
==== Front
PLOS Glob Public Health
PLOS Glob Public Health
plos
PLOS Global Public Health
2767-3375
Public Library of Science San Francisco, CA USA

10.1371/journal.pgph.0003684
PGPH-D-24-00501
Research Article
People and Places
Population Groupings
Age Groups
Children
Adolescents
People and Places
Population Groupings
Families
Children
Adolescents
Medicine and Health Sciences
Hematology
Anemia
Medicine and Health Sciences
Hematology
Anemia
Iron Deficiency Anemia
Biology and Life Sciences
Nutrition
Diet
Medicine and Health Sciences
Nutrition
Diet
Social Sciences
Sociology
Education
Schools
Biology and Life Sciences
Nutrition
Diet
Food
Medicine and Health Sciences
Nutrition
Diet
Food
Medicine and Health Sciences
Epidemiology
Medical Risk Factors
People and Places
Geographical Locations
Asia
Nepal
Prevalence of anemia and its associated factors among school-going adolescent girls in schools of Dhankuta municipality, Nepal
Prevalence of anemia and its associated factors
https://orcid.org/0009-0009-2599-7912
Ghimire Milan Conceptualization Data curation Formal analysis Methodology Project administration Resources Software Validation Writing – original draft 1 *
https://orcid.org/0009-0004-1541-780X
Bhandari Sheetal Conceptualization Data curation Formal analysis Investigation Methodology Validation Writing – review & editing 1
Rajbanshi Manish Conceptualization Data curation Formal analysis Methodology Validation Writing – review & editing 2
1 B.P. Koirala Institute of Health Sciences, Dharan, Nepal
2 Central Department of Public Health, Institute of Medicine, Tribhuvan University, Kathmandu, Nepal
Chaudhuri Sirshendu Editor
Indian Institute of Public Health Hyderabad, INDIA
The authors have declared that no competing interests exist.

* E-mail: ghmilan7@gmail.com
17 9 2024
2024
4 9 e00036848 3 2024
15 8 2024
© 2024 Ghimire et al
2024
Ghimire et al
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Adolescent girls are more vulnerable to anemia, especially in low and middle-income countries like Nepal. It is due to early marriage and pregnancy, rapid physical growth, low body weight, economic disparities, heavy menstrual bleeding, and inadequate iron diet. This study aimed to determine the prevalence of anemia and its associated factors among school-going adolescent girls. A cross-sectional study was conducted among 405 adolescent girls using a stratified random sampling technique from both public and private schools. A statistical analysis was performed using IBM Statistical Package for Social Sciences (SPSS) version 25 software. The frequencies, percentages, mean, and standard deviation were used to describe the characteristics of the participants. Binary logistic regression was performed for multivariable analysis. All the tests were performed at a 95% Confidence Interval (CI) and p-value of <0.05. The mean (± SD) age of the participants was 14.2 ± 1.2 years. The majority of the participants (64.7%) were from government schools. Around 18% (95% CI: 13.8, 21.2) of the participants were anemic in the study. Poor knowledge of anemia (AOR = 3.3, CI: 1.0, 11.1), incomplete iron and folic acid intake (AOR = 26.8, CI: 8.3, 86.4), and absence of dietary diversity (AOR = 2.5, CI: 1.1, 9.2) were significantly associated with the higher prevalence of anemia among the adolescent girls. To reduce the risk of anemia among adolescent girls, a comprehensive strategy involving a school health intervention package on anemia, IFA supplements, and deworming program should be promoted. Besides, community-focused awareness programs should be strengthened to increase dietary diversity and improve awareness of anemia in the community.

The authors received no specific funding for this work. Data AvailabilityData is uploaded as supplementary information.
Data Availability

Data is uploaded as supplementary information.
==== Body
pmcIntroduction

Anemia is the condition of low hemoglobin (Hb) level in red blood cells and is caused by iron deficiency that results in oxygen-deprived blood, red blood cells, and low oxygen-carrying capacity to the body’s cells [1]. Adolescent girls are more vulnerable to anemia, mainly due to iron deficiency and other contributing factors such as infections, infestations, genetic disorders, early marriage, adolescent pregnancy, rapid growth, low body weight, economic disparities, heavy menstrual bleeding, and inadequate iron intake in the diet [2–4].

Anemia in adolescent girls can detrimentally affect their physical and mental development, affecting education and increasing school drop-out rates. It impairs cognitive development, learning ability, and productivity, increasing infection risks and reducing physical fitness [5–10]. In pregnant adolescents, anemia can result in adverse outcomes such as premature birth, low birth weight, stillbirth, and maternal death.

Globally, the prevalence of anemia is 6% in developed countries and significantly higher in developing countries i.e., 26% [11,12]. Anemia among adolescents is a threat to low-and middle-income countries (LMICs) countries like Nepal and is becoming a significant public health concern [3]. In South Asia, more than half (55%) of adolescent girls suffer from anemia while only 40% of these girls are getting the right amount of nutrients they need through their diet [13].

In Nepal, two of every ten (i.e. 21%) non-pregnant girls aged 10 to 19 years have anemia, Among them, 14% have mild anemia, and 6% have moderate anemia, according to a national survey [8]. The government of Nepal (GoN) has been striving to curve the high burden of anemia through the implementation of anemia control programs such as iron and folic acid supplementation, deworming, and school-based intervention packages including regular screening and treatment of anemic targeting adolescent girls [14–16]. Despite these efforts, the prevalence of anemia among adolescent girls remains high, especially in rural areas of Nepal [9].

It is crucial to address the factors that contributing to anemia among adolescent girls to prevent future maternal and child mortality and morbidity outcomes [17]. Sustainable Development Goal 2.2 (SDG) aims to end all type of malnutrition by 2030, emphasizing nutrition for children, adolescent girls, pregnant/lactating women, and seniors, intersecting with SDG-3 that focus on improved health through adequate and nutritious food [18]. Several studies highlighted that the school-based interventional packages are cost-effective in reducing the prevalence of anemia and increasing the quality of life among adolescents [19–24]. Similarly, these studies revealed that fortifying or supplementing with iron and micronutrients effectively reduces the risk of anemia and enhances hemoglobin levels in children and adolescents. Therefore, this study aimed to determine the prevalence of anemia and its associated factors among school-going adolescent girls in Dhankuta municipality of Nepal. Our study findings can assist decision-makers in choosing the appropriate interventions to tackle anemia in these age groups.

Materials and methods

Study design and setting

A cross-sectional study was conducted in Dhankuta municipality from June to October of 2023. Dhankuta municipality is located in the Dhankuta district of the Koshi Province, which is the eastern hilly region of Nepal. There was a total of 19 secondary schools in this municipality, with the number of 1870 adolescent girls (10–19 years) enrolled. Reproductive health indicators in this area were low [19]. Prior to this study, no surveys were conducted related to anemia among adolescent girls in this area.

Study population

This study included adolescent girls who were between 10–19 years of age and enrolled in selected public and private schools of Dhankuta Municipality. Participants with disabilities related to hearing, mental, speech problems, drop-out students, absentee students, and pregnant adolescents were excluded from the study.

Sample size and technique

The sample size was calculated using the single population proportion formula n = Z2p q/d2 [25]. The proportion (37.8%) of adolescent girls having anemia was taken from a similar study conducted by Binaya et.al, 2018 [26]. Assuming 95% confidence interval (CI), 5% allowable error, and 10% non-response rate, the final sample size was 405 for this study.

A total of 19 secondary schools fulfilled the study criteria of 10–19 years adolescent girls in Dhankuta Municipality. Among them, 9 schools (5 public and 4 private) were selected using a stratified random sampling technique. The public and private schools were considered as strata for selecting schools. The public and private schools consisted of 65% and 35% of the total students, respectively. Then, the required number of students from the public (n = 262) and private (n = 143) schools was calculated based on population proportionate sampling technique. A systematic random sampling technique was used to select participants. A first participant was randomly taken using the lottery method and every 4th participant was taken in this study.

Variables and operational definition

Adolescent girls

It is defined as the participants age between 10 and 19 years [27].

Types of anemia

It was classified into normal, mild, moderate and severe on the basis of hemoglobin level in the blood [21] (Table 1).

10.1371/journal.pgph.0003684.t001 Table 1 Type of anemia based on hemoglobin level in the blood.

Type of anemia	10–11 years 	12–19 years	
	g/dl	g/dl	
Normal	>10.4	>11.9	
Mild	10.0–10.4	10.0–11.9	
Moderate	7.0–9.9	7.0–9.9	
Severe	<7.0	<7.0	
Source: The World Health Organization

Table 1 describes the age-based classification of anemia based on the hemoglobin level in the blood.

Hemoglobin concentrations were adjusted for smokers (-0.3 g/dl) and those at elevations above 1000 meters (-0.2 g/dl) in this study [21].

Age

It was measured in completed years during the time of the study. Adolescents of age group “10–14” years as early adolescents and “15–19” years as late adolescents.

Ethnicity

The ‘advantaged’ group referred to Brahmin/Chhetri, while the ‘disadvantaged’ group referred to Janajati, Madhesi, Muslim, and Dalit.

Religion It was classified into Hindu, and non-Hindu (Kirat, Buddhist, Christian and Muslim).

Marital status

It was categorized into married and unmarried.

Education of mothers

It was grouped into illiterate (no education), primary level (below grade 8), secondary level (grade 8 to 12) and higher secondary level (higher than grade 12).

Normal menstrual cycle

It refers to the menstrual period of every 21–35 days [26].

Normal bleeding during menstruation

It was considered normal if it lasted for 2–5 days [26].

Pattern of skipping meal

If participants had skipped at least any of the meals (snacks/breakfast/lunch/dinner) for seven consecutive days [26].

Current smoker

If the participant had smoked within one month.

Current alcohol consumption

If the participant had taken alcohol within one month.

Barefoot

If participants did not wear shoes/slippers while working in the field.

Dietary diversity

Dietary diversity was assessed by the frequency (daily,7–10 times,3–6 times,1–2 times, not at all) of consuming eight food items i.e. fish, egg, milk, fruits, pulse, vegetable, cereals over the past seven days. Those answering at least once a week were coded as 1, and those giving the response of not taking were given the code 0, to each of the 8 items. The participant’s food score was computed as the sum of the responses to these questions, ranging from a lower of 0 to 8. A score above 5 was categorized as the presence of food diversity and a score between 0 to 4 was considered as the absence of food diversity [26,28].

Knowledge on “definition of anemia”

Participants were considered to have good knowledge if they correctly answered (Yes/No) “anemia is a decrease in the amount of Hb in the blood” [1].

Knowledge on signs/symptoms of anemia

Participants were considered to have good knowledge if they correctly answered (Yes/No) at least three relevant symptoms out of the mentioned symptoms.

Knowledge on preventive dietary foods of anemia

Participants were considered to have good knowledge if they correctly answered at least three iron-rich foods.

Body mass index (BMI)

It was categorized into underweight (<18.5 kg/m2), normal (18.5–24.9 kg/m2), and overweight (≥25 kg/m2) [26,29].

Stool RE (Routine Examination) /ME (Microscopic Examination)

Stool RE/ME evaluates stool for physical, chemical, and microscopic abnormalities, aiding in diagnosing infections or digestive disorders [30].

Study tools

The study tool was adapted from the national survey on anemia among adolescent girls conducted in Nepal [20].

Participants’ height was measured with a stadiometer, and weight with a digital scale (SECA), recommended by UNICEF [31]. Blood and stool specimens were analyzed using a WHO recommended auto analyzer and microscope [9,30,32].

The pretesting of the tool was done among 10% of the similar population. Both Nepali and English translated language questionnaire was used to collect the information. A Cronbach alpha coefficient of 0.81 was obtained during the pretesting of study tool. Height and weight assessments were done two times per participants, and the average values were considered in this study [29].

Data collection and techniques

A face-to-face interview using a semi-structured questionnaire was used to collect data from the participants. Each interview took around 30 minutes.

The principal investigator and research assistants were involved during the data collection. Research assistants were provided with orientation regarding the study project, data collection procedure, and handling of the instruments for data collection. Lab technicians and technologist were responsible for collecting and testing of blood and stool samples. Complete Blood Counts were assessed through a fully automated analyzer, and stool examinations were conducted using a microscope [9,30,32].

Height, weight, and blood samples of the participants were taken after completion of the interview. Stool samples were collected among the participants with hemoglobin levels <12 g/dl following the next day of data collection.

Anemic participants were provided with IFA supplementation as per the Government of Nepal (GoN) protocol. Anemia-focused health education programs were conducted in schools in collaboration with the school health teacher and the Health Section of Dhankuta Municipality.

Data management and analysis

The collected data were entered, recorded, compiled, filtered, and cross-checked in Microsoft Excel and then exported into IBM Statistical Package for Social Sciences (SPSS) Version 25 for analysis. The descriptive results are presented in the form of frequency, percentage, mean, and standard deviation. The variables with p-value < 0.2 were included for the multivariable analysis to determine factors associated with anemia. All the tests were set at 95% Confidence Interval (CI) and p-value < 0.05 for statistically significant.

Ethical approval

Ethical approval was obtained from the Institutional Review Committee (IRC) of B.P. Koirala Institute of Health Sciences (Reference number: 659/2023). A letter of support was obtained from Dhankuta municipality and the selected school authorities.

The purpose of the study was explained to participants and their parents. Written consent was taken from the parents/caregivers. Both verbal and written informed consent was obtained from the participants. Additionally, a written assent form was obtained from the participants who were below 18 years. Participant’s information was kept confidential, and anonymity was maintained. Laboratory test reports were made available to every participant.

Results

Social and demographical characteristics of participants

This study involved a total of 405 participants. The mean ± SD age was 14.2± 1.2 years. The majority of the participants were Janajati (63%) in ethnicity and Hindu (77.5%) in religion. Nearly two-thirds of the participants were from the government schools (64.7%). Around 60% of the participants belonged to nuclear families. Most of the participant’s mothers had completed secondary education (43.4%). Meanwhile, about 60% were involved in agriculture as their main occupation (Table 2).

10.1371/journal.pgph.0003684.t002 Table 2 Social and demographical characteristics of participants.

Characteristics	Number (n)	Percentage (%)	
Age (Mean ± SD)	14.2 ± 1.2		
10–14	220	54.3	
15–19	185	45.7	
Ethnicity			
Janajati	255	63	
Brahmin/ Chhetri	119	29.3	
Dalit	20	5.0	
Madhesi	9	2.2	
Muslim	2	0.5	
Religion			
Hindu	314	77.5	
Kirat	61	15.0	
Buddhist	16	4.0	
Christian	12	3.0	
Muslim	2	0.5	
Marital status			
Unmarried	404	99.8	
Married	1	0.2	
Grade		
8	100	24.7	
9	156	38.5	
10	149	36.8	
Type of school			
Government school	262	64.7	
Private school	143	35.3	
Type of family			
Nuclear	242	59.8	
Joint/extended	163	40.2	
Size of family			
<5 member	202	49.9	
≥5 member	203	50.1	
Education of mother (n = 401)			
Illiterate	50	12.4	
Secondary level	174	43.4	
Primary level	121	30.2	
Higher than secondary level	56	14.0	
Occupation of mother (n = 401)			
Agriculture	244	60.8	
Business	80	20.0	
Government worker	46	11.5	
Foreign employee	17	4.2	
NGO/private	9	2.3	
Daily labor	5	1.2	
Occupation of father (n = 395)			
Business	108	27.3	
Agriculture	96	24.3	
Foreign employee	91	23.0	
Government worker/officer	76	19.2	
Daily labor	14	3.6	
NGO/private	10	2.6	
This table summarizes the demographic characteristics of the participants who participated in the study (Table 2).

Status of anemia among participants

This study found that 17.5% (95% CI: 13.8, 21.2) of participants were anemic. Among them, 83.1% and 16.9% were mild and moderate anemia, respectively. The range of hemoglobin level was 8.1 g/dl to 15.1 g/dl (Fig 1).

10.1371/journal.pgph.0003684.g001 Fig 1 Prevalence of anemia among school going adolescents girls.

Reproductive health and behavioral-related characteristics

Most of the participants (95.3%) experienced menarche and 67.4% of participants had a normal menstrual cycle. Around one-third (67.1%) of the participants had normal bleeding during menstruation.

The majority (91.9%) of participants were non-vegetarians. Only 4.2% of participants had a history of chronic illness. Only 23.7% of participants reported a history of worm infestations within 2 years. While 41.2% of participants reported deworming within 6 months. Most of them, 85% scored the presence of food diversity. Half of the participants (55.6%) had taken iron and folic acid intake. The study showed that 13.1% 27.4%, and 59.5% had overweight, underweight, and normal BMI, respectively (Table 3).

10.1371/journal.pgph.0003684.t003 Table 3 Reproductive health, behavioral, and BMI characteristics.

Characteristics	Number (n)	Percentage (%)	
Reproductive health			
Status of menarche			
Yes	386	95.3	
No	19	4.7	
Normal menstrual cycle (n = 386)			
Yes	260	67.4	
No	126	32.6	
Normal bleeding during menstruation (n = 386)			
Yes	259	67.1	
No	127	32.9	
Behavioral characteristics			
Drinking tea or coffee			
Yes	181	44.7	
No	224	55.3	
Pattern of skipping of meal			
No	252	62.2	
Yes	153	37.8	
Current smoker			
No	401	99.0	
Yes	4	1.0	
Current alcohol consumption			
No	384	94.8	
Yes	21	5.2	
Taking fresh lemon/pickles with food regularly			
No	12	3.0	
Yes	393	97.0	
Type of diet			
Vegetarian	33	8.1	
Non-vegetarian	372	91.9	
Times of junk food consumption (in a week)			
Daily	177	43.4	
1–6 times	197	48.3	
7–10 times	34	8.3	
History of chronic illness			
Yes	17	4.2	
No	388	95.8	
Main source of drinking water			
Tap water	284	70.1	
Surface water	121	29.9	
Purification of drinking water			
Yes	352	86.9	
No	53	13.1	
Frequency of washing hand (per day)			
≥ 3 times	213	52.6	
< 3 times	192	47.4	
Materials used for handwashing			
Soap and water	400	98.8	
Only water	5	1.2	
Using slippers/shoes while going outside			
Yes	358	88.4	
No	47	11.6	
History of worm infestation within 2 years			
Yes	96	23.7	
No	309	76.3	
Deworming within 6 months			
No	238	58.8	
Yes	167	41.2	
Food diversity (Mean± SD)	6.1 ± 1.3		
Present	343	85.0	
Absent	62	15.0	
Taking iron and folic acid			
Yes	225	55.6	
No	180	44.4	
Duration of iron and folic acid daily			
≥ 26 weeks	175	77.8	
<26 week	50	22.2	
BMI			
Normal	241	59.5	
Underweight	111	27.4	
Overweight	53	13.1	
Stool RE/ ME (n = 71)			
Negative	65	91.5	
Presence of Entamoeba histolytica	6	8.5	
This table describes the reproductive health and behavioral-related characteristics of the participants in the study (Table 3).

Dietary diversity pattern among participants

The majority of participants consumed meat, fruit, and cereals 1–2 times a day, 66.4% of participants consumed meat 1–2 times in the past week, while 69.5% did not consume fish (Table 4).

10.1371/journal.pgph.0003684.t004 Table 4 Dietary diversity pattern in the last seven days.

Dietary Pattern	Meat
(n = 372)	Fish
(n = 371)	Egg
(n = 389)	Milk
(n = 405)	Fruit
(n = 405)	Pulse
(n = 405)	Vegetable(n = 405)	Cereals
(n = 405)	
	n (%)	n (%)	n (%)	n (%)	n (%)	n (%)	n (%)	n (%)	
Daily	12
(3.2)	0 (0)	12
(3.1)	100
(24.7)	81
(20.0)	195
(48.1)	142
(35.1)	354
(87.4)	
At least
one time	302 (81.2)	113 (30.5)	284
(73)	227
(56)	294 (72.6)	173
(42.8)	247 (60.9)	48
(11.8)	
Not at all	58
(15.6)	258
(69.5)	93
(23.9)	78
(19.3)	30
(7.4)	37
(9.1)	16
(4.0)	3
(0.7)	
This table summarizes dietary diversity pattern among participants in the study. It includes consumption pattern of meat, fish, egg, milk, fruit, pulse, vegetable, and cereals within last seven days (Table 4).

Knowledge of anemia among the participants

More than half i.e., 54% correctly identified the definition of anemia, 31% correctly reported signs/symptoms of anemia, and 24% were correctly defined the diets that prevents anemia.

Factors association with anemia

Age, menarche status, menstrual cycle, type of diet, history of worm infestation, deworming and BMI were not associated with the prevalence of anemia in this study (Table 5).

10.1371/journal.pgph.0003684.t005 Table 5 Factors associated with anemia among the participants.

Characteristics	Status of anemia	p-value	Odds Ratio (95% CI)	
	Anemia
n (%)	No anemia
n (%)			
Age					
10–14	33 (15)	187 (85.0)			
15–19	38 (20.5)	147 (79.5)	0.144	1.4 (0.8,2.4)	
Status of menarche					
No	1(5.3)	18 (94.7)			
Yes	70 (18.1)	316 (81.9)	0.219	3.9 (0.5,30.3)	
Normal menstrual cycle (n = 386)					
Yes	47(18.1)	213 (81.9)			
No	23(18.3)	103 (81.7)	0.966	1.0 (0.5,1.7)	
Type of diet					
Non vegetarian	62 (16.7)	310 (83.3)			
Vegetarian	9 (27.3)	24 (72.7)	0.125	1.8 (0.8,4.2)	
Taking fresh lemon/pickles regularly with food					
Yes	68 (17.3)	325 (82.7)			
No	3 (25.0)	9 (75.0)	0.449	1.5 (0.4,6.0)	
Using slippers/shoes while going outside					
Yes	64(17.9)	294(82.1)			
No	7(14.9)	40(85.1)	0.613	0.8 (0.3,1.8)	
History of worm infestation within 2 years					
No	50 (16.2)	259 (83.8)	0.200		
Yes	21 (21.9)	75 (78.1)		1.4 (0.8,2.5)	
Deworming within 6 months					
Yes	23 (13.8)	144 (86.2)			
No	48 (20.2)	190 (79.8)	0.960	1.5 (0.9,2.7)	
BMI					
Normal	40 (16.6)	201 (83.4)			
Underweight	23 (20.7)	88 (79.3)	0.789	1.1 (0.4,2.5)	
Overweight	8 (15.1)	45 (84.9)	0.349	0.7 (0.4,1.3)	
This table describes the factors associated with the status of anemia among participants. It includes independent variables i.e. age, status of menarche, menstrual cycle, type of diet, history of worm infestation, intake of deworming, and BMI (Table 5).

Multivariate logistic regression for factors associated with anemia among participants

The odds of having anemia was 3.3 times higher among the participants who did not correctly identify the definition of anemia (AOR = 3.3, CI: 1.0, 11.1). Similarly, participants who took IFA supplementation < 26 weeks had 26.9 times higher odds of having anemia (AOR = 26.9, CI: 8.3, 86.4). The participants not having food diversity had higher odds of having anemia (AOR = 2.5, CI: 1.1, 9.2) (Table 6).

10.1371/journal.pgph.0003684.t006 Table 6 Multivariate logistic regression for factors associated with anemia.

Characteristics
	Status of anemia	p-value	COR (95%CI)	p-value	AOR
(95%CI)	
	Anemia
n (%)	No anemia n (%)					
Pattern of skipping of meal							
No	38 (15.1)	214 (84.9)		Ref		Ref	
Yes	33 (21.6)	120 (78.8)	0.096	1.5 (0.9, 2.6)	0.282	1.7 (0.6, 5.0)	
History of chronic illness							
No	65 (16.8)	323 (83.2)		Ref		Ref	
Yes	6 (35.3)	11 (64.7)	0.049*	2.7 (0.9, 7.5)	0.736	0.6 (0.0, 6.7)	
Knowledge on definition of anemia	
						
Correct	16 (7.3)	204 (92.7)		Ref		Ref	
Incorrect	55 (29.7)	130 (70.3)	0.0001*	5.3 (2.9, 9.8)	0.046*	3.3 (1.0,11.1)	
Knowledge of symptoms of anemia							
Correct	10 (7.9)	117 (92.1)		Ref		Ref	
Incorrect	61 (21.9)	217 (78.1)	0.001*	3.2 (1.6, 6.6)	0.202	2.5 (0.6, 10.6)	
Knowledge of preventive food for anemia							
Correct	9 (9.3)	88 (90.7)		Ref		Ref	
Incorrect	62 (20.1)	246 (79.9)	0.014*	2.4 (1.1, 5.1)	0.290	0.4 (0.1, 1.9)	
Duration of taking iron and folic acid daily							
≥ 26 weeks	11 (6.3)	164 (93.7)		Ref		Ref	
< 26 weeks	26 (52.0)	24 (48)	0.0001*	16.2 (7.1, 36.8)	0.0001*	26.9 (8.3, 86.4)	
Junk food consumption (per week)							
Not daily	17 (8.8)	177 (91.2)		Ref		Ref	
Daily	54 (25.6)	157 (74.4)	0.0001*	3.5 (1.9, 6.4)	0.062	3.0 (0.9, 10.1)	
Dietary diversity							
Present	42 (12.2)	301 (87.8)		Ref		Ref	
Absent	29 (48.8)	33 (53.2)	0.0001*	6.3 (3.4, 11.4)	0.010*	2.5 (1.1, 9.2)	
Ref.: Reference group, COR: Crude Odds Ratio, AOR: Adjusted Odds Ratio

*Statistically significant at the p-value <0.05.

A summary of factors associated with anemia among participants in the multivariate logistic regression analysis (Table 6).

Discussion

Anemia among adolescents is a threat to low and middle-income countries like Nepal and becoming a significant public health concern, globally [3]. The objective of the study was to determine the prevalence of anemia and its associated factors among school-going adolescent girls.

This study found around 18% of the participants were anemic. Among them, 83.1% were mild and 16.9% were moderate. This finding is aligned with previous studies conducted among adolescent girls in Nepal i.e., 20% [9], India i.e., 20% [33], and Thailand i.e., 17% [3]. In contrast to this finding, a study conducted among developed countries such as Kuwait i.e., 10.9% [34], and Turkey i.e., 8.3% [35] reported a lower prevalence of anemia among adolescent girls. The prevalence in developed countries might be due to lower than in developing countries due to better nutrition, higher health literacy, improved healthy lifestyles, and socio-economic status [4]. Another reason is due to access to healthcare services, which results increase in detection and diagnosis of anemia [36]. This study showed a lower prevalence of anemia compared to previous studies, because government of Nepal have been conducting a biannual Iron Folic Acid supplementation (IFA) program routinely.

Additionally, iron-folic acid supplements and counseling on dietary diversity have been provided to adolescents through the school health program, aiming to prevent and control anemia.

The higher prevalence of anemia was reported among late adolescents compared to early adolescents. This finding is supported by the previous studies conducted in Nepal [26], India [37], and Kenya [38]. It is because of the onset of menstrual cycle among late adolescent girls which prompts physiological blood loss, inadequate dietary intake of iron to meet the increased nutritional demand [33]. Since the trend of early marriage and child bearing is higher among late adolescent in developing countries like Nepal [26]. This finding is supported by previous studies that reported higher prevalence of anemia among late adolescents [4,39].

This study found that the prevalence of anemia was higher among adolescent girls who had menarche and excessive blood loss during menstruation. Similar patterns were observed among study conducted in Nepal [20], India [37], Ethiopia [40] and Iran [41]. It is due to blood loss which is one of the major cause of anemia [42]. Adolescent girls who were vegetarian had 1.8 times higher odds to the risk of anemia than non-vegetarian adolescent girls. This findings is coherent with the similar studies conducted in Nepal [20], Kenya [43] and India [44]. It is because vegetarians and vegans are deficient in Vitamin B12 that results in low absorption of iron causing anemia [45].

Adolescent girls working without using slippers/shoes and having a history of hookworm infestation were at greater risk of anemia. This finding is comparable with the similar study conducted in South-Western Nepal [46]. It is due to hookworm infestation which can cause intestinal inflammation and damage, leading to poor absorption of iron, exacerbating the risk of anemia [26]. Similarly, it was reported that a lower prevalence of anemia among adolescent girls who were provided with deworming medication in the past 6 months. This finding is comparable with the similar studies conducted in the eastern part of Nepal, and Baglung district of Nepal [47,48]. Deworming reduces anemia by treating parasitic infections in gut and promote iron absorption [49].

The odds of having anemia was 1.08 times higher among adolescent girls who were underweight which is coherent with the other studies conducted in Nepal [47,48], India [50], and Lao PDR [51]. It may be due to factors such as poor nutrition intake and potentially compromised immune function, leading to increased vulnerability to infections [52].

This study showed that the prevalence of anemia was higher among adolescent girls who skipped their meals. Similar findings were reported from the study conducted in Ghana [53], Pakistan [54] and Indonesia [55]. It is due to low production of red blood cells resulted by low intake of nutrients such as iron among individuals who skip their meal [55].

Adolescent girls who had a history of chronic illness were at greater risk of anemia. This finding is consistent with a study conducted in the Mid-Western Terai Region of Nepal [20]. It may be due to factors such as underlying inflammation, impaired absorption of nutrients, medication side effects, and decreased production of red blood cells contribute to the risk of anemia [1].

A higher prevalence of anemia was found among adolescent girls with poor knowledge of anemia. It is because low health literacy leads to poor help-seeking behavior, delays in diagnosis of anemia, lack of awareness regarding preventive programs such as deworming and iron-folic acid supplementation, and poor preventive practices like habit of working with barefoot, and inadequate dietary habits, all these factors contribute to the risk of anemia [20,40,56].

Adolescent girls who took IFA supplements for at least 26 weeks had a lower prevalence of anemia compared to their counterparts. Similar findings were reported in the study conducted in Nepal [57], India [58], Kenya [43], and Vietnam [49]. This findings highlighted the effectiveness of IFA supplementation program to lower the risk of anemia among adolescents [9].

Consistent with other studies conducted in India [59], Indonesia [60], and Pakistan [61]. This study showed adolescent girls who consume junk food daily were at higher risk of anemia [59]. Junk foods are deficient in essential nutrients like vitamin C which results in low absorption of iron [61]. Additionally, high levels of processed sugar and unhealthy fats in junk food can interfere with nutrient absorption in the digestive tract, further reducing the body’s ability to absorb iron and other vital nutrients [61].

Dietary diversity plays a significant role in lowering the risk of anemia among adolescent girls. This study showed that lower prevalence of anemia among adolescent girls who had dietary diversity. These findings are aligned with a study conducted in Nepal [20], Ethiopia [52], Indonesia [55], and Nigeria [62]. Consuming a diverse range of foods increases the likelihood of obtaining an adequate intake of essential nutrients including iron, folate, vitamin B12, vitamin C, and other micronutrients crucial for red blood cell production and function [63]. A diverse diet helps ensure balanced nutrient intake that prevents the risk of anemia [64].

Strengths and limitations

This study was conducted in rural areas including both public and private schools. The study investigated various characteristics such as socio-demographic, reproductive, dietary habits, behavioral, anthropometric measurements and biochemical tests that have a significant influence on anemia among adolescents.

There may be a chance of recall bias regarding dietary diversity, history of deworming, and junk food within 7 days. This study failed to consider a design effect while calculating sample size. Important factors like pregnancy, cultural and malarial infection were not taken in the study that could have a significant impact on the prevalence of anemia. Since the study is conducted in Dhankuta municipality i.e. hilly region, findings cannot be generalized to the adolescents residing in different geographical regions.

Conclusion

This study revealed that 17.5% of adolescent girls were anemic. Higher prevalence of anemia were observed among older adolescent girls, those with limited knowledge about anemia, incomplete intake of IFA supplements, and lack of dietary diversity. These findings highlight the need for targeted interventions addressing adolescent girls’ nutritional knowledge, IFA supplementation, and dietary practices. Priorities should include school-based health programs, nutritional education, and promotion of dietary diversity for the prevention and control of anemia among adolescents.

Supporting information

S1 File Participant information sheet.

(DOCX)

S1 Questionnaire (DOCX)

S1 Data (XLSX)

We would like to express our gratitude to School of Public Health and Community Medicine, BPKIHS, Nepal. Also, we are thankful towards Dhankuta district hospital, Dhankuta municipality. We are also thankful to all the participants for their time and efforts.
==== Refs
References

1 WHO. Technical Handbook on Anaemia in Adolescents. 2018;1–14. Available from: https://iris.who.int/handle/10665/205656.
2 Sexual, reproductive, maternal, newborn, child and adolescent health policy survey, 2018–2019: report. Geneva: World Health Organization; 2020. License: CC BY-NC-SA 3.0 IGO.
3 Siva PM , Sobha A , Manjula VD . Prevalence of Anaemia and Its Associated Risk Factors Among Adolescent Girls of Central Kerala. J Clin Diagn Res. 2016 Nov;10 (11 ):LC19–LC23. doi: 10.7860/JCDR/2016/20939.8938 Epub 2016 Nov 1. ; PMCID: PMC5198362.28050409
4 Wiafe MA , Ayenu J , Eli-Cophie D . A Review of the Risk Factors for Iron Deficiency Anaemia among Adolescents in Developing Countries. Anemia. 2023 Jan 3;2023 : 6406286. Available from: doi: 10.1155/2023/6406286 ; PMCID: PMC9831712.36636253
5 Srivastava S , Kumar P , Paul R , Debnath P . Effect of change in individual and household level characteristics on anemia prevalence among adolescent boys and girls in India. BMC Public Health. 2022 Aug 3;22 (10 ):1478. doi: 10.1186/s12889-022-13863-w ; PMCID: PMC9351076.35922790
6 Kaur P , Sarin J , Anemia among Adolescent girls in India: A review of literature, ijmhs, vol. 10 , no. 05 , pp. 784–789, May 2020. Available from: 10.15520/ijmhs.v10i03.289.
7 Khanal A , Paudel R , Wagle CN , Subedee S , Pradhan PMS . Prevalence of anemia and its associated factors among adolescent girls on Weekly Iron Folic Acid supplementation (WIFAS) implemented and non-implemented schools at Tokha municipality, Kathmandu. PLOS Glob Public Health. 2024 Jan 26;4 (1 ):e0002515. doi: 10.1371/journal.pgph.0002515 ; PMCID: PMC10817172.38277373
8 Ministry of Health New ERA , UNICEF EU , USAID CDC . Nepal National Micronutrient Status Survey 2016. 2018;1–315. Available from:https://www.unicef.org/nepal/sites/unicef.org.nepal/files/2018-08/NNMSS Report 2016.pdf.
9 Ministry of Health and Population [Nepal], New ERA, and ICF. 2023. Nepal Demographic and Health Survey2022. Kathmandu, Nepal: Ministry of Health and Population [Nepal].
10 WHO. Guideline: Intermittent iron and folic acid supplementation in menstruating women. World Health Organization. 2011;1–30. ISBN: 9789241502023.
11 Prasanth R. Prevalence of Anemia in both Developing and Developed Countries around the World. World J Anemia. 2017;1 (2 ):40–3. doi: 10.5005/jp-journals-10065-0009
12 Dugdale M. Anemia Obstet Gynecol Clin North Am. 2001 Jun;28 (2 ):363–81. doi: 10.1016/s0889-8545(05)70206-0 .11430182
13 World Health Organization [WHO]. Health for the world’s adolescents. A second chance in the second decade. Available from: https://apps.who.int/adolescent/ second-decade/section2/page1/recognizing-adolescence.html.
14 Department of Health Services [2024]. Ministry of Health and Population [MoHP]: Annual Health Report 2079/80. Teku, Kathmandu, Nepal. Available from: http://www.dohs.gov.np/.
15 WFP. Annual Country Report 2022 Ethiopia. WfpOrg [Internet]. 2023; Available from: https://www.wfp.org/publications/annual-country-reports-ethiopia.
16 Weekly iron and folic acid supplementation as an anaemia-prevention strategy in women and adolescent girls: lessons learnt from implementation of programmes among non‑pregnant women of reproductive age. Geneva: World Health Organization; 2018 (WHO/NMH/NHD/18.8). Licence: CC BY-NC-SA 3.0 IGO.
17 Joshi M , Gumashta R . Weekly iron folate supplementation in adolescent girls—an effective nutritional measure for the management of iron deficiency anaemia. Glob J Health Sci. 2013 Mar 20;5 (3 ):188–94. doi: 10.5539/gjhs.v5n3p188 ; PMCID: PMC4776831.23618489
18 Advocates for International Development. This Legal Guide to the Sustainable Development Goals (SDGs). 2022; Available from: https://www.a4id.org/wp-content/uploads/2018/03/ANNEX-A.pdf.
19 Mithra P , Khatib MN , Sinha AP , Kumar N , Holla R , Unnikrishnan B et al . Interventions for Addressing Anemia Among Children and Adolescents: An Overview of Systematic Reviews. Front Pediatr. 2021 Feb 16; 8 :549549. doi: 10.3389/fped.2020.549549 ; PMCID: PMC7921152.33665173
20 B Karki K. , Thapa P. MD et al . Anemia and its Determinants among Women of Reproductive Age in Mid-Western Tarai of Nepal 2015. Nepal Heal Res Counc. 2016;. Available from: https://hdl.handle.net/20.500.14356/762.
21 World Health Organization. 2011. Hemoglobin concentrations for the diagnosis of anemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva: WHO; Accessed August 3, 2018. Available from:http://www.who.int/vmnis/indicators/haemoglobin.pdf.
22 Chaparro CM , Suchdev PS . Anemia epidemiology, pathophysiology, and etiology in low- and middle-income countries. Ann N Y Acad Sci. 2019 Aug; 1450 (1 ):15–31. doi: 10.1111/nyas.14092 Epub 2019 Apr 22. ; PMCID: PMC6697587.31008520
23 Erkan T. Adolescent nutrition. Turk Pediatr Ars. 2011;46 (SUPPL.1 ):49–53. doi: 10.4274/tpa.46.34
24 Oy S , Witjaksono F , Mustafa A , Setyobudi SI , Fahmida U . Problem Nutrients in Adolescent Girls With Anemia Versus Nonanemic Adolescent Girls and the Optimized Food-Based Recommendations to Meet Adequacy of These Nutrients in Adolescent School Girls in East Java, Indonesia. Food Nutr Bull. 2019 Sep; 40 (3 ):295–307. doi: 10.1177/0379572119851326 Epub 2019 Jul 4. .31272219
25 Cochran WG . Cochran_1977_Sampling Techniques.pdf. 1977. p. 1–428.
26 Chalise B , Aryal KK , Mehta RK , Dhimal M , Sapkota F , Mehata S et.al . Prevalence and correlates of anemia among adolescents in Nepal: Findings from a nationally representative cross-sectional survey. PLoS One. 2018 Dec 14;13 (12 ):e0208878. doi: 10.1371/journal.pone.0208878 ; PMCID: PMC6294609.30551124
27 Provisions C , Us L , Up S , Readings S . Unit 1 Introduction To Diversity. 2009;5–27. Available link: https://egyankosh.ac.in/bitstream/123456789/46064/1/Unit-1.pdf.
28 Bikila H , Ariti BT , Fite MB , Sanbata JH . Prevalence and factors associated with adequate dietary diversity among pregnant women in Nekemte town, Western Ethiopia, 2021. Front Nutr. 2023 Dec 15; 10 :1248974. doi: 10.3389/fnut.2023.1248974 ; PMCID: PMC10756138.38162525
29 Center for Disease Control and Prevention. Anthropometry procedures manual. National Health and Nutrition Examination Survey. January 2007:102 : Available from://www.cdc.gov/nchs/data/nhanes/nhanes_07_08/manual_an.pdf.
30 Alireza Abdolrasouli , and Howell Susan , 2023. 10.4 Specimen Examination, Clinical Microbiology Procedures Handbook, 5th Edition. ASM Press, Washington, DC. doi: 10.1128/9781683670438.CMPH.ch10.4
31 Atzatzev. UNICEF data. 2019 [cited 2024 Mar 5]. Recommendations for data collection, analysis and reporting on anthropometric indicators in children under 5 years of age. Available from: https://data.unicef.org/resources/data-collection-analysis-reporting-on-anthropometric-indicators-in-children-under-5/.
32 Yeo CP , Ng WY . Automation and productivity in the clinical laboratory: experience of a tertiary healthcare facility. Singapore Med J. 2018 Nov;59 (11 ):597–601. doi: 10.11622/smedj.2018136 ; PMCID: PMC6250760.30498842
33 Chauhan S , Kumar P , Marbaniang SP , Srivastava S , Patel R . Prevalence and predictors of anaemia among adolescents in Bihar and Uttar Pradesh, India. Sci Rep. 2022 May 17;12 (1 ):8197. doi: 10.1038/s41598-022-12258-6 ; PMCID: PMC9114399.35581388
34 Shaban L , Al-Taiar A , Rahman A , Al-Sabah R , Mojiminiyi O . Anemia and its associated factors among Adolescents in Kuwait. Sci Rep. 2020 Apr 3;10 (1 ):5857. doi: 10.1038/s41598-020-60816-7 ; PMCID: PMC7125127.32246050
35 Isık Balci Y , Karabulut A , Gurses D , Ethem Covut I . Prevalence and Risk Factors of Anemia among Adolescents in Denizli, Turkey. Iran J Pediatr. 2012 Mar;22 (1 ):77–81. ; PMCID: PMC3448219.23056863
36 Budhathoki L , Shrestha B , Phuyal N , Shrestha L . Prevalence of Anemia in Adolescent Girls attending Specific Schools of Kavrepalanchok, Nepal. JNMA J Nepal Med Assocation. 2021 Mar 31;59 (235 ):284–287. doi: 10.31729/jnma.6330 ; PMCID: PMC8369535.34506433
37 Bodat S , Bodat R , PV V. V. G Rathore AR . Prevalence of anemia among school going adolescent girls in rural area of Pune, Maharashtra, India. Int J Reprod Contraception, Obstet Gynecol. 2020;9 (4 ):1596. doi: 10.18203/2320-1770.ijrcog20201230
38 Nadeem M , Kaur B , Agarwal S . A study on pervasiveness and knowledge of anemia of adolescent girls. J Cardiovasc Dis Res [Internet]. 2022;13 (7):877–81. ISSN: 0975-3583,0976–2833.
39 Tiruneh FN , Tenagashaw MW , Asres DT , Cherie HA . Associations of early marriage and early childbearing with anemia among adolescent girls in Ethiopia: a multilevel analysis of nationwide survey. Arch Public Health. 2021 Jun 3;79 (1 ):91. doi: 10.1186/s13690-021-00610-7 ; PMCID: PMC8173845.34082813
40 Fentie K , Wakayo T , Gizaw G . Prevalence of Anemia and Associated Factors among Secondary School Adolescent Girls in Jimma Town, Oromia Regional State, Southwest Ethiopia. Anemia. 2020 Sep 22;2020 :5043646. doi: 10.1155/2020/5043646 ; PMCID: PMC7528150.33029396
41 Ramzi M , Haghpanah S , Malekmakan L , Cohan N , Baseri A , Alamdari A et.al . Anemia and iron deficiency in adolescent school girls in kavar urban area, southern iran. Iran Red Crescent Med J. 2011 Feb;13 (2 ):128–33. Epub 2011 Feb 1. doi: 10.1038/sj.ejcn.1602306 ; PMCID: PMC3371916.22737447
42 Sinha N , Deshmukh PR , Garg BS . Epidemiological correlates of nutritional anemia among children (6–35 months) in rural Wardha, Central India. Indian J Med Sci. 2008 Feb;62 (2 ):45–54. .18319531
43 Nelima D. Prevalence and Determinants of Anaemia among Adolescent Girls in Secondary Schools in Yala Division Siaya District, Kenya. Universal Journal of Food and Nutrition Science. 2015;3 (1 ):1–9. doi: 10.13189/ujfns.2015.030101
44 Anwar S , Deshmukh P , Garg BS . Epidemiological correlates of nutritional anemia in adolescent girls of rural wardha. Indian Journal of Community Medicine. 2006;31 .(4 ):7–19.
45 Pawlak R , Berger J , Hines I . Iron Status of Vegetarian Adults: A Review of Literature. Am J Lifestyle Med. 2016 Dec 16;12 (6 ):486–498. doi: 10.1177/1559827616682933 ; PMCID: PMC6367879.30783404
46 Dubey KR , Padmavathi P , Jayan A , Gautam N , Neupane Y , Sinha AK . Prevalence of anemia amongst adolescent females in South Western Nepal. The Pharma Innovation Journal. 2013;2 (7 ).
47 Kanodia P , Bhatta M , Singh RR , Bhatta NK , Shah GS . A study of anemia among adolescent girls in eastern part of Nepal. J Coll Med Sci. 2016;12 (1 ):19–22. 10.3126/jcmsn.v12i1.14683.
48 Hamal S , Prasad Dhungana G , Shrestha P . Global Journal of Medicine and Public Health. Prevalence of anaemia and its associated factors among school adolescent girls in Baglung municipality, Nepal. 2018;79 (5 ). Available from: https://www.gjmedph.com/Uploads/O2-Vo7No5.pdf.
49 Casey GJ , Sartori D , Horton SE , Phuc TQ , Phu LB , Thach DT et.al . Weekly iron-folic acid supplementation with regular deworming is cost-effective in preventing anaemia in women of reproductive age in Vietnam. PLoS One. 2011;6 (9 ):e23723. doi: 10.1371/journal.pone.0023723 Epub 2011 Sep 8. ; PMCID: PMC3169551.21931611
50 Thaker A , Yasobant S , Saxena D . Prevalence and Predictors of Anemia Among the Ashram Shala Adolescent of Sabarkantha District, Gujarat, India. HAP J Public Heal Clin Med. 2023;1 (1 ). doi: 10.1177/jpm.221115604
51 Kounnavong S , Vonglokham M , Kounnavong T , Kwadwo DD , Essink DR . Anaemia among adolescents: assessing a public health concern in Lao PDR. Glob Health Action. 2020 Jul;13 (sup2 ):1786997. doi: 10.1080/16549716.2020.1786997 ; PMCID: PMC7480417.32741354
52 Bellizzi S , Pichierri G , Panu Napodano CM , Salaris P , Fiamma M , Fozza C et.al . Iron deficiency anaemia and low BMI among adolescent girls in India: the transition from 2005 to 2015. Public Health Nutr. 2021 May;24 (7 ):1577–1582. doi: 10.1017/S1368980020004292 Epub 2020 Oct 26. ; PMCID: PMC10195546.33100257
53 Wiafe MA , Apprey C , Annan RA . Patterns of Dietary Iron Intake, Iron Status, and Predictors of Haemoglobin Levels among Early Adolescents in a Rural Ghanaian District. J Nutr Metab. 2020 Dec 24;2020 :3183281. doi: 10.1155/2020/3183281 ; PMCID: PMC7803104.33489362
54 Channar HB , Chapsi A , Mahar S , Bhacho AH , Khan M , khan Rafique M . Prevalence, Severity of Anemia and Meal Skipping Behaviour among Undergraduate Students: A Cross Sectional Study. J Heal Rehabil Res. 2023;3 (2 ):590–4. 10.61919/jhrr.v3i2.182.
55 Agustina R , Nadiya K , Andini EA , Setianingsih AA , Sadariskar AA , Prafiantini E et.al . Associations of meal patterning, dietary quality and diversity with anemia and overweight-obesity among Indonesian school-going adolescent girls in West Java. PLoS One. 2020 Apr 23;15 (4 ):e0231519. doi: 10.1371/journal.pone.0231519 ; PMCID: PMC7179884.32324775
56 Devi NR MM . A Study to Assess the Knowledge of Adolescent Girls about iron Insufficiency and Anemia. Journal of Nursing Research,Patient Safety and Practise. 2023;(32):11–20. 10.55529/jnrpsp.32.11.20.
57 Khanal A , Paudel R , Wagle CN , Subedee S , Pradhan PMS . Prevalence of anemia and its associated factors among adolescent girls on Weekly Iron Folic Acid supplementation [WIFAS] implemented and non-implemented schools at Tokha municipality, Kathmandu. PLOS Glob Public Health. 2024 Jan 26;4 (1 ):e0002515. doi: 10.1371/journal.pgph.0002515 ; PMCID: PMC10817172.38277373
58 Shah SP , Shah P , Desai S , Modi D , Desai G , Arora H . Effectiveness and Feasibility of Weekly Iron and Folic Acid Supplementation to Adolescent Girls and Boys through Peer Educators at Community Level in the Tribal Area of Gujarat. Indian J Community Med. 2016 Apr-Jun;41 (2 ):158–61. doi: 10.4103/0970-0218.173498 ; PMCID: PMC4799641.27051093
59 Chaturvedi D , Chaudhuri PK , Priyanka , Chaudhary AK . Study of correlation between dietary habits and anemia among adolescent girls in Ranchi and its surronding area. International Journal of Contempary Pediatrics. 2017;4 (4 ):1165. 10.18203/2349-3291.ijcp20172022.
60 Utami A , Margawati A , Pramono D , Julianti H , Adespin D , Wulandari D . The effectiveness of iron-folic acid supplementation and education intervention to hemoglobin level, knowledge, and compliance among adolescent girls in Islamic boarding school. Open-Access Maced J Med Sci. 2022 May 06; 10 [E ]:1141–1146. 10.3889/oamjms.2022.9688.
61 Yahya S , Khan R , Amin S , Fatima I , Qayyum Y . Iron Deficiency Anemia and its Relation with Junk Food. Pakistan J Med Heal Sci. 2022;16 (7 ):713–5. 10.53350/pjmhs22167713.
62 Olumakaiye MF . Adolescent Girls With Low Dietary Diversity Score Are Predisposed to Iron Deficiency in Southwestern Nigeria. ICAN: Infant, Child, & Adolescent Nutrition. 2013;5 (2 ):85–91. doi: 10.1177/1941406413475661
63 Fage SG , Egata G , Dessie Y , Kumsa FA , Mizana BA . Anemia among School Adolescents in Haramaya Town, Eastern Ethiopia: Cross-Sectional Study. Nutr Metab Insights. 2020 Aug 28;13 :1178638820953131. doi: 10.1177/1178638820953131 ; PMCID: PMC7457681.32922031
64 Chaudhary V , Saraswathy KN , Sarwal R . Dietary diversity as a sustainable approach towards micronutrient deficiencies in India. Indian J Med Res. 2022 Jul;156 (1 ):31–45. doi: 10.4103/ijmr.ijmr_3314_21 ; PMCID: PMC9903373.36510896
