Improving Iron Deficiency Anemia (IDA) Prevention and Management Strategies in Indonesia: An Expert Opinion

4.1. The Importance and Urgency of Iron Deficiency Anemia (IDA) Status Assessment

In the implemented Indonesian government program, the provision of iron-folic acid tablets was done without conducting structured procedural examinations. However, experts argued that it is necessary to assess the iron status before iron supplementation or fortification in high-risk groups, particularly pregnant women and female adolescents.

Generally in Indonesia, the assessment of anemia status is conducted through a hemoglobin (Hb) test as part of the government’s program to assess the severity of the anemia problem. Hemoglobin is the primary component of red blood cells that serves as a facilitator for oxygen transfer from the lungs to the rest of the body for cell use, exchanges oxygen with carbon dioxide, and then transports carbon dioxide back to the lungs to exchange it for oxygen [12, 13]. Hemoglobin consists of four protein molecules known as globulin chains, with each chain containing a crucial structure called heme. This heme molecule contains iron, which is essential for oxygen and carbon dioxide transportation and contributes to the red coloration of blood [11]. Hemoglobin test is also a standard screening in midwifery assessment for pregnant women with a minimum of two times examination, typically in the first and third trimester. Additionally, hemoglobin level was also used as a measuring method of the anemia prevalence among high-risk groups, including pregnant women and female adolescents (aged 10 – 19 years) in the Basic Health Research (Riskesdas) [2].

In this study, experts agreed that ferritin test is a better indicator than hemoglobin test in detecting iron deficiency anemia (IDA). Ferritin is a globular protein molecule which responsible for oxidizing, storing, and binding iron [14, 15]. One ferritin molecule can bind up to 4.500 iron atoms or almost one-third of the body's iron is bound to ferritin, resulting in a strong correlation between serum ferritin and body iron storage level [14]. Discussion of the experts mainly focused on the pathophysiology of iron deficiency anemia (IDA) using the keywords “cadangan” or storage and “ferritin” to mention the importance and urgency of the ferritin test, particularly in pregnant women prior to iron-folic acid tablet consumption [14, 15].

There are three stages of iron deficiency according to the process: (1) Stage 1 – iron depletion, (2) Stage 2 – iron deficiency erythropoiesis, and (3) Stage 3 – iron deficiency anemia. The first stage or iron depletion occurs when there is a continuous lack of iron intake that causes a decrease in the body’s iron reserves, reflected by the low serum ferritin, however, there are no erythropoietic consequences yet. The iron supplied by the iron transport compartment primarily supports the production of red blood cells (RBCs), since the need for iron in erythropoiesis is significantly greater than in other tissues. If the supply becomes insufficient, it is followed by the next stage known as iron-deficient erythropoiesis, which occurs even though there may not be a significant drop in hemoglobin concentration [16, 17]. Erythropoiesis is a process of RBCs production by the proliferation and differentiation of hematopoietic cells in the bone marrow [18, 19]. Thus, if the number of RBCs in the circulation decreases, the hemoglobin level will also decrease [12, 18].

Experts pointed out that relying solely on hemoglobin test would result in missing the opportunity to detect individuals in stage (1) iron depletion and (2) iron deficiency erythropoiesis. This leads to delays in detection and interventions according to each stage. When providing iron supplementation at the low hemoglobin level stage, it only acts as therapy, however, it does not interfere with the low ferritin or circulating iron level. Therefore, it is important to conduct an iron deficiency anemia (IDA) status assessment that is capable of detecting stages 1, 2, and 3 through ferritin test. Low serum ferritin is the most sensitive and specific method to identify isolated iron deficiency as it reflects iron reserve [19]. If the test becomes the standard for iron deficiency anemia (IDA) examination, experts hope that the targets will be detected and receive interventions as early and accurately as possible.

However, there are challenges in ferritin test implementation, notably the cost, which is higher than the hemoglobin test. Experts explained that healthcare financing planner needs to consider this perspective to manage iron deficiency anemia (IDA) and the potential losses incurred from iron deficiency anemia (IDA) occurrence.

Experts recommended the Government to conduct ferritin tests periodically, with pregnant women being the main priority and targeting female adolescents gradually. Based on the expert consensus discussions, iron deficiency anemia (IDA) status examinations are primarily directed at pregnant women, as they are a high-risk group for iron deficiency anemia (IDA). Pregnancy increases blood plasma volume, leading to hemodilution and subsequently decreases the hemoglobin level [20, 21], which supports that ferritin will be a more valid test for anemia during pregnancy. If pregnant women who already have depleted iron reserve or circulated iron are only given iron supplementation, it will also affect the period of Exclusive Breastfeeding (EB), as the iron content in the breast milk will decrease. Therefore, in order to manage and reduce the risk of deleterious effects of iron deficiency anemia (IDA) during pregnancy and the postpartum period, appropriate interventions according to iron deficiency anemia (IDA) status in pregnant women are crucial.

4.2. Behavior Modification-Oriented Health Education

For iron deficiency anemia (IDA) prevention, educational intervention is required to enhance the effectiveness of dietary intervention since it promotes both behavioral and knowledge-oriented modifications [22]. Behavior modification can be done through three main stages: (1) analyzing the target's level of knowledge and comprehension of iron deficiency anemia (IDA), potential challenges, and factors that can encourage preventive behavior against iron deficiency anemia (IDA), (2) implementing preventive measures against iron deficiency anemia (IDA) and supportive social environments, (3) providing health education with the involvement of supportive social environments [23, 24].

According to expert consensus discussions, the education topic is predominantly focused on recommendations for improvement on the existing practices and experiences, which the outcomes were not as expected. Thus, reflecting on these experiences, experts agreed that to achieve different outcomes, health education should focus on behavioral change rather than solely on knowledge. Repetitive education targeted to female adolescents and pregnant women is also necessary. Expert consensus also emphasized the need for quality improvement of information provided during education, including the content of the information, as well as communication methods and styles.

Sometimes the content of information was not fully disseminated and did not engage with the local community. The community, particularly the key target audience must receive information and comprehension regarding the impact of iron deficiency anemia (IDA) and the importance of its examinations. The Health Belief Model (HBM), which is defined as a model that predicts a specific health behavior is more or less likely based on an individual's perceptions of disease severity and personal susceptibility to the disease combined with perceived benefits and barriers to that behavior. This concept is known as perceived severity or vulnerability. It encourages people to increase their comprehension regarding iron deficiency anemia (IDA) prevention and take necessary actions by making them realize the magnitude of the negative consequences of a condition [18, 25]. Previous studies also showed that pregnant women who received education based on the health belief model, particularly the perceived severity concept, have higher scores of knowledge and good dietary practices than those who did not [26, 27].

The key message of behavioral modification also needs to be designed according to the communication style, way of communication preferences, and acceptance level of the key targeted audience. To effectively modify the behavior, specific strategies need to be implemented for each level of the target audience, whether at the individual, family, or community level. Each level requires a different approach and method in message composition, communication style, and message delivery strategy. The message delivery strategy should be carried out through structural actions within educational institutions and can be internalized through social acceptance to achieve the expected behavior as a lifestyle [22].

Based on the expert discussion, the focus of education innovation or improvement is on how to enhance actions by using the term “improved” or “lebih baik.” Strategic discourse with the terms “how” or “bagaimana” is used to shift from the current condition or intervention. Subsequently, education is expected to be able to promote behavioral modification from the stage of reluctance to the desired behavior.

The closest social groups and surroundings that have the greatest influence on the key target's decision-making must be involved in behavior modification, as well as obtaining their engagement and support in order to achieve the desired outcome. Experts suggested that three social groups contribute to iron deficiency anemia (IDA) prevention in female adolescents, including family, peer groups, and school/educational environment.

In the family environment, parental involvement can be achieved through interventions in the parenting styles. For a balanced diet and iron supplementation, experts recommended the implementation of an authoritative or moderate parenting style. Parents can be educated on how to practice these parenting styles so that children can modify their behavior with parental support. The period of providing education and habituation of behavior at the family level can also begin early to facilitate behavior formation more effectively. This opinion is supported by findings implying that children raised in an authoritative parenting style have higher mealtime structure and dietary quality than those raised in a permissive style [28].

Meanwhile, in the peer group, it is important to consider the applicable subjective norms regarding behaviors related to iron deficiency anemia (IDA) prevention. Experts suggested that for the female adolescent group, the recommended approach for communication is peer group counseling. This approach focuses on building relationships between female adolescents and their peer groups. It is also necessary to understand how much the adolescents understand about iron deficiency anemia (IDA), so that the communication can be based on the empathic understanding principle. Studies found that female adolescents who have peer group support have higher adherence to iron-folic acid tablet consumption due to they tend to have a strong desire to be accepted and liked by their peers or social circle [29].

Furthermore, in the school environment, support and supervision from teachers are crucial. Schools, as formal education institutions, can play a role by providing education and internalizing health content into the curriculum. This aligns with government programs in iron-folic acid tablets provision in schools, which will fully involve the school community. Teachers, as educators, can also provide examples and serve as role models for iron deficiency anemia (IDA) prevention behavior [22].

There are social context-related factors that need to be taken into account in the pregnant women group. Experts pointed out the issue of unplanned pregnancies, which are related to the physical and health condition of the women who are not ready for pregnancy. However, it is not easy either to intervene and educate them regarding pregnancy planning due to the social pressure from both family and society on married couples to have children immediately [22]. Experts believe that prior to marriage, potential brides and grooms must receive education regarding reproductive health and contraception. If this is implemented in a structured manner, it will encourage potential brides and grooms to discuss pregnancy planning better.

Additionally, a previous study showed that compared to children with full formula feeding, the hospital admission rate was 12% lower in those with partial breastfeeding and 15% lower in those with exclusive breastfeeding for at least 6 months. The protective effect of breastfeeding on hospitalization was reduced with age. These decreased risks of subsequent hospital admission were found to remain significant until the child was 3−4 years old for non-infection respiratory, oral cavity, and non-infection genitourinary tract, and 10 years for infection and non-infection gastrointestinal tract. Several mechanisms might explain this, first, breastfed infants have better gut microbiome maturation, which leads to better immunity in later life and lower consequent hospitalization rate. Second, breastfeeding-induced inhibition of Th2 immune responses helps to prevent asthma and other allergic disease that result from an inappropriate Th2 response to environmental antigens. Third, there is a protective synergistic effect of soluble CD14 levels and breastfeeding on the risk of asthma. Fourth, maternal pathogen-specific IgAs in breast milk are crucial in preventing respiratory and gut infections in breastfed children. Therefore, encouraging breastfeeding for at least the first 6 months until 2 years and beyond is an important public health strategy to improve overall child health and lower hospital admission, as well as the government’s financial burden. However, there are challenges for breastfeeding mothers such as medical, cultural, psychological, physical discomfort, and inconvenience, especially for working mothers who have maternal leave of less than 6 months. These issues might affect breastfeeding rates and the consequent health and quality of the country’s generations. Therefore, it is crucial for the government to increase the breastfeeding rate by providing education on the benefits of breastfeeding and establishing regulations that support every breastfeeding woman [30].

The timing of complementary food (CF) introduction is also closely related to childhood health. Children with CF introduction at ≥7 months were associated with low height-for-age z-score (HAZ) and frequent (≥6 events) hospitalizations compared to those with CF introduction at 4 –< 7 months. Although exclusive breastfeeding offers clear benefits, the appropriate introduction of CF provides better growth and health for children. Delaying the introduction of CF until seven months in exclusively breastfed infants was associated with frequent hospitalization events and lower heights [31]. This might be explained by the fact that from the age of 6 months, an infant's need for energy and nutrients, including iron, starts to exceed what is provided by breast milk due to rapid growth and progressive perinatal iron storage depletion. Therefore, highly nutritious and rich in iron complementary feeding is essential to meet this gap. If complementary foods are introduced late or given inappropriately, an infant's growth and immunity might be disturbed due to nutritional deficiency [32]. According to the Scientific Report of the 2020 Dietary Guidelines Advisory Committee, CF should not be started before the age of four months, and beginning CF at 4 to 5 months of age does not offer long-term benefits or drawbacks compared with starting at 6 months of age [33]. Therefore, the government must emphasize the optimal timing and appropriate CF by providing education and establishing regulations that support CF practice.

Food labeling on food packages is crucial for providing nutritional information and helps healthy diet promotion. Increased food labeling awareness, comprehension, and usage are associated with increased interest of people towards maintaining a healthy diet. However, previous study showed that older age, male, obesity, residing in rural area, lower household income, lower educational level, smoking, and increased alcohol consumption were associated with lower food labeling awareness, comprehension, and usage. Therefore, it is recommended to personalized nutrition strategies, such as educating on the importance of a balanced diet and improving food labeling awareness, comprehension, and usage, particularly among the target population [34]. Policymakers should also ensure that citizens are provided with the right information on the labels of food packages.

Previous studies showed a significant association between higher physical activity levels and reduced risk of depression and anxiety. This might be explained by the fact that physical activity helps alleviate symptoms of depression and anxiety, improves mood, and improves cognitive function [35]. While physical activity levels do not directly correlate with iron deficiency anemia (IDA), depression and anxiety are associated with iron deficiency anemia (IDA). Persons who are depressed frequently have a poor appetite and malnutrition, which can cause nutritional deficits and potentially lead to anemia and iron deficiency anemia (IDA) [36]. Psychological stress also activates the hypothalamic–pituitary–adrenocortical (HPA) axis and increases proinflammatory cytokines, which consequently disrupt iron absorption and utilization, mediated by the IL-6 activation of hepcidin [37]. On the other hand, persons with iron deficiency anemia (IDA) may also present with psychiatric manifestations such as depression and anxiety [38]. Therefore, encouraging regular physical activity can also be one of the iron deficiency anemia (IDA) prevention strategies. However, it is also important to consider the individual's preferences and capabilities when recommending physical activity to ensure that it is enjoyable and sustainable.

4.3. Iron Deficiency Anemia (IDA) Prevention in Pregnant Women and Female Adolescents

Expert consensus targeted iron deficiency anemia (IDA) prevention at high-risk groups, namely pregnant women and female adolescents. Prevention of iron deficiency anemia (IDA) is reviewed through two main behavior categories: dietary behavior with high-protein foods and adherence to iron-folic acid tablet consumption.

Based on the expert discussion, the topic related to dietary behavior referred to the existing reality as a less-than-ideal condition, characterized by the use of terms “not” or “tidak” and “insufficient” or “kurang”. The entire discussion also revolved around the subject of the term “food” or “makanan” as the main topic. As a sub-theme, the food is also reviewed in accordance with the dietary requirements of female adolescents and pregnant women.

Dietary behavior with high-protein foods poses a challenge for both pregnant women and female adolescents due to imbalanced dietary habits or patterns. Additionally, access to fast food through online commerce is also a challenge because it provides more affordable foods with many promos or discounts and consumers can get them effortlessly. However, these foods are dominated by high carbohydrate foods instead of high protein foods [39, 40]. Surveys showed that around 90% of food merchants in online commerce sell junk food or empty-calorie foods, such as burgers, pasta, fried rice, and many more. Only 10% offer healthy foods, but still, most are not ideal for the balanced diet principle. For instance, they tend to sell fruit salad, but it is mixed with mayonnaise and cheese for topping [41].

Experts agree that female adolescents need to understand the importance of being mindful of their dietary choices, particularly foods with high iron content, as well as foods that enhance and inhibit iron absorption. Iron sources in foods are categorized into two types: heme iron, which is bound to protein, and non-heme iron, which is a complex organic iron compound. Heme iron is found in animal-based foods such as meat, fish, liver, eggs, and dairy products. On the other hand, non-heme iron is derived from plant-based foods like legumes, green leafy vegetables, fruits, and cereals [42]. Iron absorption enhancers can be obtained through consuming foods that are rich in protein and vitamin C. Protein plays an important role in transporting iron in the body, especially protein from animal sources [43]. Vitamin C helps iron absorption through the reduction process of iron from the ferric form to the ferrous form in the small intestine. Vitamin C also enhances the absorption of non-heme iron. Vitamin C can be found in vegetables and fruits, such as orange, pineapple, papaya, tomato, and guava [43, 44]. Studies have shown that pregnant women with inadequate iron, protein, and vitamin C intake are most likely to suffer iron deficiency anemia (IDA) [44, 45]. Meanwhile, iron inhibitors can be found in foods that contain caffeine, tannins, oxalates, and phytates, such as soy products, tea, and coffee [46].

Dietary habits tend to form rigid patterns that are difficult to modify; therefore, adolescents with poor dietary habits are at risk and might manifest in their health condition. Education regarding a balanced and rich-in-iron diet is a crucial part of iron deficiency anemia (IDA) prevention programs in female adolescents. Therefore, female adolescents can empower themselves to choose food preferences they enjoy while fulfilling their nutritional needs, especially those with high iron content.

It is crucial to intervene in the dietary intake of pregnant women as it affects both the mother and the fetus. If a pregnant woman does not consume a balanced diet, both the mother and the fetus are at risk of anemia due to inadequate iron. Consequently, it is associated with increased maternal infection, pre-eclampsia, and bleeding, as well as several negative impacts related to fetal growth, neurological development, low birth weight, mother and child immune system, and fetal mortality [47-49]. On the other hand, pregnant women face various challenges related to appetite changes and other pregnancy symptoms. Therefore, experts agree that it is necessary to provide counseling regarding foods that are nutritious, rich in iron, yet appetizing for them. Healthcare providers need to take a more personalized approach to understand the obstacles and challenges faced by pregnant women to meet their daily dietary requirements and provide dietary advice regarding these issues. Pregnant women can thus adopt a high-iron dietary habit to prevent iron deficiency anemia (IDA).

Additionally, the variety of foods consumed during pregnancy affects children’s eating behavior in the future, as the flavor of the maternal diet is transferred to the amniotic fluid to be perceived by the fetus. This process continues until the postnatal period, particularly when the baby starts to consume breast milk since the flavor is also transmitted through breast milk [50, 51]. The flavor experienced during the breastfeeding period then helps children to eat various foods during the transition to complementary feeding (CF) [50]. This is supported by studies that showed that infants who had early exposure to fruits and vegetables during the prenatal and/or breastfeeding period showed greater receptiveness to their flavor [52, 53]. Early exposure to flavor during the breastfeeding period may also encourage children to try novel foods and grow up to be less picky about foods [54, 55]. Thus, it is important to start eating highly nutritious foods since the pregnancy period, especially those that are rich in iron.

The second preventive behavior of pregnant women and female adolescents is to consume iron supplements in the form of iron-folic acid tablets. This intervention is a part of the Indonesian government's program in managing iron deficiency anemia (IDA). For female adolescents (10 – 19 years old), this is implemented in schools by providing one iron-folic acid tablet per week throughout the year or 52 tablets in total. Meanwhile, for pregnant women, iron-folic acid tablets are provided during pregnancy, or 90 tablets at minimum.

In the expert consensus discussion, the topic related to iron-folic acid tablets revolves around reluctance/non-adherence to consuming them as recommended, as shown by the use of the term “not” or “tidak”. The experts in the discussion then analyzed this condition by examining the implemented interventions, such as the provision of education and iron-folic acid tablets, and how they were received and consumed by the female adolescents and pregnant women. Through this analysis, it was identified that the provision of iron-folic acid tablets alone is not enough to solve the iron deficiency anemia (IDA) problem, as Indonesia’s Basic Health Research survey in 2018 revealed that not all female adolescents and pregnant women completed their iron-folic acid tablets consumption as recommended.

Furthermore, the expert consensus got into deeper discussions regarding the failure of iron supplementation in adolescent intervention, which subsequently resulted in a high prevalence of anemia among female adolescents and also aligns with the prevalence of anemia among pregnant women. Female adolescents may experience discomforts such as an unpleasant taste, strong metallic odor, and side effects like nausea after consuming iron-folic acid tablets, which subsequently causes them to stop consuming the iron-folic acid tablets [56]. In addition, there is no monitoring process to ensure adherence to iron-folic acid tablet consumption as recommended in female adolescents, which is also a challenge in the program. However, since iron deficiency or iron deficiency anemia (IDA) during pregnancy is more challenging and takes more time to overcome, iron-folic acid tablet consumption is more significant if it begins in adolescence period. Experts suggested that to optimize iron-folic acid tablet consumption adherence among female adolescents, it is necessary to create compelling messages and tempting rewards for them to voluntarily adopt behavior modifications that promote iron deficiency anemia (IDA) prevention.

Pregnant women also face the same obstacles in consuming iron-folic acid tablets; they find it unappealing and have an unpleasant odor and taste that causes discomfort and consequently results in non-adherence as recommended [57]. Therefore, experts suggested that intensive education from healthcare providers to pregnant women emphasizing the importance of iron-folic acid tablets to improve their adherence is necessary. By using a “perceived benefits” approach for pregnant women, highlighting the prevention of anemia and the maintenance of iron levels in the body, which will impact fetal development, particularly brain development and intellectual capacity, pregnant women may be more motivated to adhere to iron-folic acid tablet consumption. Studies showed that the same approach can also be implemented for female adolescents as it also increases the adherence to iron-folic acid tablet consumption [58].