Nutritional and micronutrient status of adolescent schoolgirls in eastern Sudan : A cross-sectional study

Background : Adolescents, especially girls, are susceptible to malnutrition and their diet must be adequate to support their very rapid growth and development. Currently, there is little published data on the nutritional state amongst adolescent girls in Sudan. Methods : A cross sectional study was conducted to assess the nutritional and micronutrient status of adolescent schoolgirls in eastern Sudan during the period of January-February 2015. Weight and height were measured using standard methods. Haemoglobin and ferritin levels were measured using blood samples, and blood films for malaria and stool samples for Schistosoma mansoni were investigated. Nutritional status was assessed according to the WHO 2006 reference values. Copper and zinc concentrations were measured by atomic absorption. Results : Twenty-five (13.7%) out of 183 girls were stunted. Seventy (38.3%) were thin; 17.5, 9.3 and 11.5% had mild, moderate and severe thinness, respectively. Only 10 (5.5%) and six (3.3%) girls were overweight and obese, respectively. The prevalence of anaemia was 77.0%. While there was no significant difference in the haemoglobin, ferritin, copper levels and thinness; thin children had significantly lower zinc (P=0.007). Conclusions : There is a high rate of stunting, thinness and anaemia among adolescent schoolgirls in eastern Sudan. More care has to be taken in order to provide a better nutrition status in the area.


Introduction
Adolescents (individuals aged 10 to 19 years) make up approximately one fifth of the world's population 1 . During adolescence there is an increase in nutrient demand that is needed for intense growth, where individuals can gain 15% of their ultimate adult height and half of their adult weight 2-4 . Adolescents are vulnerable groups and their diet must be adequate to support their very rapid growth and development 5 . Well-nourished adolescents can have optimum cognitive and learning skills, and energies, as well as be healthy for future parenthood 1 Unfortunately, the required optimum nutrition remains unmet for a vast numbers of adolescents, who are thus unable to achieve their full genetic developmental potential 2 . In particular, adolescents girls in developing countries are at risk, since they may become pregnant at an early age and have a greater risk of pregnancy-associated morbidity and mortality 6,7 . Furthermore, malnourished adolescent girls are at a higher risk of being stunted mothers, who are likely to suffer obstetric complications, such as delivering low birth weight babies 8 .
Research on the nutritional status of adolescent girls is of paramount importance to health planners, as well as to practicing physicians. There is little published data on the nutritional status of adolescent girls in countries with few resources, including Sudan, where malnutrition is a major health problem 9-14 . Consequently, the current study was conducted to assess the nutritional and micronutrient status of adolescent schoolgirls in eastern Sudan.

Participant sample
A cross-sectional study was conducted in the New Halfa area in eastern Sudan during the period of January-February 2015. Adolescent schoolgirls aged from 11 to 18 years were selected through a two-stage random (using computer generated number) cluster sample of adolescent girls attending three primary schools (AlHara Aloula, Tania and AlHara Althalta) in the area. Stage one, simple random sampling of the schools to randomly identify classes within the specific age range; stage two, random sampling of the class in identify individuals.
Those with chronic illnesses were excluded.
A sample size of 183 subjects was calculated using the assumption of the prevalence of stunting (9.45%) and thinness (23.7%) that was recently reported among school children in Northern Sudan 9 . This sample would provide 80% power to detect a 5% difference at α = 0.05, with an assumption that complete data might not be available for 10% of participants.
Data collection Nutritional status. Age of the adolescent schoolgirls was taken and double checked with that in the school records, which had been completed using the birth certificate.
Weight was measured using a digital scale to the nearest 0.1 kg. Height was measured using a stadiometer with a moveable headboard to the nearest 0.1 cm, while the participant was barefoot.
Body mass index (BMI) was computed as weight (kg) divided by the square of height (m 2 ).

Micronutrient status.
Venous blood (5 mls) was collected from each participant and allowed to clot in plain tubes, and serum was stored at −20°C until analysed in the laboratory in Khartoum for measurement of serum ferritin, copper and zinc. Concentrations of ferritin were determined by immunofluorescent assay using IMMULITE1000 (SIEMENS, CA, USA), according to the manufacturer's instructions.

Parasite status. Blood films for malaria (Plasmodium falciparum)
were prepared and Giemsa-stained.
Schistosoma mansoni infection was investigated in a single stool sample that was collected from each participant, and a Kato-Katz slide prepared and used to determine the infection intensity, if any 16 .

Statistical analysis
Data were entered using EpiData 3.4 and then exported to SPSS 20 for analysis. Anthropometric indices (HAZ and BAZ) were calculated using WHO child growth references for Z score 15 . Haemoglobin, ferritin, zinc and copper were tested for normality using Kolmogorov -Smirnov test. Mann-Whitney and Kruskal -Wallis tests were used to compare the continuous nonparametric data between two and more than two groups, respectively. Age was normally distributed and compared between two and more than two groups with t-test and ANOVA, respectively. Spearman's (non-parametric) correlation was used to investigate the correlations between the different variables. A P value of < 0.05 was considered significant.

Ethical statement
The study received ethical clearance from the Research Board at the Faculty of Medicine University of Khartoum (approval# 2012,18). After explaining the purpose of the study, written permission to perform the study was obtained from the local health and education office (New Halfa Head Office for Education). Written informed consent was obtained from the parents/guardians of the school girls before data collection.

Results
Two hundred adolescent schoolgirls were initially screened; 183 had complete data and were analysed. The nutritional status of the girls is shown in Table 1. Twenty-five (13.7%) out of the 183 girls were stunted. Seventy (38.3%) were thin, 17.5%, 9.3% and 11.5% had mild, moderate and severe thinness, respectively. Only 10 (5.5%) and six (3.3%) children were overweight While there was no significant difference in the haemoglobin, ferritin, copper levels and thinness, thin children had a significantly lower zinc level compared to normal, overweight and obese children (P=0.007; Table 2). No significant difference was found between age, haemoglobin and micronutrient levels, and stunting (Table 3).
While there was no correlation between BMI, height, ferritin, zinc and copper, a significant positive correlation was found between haemoglobin, zinc and copper ( Though there was no significant difference in haemoglobin, ferritin, and copper levels, a significantly lower zinc level among thin adolescent girls was found compared with girls with normal BMIs in the current study. Contrary to our findings, Bemnet and colleagues showed no association between zinc and HAZ. However, they observed a significant positive correlation between HAZ and copper levels 18 . Both zinc and copper have an important role in growth, and participate in numerous enzyme systems 23 .
Zinc deficiency is common in developing countries and can delay linear growth 24,25 . Unfortunately, recent research failed to show any benefit of zinc supplement in decreasing stunting in Malawian children 26 .
In this study, we aimed to assess the nutritional and micronutrient status of adolescent schoolgirls in eastern Sudan. A limitation of this study was that adolescent boys were not investigated, which might have under-estimated the rate of malnutrition among adolescents (both males and females), as adolescent girls have been shown to be less likely to be stunted than boys 20,27 . In addition, only schoolgirls were investigated, which might have missed the more vulnerable group of adolescent girls who do not attend school.
Another limitation of the current study was the lack of puberty history, since the onset of the menarche might have effects on the nutritional status of the adolescent girls. Moreover, there was a lack of dietary intake history, since physical growth of adolescent girls is generally related to their dietary intake. Another point that should be remembered is the lack of investigation of acute inflammatory markers, e.g. C-reactive protein, which has been to be associated with anaemia in eastern Sudan 28

Conclusions
There is a high rate of stunting, thinness and anaemia among adolescent schoolgirls in eastern Sudan. More care has to be taken in order to provide a better nutrition status in the area.

Competing interests
No competing interests were disclosed

Grant information
The author(s) declared that no grants were involved in supporting this work.

Paragraph two
In the paragraph two of the results section, you report findings after comparing means, but it is not clear which test you used to compare the means. Please indicate this in a tabular form and write its summary in the text referring to the table. Tables make it easier for the reader to understand your analysis and findings.

DISCUSSION
You may need to start your discussion with a brief statement as to why it was important to conduct this study where it was conducted.

○
In paragraph three you claim that wasting, stunting and thinness are indicators of acute nutritional insult. Kindly revisit the literature with a particular attention on stunting, then rephrase accordingly. ○ ".........C-reactive protein, which has been to be associated with anaemia in eastern Sudan"..It appears there is a missing word between the word been....and to.

CONCLUSION
The conclusion is very insufficient. Beef up your conclusion by reflecting on what you have found in your study.

Is the work clearly and accurately presented and does it cite the current literature? Yes
Is the study design appropriate and is the work technically sound? Yes