. doi: 10.1097/00006254-198211000-00001 7145246

65. Lozoff B, Jimenez E, Hagen J, Mollen E, Wolf AW. Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics. 2000;105:E51. doi: 10.1542/peds.105.4.e51 10742372

66. Brotanek JM, Gosz J, Weitzman M, Flores G. Secular trends in the prevalence of iron deficiency among US toddlers, 1976–2002. Arch Pediatr Adolesc Med. 2008;162:374–81. doi: 10.1001/archpedi.162.4.374 18391147

67. World Health Organization. Nutritional anaemias: tools for effective prevention and control. Geneva, Switzerland: WHO; 2017.

68. Central Statistical Agency and ICF International. Ethiopia Demographic and Health Survey 2011. Addis Ababa, Ethiopia and Calverton, Maryland, USA: Central Statistical Agency and ICF International. 2012.

69. Ncogo P, Romay-Barja M, Benito A, Aparicio P, Nseng G, Berzosa P, et al. Prevalence of anemia and associated factors in children living in urban and rural settings from Bata District, Equatorial Guinea, 2013. PLoS One. 2017 May 3;12(5):e0176613. doi: 10.1371/journal.pone.0176613 28467452

70. Robins EB, Blum S. Hematologic reference values for African American children and adolescents. Am J Hematol. 2007 Jul;82(7):611–4. doi: 10.1002/ajh.20848 17177189

71. Beutler E, Felitti V, Gelbart T, Waalen J. Haematological effects of the C282Y HFE mutation in homozygous and heterozygous states among subjects of northern and southern European ancestry. Br J Haematol. 2003;120:887–93. doi: 10.1046/j.1365-2141.2003.04215.x 12614226

72. Rademaker K, Hodgins G, Moore K, Zarrillo S, Miller C, Bromley GR, et al. Paleoindian settlement of the high-altitude Peruvian Andes. Science. 2014 Oct 24;346(6208):466–9. doi: 10.1126/science.1258260 25342802

73. Beall CM. Andean, Tibetan, and Ethiopian patterns of adaptation to high-altitude hypoxia. Integr Comp Biol. 2006 Feb;46(1):18–24. doi: 10.1093/icb/icj004 21672719

74. Bigham AW, Lee FS. Human high-altitude adaptation: Forward genetics meets the HIF pathway. Genes Dev. 2014 Oct 15;28(20):2189–204. doi: 10.1101/gad.250167.114 25319824

75. Bigham AW, Julian CG, Wilson MJ, Vargas E, Browne VA, Shriver MD, et al. Maternal PRKAA1 and EDNRA genotypes are associated with birth weight, and PRKAA1 with uterine artery diameter and metabolic homeostasis at high altitud. Physiol Genomics. 2014 Sep 15; 46(18):687–97. doi: 10.1152/physiolgenomics.00063.2014 25225183

76. Instituto Nacional de Estadística e Informática. Perú: Formas de Acceso al Agua y Saneamiento Básico. Lima, Perú:INEI Mar 2018.

77. Dirección General de Epidemiología, Ministerio de Salud del Perú. Número de episodios de diarreas agudas Perú 2013 a 2018 –DGE [Internet]. Available from:

78. Ministerio de Salud. Sala de situación de salud—Casos según tipo de malaria, tasas y fallecidos, Perú 2018 hasta la SE 23–2018 [Internet]. Available from:

79. Dufour DL, Piperata BA, Murrieta RS, Wilson WM, Williams DD. Amazonian foods and implications for human biology. Ann Hum Biol. 2016 Jul;43(4):330–48. doi: 10.1080/03014460.2016.1196245 27337942

80. Alaofè H, Burney J, Naylor R, Taren D. Prevalence of anaemia, deficiencies of iron and vitamin A and their determinants in rural women and young children: a cross-sectional study in Kalalé district of northern Benin. Public Health Nutr. 2017 May;20(7):1203–13. doi: 10.1017/S1368980016003608 28120735

81. Cabada MM, Lopez M, Arque E, Clinton White A. Prevalence of soil-transmitted helminths after mass albendazole administration in an indigenous community of the Manu jungle in Peru. Pathog Glob Health. 2014 Jun;108(4):200–5. doi: 10.1179/2047773214Y.0000000142 24934795

82. Pullum T, Collison DK, Namaste S, Garrett D. Hemoglobin Data in DHS Surveys: Intrinsic Variation and Measurement Error. DHS Methodological Reports No. 18. Rockville, Maryland, USA: ICF. 2017.

Článek vyšel v časopise


2020 Číslo 1
Nejčtenější tento týden