Factors Related to Anemia Prevalence Among Women of Childbearing Age in the Period of Global Pandemic

Background Health authorities in Pakistan in collaboration with local and foreign non-government organizations are working hard to achieve the targets set by World Health Organization in 2012, that is, to reduce anemia prevalence and its related factors. However, due to the prevailing COVID-19 crisis, all resources and attention were diverted toward it, which led to ignorance of existing basic health issues. Objective This study assesses anemia prevalence and its related factors among women of childbearing age in the period of global pandemic. Methods A time-lagged, cross-sectional survey was conducted using a self-administered questionnaire among 1,702 volunteer women aged between 15 and 49 years across five major cities of Pakistan from January 2021 to December 2021 using the non-probability consecutive sampling technique. Blood sample results were analyzed to determine prevalence and anemia severity. The chi-squared test and multiple logistic regression were performed to examine the relationship and effect of related factors with hemoglobin levels using SPSS version 26. Results Among the 1,702 respondents, 788 (46.3%) were non-anemic and 914 (53.7%) were anemic. Anemia prevalence in Karachi was slightly greater (n=294, 55.48%) compared to other cities, and the mean hemoglobin level was 11.98 ± 0.92 g/dL. The chi-square test and multiple logistic regression indicated that the respondents’ employment status, mother’s profession, family income, living conditions, chronic health conditions, use of iron and folic acid supplements, junk food, source of drinking water, and knowledge about anemia and its preventive measures were associated significantly with anemia during the pandemic. Conclusion Results confirmed that anemia is a multi-factor health problem and that it was totally ignored during the COVID-19 pandemic, as the prevalence increased during the pandemic. Therefore, more attention should be paid to anemia surveillance, anemia awareness programs, and mobilization of community health workers and volunteers to reach a wide range of the population, including women of childbearing age even during the pandemic.


Introduction
Iron is one of the essential minerals that our bodies require to perform some of its fundamental activities. Iron, as part of structural component of hemoglobin, plays an important role in the transportation of oxygen from the lungs to the body cells [1]. Iron is essential to produce hemoglobin by erythroblasts; thus, if there is an insufficient supply of iron, the cells fail to produce hemoglobin, resulting in a condition known as "anemia" [2]. The normal level of hemoglobin for non-pregnant women and males (aged 15 years and above) is 120 gm/L and 130 gm/L respectively, according to the World Health Organization. If the level is detected below the normal range, we call the condition as "anemia" [2][3].
In the past few decades, anemia has been one of the major global developmental health problems, and this non-communicable disease is increasing rapidly in both developed and developing countries [4]. However, the prevalence of anemia is much higher in underdeveloped countries than in developed countries due to low socioeconomic status and limited healthcare facilities [5][6]. In Pakistan, anemia is categorized as a major nutritional deficiency disorder among infants, pregnant women, and non-pregnant women [6][7]. The COVID-19 pandemic further deteriorated healthcare system and economies of the developing countries, which led to ignorance of existing basic health issues [8].
Almost two billion people across the globe are affected by anemia, either directly or indirectly. The common effects are as follows: delayed normal motor function in infants, increasing risk of low birth weight or premature babies, fatigue in adults, effect on memory, and poor academic performance [9]. An anemic person shows different signs and symptoms, but the common signs and symptoms are chronic fatigue, loss of appetite, headaches, irritability, and loss of concentration [10][11].
Various studies have been conducted among women of different ages across the globe, but no study has been conducted to date that highlights anemia and its related factors during the global pandemic. Moreover, factors such as healthcare utilization, chronic health conditions, junk food, use of iron and folic acid supplements, and availability of clean drinking water have not been studied yet. The current study aims to evaluate the prevalence of anemia in women of childbearing age and to determine the factors linked with it during the global pandemic. The results of the study can help plan nutritional intervention and address the causes that lead to anemia among women of childbearing age in the period of global pandemic.

Materials And Methods
A time-lagged, cross-sectional survey was carried out using a self-administered questionnaire in five major cities of Pakistan (Peshawar, Islamabad, Rawalpindi, Lahore, and Karachi) to study anemia prevalence and its associated characteristics among women of childbearing age between 15 and 49 years from January 2021 to December 2021. Factors such as age, education level, marital status, employment status, family size, father's profession, mother's profession, family income, BMI, menstrual period duration, healthcare utilization, exercise habits, chronic health condition, knowledge about anemia, use of iron and folic acid supplements, use of multi-vitamins, tobacco use, number of meal per day, knowledge about anemia causes, fertility status, breastfeeding, and knowledge about preventive measures were part of the designed questionnaire. The ethical clearance of the study was taken from the Institutional Review Board of Riphah International University, Rawalpindi, Pakistan (Reference no. FMS/RSL/ERC.009). A total of 1,702 respondents' blood samples were taken, and the questionnaires were distributed after orally explaining to them the purpose of the study and after taking written informed consent from them. Respondents with cognitive or perceptive problems were excluded from the study. The data were collected, compiled, and analyzed using the SPSS (Statistical Package for the Social Science) Version 26 (IBM Corp. Armonk, NY). The blood sample results were used for classification of anemia severity. The independent variable of the study was all related factors, and the dependent variable was hemoglobin levels in women of childbearing age. Descriptive statistics was used to describe the study population characteristics. The chi-square test was used to assess the relationship between associated characteristics and hemoglobin levels, whereas multiple logistic regression analysis was used to assess the individual factors affecting hemoglobin levels. A p-value of ≤0.05 was considered statistically significant. Table 1 shows the results of anemia severity in women of childbearing age based on hemoglobin levels. Among the respondents, 788 (46.3%) were non-anemic and 914 (53.7%) were suffering from anemia. Among the 914 (53.6%) respondents with anemia, the prevalence of mild, moderate, and severe anemia was 493 (29.0%), 342 (20.1%), and 79 (4.9%) respectively. The sum of mean hemoglobin levels among all women of childbearing age was 11.98 ± 0.92 g/dL.      The computed results of multiple logistic regression analysis in Table 4 showed that BMI, family size, healthcare utilization, exercise habits, tobacco use, number of meals per day, and place of residence did not show a significant association with hemoglobin levels, whereas education level, employment status, chronic health conditions, junk food, anemia cause knowledge, preventive measure knowledge, breastfeeding, husband's or father's occupation, contraception use, and repeated pregnancy have a negative association with hemoglobin levels. On the other hand, age, source of drinking water, marital status, mother's profession, family income, menstrual period duration, living conditions, iron supplement use, folic acid use, fertility status, number of children, and adverse pregnancy outcome have a positive impact on hemoglobin levels among women of childbearing age.

Discussion
Anemia is the most common nutritional deficiency disorder among infants, pregnant women, and nonpregnant women [6]. The targets and action plans were designed and approved by the World Health Organization for reducing the prevalence of anemia [12][13]. The current study was designed to reveal the factors that influence anemia and its prevalence among women of childbearing age in Pakistan during this period of the COVID-19 pandemic.
The results from this study showed total anemic respondents to be greater (53.7%) than non-anemic respondents (46.3%). The results from previous studies were in accord with the present findings, but the prevalence of anemia increased during the pandemic [9]. Around half a million women of reproductive age are anemic worldwide, with a higher burden of anemia in low-and middle-income countries. Specifically, the maximum of anemia burden lies in Southeast Asian countries [10]. This study also indicated severe anemia to be present in 4.9% of women of childbearing age. A long-term vitamin and mineral deficiency, especially of iron, can lead toward anemia [14]. Anemia, especially iron deficiency anemia, progresses gradually usually without any signs and symptoms until anemia attains severity [15]. The mean hemoglobin level reported in this study was 11.98 ± 0.92 g/dL, which is in close accord with previous findings (12.35 ± 1.80 g/dL) [16]. Table 2 shows the citywise distribution of anemia in Pakistan. Karachi is the largest city with anemia prevalence (n=294, 55.48%) followed by Peshawar (n=209, 55.00%) and Rawalpindi and Islamabad (n= 211, 54.42%). Previous studies conducted in Agha Khan University also reported similar findings [17]. While the prevalence of anemia was reported to be low in this study, a previous study conducted in Lahore reported low income to be the most significant factor of anemia presence [18]. Therefore, a greater understanding of the various determining factors that can potentially lead towards anemia is of great importance for local investors to effectively resolve this issue [19]. Table 3 presents the results of the chi-square test to reveal the relationship between associated factors and hemoglobin levels, while Table 4 shows results of multiple logistic regression to reveal the effect of associated characteristics on hemoglobin levels. All the other factors showed a significant relationship with hemoglobin levels similar to the ones revealed by the chi-square test except for BMI, healthcare utilization, family size, exercising habits, tobacco use, number of meals per day, and place of residence, which all had an insignificant impact on hemoglobin levels. The results showed age to have a significant relationship with hemoglobin levels. The World Health Organization estimated that the majority (56%) of pregnant and women of childbearing age were anemic. Iron deficiency at this age is thought to be caused by a multitude of factors such as previously decreased iron supplies, growing requirement of the fetus, and increased blood volume [20]. Level of education was also significantly associated with hemoglobin levels. Previous studies conducted in this regard reported contradictory findings. In a study of low-and middle-income countries, education levels along with cultural norms were a major determinant of anemia severity [21]. Another study suggested level of schooling to not be the determining factor for anemia in Nepal and Pakistan, whereas it was inverse for countries like India and Bangladesh where there existed a relationship between the two factors [22]. Moreover, the results of this study regarding family income, fathers' and mothers' profession, and family size were also in accord with previous findings that higher monthly income of both parents was associated with a lower occurrence of anemia [9]. Similarly, menstrual period duration and exercise habits were also significantly related to anemia. According to Kamruzzaman et al., high menstrual bleeding decreases iron levels and hemoglobin amount, leading to severe anemia if not treated [23]. The results of this study also indicated economic status and living conditions to be significantly associated with hemoglobin levels, which is also in agreement with previous findings of studies from different parts of the world and in Pakistan [24]. Moreover, the prevalence of anemia was higher among women whose mothers were housewives as compared with government employee or businesspersons. Similarly, the prevalence was low among women with fathers or husbands who were government employees, and these findings were synchronous with the findings of previous studies [25].
As this study indicated that anemia has a strong association with chronic health conditions, such as infections, autoimmune diseases, cancer, and chronic kidney disease, it is a matter of great concern to prevent such chronic conditions; the results were coeval with previous findings [24]. The use of supplements especially iron supplement was significantly associated with hemoglobin level. Therefore, all women of reproductive age should take supplements especially of iron to prevent anemia [26]. The past literature suggested junk food consumption and smoking to be associated with anemia presence. Factors such as consuming tea and coffee after meals, not using iron supplements, decreased consumption of vegetables, and more emphasis on junk food were linked to anemia severity [27]. Similarly, the presence of anemia was significantly higher in smokers and opium users, which is in accord with the present findings [28]. Previous literature also suggested that receiving antenatal and perinatal care and proper follow-ups was associated with decreased likelihood of anemia. Anemia was much higher for mothers with less or no antenatal care [29]. Similarly, the number of children in the family, meals consumed in a day, contraception use, and adverse pregnancy outcomes were all associated with anemia presence. As there is a need to feed more children, the demand for food will increase, leading to poor quality of care and a greater anemia risk [25].
The risk was also greater among meal skippers or people who consumed a smaller number of meals a day. It was reported that meal frequency of less than two meals a day was found to be associated with anemia presence in pregnant women [1]. Anemia in the third trimester of pregnancy is associated with adverse maternal and neonatal outcomes. A retrospective study from Pakistan reported both adverse maternal and neonatal outcomes such as postpartum hemorrhage, prolonged or obstructed labor, gestational hypertension, and preeclampsia, with neonatal complications ranging from early neonatal death, stillbirth, preterm delivery, to low birth weight [2]. Moreover, anemia risk in urban women is reduced up to 73% due to better health and sanitation facilities [3]. Similarly, the study indicated a strong association of living conditions and source of drinking water, with hemoglobin levels, as women living in houses with unhygienic toilet facility and source of drinking water were more likely to develop anemia as they could be more prone to both water-and food-borne infections such as helminthic infections such as hookworm, which might, in turn, increase anemia severity [4]. While the results revealed some significant factors, BMI and pregnancy gap had no significant association with hemoglobin levels. A study conducted by Habib et al. found no significant association between anemia and BMI [5]. Another study suggested odds of anemia decrease with obesity [7]. The difference in results between studies might be due to difference in age and geographic location of the study participants, as suggested by Hess et al. [1]. The present study findings suggested an insignificant relationship between pregnancy gap and hemoglobin levels, which is in contradiction to previous studies. A systematic review on effect of birth spacing on maternal and child health revealed that short birth intervals were associated with maternal anemia [8]. Women who had less than two years between pregnancies were more likely to be anemic this can be justified by the fact that such women got less time to recover from depleted nutrients, thereby increasing anemia severity [3].
Lastly, the results of this study were convergent with previous studies that indicated that family income [19], exercise habits [10], number of meals [24], and education levels [11] were the societal determinants of anemia among women of reproductive age. Awareness about appropriate age for marriage, education status, employment opportunities, healthcare utilization, avoidance of excessive blood loss, provision of iron and folic acid supplements, adverse, junk food, and family planning should be imparted to masses especially in slums and rural areas to reduce the prevalence of anemia among women of childbearing age. Furthermore, the results showed that anemia is a multi-factorial health problem, and prevention strategies should focus on addressing these significant determinants for reducing the severity of anemia even during the time of a global pandemic.

Limitations of the study
The current study had a few limitations. First, we had no knowledge of the hemoglobin levels before the pandemic; therefore, we classified anemia based on the current hemoglobin levels as per defined guidelines by the World Health Organization. Second, we did not assess serum iron, ferritin, or transferrin levels, which are further anemia indicators. Third, factors such as cultural background, domestic violence, and drug abuse have not been studied.

Conclusions
The current study illustrates the risk factors for anemia among women of childbearing age in Pakistan during the COVID-19 pandemic. It is evident from the current findings that significant improvement should need to be made to further improve the overall health status of women. The prevalence of anemia is 53.7% according to this study, which was significantly more than the previous study conducted before the COVID-19 pandemic. The results also confirmed that anemia is a multi-factor health problem and was ignored during the pandemic. It was also found that awareness about the appropriate age for marriage, education status, employment opportunities, clean drinking water, healthcare utilization, avoidance of excessive blood loss, provision of iron and folic acid supplements, junk food, and family planning should be imparted to masses especially in slums and rural areas to reduce the anemia prevalence; therefore, more attention should be given to anemia surveillance and awareness programs, as well as mobilization of community health workers and volunteers to reach a wide section of the populace, including women of childbearing age during the times of pandemic.

Additional Information Disclosures
Human subjects: Consent was obtained or waived by all participants in this study. Muhammad Hammad issued approval FMS/RSL/ERC.009. This is to certify that Muhammad Hammad presented his proposal to conduct a research study on "Factors Related to Anemia Prevalence Among Women of Childbearing Age in the Period of Global Pandemic." He has devised the plan by following the guidelines for Ethical Approval of Research involving human participants and has accepted the responsibility for the conduct of the procedures set out in the participation. The Ethical Review Committee (ERC) has received this project and considers the methodological aspects of the presented proposal to be appropriate. They study project doesn't raise any ethical issues. Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.