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Profiles of anemia among school-aged children categorized by body mass index and
waist circumference in Shandong, China

Ying-xiu Zhang, Jian Chen, Xiao-hui Liu

PII: S1875-9572(20)30192-3
DOI: https://doi.org/10.1016/j.pedneo.2020.11.002
Reference: PEDN 1113

To appear in: Pediatrics & Neonatology

Received Date: 2 July 2020

Revised Date: 29 July 2020
Accepted Date: 27 November 2020

Please cite this article as: Zhang Y-x, Chen J, Liu X-h, Profiles of anemia among school-aged children
categorized by body mass index and waist circumference in Shandong, China, Pediatrics and
Neonatology, https://doi.org/10.1016/j.pedneo.2020.11.002.

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Copyright © 2020, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. All rights reserved.
Profiles of anemia among school-aged children categorized by body

mass index and waist circumference in Shandong, China

Ying-xiu Zhang 1*, Jian Chen 2#, Xiao-hui Liu 2

1
Shandong Center for Disease Control and Prevention, Shandong University

Institute of Preventive Medicine, Shandong, China

2
Qingdao Municipal Center for Disease Control and Prevention, Qingdao

Institute of Preventive Medicine, Shandong, China

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* Correspondence:

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Ying-xiu Zhang, Shandong Center for Disease Control and Prevention,
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Shandong University Institute of Preventive Medicine, Shandong, China,
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16992 Jingshi Road, Jinan, Shandong 250014 China
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Tel: 86-0531-82679413 Fax: 86-0531-82679413

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E-mail: sdcdczyx@163.com
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Jian Chen, Qingdao Municipal Center for Disease Control and Prevention,
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Qingdao Institute of Preventive Medicine, Shandong, China, 175 Shandong

Road, Qingdao, Shandong 266033 China.

Tel: 86-0532-85650274 Fax: 86-0532-85650274

E-mail: qdcdcchenjian@163.com

# Jian Chen and Ying-xiu Zhang have contributed equally to this work should

be considered as co-first authors.

18 pages for total text

2400 words, 3 tables, 2 figures, 40 References

 PEDN-D-20-00418_After Eng edited_final

Profiles of Anemia Among School-aged Children Categorized by Body

Mass Index and Waist Circumference in Shandong, China

Ying-xiu Zhang 1*, Jian Chen 2#, Xiao-hui Liu 2

1
Shandong Center for Disease Control and Prevention, Shandong University

Institute of Preventive Medicine, Shandong, China

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2

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Qingdao Municipal Center for Disease Control and Prevention, Qingdao

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Institute of Preventive Medicine, Shandong, China
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* Correspondence:

Ying-xiu Zhang, Shandong Center for Disease Control and Prevention,

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Shandong University Institute of Preventive Medicine, Shandong, China,

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16992 Jingshi Road, Jinan, Shandong 250014 China

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Tel: 86-0531-82679413 Fax: 86-0531-82679413

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E-mail: sdcdczyx@163.com

Jian Chen, Qingdao Municipal Center for Disease Control and Prevention,

Qingdao Institute of Preventive Medicine, Shandong, China, 175 Shandong

Road, Qingdao, Shandong 266033 China.

Tel: 86-0532-85650274 Fax: 86-0532-85650274

E-mail: qdcdcchenjian@163.com

# Jian Chen and Ying-xiu Zhang have contributed equally to this work and

should be considered as co-first authors.

18 pages for total text

2400 words, 3 tables, 2 figures, 40 References

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Profiles of Anemia Among School-aged Children Categorized by Body

Mass Index and Waist Circumference in Shandong, China

Abstract

Background: The prevalence of childhood obesity has been increasing

worldwide. The connection between iron deficiency and obesity has received

much research interest. The present study examined the profiles of anemia

among school-aged children categorized by obesity-related index in Shandong,

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China.

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Methods: A total of 20 172 children aged 7, 9, 12, and 14 years participated in
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the study, whose hemoglobin (Hb) concentration was measured by laboratory
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technicians. The prevalence rates of anemia among children within each

subgroup categorized by body mass index (BMI), waist circumference (WC)

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and waist-to-height ratio (WHtR) were determined.

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Results: On the whole, 3.99% of boys and 6.68% of girls suffer from anemia.
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Disparities in the prevalence of anemia were observed between different

subgroups categorized by BMI, WC and WHtR. For both boys and girls, the

prevalence of anemia increased with the severity of thinness and obesity,

suggesting that both severe thinness and severe obesity are associated with

an elevated prevalence of anemia.

Conclusion: In the era of the obesity pandemic, obesity could potentially add

to the burden of anemia, suggesting that obese children should not be ignored

when establishing strategies targeted at preventing anemia.

Key words: anemia; obesity; prevalence; body mass index; waist

circumference; waist-to-height ratio; children.

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1 Introduction

Anemia refers to a condition in which the number of red blood cells or their

oxygen-carrying capacity is insufficient to meet physiological needs; it

continues to be an important public health problem worldwide, especially in

developing countries 1. Iron deficiency (ID) is the most common cause of

anemia, which is responsible for around 25% to 50% of all the cases of anemia

worldwide 2. Children and adolescents have increased demand for iron due to

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their rapid growth and development, and ID and anemia are common

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nutritional problems in these age groups, leading to adverse effects on
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3,4
cognitive development and physical growth . Globally, around 600 million
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preschool and school-aged children suffer from anemia 5. China has been

undergoing rapid economic transition over recent decades, children's dietary

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patterns and nutritional status have improved considerably, and the prevalence
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of anemia among school-aged children decreased from 18.8% in 1995 to 9.9%

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in 2010 6.

The prevalence of childhood obesity has been increasing worldwide at an

alarming rate. A recent analysis of population data of children and adolescents

aged 5–19 years estimated that 50 million girls and 74 million boys worldwide

were obese in 2016 7. Following the worldwide trends, Chinese children and

adolescents are becoming increasingly overweight and obese; it was

estimated that 9.9% and 5.1% of Chinese children and adolescents aged 7–18

years were overweight and obese, representing an estimated 30.43 million

individuals in 2010 8. More interestingly, a meta-analysis concluded that

obesity was significantly associated with ID, and early monitoring and

treatment of ID was recommended in overweight and obese individuals 9.

Therefore, we hypothesized that a connection between obesity and anemia

may exist in children and adolescents.

Body mass index (BMI) is perhaps the most commonly used measure for

10
general obesity in clinical practice and population surveys . Waist

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circumference (WC) and waist-to-height ratio (WHtR), giving relevant

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information about fat distribution, have commonly been used to identify
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11,12
abdominal obesity . In our study, based on a large sample, we examined
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the profiles of anemia among school-aged children categorized by

obesity-related index (BMI, WC and WHtR) in Shandong, China.

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2 Subjects and methods

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The study was approved by the Ethical Committee of the Shandong Center
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for Disease Control and Prevention, Shandong, China.

2.1 Study population

Data for this study were obtained from the National Survey on Chinese

Students’ Constitution and Health, which was carried out from September to

October 2014. The sampling method was stratified multi-stage sampling based

on selected schools. Six public schools (two primary schools, two junior high

schools, and two senior high schools) from each of the 17 districts in

Shandong were randomly selected and invited to participate in the survey.

From participating schools, two classes in each grade were selected, and all

students of the selected classes were invited to join the study. All subjects

ranged from 7 to 18 years of age, and all were of Han ancestry that accounts

for ~99.32% of the total population in Shandong. For subjects aged 7, 9, 12,

and 14 years, determination of Hb was implemented. Thus, the present study

only included those children in the four age groups who had data on Hb

collected, and a total of 20 172 participants were included in the analysis. All

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districts sampled in our study were located at an altitude below 200 m.

2.2 Measurements -p
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All measurements were performed by a team of trained health professionals
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in each of the 17 districts. Each professional is required to pass a training

course for anthropometric measurement organized by the investigation team in

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Shandong. All measurements were taken using the same type of apparatus
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and followed the same procedures. Height without shoes was measured using
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metal column height-measuring stands to the nearest 0.1 cm. Weight was

measured using lever scales to the nearest 0.1 kg while the subjects wore light

clothing. BMI was calculated from their height and weight (kg/m2). WC was

measured midway between the lowest rib and the superior border of the iliac

crest with an inelastic measuring tape at the end of normal expiration to the

nearest 0.1 cm; and WHtR was calculated as WC divided by height. BMI and

WC were categorized into eight subgroups (<5th, 5th–14th, 15th–24th,

25th–49th, 50th–74th, 75th–84th, 85th–94th and ≥95th percentile) according

to the sex- and age- specific percentiles. WHtR was categorized into seven

subgroups (0.30–0.34, 0.35–0.39, 0.40–0.44, 0.45–0.49, 0.50–0.54, 0.55–0.59,

and ≥0.60) according to the WHtR values (WHtR is proposed as independent

13
of age and gender . Hemoglobin (Hb) concentration was measured by

laboratory technicians for the selected students. Samples of capillary blood

from the fingertip of each child were collected after discarding the first drop. Hb

determination was detected with the cyanmethemoglobin method using a

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spectrophotometer.

2.3 Definitions -p
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The BMI cut-offs recommended by the International Obesity Task Force
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(IOTF) were used to define thinness (grade 1–3), normal weight, overweight

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and obesity (grade 1–3) . The categories of body weight status and
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corresponding BMI cut-offs at 18 years are as follows: thinness grade 3 (BMI

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<16 kg/m2); thinness grade 2 (BMI 16 to <17 kg/m2); thinness grade 1 (BMI 17
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to <18.5 kg/m2); normal weight (BMI 18.5 to <25 kg/m2); overweight (BMI 25 to

<30 kg/m2); obesity grade 1 (BMI 30 to <35 kg/m2); obesity grade 2 (BMI 35 to

<40 kg/m2); and obesity grade 3 (BMI ≥40 kg/m2). The age- specific Hb

cut-offs recommended by WHO were used to define anemia, and Hb status

was categorized as follows: (1) for children aged 7–9 years, ≥115 g/L normal,

110–114 g/L mild anemia, 80–109 moderate anemia, and <80 g/L severe

anemia; (2) for children aged 12–14 years, ≥120 g/L normal, 110–119 g/L mild

anemia, 80–109 moderate anemia, and <80 g/L severe anemia 16.
2.4 Statistical analyses

Comparisons of Hb concentration and the prevalence rates of anemia

between different groups were made by t-test or χ2 test. All analyses were

performed with the statistical package SPSS 11.5. Significance was defined at

the 0.05 level.

3 Results

3.1 Hb concentration and prevalence of anemia

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The mean values of Hb concentration and prevalence of anemia by gender

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and age groups in the sample are shown in Table 1. For boys, Hb
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concentration increased with age, from 134.29 g/L at 7 years to 145.22 g/L at
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14 years (P <0.05). For girls, Hb concentration increased from 132.60 g/L at 7

years to 134.24 g/L at 12 years (P <0.05), and then dropped slightly to 133.73
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g/L at 14 years (P >0.05). A obvious gender difference was observed, with

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boys having a higher Hb level than girls (P <0.01). On the whole, the total
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prevalence rates of anemia were 3.99% (95% CI 3.61–4.37%) for boys and

6.68% (95% CI 6.19–7.17%) for girls (P <0.01). In all cases of anemia, mild

anemia accounts for 65.66% (boys) and 72.31% (girls), and moderate anemia

accounts for 34.34% (boys) and 27.69% (girls), respectively; no severe

anemia cases were observed in the sample. Gender differences in the

prevalence of anemia were observed at 12 and 14 years, with girls having a

higher prevalence of anemia than boys (8.25 vs. 5.04% and 9.79 vs. 2.73%, P

<0.01). No statistically significant differences were observed at 7 and 9 years

(P >0.05).

3.2 Anemia within different subgroups by BMI, WC and WHtR

The prevalence of anemia among children within each subgroup categorized

by BMI and WC percentiles is shown in Figure 1. Children in the BMI <5th

subgroup had the highest prevalence of anemia (6.01% for boys and 10.91%

for girls), while those in the BMI ≥95th subgroup also had a sub-high

prevalence of anemia (4.60% for boys and 8.12% for girls). Similar distribution

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was also observed across the subgroups categorized by WC.

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The prevalence of anemia within each subgroup categorized by WHtR is
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shown in Figure 2. Children in the low and large WHtR subgroups had a high
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prevalence of anemia; for example, the prevalence rates of anemia were

8.96% (boys) and 10.53% (girls) in the WHtR 0.30–0.34 subgroup, 7.41%
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(boys) and 14.29% (girls) in the WHtR ≥0.60 subgroup, respectively.

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3.3 Anemia within different BMI categories based on the IOTF cut-offs
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Distribution of BMI categories based on the IOTF cut-offs is shown in Table

2. The total prevalence of thinness grades 1–3, and overweight and obesity

grades 1–3 were 6.78% (95% CI 6.29–7.27%), 19.61% (95% CI

18.83–20.39%) and 9.95% (95% CI 9.37–10.53%) for boys, and 11.17% (95%

CI 10.56–11.78%), 14.96% (95% CI 14.26–15.66%) and 4.49% (95% CI

4.09–4.89%) for girls, respectively. Boys had a higher prevalence of

overweight and obesity and a lower prevalence of thinness than girls (P <0.01).

The profiles of anemia in different subgroups categorized by the severity of

thinness and obesity are shown in Table 3. For both boys and girls, the

prevalence of anemia increased with the severity of thinness and obesity (P

<0.05).

4 Discussion

Based on a large sample in Shandong, China, this study examined the

profiles of anemia among school-aged children categorized by obesity-related

index (BMI, WC and WHtR). Disparities in the prevalence of anemia were

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observed between different subgroups categorized by BMI, WC and WHtR,

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suggesting that both severe thinness and severe obesity were associated with
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an elevated prevalence of anemia. These findings provide a scientific basis for
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the prevention and control of anemia among school-aged children.

Anemia continues to be an important public health problem worldwide,

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especially in developing countries. In this study, we found that the total

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prevalence of anemia among school-aged children was 5.34% (3.99% for boys
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and 6.68% for girls) in Shandong Province in 2014, which can be classified as

16
a mild public health severity problem according to the WHO criterion .

Although the current prevalence of anemia among school-aged children was at

a relatively low level in this region, considering the huge population base (more

than 100 million people in Shandong Province), the absolute number of

children with anemia should not be ignored. Gender difference in the

prevalence of anemia was found in the ages of puberty (5.04 vs. 8.25% at 12

years; 2.73 vs. 9.79% at 14 years). The menstruation in girls could be a

possible explanation because girls lose blood during menstruation when they

enter puberty and thus are more vulnerable to anemia than boys. Evidence

has shown that a 1 mL loss of blood translates into a 0∙5 mg loss of iron, and

heavy menstrual blood loss (>80 mL per month in about 10% of women)

17
sharply increases the risk for iron deficiency . Eating behavior and pattern

may also play a role in the gender difference. Evidence has shown that

Chinese boys ate animal products more frequently, and fruits and vegetables

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less frequently than girls 18.

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It is understandable that a high prevalence rate of anemia was found
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among thin children and the prevalence of anemia increased with the severity
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of thinness. Under-nutrition may be the main reason because normal growth of

children and adolescents is dependent on adequate nutrition, thinness is

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19
frequently associated with nutritional deficiencies and eating disorders .
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Intervention strategies should include nutrition improvement, micronutrient

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supplementation, and health education for both children and their parents.

It seems counter intuitive that obesity, especially severe obesity, is also

associated with anemia because obesity is usually considered to be

over-nutrition. A higher prevalence of ID among obese children and

20-22
adolescents has been consistently observed in previous studies . For

example, Pinhas-Hamiel et al showed that low iron levels were present in

38.8%, 12.1% and 4.4% of obese, overweight and normal-weight children,

respectively 22. A study from China showed that the prevalence of ID increased
with the BMI categories among children and adolescents, from 4.7% in the

normal weight group to 8.9% in the obesity group 23. Various hypotheses have

been proposed for the association between obesity and ID, including

imbalanced nutrition and increased iron requirement due to larger blood

22
volume and/or body size in obese subjects . Nevertheless, several studies

examined daily dietary iron intake in obese and non-obese individuals, and

24-26
they found no significant difference between these two groups . In other

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words, current evidence does not suggest that dietary factors are important

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contributors to the differences in iron status between obese and non-obese
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subjects. By contrast, more studies suggested that adiposity-related
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inflammation could provide an explanation for the ID in obese subjects.

Because of obesity is characterised by a chronic, low-grade, systemic

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inflammation 27-30, this adiposity-related inflammation promotes the expression

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31,32
of hepcidin which in turn reduces iron absorption and serum iron .
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Evidence has shown that weight loss can result in an improvement in

33
inflammatory status and indicators of iron status in obese children . In

addition, obesity has been reported to be associated with anemia in adults 34,35.

Together with above-mentioned studies, obesity-related inflammation and

comorbidities may partly explain why severely obese children had a greater

prevalence of anemia in the current study. Naturally, intervention strategies

should focus on weight loss and promoting iron absorption.

Childhood obesity has increased dramatically during past decades, both in

 36,37
developing and developed countries . As the most populous nation in the

world, China is undergoing economic transition. Chinese children and

adolescents are becoming increasingly overweight and obese along with rapid

economic growth, and it can be inferred the increasing trend will continue in

8,38
future decades . Considering the fact that obesity could potentially add to

20
the burden of ID and anemia , we suggest that obese children should not be

ignored when establishing strategies targeted at preventing anemia.

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Despite including a large sample, our study has several limitations. Firstly,

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ID, other nutrient indicators and diseases were not assessed directly, and
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testing for hemoglobinopathies was not conducted because these would have
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required venous blood and significantly increased costs. However, studies

have shown that the prevalence of hemoglobinopathies is low (0.14–0.36%) in

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39,40
China . Secondly, the study sample did not include all age groups of
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children and adolescents because of limited testing capacity and economic

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reasons. Determination of Hb was implemented only in the four age groups

aged 7, 9, 12, and 14 years, preventing us from observing the complete picture

of age characteristics of Hb. Thirdly, the absence of detailed information

concerning family economic conditions, living environments, dietary patterns

and nutritional status at the individual level also limited our study.

Conflict of interest

There are no conflicts of interest on behalf of any of the authors.

Acknowledgments
 This study was supported by the medical and health program of Shandong,

China (2014WS0376). Surveys on students’ constitution and health are

conducted under the auspices of the department of education in Shandong

Province, China. We thank all the team members and all participants. Special

thanks to Mr. B Yu for providing access to the survey data.

Authorship: Ying-xiu Zhang designed the study, performed data analysis and

drafted the manuscript; Jian Chen and Xiao-hui Liu helped with data collection

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and gave instructions on data analysis and drafting manuscript. All authors

read and approved the final manuscript. -p

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39. Lin M, Wang Q, Zheng L, Huang Y, Lin F, Lin CP, et al. Prevalence and
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molecular characterization of abnormal hemoglobin in eastern

Guangdong of southern China. Clin Genet 2012; 81:165–71.

40. Lin M, Han ZJ, Wang Q, Zheng L, Wang Y, Yang H, et al. Molecular

epidemiological survey of hemoglobinopathies in the Wuxi region of

Jiangsu Province, eastern China. Hemoglobin 2013; 37:454–66.

Figure 1 Prevalence of anemia among children across different percentile

values of BMI (a) and WC (b).
Figure 2 Prevalence of anemia among children categorized by WHtR.

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Table 1. Mean values of Hb concentration and the prevalence of anemia.

Boys Girls
Age/years
n Hb (g/L) Anemia (95% CI) n Hb (g/L) Anemia (95% CI)

7 2593 134.29±11.76 3.93 (3.18－4.68) 2587 132.60±11.57* 4.29 (3.51－5.07)

9 2479 135.08±12.74 4.24 (3.45－5.03) 2569 133.38±12.54* 4.59 (3.78－5.40)

12 2538 138.34±12.69 5.04 (4.19－5.89) 2508 134.24±11.85* 8.25 (7.17－9.33)*

14 2456 145.22±13.56 2.73 (2.09－3.37) 2442 133.73±12.16* 9.79 (8.61－10.97)*

Total 10066 138.17±13.39 3.99 (3.61－4.37) 10106 133.48±12.05* 6.68 (6.19－7.17)*

Data presented as mean±SD or percentage. Gender difference *P﹤0.01.

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Table 2. Distribution of BMI categories based on the IOTF cut-offs

Boys Girls
BMI categories
(n=10066) (n=10106)

Thinness grade 3 0.47 (0.34－0.60) 0.59 (0.44－0.74)

Thinness grade 2 0.89 (0.71－1.07) 1.83 (1.57－2.09)*

Thinness grade 1 5.42 (4.98－5.86) 8.75 (8.20－9.30)*

Thinness grade 1-3 6.78 (6.29－7.27) 11.17 (10.56－11.78)*

Normal weight 63.66 (62.72－64.60) 69.37 (68.47－70.27)*

Overweight 19.61 (18.83－20.39) 14.96 (14.26－15.66)*

Obesity grade 1 7.49 (6.98－8.00) 3.41 (3.06－3.76)*

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Obesity grade 2 1.83 (1.57－2.09) 0.82 (0.64－1.00)*

Obesity grade 3 0.63 (0.48－0.78) 0.26 (0.16－0.36)*

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Obesity grade 1-3 9.95 (9.37－10.53) 4.49 (4.09－4.89)*

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Data presented as percentage (95% CI). Gender difference *P﹤0.01.
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Table 3. Prevalence of anemia in different subgroups categorized by the severity of thinness and obesity.

Thinness Obesity

Groups Boys Girls Boys Girls

n Anemia n Anemia n Anemia n Anemia

Grade 1 546 4.58 (2.83-6.33) 884 6.79 (5.13-8.45) 754 2.65 (1.50-3.80) 345 5.22 (2.87-7.57)

Grade 2-3 137 10.22 (5.15-15.29)* 245 11.84 (7.79-15.89)* 247 5.67 (2.79-8.55)* 109 11.93 (5.84-18.02)*

Data presented as percentage (95% CI). *P<0.05 compared with grade 1 group.

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