Barriers and enablers for iron folic acid (IFA) supplementation in pregnant women.

Abstract In order to inform large scale supplementation programme design, we review and summarize the barriers and enablers for improved coverage and utilization of iron and folic acid (IFA) supplements by pregnant women in 7 countries in Africa and Asia. Mixed methods were used to analyse IFA supplementation programmes in Afghanistan, Bangladesh, Indonesia, Ethiopia, Kenya, Nigeria, and Senegal based on formative research conducted in 2012–2013. Qualitative data from focus‐group discussions and interviews with women and service providers were used for content analysis to elicit common themes on barriers and enablers at internal, external, and relational levels. Anaemia symptoms in pregnancy are well known among women and health care providers in all countries, yet many women do not feel personally at risk. Broad awareness and increased coverage of facility‐based antenatal care (ANC) make it an efficient delivery channel for IFA; however, first trimester access to IFA is hindered by beliefs about when to first attend ANC and preferences for disclosing pregnancy status. Variable access and poor quality ANC services, including insufficient IFA supplies and inadequate counselling to encourage consumption, are barriers to both coverage and adherence. Community‐based delivery of IFA and referral to ANC provides earlier and more frequent access and opportunities for follow‐up. Improving ANC access and quality is needed to facilitate IFA supplementation during pregnancy. Community‐based delivery and counselling can address problems of timely and continuous access to supplements. Renewed investment in training for service providers and effective behaviour change designs are urgently needed to achieve the desired impact.

supplementation programmes in many countries have had difficulty in achieving the high levels of coverage and adherence necessary to effectively reduce anaemia (Sanghvi, Harvey, & Wainwright, 2010;Yip, 1996). In most countries, antenatal care (ANC) services act as the key entry point for delivery of IFA supplements to pregnant women; women who attend ANC are more likely to use IFA supplements, and the number of tablets consumed increases with the number of ANC visits (Klemm et al., 2011;Sununtnasuk, D'Agostino, & Fiedler, 2015). Yet the often poor quality of ANC and lack of attention to nutrition, including inadequate counselling and supplement supply, make it difficult for women to consume the recommended number of IFA tablets during pregnancy (Alam et al., 2015;Galloway et al., 2002;Lacerte, Pradipasen, Temcharoen, Imamee, & Vorapongsathorn, 2011;Lutsey, Dawe, Villate, Valencia, & Lopez, 2008;Stoltzfus, 2011). Consumption of the recommended dose is also often hampered by personal and social barriers, including management of side effects, low priority given to IFA and anaemia, forgetfulness, and conflicting advice where IFA supplement use during pregnancy is not a social norm (Galloway & McGuire, 1994).
With an interest in revitalizing existing IFA programmes, the Micronutrient Initiative (MI) conducted formative research in seven countries in the Africa and Asia regions with high burdens of maternal anaemia and low birthweight to better understand the context-specific barriers and enablers to improving IFA supplementation coverage and adherence. This paper synthesizes the findings and extracts implications for large-scale supplementation programmes.

| PARTICIPANTS AND METHODS
Formative research was conducted with mixed qualitative and quantitative methods in selected districts or areas of Afghanistan, Bangladesh, Ethiopia, Indonesia, Kenya, Nigeria, andSenegal between 2012 and to better understand IFA supplementation knowledge, attitudes, and practices among pregnant women, health care providers, and social influencers, identifying the barriers and enablers associated with coverage and adherence. Local research teams were recruited to carry out the fieldwork in each country and developed and pretested their own adapted versions of the study tools, with technical guidance and quality assurance provided by MI on overall study objectives, study design, sampling, questionnaire development, and reporting of key indicators and themes. Minimum standards for study implementation were assured across contexts, including qualifications of researchers, training duration and content, pretesting of questionnaires, and approval of local adaptations to study protocols.
The studies used a variety of qualitative methods, including focusgroup discussions and key informant or in-depth interviews, see Table 1 for a description of the methods and respondents in each country. The study instruments were developed in coordination with regional technical advisors and local government, academic and nongovernmental organization partners. In most cases, the formative research studies were designed to address data gaps and deepen the understanding of programme implementation issues in the specific context. Focus group discussions were held with pregnant women or mothers who already had one child. In some countries, focus-group discussions were also held with husbands and mothers or mothersin-law who were considered key influencers in household decisionmaking processes. In-depth interviews were conducted with women, key influencers, and health care providers, including community health workers. Purposive sampling was used to represent the diversity of target beneficiaries and health providers.
Ethical approval was sought by each local partner agency. Informed consent (verbal or written) was obtained from all participants as per recommendation and acceptable standards of each local review board. Voluntary participation and confidentiality were ensured in each of the studies. No remuneration was given. Management of and access to data files followed guidelines from local ethics review boards in each case.

| Data analysis
Key features of each country's IFA programme were summarized using the WHO/Centers for Disease Control (CDC) logic model for micronutrient interventions in public health (WHO/CDC, 2011). Where necessary, additional document review (e.g., national policy) and consultation with country representatives helped to fill information gaps.
The review and synthesis of the formative research results were guided by a socioecological framework blended with an adapted version of the Theory of Triadic influence (Flay, Snyder, & Petraitis, 2009) to identify internal, external, and relational barriers and enablers that impact pregnant women and health providers with regard to target behaviours associated with improved IFA coverage and adherence in the programme impact pathway (see Figure 1). Increasing coverage (defined as receiving any amount of IFA during pregnancy) and adherence (defined as regularly consuming IFA throughout pregnancy as recommended by provider) were considered as two essential outcomes that would contribute to optimal IFA supplementation. Analysis of barriers and enablers to increased coverage focused on the target behaviour of accessing any IFA during pregnancy either through attending

Key messages
• The symptoms of anaemia during pregnancy are well known, but many women do not feel personally at risk.
• ANC is the primary delivery channel for prenatal IFA supplements in most countries, but accessibility and delayed first visit remain critical barriers to increased coverage and adherence.
• Health workers require training on prenatal supplementation guidelines and counselling skills to manage side effects and monitor adherence.
• Governments should consider community-based delivery to improve frequency of contacts and personalized support for women throughout pregnancy.

| Women's perceived barriers or enablers to receiving IFA through ANC
Women were asked about their beliefs, attitudes, and practices with regard to ANC, the primary delivery platform for IFA supplementation in these countries. Although attending ANC at least once during pregnancy was very common, various reasons were given for not attending ANC frequently or only late in pregnancy. Some women interviewed in Ethiopia, Kenya, and Senegal perceived ANC as primarily for curative purposes (dealing with pain, complications, or illness) and did not feel the need to go if they were having a healthy pregnancy. Kenyan women also spoke of fears of attending ANC, such as fear of hospitals, HIV testing, or pregnancy confirmation. Low perceived value and need for ANC visits during pregnancy was an important internal barrier among women in Bangladesh.
The most commonly reported external barrier to IFA supplementation coverage through ANC was accessibility, both geographic accessi-    Note In terms of relational barriers and enablers to attending ANC, there was general agreement that historical social barriers to ANC attendance were no longer an issue. Yet women were still highly influenced by family members. In Afghanistan, Nigeria, and Senegal, the decision to attend ANC was made by other family members, usually the husband and/or mother-in-law, not women themselves. In Bangladesh and Nigeria, some older adult women discouraged younger women from attending and using medicines during pregnancy. Kenyan women described their husbands as being generally supportive but a minority felt that these men did not value ANC or discouraged them from early ANC attendance. Perceived low quality of ANC service delivery and poor treatment by health care providers were also important relational barriers. In Bangladesh, women did not receive adequate counselling or understand the messages given by health workers. In Ethiopia, women saw ANC as synonymous with injections and felt that limited services were provided. Senegalese respondents felt the offered ANC services did not meet expectations, but some women were still motivated to go in order to establish a relationship with the midwife as a means of accessing support during labour and getting a birth certificate afterwards.

| Women's perceived barriers or enablers to receiving IFA through community delivery platforms
Community-based delivery of IFA supplementation was rare in the areas included in this study. In Indonesia, village midwives and community health volunteers were an important delivery channel for IFA tablets for pregnant women. In Afghanistan, where some communitybased delivery was reported, women had concerns whether community health workers and traditional birth attendants had received sufficient training. They felt that community-based providers were "illiterate, not knowledgeable, not a doctor". Yet the proximity of these service providers was seen as a major enabler to improve access and thus coverage of IFA.

| Health workers' perceived barriers or enablers to provide IFA supplementation during ANC
Lack of IFA supplementation-specific training and capacity gaps were reported by health care providers in all countries, summarized in Table 3. In Nigeria, health personnel were either not aware of existing guidelines or had no access to them, relying on their own experience to make care decisions as opposed to using national evidence-based guidelines. In Senegal, midwives (the most frequent prescribers of IFA supplements to pregnant women) had a high level of knowledge regarding anaemia and IFA supplementation but varied in their prescription practices due to perceived lack of value to the mother in early pregnancy and concerns with nausea during the first trimester. Reliance by health workers on signs and symptoms of anaemia for diagnosis as well as lack of awareness regarding IFA being recommended for all pregnant women was also identified in interviews.
Inadequate supply of IFA supplements was cited as a barrier by health care providers in every country. In most cases, the supply issue was seen as a problem of inadequate procedures for procurement at the local level instead of inadequate stocks at upper or central levels.
In Senegal, respondents described concerns that women were purchasing poor quality IFA supplements from other sources due to variability in the price of supplements and frequent stock outs at health facilities.
In Ethiopia, health care providers reported growing demand for IFA supplements by women attending ANC and through communitybased services as enabling higher IFA coverage. Health extension programme strengthening, the versatile role of Voluntary Community Health Promoters in social mobilization, community education and identification of pregnant women for ANC, as well as the strong Bangladesh • Need to improve capacity of service providers to administer IFA, monitor supply and track individuals on supply and utilization, provide quality counselling • Need to strengthen capacity of supply chain managers in forecasting

Indonesia
• Village midwives trained on general MCH topics but not IFA supplementation specifically • Need to improve capacity of health centre staff, village midwives, and CHWs to counsel pregnant women in interpersonal communication and group counselling • Need for regular supportive supervision Ethiopia • No in-service or refresher training • Insufficient supportive supervision from HEW supervisors to help build capacity • Lack of knowledge and interest in IFA programme among health workers Kenya • "Limited" level of preservice and in-service training on focused ANC and IFA supplementation (per Kenya Services Provision Assessment) contributing to low quality of counselling by health workers • Incomplete District Health Information System reporting by facilities and inadequate data analysis, feedback, and reviews by concerned focal persons at district, regional, and national levels • Capacity building on IFA service delivery needed for both facility-based and community-based health workers (coverage a major challenge identified)

Nigeria
• No specific IFA supplementation training provided to health workers • Need training in counselling on management of side effects and encouragement of adherence, using new guidance provided by government • Need capacity strengthening in point of delivery supply management and forecasting Senegal • Need for training CHWs to distribute IFA, especially counselling skills to improve adherence • Need for training health workers to train, support, and monitor CHWs in IFA distribution Note. ANC = antenatal care; IFA = iron folic acid; MCH = maternal child health; CHW = community health worker; HEW = health extension worker.
relationships between health extension workers and pregnant women were also cited as enabling factors.

| Barriers and enablers to adherence
3.3.1 | Women's perceived barriers/enablers to timely access to IFA supplementation Barriers to timely initiation of IFA supplementation were closely related to those for seeking ANC in the first trimester. Few women knew the importance of or saw value in seeking ANC during the first trimester. Most women thought the first ANC visit was recommended around the third month of pregnancy (beginning of 2nd trimester), but some felt that ANC was only needed if a problem came up. Women in Ethiopia and Senegal expressed reluctance to reveal the pregnancy publicly during the first trimester; women in rural areas of Senegal in particular believed that this would put the fetus at risk ("some pregnancies cannot support being known"). Relational barriers to early ANC attendance included various social implications of revealing a pregnancy and requiring the support of their husband and/or motherin-law. Health care provider reluctance to prescribe IFA supplements during the first trimester was also observed in several contexts.
Women's perceptions of the purpose and value of IFA supplementation also influenced when they believed it was important to start taking the tablets. In Senegal, women perceived iron supplements as useful for restoring blood, avoiding complications during delivery, and giving strength for the delivery. Under this paradigm, it made sense for pregnant women to take the supplements later in the pregnancy in preparation for the delivery. The utility of IFA supplementation for anaemia prevention or treatment of asymptomatic anaemia was less well understood or important to these women.

| Women's perceived barriers/enablers to receive regular refills of IFA supplementation
Accessing at least 90 tablets, and preferably 180 tablets, during the course of the pregnancy requires multiple ANC visits or accessing IFA tablets from other sources, including community-based providers.
In general, women did not know the recommended number of ANC Learning how internal or personal factors impact women's experience with ANC and IFA supplements helps to inform programmes.
Recognizing and valuing the potential for micronutrient supplements to directly and positively impact their own health, especially in early pregnancy, are important for increasing acceptance and demand for this intervention among pregnant women. These perceived benefits are necessary to outweigh the social, financial, and resource costs and physical discomforts currently associated with IFA supplements.
Other studies have shown a positive association between the perceived health benefits of micronutrient supplementation and increased coverage and adherence (Aikawa et al., 2006;Galloway et al., 2002;Klevor et al., 2016;Lutsey et al., 2008;Nechitilo et al., 2016;Zavaleta, Caulfield, Figueroa, & Chen, 2014 Addressing supply chain management issues and improving product stock monitoring are also needed to ensure the availability of supplements for women, especially in contexts where the tablets are provided free of charge. Procurement of high quality tablets is also expected to improve adherence because our study and others have shown that the colour, size, coating, and packaging of iron tablets can affect consumption behaviour (Galloway et al., 2002).
Improving continued access to supplements throughout pregnancy is also a priority as fewer prenatal visits are associated with a lower number of IFA tablets consumed (Lutsey et al., 2008;Onyeneho et al., 2016;Sununtnasuk et al., 2015). In Vietnam, the most important factor enabling taking iron tablets for at least 5-9 months was a frequent supply of iron tablets (Aikawa et al., 2006). Establishing community-based delivery of IFA supplements and/or community health workers providing follow-up are key components of the strategies used in Indonesia, Nepal, Nicaragua, and Thailand to successfully increase IFA supplementation coverage (Pokharel, Maharjan, Mathema, & Harvey, 2011;Sanghvi et al., 2010). Community-based distribution of IFA supplements was positively viewed by the women in our study.
A delay in the first ANC visit has been shown to be associated with lower haemoglobin levels (Lutsey et al., 2008). Due to personal and social ramifications of revealing a pregnancy too early, programmes seeking to encourage early adoption of micronutrient supplementation in pregnancy should explore alternative sources of supplements that are easily accessed at the community level. Distribution of IFA and referral to ANC are performed at the community level by Female Community Health Volunteers in Nepal as part of an integrated delivery platform, where adherence and coverage rates are among the highest (Pokharel et al., 2011). Recent evidence from Nepal shows an association between IFA and newborn or child survival, with the greatest effect in women who started taking IFA early in pregnancy and took 150-240 supplements (Nisar et al., 2015). Yet regardless of the distribution point, supply-side issues of adequate supplies of quality IFA tablets and distributing them in adequate amounts to women must also be addressed (Ayoya, Bendech, Zagre, & Tchibindat, 2012;Galloway et al., 2002).
Strategies involving multiple stakeholders are required to support improved adherence with IFA supplementation in order to address the various barriers expressed by women in this study. Creating an environment where it is normalized, valued, and prioritized for a pregnant woman to take "one tablet a day" and "take iron supplements throughout pregnancy" will require broad efforts, starting with renewed political commitment and, in some cases, removal of restrictions on who can provide the supplements (WHO, 2012b). Advantages to community based platforms include easier access to refills, personalized counselling on managing side effects and opportunities for educating and involving other key decision makers in the household. The critical role of the family for social support and advice during pregnancy has been observed by others (Martin et al., 2016;Matare, Mbuya, Dickin, Humphrey, & Stoltzfus, 2015;Wulandari & Klinken Whelan, 2011). Engaging influencers in the community, such as husbands and mothers or mothers-in-law, in health promotion activities for ANC attendance, and micronutrient supplementation during pregnancy, is expected to address some of the barriers at the household decision-making level observed in this study. Engaging family members as adherence partners (Martin et al., 2016) or using innovative technology for reminder messages (Matiri, Pied, Velez, Cantor, & Galloway, 2015) can also improve adherence.

| CONCLUSION
In each context studied, specific cultural beliefs and practices were identified that act as barriers to IFA supplement consumption. Formative research is essential prior to the development of behaviour change interventions to design context-specific interventions that motivate pregnant women, their families, and health care providers to increase access to and consumption of IFA supplements. In addition, to improved facility-based ANC access and quality, community-based delivery and counselling have the potential to address concerns found in IFA supplementation programmes, with earlier contact, potential for frequent resupply and more personal support for pregnant women.
Renewed investment in prenatal supplementation programmes with strong behaviour change interventions at policy, provider, community, and individual levels is urgently needed to achieve the World Health Assembly nutrition global targets for anaemia and low-birthweight reduction.