ABSTRACT:

Objective:

To verify the prevalence of anemia in Brazilian adults and elderly.

Methods:

This is a cross-sectional study consisted of 8,060 subjects aged over 18 years old in all Brazilian states. We used data from laboratory tests of the Brazilian National Health Survey (Pesquisa Nacional de Saúde - PNS). The following indicators obtained by erythrogram were used: hemoglobin, mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), and red cell distribution width (RDW). Reference values of the World Health Organization (WHO) were used to determine anemia, which considers hemoglobin levels below 13.0 g/dL for men and less than 12.0 g/dL for women. Sociodemographic information was obtained by interview.

Results:

The prevalence of anemia among Brazilian adults and elderly was 9.9%. Higher prevalence of anemia and more severe cases were found among women, elderly, people with low schooling, black skin color and residents of the North and Northeast regions. Normocytic normochromic anemia was the most common type of anemia (56.0%).

Conclusion:

The anemia prevalence found in the study was in agreement with the literature. It must be stressed that higher anemia prevalence was found in disadvantaged and older population. Considering the increase of the population over 60 years of age, interventions to prevent and treat anemia among adults and elderly is imperative in the health service network.

Keywords:
Anemia; Nutritional anemias; Risk factors; Adult; Aged

INTRODUCTION

Anemia is defined as a reduction in the number of red blood cells or their ability to carry oxygen through hemoglobin to meet physiological needs¹1. World Health Organization, Fundo das Nações Unidas para a Infância, Universidade das Nações Unidas. Iron deficiency anaemia: assessment, prevention, and control [Internet]. Genebra: World Health Organization; 2001 [acessado em 14 jul. 2018]. Disponível em: Disponível em: http://www.who.int/nutrition/publications/en/ida_assessment_prevention_control.pdf
http://www.who.int/nutrition/publication... . Worldwide, according to results from the Global Burden of Disease Study 2017, anemia prevalence was estimated at 27%²2. Kassebaum NJ, GBD 2013 Anemia Collaborators. The Global Burden of Anemia. Hematol Oncol Clin North Am 2016; 30(2): 247-308. http://doi.org/10.1016/j.hoc.2015.11.002
http://doi.org/10.1016/j.hoc.2015.11.002... . The World Health Organization (WHO) estimated a global prevalence of anemia between 1993 and 2005 of 24.8%, ranging from 12.7% in adult men to 47.4% in children aged 0 to 5 years³3. World Health Organization. Worldwide prevalence of anaemia 1993-2005: WHO Global Database on Anaemia [Internet]. Genebra: World Health Organization ; 2008 [acessado em 14 jul. 2018]. 40 p. Disponível em: Disponível em: http://apps.who.int/iris/bitstream/handle/10665/43894/9789241596657_eng.pdf?ua=1
http://apps.who.int/iris/bitstream/handl... .

Anemias are a widely distributed public health problem that increases the risk of morbidity and mortality, especially in children, pregnant women and the elderly⁴4. Kassebaum NJ, Jasrasaria R, Naghavi M, Wulf SK, Johns N, Lozano R, et al. A systematic analysis of global anemia burden from 1990 to 2010. Blood 2014; 123(5): 615-24. http://doi.org/10.1182/blood-2013-06-508325
http://doi.org/10.1182/blood-2013-06-508... . Consequences of morbidity associated with chronic anemia include loss of productivity, cognitive difficulties and increased susceptibility to infections, which also contributes to substantial economic loss⁵5. Haas JD, Brownlie T4th. Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. J Nutr 2001; 131(2): 676S-90S. http://doi.org/10.1093/jn/131.2.676S
http://doi.org/10.1093/jn/131.2.676S... . In women, a recent review study found that anemia is also related to premature birth, low birth weight, and infant and maternal mortality⁶6. Rahman MM, Abe SK, Rahman MS, Kanda M, Narita S, Bilano V, et al. Maternal anemia and risk of adverse birth and health outcomes in low- and middle-income countries: systematic review and meta-analysis. Am J Clin Nutr 2016; 103(2): 495-504. http://doi.org/10.3945/ajcn.115.107896
http://doi.org/10.3945/ajcn.115.107896... .

Anemias have several causes and are often multifactorial. Risk factors for the development of anemia include nutritional aspects, such as vitamin and mineral deficiencies, and non-nutritional ones, such as hemoglobinopathies, acute and chronic blood loss, malaria, infections, chronic kidney disease, and gastrointestinal and gynecological conditions¹1. World Health Organization, Fundo das Nações Unidas para a Infância, Universidade das Nações Unidas. Iron deficiency anaemia: assessment, prevention, and control [Internet]. Genebra: World Health Organization; 2001 [acessado em 14 jul. 2018]. Disponível em: Disponível em: http://www.who.int/nutrition/publications/en/ida_assessment_prevention_control.pdf
http://www.who.int/nutrition/publication... . However, considering the role of iron in oxygen transport and the low availability of this micronutrient in the diet of a large proportion of the world’s population, such deficiency is the leading cause of anemia, accounting for more than 50% of cases globally¹1. World Health Organization, Fundo das Nações Unidas para a Infância, Universidade das Nações Unidas. Iron deficiency anaemia: assessment, prevention, and control [Internet]. Genebra: World Health Organization; 2001 [acessado em 14 jul. 2018]. Disponível em: Disponível em: http://www.who.int/nutrition/publications/en/ida_assessment_prevention_control.pdf
http://www.who.int/nutrition/publication... ^,44. Kassebaum NJ, Jasrasaria R, Naghavi M, Wulf SK, Johns N, Lozano R, et al. A systematic analysis of global anemia burden from 1990 to 2010. Blood 2014; 123(5): 615-24. http://doi.org/10.1182/blood-2013-06-508325
http://doi.org/10.1182/blood-2013-06-508... .

Thus, the prevalence of this condition is especially high in populations of low socioeconomic status, low body weight and pregnant and postpartum women³3. World Health Organization. Worldwide prevalence of anaemia 1993-2005: WHO Global Database on Anaemia [Internet]. Genebra: World Health Organization ; 2008 [acessado em 14 jul. 2018]. 40 p. Disponível em: Disponível em: http://apps.who.int/iris/bitstream/handle/10665/43894/9789241596657_eng.pdf?ua=1
http://apps.who.int/iris/bitstream/handl... ^,77. Brasil. Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da criança e da Mulher (PNDS-2006) [Internet]. Brasil: Ministério da Saúde; 2008 [acessado em 19 jul. 2018]. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_pnds2006.pdf
http://bvsms.saude.gov.br/bvs/pnds/img/r... . In this context, because of the need to collect biological material for prevalence studies, which increases cost and logistical difficulty, most national and international studies on anemia include a sample composed mainly of children and women of childbearing age³3. World Health Organization. Worldwide prevalence of anaemia 1993-2005: WHO Global Database on Anaemia [Internet]. Genebra: World Health Organization ; 2008 [acessado em 14 jul. 2018]. 40 p. Disponível em: Disponível em: http://apps.who.int/iris/bitstream/handle/10665/43894/9789241596657_eng.pdf?ua=1
http://apps.who.int/iris/bitstream/handl... ^,77. Brasil. Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da criança e da Mulher (PNDS-2006) [Internet]. Brasil: Ministério da Saúde; 2008 [acessado em 19 jul. 2018]. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_pnds2006.pdf
http://bvsms.saude.gov.br/bvs/pnds/img/r... . Studies that include other life cycles are generally local in scope and target specific populations⁸8. Buffon PLD, Sgnaolin V, Engroff P, Viegas K, Carli GA. Prevalência e caracterização da anemia em idosos atendidos pela Estratégia Saúde da Família. Rev Bras Geriatr Gerontol 2015; 18(2): 373-84. https://dx.doi.org/10.1590/1809-9823.2015.14033
https://dx.doi.org/10.1590/1809-9823.201... ^,99. Milagres CS, Moraes KBD, Franceschini SCC, Sant’Ana LFR, Lima LM, Ribeiro AQ. Prevalência e fatores associados à presença de anemia em idosos do município de Viçosa (MG), Brasil. Ciênc Saúde Coletiva 2015; 20(12): 3733-741. http://doi.org/10.1590/1413-812320152012.20752014
http://doi.org/10.1590/1413-812320152012... ^,1010. Fabian C, Olinto MTA, Dias-da-Costa JS, Bairros F, Nácul LC. Prevalência de anemia e fatores associados em mulheres adultas residentes em São Leopoldo, Rio Grande do Sul, Brasil. Cad Saúde Pública 2007; 23(5): 1199-205. http://dx.doi.org/10.1590/S0102-311X2007000500021
http://dx.doi.org/10.1590/S0102-311X2007... .

In Brazil, data from the National Child and Women’s Demographic and Health Survey (Pesquisa Nacional de Demografia e Saúde da Criança e da Mulher - PNDS) 2006 show that 29.4% of women aged 15 to 49 years had anemia, while the prevalence in children was 20.9%⁷7. Brasil. Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da criança e da Mulher (PNDS-2006) [Internet]. Brasil: Ministério da Saúde; 2008 [acessado em 19 jul. 2018]. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_pnds2006.pdf
http://bvsms.saude.gov.br/bvs/pnds/img/r... . Studies with the female population of childbearing age reveal anemia prevalence ranging from 18.6% in women in the municipality of Pernambuco¹¹11. Bezerra AGN, Leal VS, Lira PIC, Oliveira JS, Costa EC, Menezes RCE, et al. Anemia e fatores associados em mulheres de idade reprodutiva de um município do Nordeste brasileiro. Rev Bras Epidemiol 2018; 21: e180001. http://dx.doi.org/10.1590/1980-549720180001
http://dx.doi.org/10.1590/1980-549720180... to 38.0% in indigenous women¹²12. Borges MC, Buffarini R, Santos RV, Cardoso AM, Welch JR, Garnelo L, et al. Anemia among indigenous women in Brazil: findings from the First National Survey of Indigenous People’s Health and Nutrition. BMC Womens Health 2016; 16: 7. https://doi.org/10.1186/s12905-016-0287-5
https://doi.org/10.1186/s12905-016-0287-... . In pregnant women users of Basic Health Units of Maceió, the prevalence was 28.3% in 2014¹³13. Oliveira AC, Barros AM, Ferreira RC. Fatores de associados à anemia em gestantes da rede pública de saúde de uma capital do Nordeste do Brasil. Rev Bras Ginecol Obstet 2015; 37(11): 505-11. http://dx.doi.org/10.1590/SO100-720320150005400
http://dx.doi.org/10.1590/SO100-72032015... .

Among the elderly, a household survey in Porto Alegre, Rio Grande do Sul, showed anemia prevalence of 8.8% in 2012⁸8. Buffon PLD, Sgnaolin V, Engroff P, Viegas K, Carli GA. Prevalência e caracterização da anemia em idosos atendidos pela Estratégia Saúde da Família. Rev Bras Geriatr Gerontol 2015; 18(2): 373-84. https://dx.doi.org/10.1590/1809-9823.2015.14033
https://dx.doi.org/10.1590/1809-9823.201... . Among the elderly population using the Unified Health System (SUS) in Campina Grande, the prevalence was 12.5%. % in 2010¹⁴14. Sousa NDS, Menezes TN, Silva NA, Eulálio MC, Paiva AA. Prevalência de anemia e correlação da concentração de hemoglobina com fatores cognitivos em idosos. Ciênc Saúde Coletiva 2018; 23(3): 935-44. http://dx.doi.org/10.1590/1413-81232018233.09082016
http://dx.doi.org/10.1590/1413-812320182... . In the elderly in long-term care facilities, the prevalence of anemia reached 38.0% in Salvador¹⁵15. Silva EC, Roriz AKC, Eickemberg M, Mello AL, Côrtes EBQ, Feitosa CA, et al. Factors Associated with Anemia in the Institutionalized Elderly. PLoS One 2016; 11(12): e0169377. http://doi.org/10.1371/journal.pone.0162240
http://doi.org/10.1371/journal.pone.0162... .

Thus, although anemia is a global public health problem, current data on its prevalence in the general Brazilian population are not available. Thus, it is necessary to provide current information on the situation of anemia in the Brazilian adult population and to detect the groups most affected by this condition in order to support public policies.

The objective of the present study was to describe the prevalence of anemia in adults and elderly in Brazil, according to sociodemographic characteristics, using data from the National Health Survey Laboratory (Pesquisa Nacional de Saúde - PNS).

METHODS

The PNS is a household-based survey conducted in 2013 by the Brazilian Institute of Geography and Statistics (Instituto Brasileiro de Geografia e Estatística - IBGE) in partnership with the Ministry of Health. Information was collected from households using a three-stage cluster sampling plan. Primary sampling units (PSU) were the census sectors or set of sectors; the secondary units, the households; and tertiary units, adult residents aged 18 years old or older. Further details on PNS and its sampling procedures can be obtained from previous publications¹⁶16. Szwarcwald CL, Malta DC, Pereira CA, Vieira MLFP, Conde WL, Souza Júnior PRB, et al. Pesquisa Nacional de Saúde no Brasil: concepção e metodologia de aplicação. Ciênc Saúde Coletiva 2014; 19(2): 333-42. http://doi.org/10.1590/1413-81232014192.14072012
http://doi.org/10.1590/1413-81232014192.... .

The PNS had 60,202 interviews, and, in one subsample, biological material was collected for biochemical analysis. The subsample was designed to include 25% of the sample of respondents, and for its composition, we considered the municipalities that had the best infrastructure for performing examinations, by means of probability proportional to the inverse distance from the city where the PSU is located and the nearest municipality with 80 thousand inhabitants or more¹⁷17. Szwarcwald CL, Malta DC, Júnior PRS, Almeida WS, Damacena GN, Pereira CAP, et al. Exames laboratoriais da Pesquisa Nacional de Saúde: Metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019. (no prelo)..

The final sample of individuals who had biological material collected consisted of 8,955 individuals. Among the causes of the losses, we highlight not locating the household, participants’ refusal to collect biological material, lack of knowledge of the project and objectives, and unavailability of time to attend to the research. No samples were collected from pregnant women. More details about the sample and data collection methods are available in another publication in the same series¹⁷17. Szwarcwald CL, Malta DC, Júnior PRS, Almeida WS, Damacena GN, Pereira CAP, et al. Exames laboratoriais da Pesquisa Nacional de Saúde: Metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019. (no prelo).. From the final sample, 892 participants were excluded, due to their having an inadequate sample to perform laboratory tests. Figure 1 illustrates the flow of losses.

Samples were collected by peripheral venipuncture in vacuum blood collection tubes with ethylenediaminetetraacetic acid (EDTA) and evaluated with an automated cell analyzer. The results of the exams were informed directly to the participant by the hired laboratory. Individuals with altered exams received indications for seeking medical attention. Cases with results considered critical were immediately identified by the associated laboratory and assistance was provided in the SUS health service network.

In the current study, the following hematimetric indexes were analyzed: hemoglobin; mean corpuscular volume (MCV), which indicates the average volume of red blood cells; mean corpuscular hemoglobin (MCH), which indicates the amount of hemoglobin in the red blood cell; and red cell distribution width (RDW), which evaluates the size variation between red blood cells.

For the definition of anemia, the diagnostic criteria and severity assessment for adults proposed by the WHO were used¹⁸18. World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System [Internet]. Genebra: World Health Organization ; 2011 [acessado em 20 ago. 2018]. Disponível em: Disponível em: http://www.who.int/vmnis/indicators/haemoglobin.pdf
http://www.who.int/vmnis/indicators/haem... :

The MCV and MCH hematimetric indexes were classified according to the reference values proposed by Malvezzi¹⁹19. Malvezzi M. Valores eritrocitários normais em população adulta de Curitiba após exclusão dos indivíduos deficientes em ferro [dissertação]. Curitiba: Faculdade de Medicina, Universidade Federal do Paraná; 1983., for the Brazilian population, for the definition of hypochromia, normochromia and hyperchromia, microcytosis, normocytosis and macrocytosis. RDW was classified according to the normality limits proposed by Adeli et al.²⁰20. Adeli K, Raizman JE, Chen Y, Higgins V, Nieuwesteeg M, Abdelhaleem M, et al. Complex biological profile of hematologic markers across pediatric, adult, and geriatric ages: establishment of robust pediatric and adult reference intervals on the basis of the Canadian Health Measures Survey. Clin Chem .2015; 61(8): 1075-86. http://doi.org/10.1373/clinchem.2015.240531
http://doi.org/10.1373/clinchem.2015.240... , as presented:

Analyses were stratified by gender, age group (18 to 29, 30 to 44, 45 to 59, 60 to 74, and 75 years old or older), education (uneducated and incomplete elementary education, complete elementary education and incomplete high school education, complete high school education and higher), skin color (white, black, brown, other) and region (North, Northeast, Southeast, South, Midwest). Data were analyzed by Stata v. 14, using the survey command set, which allows analysis of complex sample survey data incorporating post-stratification weights specifically created for the PNS laboratory sample - which included the variables gender, age, skin color, level of education and region - to reduce the bias of non-representation. More information on weighting is available in another publication in this same issue¹⁷17. Szwarcwald CL, Malta DC, Júnior PRS, Almeida WS, Damacena GN, Pereira CAP, et al. Exames laboratoriais da Pesquisa Nacional de Saúde: Metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019. (no prelo).. Pearson’s χ² test and analysis of 95% confidence intervals (95%CI) were used to identify differences between proportions. The significance level established in the analyses was 5%.

Individuals participated voluntarily in the PNS, which was approved by the National Research Ethics Commission (CONEP) of the National Health Council (Conselho Nacional de Saúde - CNS) of the Ministry of Health, under Report No. 328.159, of June 26, 2013.

RESULTS

This study had a sample of 8,060 individuals aged between 18 and 101 years old, in which 52.9% of the participants were female. The prevalence of anemia in the study population was 9.9%, 7.2% in men and 12.3% in women. Higher prevalence of anemia was observed among women, elderly, black-skinned population, low level of education and residents of the North and Northeast regions (Table 1).

Important differences were observed between genders. Women had higher prevalence in younger age groups, but from 45 years of age on, there was no difference in the prevalence of anemia between genders. In men, the lowest prevalence was found among those who had complete high school education or higher. Among women, there was no significant difference in relation to education. With regard to skin color, black men exhibited much higher prevalence of anemia than other categories (Table 1).

Regarding the severity of anemia classification, 1.9% presented moderate to severe anemia and 8.0% mild anemia. Higher prevalence of moderate to severe anemia was found in females, elderly, black people and in the North and Northeast regions (Table 2).

Regarding the other hematimetric indexes, 23.2 and 10.2% presented, respectively, reduced and increased MCV; 32.1% showed reduced MCH; and 75.5% increased RDW. In females, there was a higher proportion of individuals with reduced MCV and MCH (Table 3).

Regarding the classification of anemias according to MCV and MCH values, the highest proportion of those considered anemic presented normocytic and normochromic anemia (56.0% in the total population, 58.8% among men and 54.5% among women); followed by hypochromic and microcytic anemia (21.4% in the total population, 16.5% among men and 24.0% among women); and macrocytic normochromics (10.2% in the total population, 14.0% among men and 8.1% among women). Hypochromic and microcytic anemia were more frequent in females, and normochromic and macrocytic anemia in males, although there was an overlap of 95%CI (Graphic 1A). The age group 60 years old or older presented lower frequency of hypochromic and microcytic anemia and higher frequency of normocytic and normochromic anemia (Graphic 1B). Increased RDW was observed in 94.5% of those with homochromic and microcytic anemia and 67.0% of those with normochromic and normocytic anemia (Graphic 1C).

DISCUSSION

Anemia is a public health problem worldwide and varies according to cultural, dietary and morbidity patterns due to infectious diseases and chronic conditions in high, middle and low income countries⁴4. Kassebaum NJ, Jasrasaria R, Naghavi M, Wulf SK, Johns N, Lozano R, et al. A systematic analysis of global anemia burden from 1990 to 2010. Blood 2014; 123(5): 615-24. http://doi.org/10.1182/blood-2013-06-508325
http://doi.org/10.1182/blood-2013-06-508... . Anemia is estimated to reach 27% of the world’s population²2. Kassebaum NJ, GBD 2013 Anemia Collaborators. The Global Burden of Anemia. Hematol Oncol Clin North Am 2016; 30(2): 247-308. http://doi.org/10.1016/j.hoc.2015.11.002
http://doi.org/10.1016/j.hoc.2015.11.002... , although prevalence may range from 9% in high-income countries to 43% in low-income ones²¹21. McLean E, Cogswell M, Egli I, Wojdyla D, Benoist B. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr 2009; 12(4): 444-54. http://doi.org/10.1017/S1368980008002401
http://doi.org/10.1017/S1368980008002401... .

In this study, the prevalence of anemia among adults and the elderly in Brazil alone was almost 10%. According to the classification of anemia as a public health problem proposed by the WHO¹⁸18. World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System [Internet]. Genebra: World Health Organization ; 2011 [acessado em 20 ago. 2018]. Disponível em: Disponível em: http://www.who.int/vmnis/indicators/haemoglobin.pdf
http://www.who.int/vmnis/indicators/haem... based on the estimated prevalence of hemoglobin blood levels, anemia in Brazil between adults and the elderly can be considered a problem of low expression in relation to the worldwide prevalence; however it should be noted that the present study did not include a sample of children, who are at high risk of having anemia and suffering the most serious consequences of this condition²2. Kassebaum NJ, GBD 2013 Anemia Collaborators. The Global Burden of Anemia. Hematol Oncol Clin North Am 2016; 30(2): 247-308. http://doi.org/10.1016/j.hoc.2015.11.002
http://doi.org/10.1016/j.hoc.2015.11.002... , which justifies the lower prevalence compared to other studies involving populations of all age groups.

Anemia was more prevalent and presented more severe levels among women and among the elderly, individuals with low education and black skin color and residents of the North and Northeast regions. The identification of these risk groups is consistent with previous studies regarding gender²²22. Marques F, Fonseca C, Nunes AR, Belo A, Brilhante D, Cortez J. Contextualizando a elevada prevalência de anemia na população portuguesa: percepção, caracterização e preditores: um sub-estudo do EMPIRE. Medicina Interna 2016; 23(4): 26-38., race²³23. Le CHH. The Prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003-2012). PLoS One 2016; 11(11): e0166635. http://doi.org/10.1371/journal.pone.0166635
http://doi.org/10.1371/journal.pone.0166... , education/socioeconomic status⁹9. Milagres CS, Moraes KBD, Franceschini SCC, Sant’Ana LFR, Lima LM, Ribeiro AQ. Prevalência e fatores associados à presença de anemia em idosos do município de Viçosa (MG), Brasil. Ciênc Saúde Coletiva 2015; 20(12): 3733-741. http://doi.org/10.1590/1413-812320152012.20752014
http://doi.org/10.1590/1413-812320152012... and elderly²²22. Marques F, Fonseca C, Nunes AR, Belo A, Brilhante D, Cortez J. Contextualizando a elevada prevalência de anemia na população portuguesa: percepção, caracterização e preditores: um sub-estudo do EMPIRE. Medicina Interna 2016; 23(4): 26-38.^,2323. Le CHH. The Prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003-2012). PLoS One 2016; 11(11): e0166635. http://doi.org/10.1371/journal.pone.0166635
http://doi.org/10.1371/journal.pone.0166... ^,2424. Patel KV. Epidemiology of anemia in older adults. Semin Hematol 2008; 45(4): 210-7. http://doi.org/10.1053/j.seminhematol.2008.06.006
http://doi.org/10.1053/j.seminhematol.20... . In women, those of reproductive age also exhibited high prevalence of anemia, in agreement with previous literature²³23. Le CHH. The Prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003-2012). PLoS One 2016; 11(11): e0166635. http://doi.org/10.1371/journal.pone.0166635
http://doi.org/10.1371/journal.pone.0166... .

According to the PNDS conducted in 2006, the prevalence of anemia in women of childbearing age was 29.4%⁷7. Brasil. Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da criança e da Mulher (PNDS-2006) [Internet]. Brasil: Ministério da Saúde; 2008 [acessado em 19 jul. 2018]. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_pnds2006.pdf
http://bvsms.saude.gov.br/bvs/pnds/img/r... . In the present study, the prevalence of anemia in women aged 18 to 29 and 30 to 44 years old was less than half of that found in 2006, using the same diagnostic criteria. This difference may be due to the great effort of the Brazilian government, aligned with international recommendations, to minimize anemia among the public health problems of the Brazilian population, especially with the Wheat Flour, Corn and By-Products Fortification Program, to all purposes, with iron and folic acid, whose effective implementation took place in 2004²⁵25. Szarfarc SC. Políticas públicas para o controle da anemia ferropriva. Rev Bras Hematol Hemoter 2010; 32(Supl. 2): 2-8. http://dx.doi.org/10.1590/S1516-84842010005000065
http://dx.doi.org/10.1590/S1516-84842010... . It is also noteworthy that, in 2005, the National Iron Supplementation Program was implemented, which consists of the prophylactic supplementation of this micronutrient for children from 6 to 24 months of age, pregnant and postpartum women, and supplementation of pregnant women with folic acid. In addition to these programs, it is also the attribution of primary health care, within the scope of SUS, the promotion of adequate and healthy diet to increase the consumption of iron source foods to prevent anemia²⁶26. Brasil. Ministério da Saúde. Secretaria de Atenção à Saúde. Departamento de Atenção Básica. Programa Nacional de Suplementação de Ferro: manual de condutas gerais [Internet]. Brasília: Ministério da Saúde; 2013 [acessado em 5 fev. 2018]. 24 p. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/publicacoes/manual_suplementacao_ferro_condutas_gerais.pdf
http://bvsms.saude.gov.br/bvs/publicacoe... .

Anemia in the elderly is a common problem, with an increase in its prevalence every decade of life, from 70 years old²⁴24. Patel KV. Epidemiology of anemia in older adults. Semin Hematol 2008; 45(4): 210-7. http://doi.org/10.1053/j.seminhematol.2008.06.006
http://doi.org/10.1053/j.seminhematol.20... . In the current study, the age group 75 years old or older had the highest proportion of anemia and moderate to severe anemia. These high rates are noteworthy, since anemia in the elderly is associated with disabilities, worse cognitive function and increased morbidity and mortality²³23. Le CHH. The Prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003-2012). PLoS One 2016; 11(11): e0166635. http://doi.org/10.1371/journal.pone.0166635
http://doi.org/10.1371/journal.pone.0166... ^,2727. Lucca U, Tettamanti M, Mosconi P, Apolone G, Gandini F, Nobili A, et al. Association of mild anemia with cognitive, functional, mood and quality of life outcomes in the elderly: the “Health and Anemia” study. PLoS One 2008; 3(4): e1920. https://doi.org/10.1371/journal.pone.0001920
https://doi.org/10.1371/journal.pone.000... . In addition, chronic conditions that greatly affect the elderly population, such as cancer and chronic kidney disease, may result in anemia and lead to a worse prognosis²³23. Le CHH. The Prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003-2012). PLoS One 2016; 11(11): e0166635. http://doi.org/10.1371/journal.pone.0166635
http://doi.org/10.1371/journal.pone.0166... . Thus, anemia in older individuals requires greater public health attention, not only for its high prevalence, but also for its potential health consequences.

Regarding age, it is noteworthy that differences were observed between the genders. Among men, the prevalence of anemia was lower in the 18 to 44 years age group, while for women it was less common in the 45 to 59 years age group. The increased proportion of age-associated anemia was also more marked in men, to the point of becoming more common in individuals over 75 years of age. The same pattern was observed in an American study²⁴24. Patel KV. Epidemiology of anemia in older adults. Semin Hematol 2008; 45(4): 210-7. http://doi.org/10.1053/j.seminhematol.2008.06.006
http://doi.org/10.1053/j.seminhematol.20... . Brazilian investigations with the elderly also found higher prevalence of anemia in the males compared to the femals⁸8. Buffon PLD, Sgnaolin V, Engroff P, Viegas K, Carli GA. Prevalência e caracterização da anemia em idosos atendidos pela Estratégia Saúde da Família. Rev Bras Geriatr Gerontol 2015; 18(2): 373-84. https://dx.doi.org/10.1590/1809-9823.2015.14033
https://dx.doi.org/10.1590/1809-9823.201... ^,99. Milagres CS, Moraes KBD, Franceschini SCC, Sant’Ana LFR, Lima LM, Ribeiro AQ. Prevalência e fatores associados à presença de anemia em idosos do município de Viçosa (MG), Brasil. Ciênc Saúde Coletiva 2015; 20(12): 3733-741. http://doi.org/10.1590/1413-812320152012.20752014
http://doi.org/10.1590/1413-812320152012... ^,1414. Sousa NDS, Menezes TN, Silva NA, Eulálio MC, Paiva AA. Prevalência de anemia e correlação da concentração de hemoglobina com fatores cognitivos em idosos. Ciênc Saúde Coletiva 2018; 23(3): 935-44. http://dx.doi.org/10.1590/1413-81232018233.09082016
http://dx.doi.org/10.1590/1413-812320182... . The effect that men are more likely to have anemia in older age groups may be related to the reduction in testosterone production, which has a significant impact on lowering hemoglobin levels in the body²⁸28. Roy CN, Snyder PJ, Stephens-Shields AJ, Artz AS, Bhasin S, Cohen HJ. Association of Testosterone Levels With Anemia in Older Men: A Controlled Clinical Trial. JAMA Intern Med 2017; 177(4): 480-90. http://doi.org/10.1001/jamainternmed.2016.9540
http://doi.org/10.1001/jamainternmed.201... .

Regarding the differences between regions and educational levels, it is important to emphasize the importance of nutritional factors, which are the ones that most contribute to the occurrence of anemia in both genders¹1. World Health Organization, Fundo das Nações Unidas para a Infância, Universidade das Nações Unidas. Iron deficiency anaemia: assessment, prevention, and control [Internet]. Genebra: World Health Organization; 2001 [acessado em 14 jul. 2018]. Disponível em: Disponível em: http://www.who.int/nutrition/publications/en/ida_assessment_prevention_control.pdf
http://www.who.int/nutrition/publication... . A population-based study in Brazil with children and women of childbearing age also found higher prevalence of anemia in the Northeast Region⁷7. Brasil. Ministério da Saúde. Pesquisa Nacional de Demografia e Saúde da criança e da Mulher (PNDS-2006) [Internet]. Brasil: Ministério da Saúde; 2008 [acessado em 19 jul. 2018]. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/pnds/img/relatorio_final_pnds2006.pdf
http://bvsms.saude.gov.br/bvs/pnds/img/r... , indicating a relationship between anemia and socioeconomic and cultural conditions. Studies have also shown that people with poorer socioeconomic status and lower education are more likely to have anemia because of poor access to adequate and varied food¹⁰10. Fabian C, Olinto MTA, Dias-da-Costa JS, Bairros F, Nácul LC. Prevalência de anemia e fatores associados em mulheres adultas residentes em São Leopoldo, Rio Grande do Sul, Brasil. Cad Saúde Pública 2007; 23(5): 1199-205. http://dx.doi.org/10.1590/S0102-311X2007000500021
http://dx.doi.org/10.1590/S0102-311X2007... ^,1111. Bezerra AGN, Leal VS, Lira PIC, Oliveira JS, Costa EC, Menezes RCE, et al. Anemia e fatores associados em mulheres de idade reprodutiva de um município do Nordeste brasileiro. Rev Bras Epidemiol 2018; 21: e180001. http://dx.doi.org/10.1590/1980-549720180001
http://dx.doi.org/10.1590/1980-549720180... ^,2929. Fabian C, Olinto MTA, Dias-da-Costa JS, Bairros F, Nácul LC. Prevalência de anemia e fatores associados em mulheres adultas residentes em São Leopoldo, Rio Grande do Sul, Brasil. Cad Saúde Pública 2007; 23(5): 1199-205. http://dx.doi.org/10.1590/S0102-311X2007000500021
http://dx.doi.org/10.1590/S0102-311X2007... .

Skin color was a poorly evaluated factor in studies available in the literature. A study with the North-American population found that anemia was three times higher in black than in white/Caucasian people, and only part of this racial difference was due to differences in risk factors for anemia³⁰30. Olinto MTA, Costa JSD, Gigante DP, Menezes AMB, Macedo S, Schwengber R, et al. Prevalência de anemia em mulheres em idade reprodutiva no sul do Brasil. Boletim da Saúde 2003; 17(1): 135-44.. In the current study, the same was observed among men. Such differences need to be better studied in order to investigate the need to establish different hemoglobin reference values according to gender and skin color.

Hypochromic microcytic anemia with high RDW is characteristic of iron deficiency and may be due to nutritional deficiency, iron absorption deficiency due to gastrointestinal changes and chronic loss of this micronutrient. Moreover, it is more frequent in women of childbearing age³¹31. Zakai NA, McClure LA, Prineas R, Howard G, McClellan W, Holmes CE, et al. Correlates of anemia in American blacks and whites: the REGARDS Renal Ancillary Study. Am J Epidemiol 2009; 169(3): 355-64. http://doi.org/10.1093/aje/kwn355
http://doi.org/10.1093/aje/kwn355... . In the present study, 95% of individuals with hypochromic and microcytic anemia had high RDW, which represented 20% of anemic individuals and 2% of the population studied. These findings show the magnitude of iron deficiency and reinforce the importance of continuing and strengthening drug supplementation and food fortification programs.

Microcytic and hypochromic anemia with normal RDW and enlarged red blood cells is suggestive of thalassemia hemoglobinopathy, to be confirmed by hemoglobin electrophoresis, capillary electrophoresis, or high performance liquid chromatography (HPLC)²⁰20. Adeli K, Raizman JE, Chen Y, Higgins V, Nieuwesteeg M, Abdelhaleem M, et al. Complex biological profile of hematologic markers across pediatric, adult, and geriatric ages: establishment of robust pediatric and adult reference intervals on the basis of the Canadian Health Measures Survey. Clin Chem .2015; 61(8): 1075-86. http://doi.org/10.1373/clinchem.2015.240531
http://doi.org/10.1373/clinchem.2015.240... ^,3232. Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, Arber DA, et al. Wintrobe’s clinical hematology. 13ª ed. Filadélfia: Lippincott Williams and Wilkins; 2014..

Macrocytic anemia is commonly associated with gastrointestinal changes with deficiency in absorption or loss of vitamin B12 (cyanocobalamin) and folate²⁰20. Adeli K, Raizman JE, Chen Y, Higgins V, Nieuwesteeg M, Abdelhaleem M, et al. Complex biological profile of hematologic markers across pediatric, adult, and geriatric ages: establishment of robust pediatric and adult reference intervals on the basis of the Canadian Health Measures Survey. Clin Chem .2015; 61(8): 1075-86. http://doi.org/10.1373/clinchem.2015.240531
http://doi.org/10.1373/clinchem.2015.240... ^,3232. Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, Arber DA, et al. Wintrobe’s clinical hematology. 13ª ed. Filadélfia: Lippincott Williams and Wilkins; 2014.. This anemia may also be associated with consumptive and even neoplastic states²⁰20. Adeli K, Raizman JE, Chen Y, Higgins V, Nieuwesteeg M, Abdelhaleem M, et al. Complex biological profile of hematologic markers across pediatric, adult, and geriatric ages: establishment of robust pediatric and adult reference intervals on the basis of the Canadian Health Measures Survey. Clin Chem .2015; 61(8): 1075-86. http://doi.org/10.1373/clinchem.2015.240531
http://doi.org/10.1373/clinchem.2015.240... ^,3232. Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, Arber DA, et al. Wintrobe’s clinical hematology. 13ª ed. Filadélfia: Lippincott Williams and Wilkins; 2014.. Macrocytosis is also a very common condition in alcoholism with or without cirrhosis, due to several factors: marked hemolysis of red blood cells, folate deficiency and direct alcohol toxicity on the marrow²⁰20. Adeli K, Raizman JE, Chen Y, Higgins V, Nieuwesteeg M, Abdelhaleem M, et al. Complex biological profile of hematologic markers across pediatric, adult, and geriatric ages: establishment of robust pediatric and adult reference intervals on the basis of the Canadian Health Measures Survey. Clin Chem .2015; 61(8): 1075-86. http://doi.org/10.1373/clinchem.2015.240531
http://doi.org/10.1373/clinchem.2015.240... . This condition was present in one tenth of the population, reaching a prevalence of 15% among the elderly. Therefore, the magnitude of chronic diseases and nutritional deficiencies in this population is highlighted.

Another form of anemia common in the elderly population is the normocytic and normochromic with normal RDW, which can be found in acute bleeding and anemia of chronic diseases. This anemia may be associated with thyroid alterations, rheumatological, autoimmune and neoplastic diseases, among other chronic pathologies²⁰20. Adeli K, Raizman JE, Chen Y, Higgins V, Nieuwesteeg M, Abdelhaleem M, et al. Complex biological profile of hematologic markers across pediatric, adult, and geriatric ages: establishment of robust pediatric and adult reference intervals on the basis of the Canadian Health Measures Survey. Clin Chem .2015; 61(8): 1075-86. http://doi.org/10.1373/clinchem.2015.240531
http://doi.org/10.1373/clinchem.2015.240... ^,3232. Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, Arber DA, et al. Wintrobe’s clinical hematology. 13ª ed. Filadélfia: Lippincott Williams and Wilkins; 2014.. Such anemia was present in 18.5% of the anemic identified here and in 1.7% of the total population.

Due to its high prevalence and health consequences, coping with anemia is one of the priorities in public health, finding political support in Brazil’s commitment to reduce iron deficiency anemia not only nationally but also internationally. In 2016, the United Nations General Assembly proclaimed the United Nations Decade of Action on Nutrition (2016-2025). Led by WHO and the United Nations Food and Agriculture Organization (FAO), the resolution is a milestone for making commitments, tracking progress and ensuring mutual accountability in line with the global nutrition goals of eradicating hunger and avoiding all forms of malnutrition around the world³³33. Organização Pan-Americana de Saúde. Brasil é primeiro país a assumir compromissos específicos na Década de Ação para Nutrição da ONU [Internet]. Organização Pan-Americana de Saúde; 2017 [acessado em 5 fev. 2018]. Disponível em: Disponível em: https://www.paho.org/bra/index.php?option=com_content&view=article&id=5423:brasil-e-primeiro-pais-a-assumir-compromissos-especificos-na-decada-de-acao-para-nutricao-da-onu&Itemid=820
https://www.paho.org/bra/index.php?optio... . The 2030 Agenda for Sustainable Development also includes the goal of,

For the country to reach the agreed goals, it is necessary to intensify actions in the field of food and nutrition security, with special attention to the most vulnerable groups

This study contains some limitations. First, the sample size made it possible to accurately estimate the prevalence of anemia and its forms according to hematimetric values in the total population; however, in some age and skin color groups, estimates with wide confidence intervals were observed and should be interpreted with caution. The research showed higher prevalence of anemia in the elderly and individuals with low education. Considering that the elderly have lower education in Brazil, it is recommended in future analyzes that age be controlled to know the effect of schooling in isolation.

CONCLUSION

The prevalence of anemia was higher among women, elderly, low-educated, and black people, and residents of the North and Northeast. Because anemia is associated with increased morbidity and mortality in older adults, given the increasing elderly population, and because higher prevalence and more severe forms of the condition are found in the most vulnerable populations, interventions to treat and prevent anemia in order to reduce iniquities are necessary.

The results presented here provide an overview of anemia in the population over 18 years of age in Brazil. It is noteworthy that surveillance systems for anemia with blood samples from a representative sample of the population are essential for decision-making in public health and for monitoring the control program, allowing the monitoring of the goals established in national and international agreements.

ACKNOWLEDGEMENTS

To the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq) for the Junior Postdoctoral fellowship received by author Ísis Eloah Machado and Research Productivity received by author Deborah Carvalho Malta.

References

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