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Obesity Research & Clinical Practice (2013) 7, e218e229

ORIGINAL ARTICLE

Overweight is associated with low hemoglobinlevels in adolescent girls

Ursula Viana Bagnia,, Ronir Raggio Luiz b, Gloria Valeria da Veiga a

a Department ofNutrition, Federal UniversityofRio de Janeiro.Av. Carlos Chagas Filho 373, Bloco J, 2

andar, Ilha do Fundo, Rio deJaneiro, RJ - CEP21941-902, Brazilb Department ofPublic Health Studies, Federal UniversityofRio deJaneiro. PracaJorge Machado Moreira100, Cidade Universitria, Ilha do Fundo - Rio deJaneiro, RJ CEP21941598, Brazil

Received 12 September 2011; received in revised form 17 December 2011; accepted 29 December 2011

KEYWORDS

Adolescent;

Iron deficiency anemia;

Hemoglobin;

Overweight;

Body fat

Summary

Objective: To verify the prevalence of iron deficiency anemia according to sexualmaturation stages and its association with overweight as well as excessive body fatin adolescents.Design: A school-based cross-sectional study was performed. Anemia was assessed

by measuring the hemoglobin level (Hb). Nutritional status was defined by sex andage specific body mass index (BMI) cutoffs, and body fat (BF) was determined bybioelectrical impedance. Sexual maturation was assessed by breasts/genitalia andpubic hair development stages. Statistical analyses considered the effect of clustersampling design (classes) and sampling expansion corrected by relative weight. Oddsratio and general linear modeling were used to assess the associations, regarding thevalue of p < 0.05 for statistical significance.Setting: Public schools in the Metropolitan area of Rio de Janeiro, Brazil.Subjects: Probabilistic sample of 707 teenagers between 11.0 and 19.9 years old.Results: The prevalence of anemia among the adolescents was 22.8% (95%CI16.730.2%), higher among girls than among boys (30.9% vs. 10.9%; p < 0.01). Thechance of developing anemia did not change with the nutritional status accordingBMI or BF percentage, however, overweight girls presented lower Hb levels thanthose who were not overweight (12.2 g/dL vs. 12.8 g/dL, p < 0.01). In boys this asso-ciation was not observed. Sexual maturation did not change the association of Hband anemia with overweight and excessive body fat.Conclusion: The reduction of Hb levels points at overweight as a risk factor for thedevelopment of iron deficiency among adolescents. 2012 Asian Oceanian Association for the Study of Obesity. Published by ElsevierLtd. All rights reserved.

Corresponding author at: Instituto de Nutrico Josu de Castro, Centro de Cincias da Sade, Universidade Federal do Rio deJaneiro. Av. Carlos Chagas Filho 373, Bloco J, 2 andar, Ilha do Fundo, Rio de Janeiro, RJ - CEP 21941-902, Brazil.Tel.: +55 21 2562 6432.

E-mail addresses:[email protected] (U.V. Bagni), [email protected] (R.R. Luiz), [email protected] (G.V.d. Veiga).

1871-403X/$ see front matter 2012 Asian Oceanian Association for the Study of Obesity. Published by Elsevier Ltd. All rights reserved.

doi:10.1016/j.orcp.2011.12.004


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Overweight and low hemoglobin levels e219

Introduction

Iron deficiency anemia is the most prevalent nutri-tional disorder around the world, with pregnantwomen and children as the main risk groups [1,2].Adolescents, however, also have a high vulnerabilityto anemia [3]. In this age group, anemia can resultin impaired immune function and cause highervulnerability to infections; reduction of physicalresistance and tolerance to efforts, as well as dam-ages to growth and intellectual capacity, hence,difficulty to concentrate and memorize, which canlead to negative results in the learning develop-ment and school performance [2,4,5].

Anemia affects approximately 30% to 55% ofadolescents of all over the world [6], and the vul-nerability in this age group has been traditionallyassociated with the intense physical modifications

that happen during puberty, which impose anincreasing need for energy, macronutrients, vita-mins, and minerals, especially during the growthspurt [3]. The iron requirement increases more thantwofold in boys and girls during the sexual mat-uration, due to the total blood volume increase,total body mass gain, myoglobin synthesis and mus-cle mass gain, respiratory capacity increase, as wellas menstrual losses [3].

Inappropriate food habits also can be related tothe occurrence of iron deficiency anemia amongadolescents. Habits frequently observed in this

group, such as changing the principal meals forsnacks, skipping breakfast, reducing the intake offruits and vegetables, and the increasing consump-tion of sodas and high calorie foods [79], notonly can result in of iron deficiency due to insuf-ficient consumption of its sources [10], but canalso increase the risk of chronic diseases suchas obesity [11,12], which has been reported asa risk factor for iron deficiency anemia indepen-dently of food consumption [1315]. Many studieshave verified a higher proportion of iron deficiencyand anemia among overweight adults and elders[13,14,1618], and also among overweight chil-

dren and adolescents [13,1921], and such fact hasbeen attributed to the mineral homeostasis damagecaused by increased inflammatory activity in theadipose tissue of overweight people [13,2224].

In Brazil, research on the prevalence of irondeficiency anemia in adolescents, as well as itsassociated factors, are still scarce, and the inves-tigation focusing on this part of the population isnot yet included in large epidemiologic studies andnational surveys [25]. However, a high prevalence ofthe problem has been observed in local studies withadolescents, reaching 24.4% and 43.0% in southeast

[26] and southern [27] cities, as well as 35.7% and

42.6% in northeastern [28] and northern cities ofthe country [29].

Only a few studies developed in Brazil inves-tigated the problems related to the occurrenceof iron anemia specifically during adolescence,

such as the influence of sexual maturation stages,the occurrence of menarche, and the variationsof the menstrual cycle. Besides, the results arestill extremely controversial. Although a highprevalence of anemia and a low hemoglobin con-centration during the growth spurt have alreadybeen identified among Brazilian boys [30] and girls[3032], some researchers did not find any associ-ation [33,34].

Most of the studies addressing nutritional status[10,28,3537] focused on the association of anemiawith malnutrition, and used only anthropometricindices for nutritional assessment. The associa-

tion of anemia with obesity has not been deeplyinvestigated, however, the current epidemiologicalscenario requires new investigations regarding thisaspect, as obesity and iron deficiency anemia havereached epidemic proportions around the world[1,38], including Brazil [25,39], and both can dam-age growth and development during adolescence.In this context, it is believed that the body composi-tion assessment, in conjunction with anthropomet-ric indices, could help clarify such an association.

Thus, the current study was developed to reachtwo main objectives: (a) to describe the preva-

lence of iron deficiency anemia and its distributionaccording to sexual maturation stages and the vari-ables related to the menstrual cycle; and (b) toverify the association of anemia with overweightand body fat in adolescent students from publicschools in the Metropolitan area of Rio de Janeiro,Brazil.

Methods

A probabilistic sample including adolescent stu-dents aged 1119.9 years, from 5th grade of apublic elementary school to 3rd year of high school,in the city of Niteri, Southeastern Brazil, wasassessed in a cross-sectional study. The studentswere enrolled in 13 out of 34 public state schoolswho took part in a larger research, in which themain objective was to assess the evolution of over-weight and obesity in teenagers by comparing twocross-sectional studies made between the years2003 and 2008/2009. In Brazil, public schools areusually attended by students with low socioeco-nomic status.

Niteri is a city located in the metropolitan east

side of Rio de Janeiro, and it is approximately 15 km


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e220 U.V. Bagni et al.

away from the state capital. It encompasses an areaabout 130,000 km2, and is the sixth most populouscity of the state, with approximately 480,000 inhab-itants.

The data analyzed in this article were obtained

in the second study, collected between May 2008and April 2009. The sampling size was estimatedin 780 students distributed among 34 classes (withabout 23 students each), taking into account 30% ofnon-response, as observed in the pilot study. Withthis sampling size, it would be possible to estimate35% of anemia prevalence [34], at a 95% confidenceinterval with 5% precision, and considering the clus-ter sampling in one stage (random classes).

All adolescents in the established age group withregular attendance to classes were invited to takepart in the study. The participation was voluntary,and only those who had consent forms signed by

their parents were allowed to participate.The physically impaired adolescents who were

unable to take part in the anthropometric assess-ment, pregnant teenagers, and the ones whoreported, in the interview right before the bloodtest, having history of diseases leading to ane-mia not caused by iron deficiency, or having ironaccumulation diseases or capillary fragility and/orcoagulation abnormality were considered ineligi-ble.

The presence of anemia was assessed bymeasuring blood hemoglobin (Hb) concentration,

using a portable -hemoglobinometer (HemoCue

).Adolescents between 10 and 11 years old withHb < 11.5 g/dL, between 12 and 14 years oldwith Hb < 12.0 g/dL, boys over 15 years old withHb < 13.0 g/dL, and girls over 15 years old withHb < 12.0 g/dL were considered anemic [2].

Weight was measured with an electronic plat-form scale (Kratos), that has a 150 kg capacityand a 50 g resolution. Height was assessed usinga portable anthropometer manufactured in Brazil(Alturexata), which has a 213 cm amplitude and a0,1cm resolution. The height was measured twice;a 0.5 cm maximum variation was allowed betweenthe two measures, and then the mean value wascalculated. The adolescents wore light clothes,with no shoes on. Body mass index was calculated(BMI=weight/height2), and the nutritional statuswas classified according to the criteria of the WorldHealth Organization [40], based on the followingcutoff points: 1 to 2 Z-scores (overweight) and >2 Z-scores (obesity).

Body composition was assessed by bioelectricalimpedance analysis (RJL System, model 101Q),and the fat free mass was estimated by using the

equation validated by Houtkooper et al. [41] for

adolescents from 10 to 19 years old. Body fat (BF)mass (kg) was calculated as the difference betweenweight (kg) and fat free (FF) mass (kg). The body fatpercentage (BF%) was obtained, regarding as excessthe values 25% for boys and 30% for girls, which

were related to morbidity associated with BF excessin teenagers [42].Sexual maturation stage was investigated, focus-

ing on the development of breasts, genitalia,and pubic hair, in accordance with the crite-ria of Tanner [43], and using the self-evaluationtechnique validated by Saito [44]. Both mea-surements were included in the analysis, oncethe breasts and genitalia reflect the activity ofthe hypothalamic-pituitary-gonadal axis, while thedevelopment of pubic hair is associated withactivity of both the hypothalamic-pituitary-gonadaland hypothalamic-pituitary-adrenal axis. For both

sexes, the prepubertal period was classified asStage 1; the beginning of the growth spurt as Stages2 and 3 for boys and Stage 2 for girls; the peak ofgrowth velocity as Stage 4 for boys and 3 for girls;and growth deceleration as Stage 5 for boys andStages 4 and 5 for girls. For the girls, the age ofmenarche occurrence, as well as the last menstru-ation date, was also obtained.

The current use of supplements with iron, cur-rent smoking habits, current and/or past diagnosisof parasitic diseases and information related to themenstrual cycle were investigated using a ques-

tionnaire previously completed by the adolescentsthemselves.Statistical analyses were made regarding the

cluster sampling design and the sampling expan-sion corrected by the relative weight, using thecommands for complex samples (ComplexSamples)of the software Statistical Package for the SocialSciences SPSS version 19.0. For the associationanalyses, general linear model procedures wereused for continuous variables; and logistic regres-sion was performed for categorical variables. Allthe analyses were stratified by sex, due to the rec-ognized heterogeneity of anemia prevalence andthe associated factors between boys and girls.

An exploratory analysis of the dependentvariables, hemoglobin and anemia, and the inde-pendent variables, nutritional status (underweight;adequate weight; overweight; obesity) and BF%classification (without excess; with excess), wasconducted. An analysis of the covariates sex, agegroup (from 11 to 13.9 years old; 14 to 16.9 yearsold; 17 to 19.9 years old), sexual maturation stage(beginning of growth spurt; peak of growth velocity;growth deceleration), use of iron supplementation,current use of cigarettes, current and/or past diag-

nosis of parasitic diseases, menarche occurrence,


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menarche date (less than 2 years before the assess-ment; 2 or more years before the assessment), andlast menstruation date (less than 7 days before theassessment; from 7 to 15 days before the assess-ment; more than 15 days before the assessment)

was also performed, presenting the prevalenceand 95% confidence interval (95%CI) for categori-cal variables and means and standard error (SE) forcontinuous variables.

The strength of the association between anemiaand the exposure variables and co-variables wasmeasured by odds ratio (OR) with its respective95%CI, analyzing as dummy the categorical non-binary variables.

Multivariate analysis were made in order toinvestigate the association of both anemia andblood Hb concentration with nutritional status eval-uated by BMI (not overweight; overweight) and

BF% (without excess; with excess), adjusted forthe effect of age and sexual maturation stages(both pubic hair and breasts/genitalia), as theyare potential confounders of these associations,regardless of the statistical significance in thebivariate analysis. We also adjusted for other pos-sible confounding variables (FF mass, use of ironsupplementation, current use of cigarettes, cur-rent and/or past diagnosis of parasitic diseases)that presented p < 0.20 in bivariate analysis. Themultivariate analysis was made using the back-ward selection procedure, remaining in the model

the variables age and sexual maturation stages(pubic hair, breasts/genitalia) regardless of theirstatistical significance, and the possible confound-ing variables that demonstrated p< 0.05. For thecovariates that demonstrated p < 0.05 in multivari-ate analysis, we tested the existence of interactionwith nutritional status.

The correlation of Hb concentration (g/dL) withthe following variables was verified: age (years),BMI for age (Z-score), FF mass (kg), BF mass (kg),BF%, age at menarche period (years), date of thelast menstruation (days), with ap-value < 0.05 indi-cating statistical significance.

The research was approved by the Committee forEthics in Research of the Instituto de Pediatria ePuericultura Martago Gesteira of the Federal Uni-versity of Rio de Janeiro (protocol number 27/08).

Results

From the total number of 707 participants,59.3% (95%CI: 53.465.0%) were girls and agreater proportion of the adolescents were about1416.9 years old. Most of the boys were experi-

encing the growth spurt and most of the girls were

experiencing the growth deceleration (Table 1).The menarche had already happened among 94.1%(95%CI: 86.797.5%) of the girls, at the mean ageof 12.0 years (95%CI: 11.912.2 years). In 82.9%(95%CI: 71.890.2%) of these participants, menar-

che occurred 2 or more years before the assessmentdate. The beginning of the last menstruation hadhappened in 51.4% (95%CI: 44.957.9%) of theteenagers 2 or more weeks before the assessmentdate, although among the other girls, it occurred inthe week before (22.7%; 95%CI:19.326.6%) or dur-ing the week of the study assessment (25.9%; 95%CI:20.132.6%).

The nutritional status according to BMI wassimilar in both sexes, once its verified that theproportion of overweight being much higher thanthat of underweight in both boys (20.4% and 2.3%)and girls (21.8% and 0.9%). Due to the low preva-

lence of underweight (1.5%; 95%CI: 0.82.7%) andobesity (4.5%; 95%CI: 2.77.6%) in the populationassessed, the nutritional status was presented inthe remaining analyses as a binary variable (notoverweight; overweight). Regarding BF%, girls pre-sented a higher proportion of excessive body fatwhen compared to boys (29.6% vs. 10.1%;p < 0.01),whereas the FF mass showed no differences regard-ing sex (Table 1).

Iron deficiency anemia was present in 22.8%(95%CI: 16.730.2%) of the adolescents. The girlshada three-times-higher chance of developing ane-

mia than the boys (OR = 3.64 95%CI 2.156.22),and both boys and girls from 14 to 16.9 yearsold had more chance of having have anemia.Among males, the chance of developing anemiawas six times higher in boys experiencing thepeak of growth velocity according to their pubichair, when compared to those already experiencinggrowth deceleration (OR = 6.43 95%CI 1.2533.38)(Table 2).

The mean Hb concentration was 13.1 g/dL(95%IC: 12.813.3), with minimum and maximumconcentrations of 9.0 g/dL and 17.9 g/dL, respec-tively. The Hb was lower in girls than in boys(12.5g/dL vs. 14.0 g/dL, p


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Table 1 Characteristics of the adolescents regarding the biological and health variables and nutritional status Niteri, Rio de Janeiro, Brazil, 2008/2009 (n = 707).

Boys (n = 288) Girls (n = 419) p*

n % 95%CI n % 95%CI

Age 288 41911 to 13.9 years old 55 19.0 9.334.8 103 24.5 13.440.6 0.3614 to 16.9 years old 150 52.3 41.363.0 185 44.2 32.856.317 to 19.9 years old 83 28.8 17.842.9 131 31.2 19.546.0

Sexual maturation stage

(breasts/genitalia)

288 416

Beginning of growth spurt 113 39.3 32.446.6 16 3.9 1.211.7


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Table 2 Odds ratio (OR) and 95% confidence interval (95%CI) of anemia according to biological and health variables,and nutritional status Niteri, Rio de Janeiro, Brazil, 2008/2009.

Boys Girls

% Crude OR 95%CI % Crude OR 95%CI

Nutritional statusNot overweight 11.0 1.00 29.5 1.00Overweight 10.6 0.96 0.392.41 35.6 1.32 0.722.43

Body fat percentageWithout excess 10.8 1.00 32.5 1.00With excess 9.1 0.82 0.213.30 26.9 0.77 0.441.33

Age11 to 13.9 years. 7.0 1.16 0.284.76 31.1 1.58 0.623.9914 to 16.9 years. 15.0 2.69 1.046.93 36.9 2.04 1.073.9117 to 19.9 years. 6.1 1.00 22.2

Sexual maturation stage (breasts/genitalia)Beginning of growth spurt 10.5 4.98 0.6339.71 0.0 Peak of growth spurt 12.4 4.11 0.6647.62 33.2 1.08 1.081.08Growth deceleration 2.8 1.00 31.6 1.00

Sexual maturation stage (pubic hair)Beginning of growth spurt 8.7 3.26 0.7614.05* 49.3 2.04 0.508.37*

Peak of growth spurt 15.7 6.43 1.2533.38 22.8 0.62 0.351.11Growth deceleration 2.8 1.00 32.3 1.00

Menarche occurenceYes 31.7 2.14 0.528.85No 17.8 1.00

Menarche date


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Table 3 Mean and 95% confidence interval (95%CI) of hemoglobin concentration to biological, health and nutritionalstatus Niteri, Rio de Janeiro, Brazil, 2008/2009.

Boys Girls

Crude mean

(g/dL)

95%CI p* Crude mean

(g/dL)

95%CI p*

Nutritional StatusWithout overweight 14.1 13.714.5 0.31 12.6a 12.312.8


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Figure 1 Correlation of hemoglobin concentration with body mass index, and with body fat percentage Niteri, Riode Janeiro, Brazil, 2008/2009.

during the peak of growth velocity, on the basisof the assessment of pubic hair development,boys presented higher chances of having anemia,a tendency also observed by Silva et al. [30] andIuliano et al. [31]. In girls, the reduction of Hbconcentration that begins with the peak of growthvelocity according based on the assessment of

breast development corroborates with the increaseof vulnerability to the disease in puberty, as provenby other authors [3032]. The hypothesis that theoccurrence of menarche as well as the onset of themenstrual cycles would be associated with a higherprevalence of anemia was not, however, confirmedin this study. It is believed that, because only 6%of the girls still had not experienced their firstmenstruation, this association became weakened.In addition, the power of the sample to investigatethe association between anemia and menarchewas low, which impaired statistical significance for

this association even though the chance of anemia

among postmenarcheal girls was 2.4 times higherthan among those who had not yet had their firstmenstruation.

The fact that overweight girls presented sig-nificantly lower Hb concentrations in comparisonwith those who were not overweight, is in agree-ment with the results observed by Eftekhari et al.

[47] among Iranian girls from 13 to 20 years old, inwhich the Hb concentrations reduced significantlyfrom 13.1 to 12.5 g/dL when the BMI classifica-tion changed from normal to overweight (BMI forage 95th percentile).

An explanation for the relation between over-weight and the impairment in iron status wouldbe the increase of inflammatory activity in theadipose tissue of obese individuals, which wouldlead to a higher production of hepcidin, a keyhormone for the regulation of intestinal absorp-tion and iron homeostasis [2224]. Inflammatory

cytokines, particularly interleukin-6, act directly


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in the hepatocytes, stimulating the expression ofthe hormone, which, when in contact with thebloodstream, binds to the cellular ferroportin, aniron exporter transmembrane protein. This bindinginduces the ferroportin internalization and degra-

dation by the lysosomes, and with the loss of thistransporter, iron export is blocked and the degradediron is retained within the macrophage cell, favor-ing the reduction of circulating iron [2224]. Inthe enterocytes, the ferroportin internalization anddegradation blocks the transfer of iron from thecytoplasm to the plasma transferrin [23], and suchiron retention inhibits the apical uptake and theutilization of the dietary iron by intestinal cells[22], further increasing the effect over the con-centration of the circulating mineral. Thus, evenwhen the iron intake is adequate, individuals whowere overweight and with excessive body fat have

higher predisposition to develop iron deficiencyanemia, because there is lower utilization of themineral in the body, as evidenced by several authors[1315,48,49].

Although, in this study, the change in nutritionalstatus from not overweight to overweight did notincrease significantly the adolescents chance ofdeveloping anemia, the reduction in the Hb concen-tration observed, especially among girls, pointedat the important fact that the iron homeostasismay have been damaged among the individualswith higher a BMI. The impairment in iron sta-

tus, whether the youngster present anemia ornot, is cause for concern and can bring negativerepercussions during adolescence, such as poor cog-nitive development, disruptions in learning and badschool performance [2,5,37,50,51].

A limitation of this study was that the sam-ple was calculated to assess the prevalence ofanemia, resulting in a reduction in the power ofthe study to investigate the association of ane-mia and hemoglobin with the exposure variables.However, despite this limitation, it was possibleto show that overweight was associated with lowhemoglobin concentration in girls, indicating that ifthe sample had been larger, stronger and significantassociations could have been detected with othervariables, such as body fat percentage in boys, forwhich p value was borderline (Table 3).

Other factor that can be related to the weakassociations and correlations observed in this studyconcerning the impact of overweight in hemoglobinconcentration and anemia prevalence was thereduced number of adolescents with obesity (4.5%of the total sample). The impairment of ironmetabolism seems to be more evident when thelevel of overweight is higher, as noticed by Eftekhari

et al. [47] in Iranian girls, in which the prevalence of

anemia between girls with weight between the 85thand the 95th percentiles of BMI for age (28.8%) wassimilar to the normal weight ones (27.8%), whereasthose over the 95th percentile presented more ane-mia than the rest of the group (34.1%).

Because the BMI has limitations in diagnos-ing obesity in teenagers (it does not adequatelydescribe the variations of body composition duringgrowth), in this study, we assessed the adolescentsbody composition by bioelectrical impedance, aim-ing to identify the effect of BF% excess in theprevalence of anemia and the concentration ofHb. However, no association or correlation wasobserved.

A possible explanation would be that the Hb con-centration, the parameter used in this study, isgenerally affected only at the final stage of irondeficiency [2], and thus, early and discrete alter-

ations in the mineral homeostasis, which couldalready be occurring due to the excessive weightand BF, could not be observed in the adolescentsassessed. However, given the difficulty to collect,store, and process blood in epidemiological studieslike this, we chose to assess the Hb concentra-tion, the most commonly used marker when theobjective is to evaluate anemia itself and not irondeficiency, as recommended by the World HealthOrganization [2]. In future studies, we suggest thatiron status, transferrin saturation and other earlymarkers of iron deficiency should also be assessed.

The biochemical assessment of inflammatory indi-cators, such as the C-reactive protein, can also helpclarify the relation between excessive adiposity,inflammation and iron deficiency.

In this study, there was an initial loss of 23.8%of eligible adolescents, which could representa limitation in the results interpretation. How-ever, it is believed that such losses have nothad any influence on the results, because uponcomparison of the adolescents enrolled in thestudy with those eligible non-participants, no sig-nificant difference was observed regarding theage mean (16.01.9 years old vs. 15.91.9 yearsold, p = 0.88) and the distribution by age group(p = 0.52), variables that are significantly associ-ated with anemia and sexual maturation. Althoughparticipants and non-participants had been hetero-geneous regarding sex, a higher frequency of girlsamong the participants (60.3% vs. 43.3%), did notinfluence the associations, as all the analyses werestratified by sex.

We conclude that overweight had a negativeinfluence on the nutritional status of iron inthe adolescents investigated, particularly amonggirls. Longitudinal studies may help understand

the dynamics of iron homeostasis during puberty,


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pointing with more certainty the periods of greatestrisks of developing this mineral deficiency. Facingthe impressive increase of overweight prevalenceamong adolescents, the development of studies toidentify cutoff points for overweight and exces-

sive body fat that define the risk of iron deficiencyanemia in this age group is recommended, so thatactions and programs focused on youngsters caninclude anemia among their priorities.

Conflicts of interest

There are no conflicts of interest associated withthe publication of this work, and that werenot omitted information about any affiliations orfinancial agreements between the authors and com-

panies or individuals who might have interest in thesubject matter in the article.

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