Abbas Khan  ( College of Food Science and Engineering, Jilin University, Changchun )
Rattan Kaur Chawla  ( Department of Food Science and Human Nutrition, University of Veterinary & Animal Sciences, Lahore-Pakistan )
Cuina Wang  ( College of Food Science and Engineering, Jilin University, Changchun )
Mingruo Guo  ( College of Food Science and Engineering, Jilin University, Changchun, China )

Objective: To assess the risk factors associated with anaemia among adolescent girls.
Methods: The cross-sectional study was conducted at 10 schools in district Peshawar, Khyber Pakhtunkhwa, Pakistan, and comprised adolescent girls aged 10-14 years who were divided into two equal groups on the basis of haemoglobin levels; group 1 had those with haemoglobin <12, and group 2 12gm/dl. Anthropometric measurements were taken and haemoglobin concentration was determined by the Hemo'cue method. Physical activity was determined by Modified Harvard step test, cognitive functions were assessed by Raven's Coloured Progressive Matrices. SPSS 16 was used for data analysis.
Results: Of the 100 subjects, 50(50%) each were in the two groups. Illiteracy rate was significantly higher among the fathers and mothers of group 1 girls (p0.05). Mean haemoglobin in group 1 was 10.28±1.33 g/dl and group 2 12.73±0.58 g/dl. Mean number of steps climbed by group 1 girls were 154.6±54.6 and a longer period of time was taken to recover the basal pulse rate by them compared to group 2 counterparts (p0.05). The mean resting pulse rate in group 1 was significantly higher compared to group 2 (p0.05). Also, group 1 scored significantly lower in the cognitive function test(p0.05).
Conclusion: Socio-economic status, parent education, body mass index, physical work capacity, cogn itive func tion of anaemic girls was significa ntly lower than non anaemic girls.
Keywords: Anaemia, Cognitive function, Physical work capacity, Raven's Coloured Progressive Matrices. (JPMA 69: 1591; 2019). doi: 10.5455/JPMA.295006.

Introduction

The adolescents represent a nutritionally vulnerable segment of population, as adolescence is a period of rapid physical and psychological growth. Increased nutrient requirements combined with the marginal nutrient intake place this group at a risk of various deficiency diseases.1 Among nutritional deficiencies, anaemia affects a large fraction of female population, particularly adolescents and pregnant women. 2 Anaemia is globally considered a serious public health issue which affects 1.62 billion people, including 25.5% of school-going adolescent girls worldwide. 3 In the developing countries, 27% adolescent girls are found to be anaemic compared to only 6% in the developed countries. 4 In Pakistan, 39% adolescent girls and 20% adolescent boys are anaemic with a haemoglobin (Hb) level <10mg/dl. 5 Anaemia in adolescents is mainly caused by iron deficiency due to the increased iron demand for pubertal growth, increased blood volume, and menstrual losses. Limited iron intake in the diet is another reason. 6 Reduction in the physical work capacity is due to the reduced Hb concentration, which leads to less oxygen availability to the tissues and cardiac output. 7 Decreased Hb is in turn due to the reduction in iron store affecting physical performance, and results in minimal oxygen consumption among anaemic subjects during exercise. 8 Cognitive function is affected due to the alteration in iron content of the brain and neurotransmitters. 9 Moreover, anaemia can cause the impairment of iron-dependent enzymes such as noradrenalin, serotonin, and dopamine that are important for normal functioning of the neurotransmitters. 10 The risk factors associated with anaemia during ] adolescence justify the need for interventions, as most of the programmes are usually designed to prevent anaemia in infants, young children, lactating and pregnant women, but not necessarily in adolescents whose needs remain neglected despite them being at a high risk of facing detrimental health effects. The current study was planned to determine risk factors associated with anaemia among school-going adolescent girls.

Subjects and Methods

The cross-sectional study was conducted at 10 high schools in district Peshawar, Khyber Pakhtunkhwa (KP), Pakistan, from October 2016 to June 2017, using convenience sampling and giving consideration to the fac t that the selected sample should cover the geographical, ethical and economic variability of the study region. Those included were school-going adolescent girls aged 10-14 years. Those with blood Hb level <12 g/dl were taken as cases, and those with Hb 12 g/dl acted as controls.2 Girls with terminal illness, physical disability, chronic diseases, and metabolic disorders were excluded, and so were those who failed to provide informed consent. A pre-designed and pre-tested questionnaire was used for data collection regarding socio-demographic, anthropometry, dietary intake pattern, physical work capacity and cognitive function of the subjects. Data regarding age, gender, socioeconomic status, family size, family education, family occupation and family type were collected by interviewing the subjects, and were recorded. Water/Sanitation, Assets, Maternal education and Income (WAMI) index was used to measure socioeconomic status (SES). This includes four variables, i.e., access to improved water and sanitation, mother's year of schooling up to 16 years, presence of 8 priority assets, and monthly household income. Each variable was scaled ranging 0-8. The scores were summed up and divided by 32 to obtain WAMI index range 0-1; 0 denoting poor SES, and 1 denoting high SES. All score were converted into quintiles. 11 Nutritional status of the subjects was assessed by measuring their weight, height, and body mass index (BMI) using standard procedures. Height for age and weight for age z-score was determined using World Health Organisation (WHO) growth standards. 12Blood Hb concentration was determined by using Hemocue method, while the dietary intake pattern was assessed using a 24-hour recall method. Physical work capacity of the subjects was assessed using Modified Harvard's Step test with slight modification. 13 Pulse rate of the subjects was first checked at rest, and they were asked to climb up and down a set of five steps for up to three minutes as fast as they could. The total number of steps climbed up and down was counted. 13 Pulse rate of the subjects was measured after the physical activity and was recorded after every minute up to 3 minutes. 14A specially-designed intelligence quotient (IQ) questionnaire, Raven's Coloured Progressive Matrices, obtained from the Psychology Department of the University of Peshawar, was used for this purpose. Time for the test was 30-60 minutes. It is a very simple and easy test which is culture-free, language-free, nationality-free, and usually covers a wide range of age and ability. It is used to assess a person's immediate capacity for observation, clear thinking and accurate intellectual work. 15 Data was analysed using SPSS 16. 16 Descriptive statistics like mean and standard deviation (SD) were used for quantitative variables, and frequencies and percentages for qualitative variables. Association between categorical variables was tested with Chi-square test. Independent t-test was applied to compare the means between cases and controls for physical work capacity and cognitive functions. Correlation of different variables with anaemia was determined using Pearson's correlation test. 17 All tests were per formed at a significance level of 0.05.

Results

Of the 100 subjects, 50(50%) each were in the two groups. Illiteracy rate was found significantly higher (p0.05) among the cases 10(20%) compared to the controls 1(2%) (Table 1).



Anaemia was more prevalent in adolescent girls whose families scored less than 0.4 om the WAMI index 34(78%). Among the families of the control group, 20(40%) scored >0.5. There were 17(34%) underweight girls among the cases compared to 14(28%) controls. 12 Mean Hb concentration of the cases was 10.28±1.33 gm/dl, which was significantly lower (p0.05) compared to the controls 12.73±0.58mg/dl. The cases had significantly lower (p<0.05) intake of carbohydrates, protein and fats than the Recommended Dietary Allowance (RDA) (Table 2).

Mean number of steps climbed by the cases were 154.6±54.6 and a longer period of time was taken to recover the basal pulse rate by them compared to the controls (p0.05). The mean resting pulse rate in the cases was significantly higher compared to the controls (p0.05). Also, the cases scored significantly lower in the cognitive function test (p0.05). Bivariate regression analysis showed a significant positive correlation (r =.685; p<0.05) between Hb level and total intelligence scores of the schoolgoing adolescent girls.


Discussion

The current study is the first to assess the risk factors associated with anaemia in school-going adolescent girls in KP province of Pakistan. Illiteracy rate was found to be higher among the parents of anaemic girls. In contrast, higher education level was found in fathers of nonanaemic girls (62%). A study conducted on adolescent girls reported that fathers and mothers' education was positively associated with Hb level of low as well as high SES. 17,18Anaemia was more prevalent in adolescent girls, who belonged to low SES families (78%). The result was supported by a previous study. 19 Majority of anaemic girls were underweight (34%) and no obesity was reported. 12 Furthermore, mostly anaemic girls had moderate anaemia (54%) followed by 42% mild and 4% severe anaemia. 2 Similar results have been reported earlier. 14 Macronutrient intake of the anaemic girls was lower than RDA, micronutrient intakes, such as iron and vitamin C of the anaemic girls were statistically lower than the mean intake of non-anaemic, indicating that anaemia was associated due to low dietary intake of iron and vitamin C. These findings were in line with a previous study. 13 One study previously reported average energy and protein intake of the subjects as 1513.5±6.94 kcal and 45.5±9.8g, respectively. 19 The values were very much lower than those recommended by Indian Council of Medical research (ICMR). 20 However, improving dietary intake could prevent anaemia; anaemic subject whose mean Hb level was 8mg/dl significantly improved to 9mg/dl through dietary intake of iron and vitamin C-rich fruits and vegetables. 21The current study found that anaemia was likely to compromise physical work capacity of school-going adolescent girls. Physical work capacity test revealed that the mean time spent (1.1±0.42 minutes) in activity by anaemic girls was shorter, and they got tired easily while having climbed less number of steps (154.6±54.6) compared to the non-anaemic girls who climbed significantly higher (p0.05) number of steps over a long period of time. The results are parallel with a study which determined that the time taken by adolescent anaemic girls for physical activity was shorter (1.30 minutes) compared to the non-anaemic (1.92 minutes) due to fatigue in anaemic girls. 22 Moreover, mean resting pulse rate of the anaemic girls was significantly higher (p0.05) compared to the non-anaemic. A similar study done with Indian school girls also reported that anaemic girls covered fewer steps (143) compared to the non-anaemic girls (174) (p<0.05). 23It determined that anaemia affected the physical activity of adolescent girls and could reduce performance of anaemic girls in activity due to low supply of oxygen to the tissues and cells. 24Post-activity, longer time was taken by anaemic girls to recover to the basal pulse rate. A study on adolescent girls reported that anaemic girls had significantly high pulse rate immediately after 1-2 minutes of activity compared to non-anaemic because of low supply of oxygen to blood and tissue. 14 Anaemia can compromise the cognitive function of schoolgoing adolescent girls. Raven's Coloured Progressive Matrices test results showed that anaemic girls scored significantly (p0.05) lower in sections A, AB, and B compared to the non-anaemic girls. Similarly, total score of the anaemic girls was 15.5±4.75, which was significantly lower (p<0.05) compared to the non-anaemic girls (28.00±2.38). The anaemic girls fell in the range 5th to 10th percentile, which comes in grades IV and V, which confirmed that the anaemic girls were intellectuallyd eficient. 15 Cognitive function was affected due to thea lteration in iron content of the brain and neurotransmitters. 9 Further, anaemia can cause the impairment of iron-dependent enz ymes, such as noradrenalin, serotonin and dopamine that are important for normal functioning of the neurotransmitters. 2 The results of the current study were in line with a previous study which revealed that mean total score of Raven's test of anaemic girls (25.3 ±7.07) was significantly (p>0.05) lower than that of the non-anaemic girls (28.6 ±6.88). 25However, iron supplementation showed a positive impact on cognitive function of the anaemic girls with a low IQ score. After iron therapy, Hb level and intelligence scores improved. 26 In terms of limitation, this study was conducted at a single district with small sample size, which limits the statistical power and generalization of its findings. However, these results are considered good enough in understanding the risk factors associated with anaemia in adolscent girls. It is recommended that awareness programme should be initiated for parents and teachers to sensitise them about consequences and prevention of anaemia. Also, fortification and supplementation programmes should bestarted for school-going adolescent girls.

Conclusions

The major risk factors associated with anaemia were low SES, high illiteracy of parents, poor intake of macro- andmicro-nutrients. Moreover, anaemia compromised the cognitive function and physical work capacity of schoolgoing adolescent girls. Hb and IQ levels were found to be positively correlated.

Disclaimer: The manuscript is part of a PhD thesis.
Conflict of interest: None.
Source of Funding: This project was funding by the Matching Funds Project of Northeast Agricultural University.

References

1. Urbano MR, Vitalle MS, Juliano Y, Amancio OM. [Iron, copper and zinc in adolescent during pubertal growth spurt]. J Pediatr (Rio J) 2002; 78: 327-34.

2. WHO: Iron deficiency anaemia assessment, prevention, and control. A guide for programme managers. Geneva,: World Health Organization, 2001.

3. WHO: Reducing risks, promoting healthy life:The World Health Report, Geneva: World Health Organization, 2002.

4. Dugdale M. Anemia. Obstet Gynecol Clin North Am 2001; 28: 363-81.

5. Qureshi AF, Hashmi HH, Akhtar DS. Adolescent reproductive health- A Manual for family physicians, Karachi: College of Physician and Surgeons Pakistan; 1999- public health

6. Bruner AB, Joffe A, Duggan AK, Casella JF, Brandt J. Randomised study of cognitive effects of iron supplementation in non-anaemic iron-deficient adolescent girls. Lancet 1996; 348: 992-6

7. Beaton G, Corey PN, Steel C. Conceptual and methodological issues regarding the epidemiology of iron deficiency. Ann Clin Nutr 1989; 50: 575-85.

8. Zhu YI, Haas JD. Iron depletion without anemia and physical performance in young women. Am J Clin Nutr 1997; 66: 334-41
9. Beard J. Iron Deficiency Alters Brain Development and Functioning. J Nutr 2003; 133: 1468S-72S.
10. Dallman PR. Biochemical Basis for the Manifestations of Iron Deficiency. Ann Rev Nutr 1986; 6: 13-40.

11. Pradhan NA, Ali TS, Hasnani FB, Bhamani SS, Karmaliani R. measuring socio-economic status of an urban squatter settlement in Pakistan using WAMI Index. J. Pak Med Assoc 2018; 68: 709-14.

12. WHO Multicentre Growth Reference Study Group. Assessment of differences in linear growth among populations in the WHO Multicentre Growth Reference Study. Acta Paediatr Suppl 2006; 450: 56-65.

13. Skubie V, Hodgikns J. Cardiovascular efficiency test scores for junior and senior high school girls in the United States. Res Q 1964; 35: 184-92

14. Siddharam SM, Venketesh GM, Thejeshwari HI. A study of anemia among adolescentGirls in rural area of Hassan district, Karnataka, South India. Int J Biol Med Res 2011; 2: 922 -4.

15. Raven J, Raven JC, Court JH. Manual for Raven's Progressive Matrices and Vocabulary Scales. Section 1: General Overview. San Antonio, TX: Harcourt Assessment; 2003.
16. Bryman A, Cramer D. Quantitative Data Analysis with SPSS for Windows: A Guide for Social Scientists; 2002.

17. Mikki N, Abdul-Rahim HF, Stigum H, Ottesen HG. Anaemia prevalence and associated socio demographic and dietary factors among Palestinian adolescents in the West Bank. East Mediterr Health J 2011; 7: 208-17.

18. Caturvedi S, Kapil U, Gnanasekaran N, Sachdev HP, Pandey RM, Bhanti T. Nutrient intake amongst adolescent girls belonging to Poor socioeconomic group of rural area of Rajasthan. Indian Pediatr 1996; 197: 197-201

19. Gupta N, Kochar G. Pervasiveness of anemia in adolescent girls of low socio-Economic group of the district of kurukshetra. The Internet Journal of Nutrition and Wellness 2008; 7: 22-34.
20. Rao BSN, Sivakumar B. Nutrient Requirements & Recommended Dietary Allowances for Indians. 2nd ed. India: Indian Council of Medical Research, 2010

21. Creed-Kanashiro HM, Uribe TG, Bartolini RM, Fukumoto MN, Lo?pez TT, Zavaleta NM, et al. Improving dietary intake to prevent anemia in adolescent girls through Community kitchens in a peri urban population of lima. J Nutr 2000; 130: 459-46.

22. Rowland TW, Deisroth MB, Green GM, Kelleher JF. The effect of iron therapy on the exercise capacity of non-anemic iron-deficient adolescent runners. Am J Dis Child 1988; 142: 165-9

23. Sen A, Kanani SJ. Deleterious Functional Impact of Anemia on Young Adolescent School Girls. Indan Pediatr 2006; 43: 219-26.

24. Satyanarayan K, Pradhan R, Ramnath D, Rao P. Anaemia and physical fitness of school children of rural Hyderabad. Indian J Pediatr 1990; 27: 715-21.

25. Bandhu R, Shankar N, Tandon OP, Madan N. Effects of iron therapy on cognition inanemic School going boys. Indian J Physiol Pharmcol 2003; 47 : 301-10.

26. Sen A, Kanani SJ. Impact of iron-folic acid supplementation on cognitive Abilities of school girls in Vadodara. Indian Pediatr 2007; 46: 137-42.