Introduction

There is increasing evidence that micronutrient deficiencies play a central role in preventing children from achieving their full developmental potential and compromising irreversibly their cognitive development [1]–[3]. Anemia is a global concern [4] and represents an ongoing challenge worldwide [5] since human development and social equality are also depending on an adequate micronutrient intake early in life [6]. A recent systematic review on all studies on the prevalence of anemia in Brazil has shown that for children under the age of 5 the median anemia prevalence in the entire country is 53% [7]. Surprisingly, there is also evidence for an increasing prevalence of anemia and obesity, which has been attributed to a “nutrition transition” observed in Brazil [8]. There are few published studies on the prevalence of anemia in fertile, non-pregnant women in Brazil. According to a National Surveillance published in 2006 by the Brazilian Health Ministry, the prevalence of anemia in this population is 25 to 30% [9].

Of the children referred to the Pediatric Hematology out-patient clinic in the Hospital de Clinicas de Porto Alegre (HCPA), the University Hospital of the Federal University of RS (UFRGS), an estimated 40% had iron deficiency anemia (IDA). Based on this and on the findings mentioned above, we decided to launch an educational program called “Children without Anemia in RS”, to draw attention to the prevalence of anemia and to establish measures to prevent and treat it. As part of this program, we ran a population based study on anemia prevalence and its relation to socioeconomic status (SeS) in the state of Rio Grande do Sul (RS) which we report here.

Rio Grande do Sul is Brazil’s most southern state with nearly 11 million inhabitants, a GDP of R$193 billion (∼ USD $ 107 billion) and a life expectancy of 75.3 years [10]. Being a subtropical area, the commoner tropical diseases are rare, the prevalence of hemoglobinopathies is relatively low [11]–[13] and the childhood mortality rate is 8.19 per 1000 live births, mostly related to low birth weight [14].

Materials and Methods

Results

From the total of 2376 children and 2072 women tested, it was possible to evaluate 2198 and 1999, respectively with a loss of 7.5% for children and 3.5% for women due to incomplete forms. Of the evaluable population of children, the median age was 51 months, 1132 (51.5%) were girls, the median age of their mothers was 29 years, and the median number of siblings per child was 2 (zero to 16). Of the evaluable fertile non-pregnant women tested, the median age was 22 years (14 to 30 years of age), the median number of previous offspring was 1.4, ranging from zero to 12, and 715 (36%) were nulliparous. Among the 363 adolescents (with 16 years of age or less), there were 31 with one, 4 with two and 1 with three previous pregnancies; of the older women, 76% (1248/1636) have had at least one pregnancy.

Prevalence of Anemia

The prevalence of anemia for children was 45.4%(IC95% 43.3%–47.5%) and 36.4%(IC95% 34%–38.3%) for women. The median hemoglobin concentration for children and women was 9.9 g/dL (4.0 to 10.9 g/dL) and 12.5 g/dL (5.2 to 17.8 g/dL), respectively. According to the age group the prevalence of anemia for children under 23 months and older than 72 months was 76% and 31%(Table 1). For women there was no correlation between age and anemia prevalence (Table 2). Of the nulliparous women anemia affected 38.2% (125/327) and 34.8% (135/388) of those with 16 years of age or less and older, respectively (p = 0.342). For women that have had at least one pregnancy 47.2% (17/36) of the adolescents and 36.2% (425/1248) of the older were anemic (p = 0.176).

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Table 1. Univariate analysis of predicting factors for anemia in children in Rio Grande do Sul, Southern Brazil, 2006–2007.

https://doi.org/10.1371/journal.pone.0068805.t001

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Table 2. Univariate analysis of the predicting factors for anemia in women and crude PR of anemia according to age, social class and skin color in RS, Southern Brazil, 2006–2007.

https://doi.org/10.1371/journal.pone.0068805.t002

Anemia Crude Prevalence Ratio (PR) And Predicting Factor For Anemia In Non-Pregnant Women

Table 2 shows the univariate analysis of predicting factors for anemia and its crude PR in women according to age, social class, and skin color. For the variable age, no significant association was found in any category. Women belonging to SeS class D and E were 24.9% and 42.3% more anemic than the ones in Class AB, respectively. A significant association (p<0,001) was also observed for black women, with a gross PR of 28.9% when compared to white women. Unfortunately, the age at first pregnancy was not recorded precluding further conclusions.

In the Hierarchic Multiple Poisson Regression (Table 3) the association of anemia with age in children, remains significant for the 18 to 59 months category with younger age as an independent risk factor for anemia. Belonging to the D and E SeS and being black were independent risk factors for anemia in children as well. The multivariate analysis for independent risk factors for anemia in women (Table 4) also showed black skin color and lowers SeS (class D and E) as independent risk factors.

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Table 3. Hierarchic Multiple Poisson Regression analysis of the predicting factors for anemia in children, RS, Southern Brazil, 2006–2007.

https://doi.org/10.1371/journal.pone.0068805.t003

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Table 4. Hierarchic Multiple Poisson Regression analysis of the predicting factors for anemia in women, RS, Southern Brazil, 2006–2007.

https://doi.org/10.1371/journal.pone.0068805.t004

Discussion

In this study, 45.4% (CI 95%; 43.3%–47.5%) of the 2198 children between 18 months and 7 years old and 36.4% (CI 95%; 34%–38.3%) of the 1999 non-pregnant women aged between 14 and 30 years old in the state of RS were found to be anemic in 2006–2007. Anemia affected 76% of the children under 24 months old, and this prevalence gradually declined to 31% for children over 72 months old. Although there were cases in which the anemia was severe, in most of our anemic population the anemia was mild; the median hemoglobin concentration was 12.4 g/dl and 9.9 g/dL for women and children, respectively. Lower SeS classes were an independent risk factor for anemia for both children and women, but anemia was also identified in the upper classes impressive (Table 1 and 2); in the upper SeS it affected 34.3% of children and 31.4% of adult women.

The overall prevalence of 36.4% of anemia in fertile women in our study was higher than in the country [9], and the 21.9% to the 19.2% reported by others in the same region [18]. It should however be pointed out that the comparison of our data with theirs is hampered by the inclusion in their study of women with ages from 20 to 60 years old. As can be seen at Table 2, anemia equally affected women of all ages. We could speculate that untreated adolescents evolve to be adults with anemia aggravated by pregnancies, since 76% of the women older then 16 years had already had at least one pregnancy.

A national program of iron supplementation for children from 6 to 18 months of age and for pregnant women was launched in 2005 [19] and its implementation have had several caveats with low adhesion among other reasons because of gastrointestinal intolerance and lack of enforcement [20]. As for iron fortification of the flour, established by law in Brazil in 2004, its effect on anemia in preschool children, in RS, was found to be irrelevant due to inadequate flour intake and/or low bioavailability of dietary iron [21]. In spite of that, those are the first national effort to overcome the deleterious effects of micronutrient deficiency in pregnancy and childhood in Brazil. Because of such a recent effort, awareness to that is still been built all over the country.

The prevalence of anemia we found in children accords with that shown for the whole of Brazil [7]. In RS, in a result similar to ours, in 2004 in the city of São Leopoldo, metropolitan region of Porto Alegre, RS, a prevalence of 63.7% of anemia was found in children from 12 to 16 months of age [22]. The inverse association of anemia and age we found has been described in several regions of the country [23]–[27] as well as in RS [22], [28]. Although we did not attempt to investigate the cause of anemia in our sample, in the aforementioned study [22] including 397 children, 95% of the 63.7% of anemic individual were iron deficient, and this deficiency as well as the prevalence of anemia declined with age. Since their study population belongs to the same region as ours, we can probably assume that iron deficiency might play a role in our study population as well. Stunting was recently evaluated in RS in a population of children covered by the Food and Nutritional Surveillance System (SISVAN) [29] and was found in 7.1% of a population of 63.320 children fewer than 10 years of age. Interestingly, 8.4% of the children were overweighed. The authors concluded for the coexistence of high overweight and stunting rates in this age group. Neri [30], referring to the steady decline of stunting in Brazil, and trends to a rapid increase in overweight and obesity for adolescents and adults, attributed these findings to a better income distribution due, among other reasons, to a major expansion of cash transfer programs for poor families [31].

Hemoglobinopathies could have explained the anemia we observed but this seems to be an unlikely explanation. RS did indeed receive immigrants from Northern Italy (Piedmont) [32] but in practice severe thalassaemia cases are rare in RS. In 117.320 newborns in RS screened for hemoglobinopathies in the first few days of life a hemoglobin variant was found in 1.4% [12]. The most frequent abnormality was sickle cell trait (1.342 newborns). As for sickle cell anemia (SCA), the most prevalent hemoglobin abnormality in Brazil [33], there are only about one thousand patients in RS, one out of 11.000 newborns [12].

As has been described by others in the same region of the country [34]–[35], colored individuals of all ages and SeS were at greater risk for anemia. In the United States, after removing alpha-thalassemia, iron deficiency, renal insufficiency or sickle cell trait, African Americans still had lower Hb compared to the white population [36]. There is no similar study in Brazil.

Although in our study we only included children older then 18 months of age, we could speculate that the very high prevalence of anemia detected in children between 18 and 24 moths of age (76%) is a reflection of early life nutrition.

In RS, a nested cross-sectional study was conducted in a contemporary cohort in the city of Porto Alegre [37]. The authors found that the incidence rate of bottle-feeding was 21.3% for newborns at Day 7, and 46.9% for infants at Day 30 of life, suggesting the early introduction of cow milk. The use of cow’s milk in lieu of other foods rich in bio available iron was shown to be a risk factor for childhood anemia in several studies in Brazil and abroad [38]–[42].

Low SeS, known to be a risk for anemia, was also an independent risk factor for anemia in women and children in our population, as was also demonstrated by others in the same region [43]. Although to belong to the upper social stratus was not an independent risk factor, anemia was also very prevalent in the upper social classes for both women and children (Tables 1 and 2).

In conclusion, anemia is a public health issue in RS, affecting all social stratus, fertile women at all ages and 76% of the children from 18 to 24 months of age. National efforts to overcome micronutrient deficiencies are recent and still in progress in Brazil. The evidences brought by our study underline the need of implementing educational programs such as “Children without Anemia in RS” designed to built awareness to the problem among physicians, nurses, nutritionists and professionals involved in primary health care, as well as to the society, in general.

Acknowledgments

We wish to thank HEMOAMIGOS HCPA, Pastoral da Criança do RS, Serviço Social do Comercio RS, Universidade Federal do Rio Grande do Sul, Fundação Faculdade Federal de Ciências Médicas de Porto Alegre, Pontificia Universidade Católica RS, Universidade Luterana do Brasil, Federal University of Pelotas, University of Passo Fundo, Universidade Católica de Pelotas, Universidade Federal de Santa Maria, Universidade de Caxias do Sul and Universidade Federal de Rio Grande.