Why do rural women in the most remote and poorest areas of Zambia predominantly attend only one antenatal care visit with a skilled provider? A qualitative inquiry

Why do rural women in the most remote and poorest areas of Zambia predominantly attend only one... Background: While focused antenatal care (ANC) has served as an entry point in the continuum of care for both mothers and children, fewer than a third of pregnant women in the most remote and poorest communities of Zambia achieve the four ANC visits recommended by the World Health Organization. Current evidence suggests that attending ANC provided by a skilled healthcare worker at least once is common and associated with skilled birth attendance. The aim of this study was to explain why one ANC visit with a skilled provider seemed more common than four ANC visits among women in the remote and poorest districts of Zambia. Methods: A qualitative case study design was conducted in 2012 among 84 participants in the selected remote and poorest districts of Zambia. Focus group discussions were conducted with mothers and community health volunteers, while key informant interviews were conducted with healthcare providers. Thematic analysis was conducted. Results: Most women delayed starting antenatal care visits due to uncertainties about the timing for initiation of ANC and due to waiting for confirmation of the pregnancy by an elderly woman. Attendance of ANC once with a skilled provider was due to the need to assess their health status and that of their baby. In some facilities, attendance of ANC at least once was enforced by financial charges imposed on women for late ANC initiation, and/or incentives provided by nongovernmental organisations. Unavailability of services at health posts closest to these remote communities led to failure to return for subsequent ANC visits. Women’s livelihoods such as nomadic lifestyles made it harder for them to initiate and make additional ANC visits. Conclusion: The popularity of ANC attendance once by a skilled provider among the remote and poorest women of Zambia was explained through perceived unavoidable social and economic barriers to care, and the punitive and incentive procedures implemented by health services. Maximising comprehensive care by skilled healthcare workers in the one visit a woman makes at the health facility, may lead to optimal utilisation of quality focused ANC. Enhancing community-based interventions may increase the potential to reach the vulnerable populations. Keywords: Antenatal care, Appreciative inquiry, Access to care, Healthcare utilisation, Rural, Remote, Zambia * Correspondence: choolwe2003@yahoo.com School of Nursing and Public Health, University of KwaZulu-Natal, Durban, South Africa School of Public Health, Department of Epidemiology & Biostatistics, Section for Surveillance & Disease Control, University of Zambia, Lusaka, Zambia Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Jacobs et al. BMC Health Services Research (2018) 18:409 Page 2 of 9 Background Since 2016, the WHO released new guidelines for fo- The World Health Organization (WHO) recommends cused ANC, recommending a minimum of eight visits focused antenatal care (ANC) as an essential approach during pregnancy from four ANC visits [1]. Zambia is to the care of pregnant women [1]. The main goal of the currently transitioning from four ANC visits to eight ANC WHO’s focused ANC is to facilitate early detection and visits forfocused ANC. In acountry wherefour visitsare treatment of pregnancy-related complications with the difficult to meet, eight visits will likely be even harder to minimum number of visits [2]. Each visit includes care achieve for these pregnant women. There was, however, a that is appropriate to the woman’s overall condition and promising observation from our recent survey of the most stage of pregnancy and facilitates preparation for birth remote and poorest women in Zambia, in that attendance and care of the newborn. According to the WHO [2], of ANC with one visit provided by a skilled healthcare antenatal care provides a platform for important health- worker was more common at 69%, and a significant pre- care functions, including health promotion, screening dictor for skilled birth attendance and postnatal care [15]. and diagnosis, and disease prevention. There was no explanation found in our survey as to why a When utilised, focused ANC can improve women’s single visit with a skilled provider seemed common and likelihood of accessing skilled birth attendance [3] and positively associated with outcomes among women in the postnatal care [4], and improve maternal and newborn remote and poorest areas. We therefore embarked on an health outcomes [5, 6]. For instance, some studies have in-depth qualitative study to explain why one ANC visit with shown that receiving focused ANC from a skilled health a skilled provider seemed more common than four ANC attendant is associated with better infant care practices, visits among women in the remote and poorest districts of increased use of postnatal check-ups and decreased risk Zambia. Such understanding may help policymakers and of both maternal and neonatal mortality [7–9]. Conversely, implementers in designing appropriate ANC services with a women who attend fewer than four ANC visits were less limited number of visits in remote and poverty-stricken likely to receive skilled attendance at delivery [10, 11]. In communities, without compromising desired outcomes of Egypt, a study among high-risk women (pre-eclamptic) skilled birth attendance and postnatal care. who did not attend the WHO-recommended four ANC visits had a 12-times greater risk of poor maternal out- Methods come, a 53-times greater risk of poor fetal outcome, and a Study setting significantly high risk of neonatal mortality, compared to Thestudy wasconducted in four of themostrural and women who attended the recommended four antenatal poorest districts of Zambia: Chiengi and Samfya districts visits [11]. from Luapula province, and Mungwi and Luwingu from the Zambia, like many developing countries, adopted the northern provinces of Zambia. The selection of these dis- WHO model of focused ANC in 2003 which entails that tricts was purposive representing the districts classified as the expectant woman visits the health facility a minimum poorest, inhabited by the most marginalised people in the of four times, at 16 weeks, between 24 and 28 weeks, at country, and with the highest maternal and child mortality 32 weeks and the last one at 36 weeks, for women whose rates [20]. Most people are peasant farmers, engaged in crop pregnancies were progressing normally [12]. Focused and livestock production as well as fishing. Due to fishing as ANC also requires that for each visit a woman makes she the main livelihood for many households, most women and should be attended by a skilled healthcare provider [13]. their families are usually away for extended periods of time While focused ANC has served as an entry point in the and only return home occasionally. Most of the surface continuum of care for both mothers and children [14], the areas in these districts have poor terrain and are covered by achievement of ANC at least four times is not common lakes, rivers and hills. For instance, in the Samfya district, in many low- and middle-income countries, including approximately 40% of the surface area is covered by wet- Zambia [12–15]. It was demonstrated in a recent survey lands. The total estimated population size of these four dis- that less than a third of pregnant women in the most tricts is 580,090 inhabitants. In Zambia, the health system is remote and poorest communities of Zambia achieved organised into different levels of health facilities for service the WHO-recommended four ANC visits, 53% lower provision. Maternal health services are provided at health than the national estimates [15]. Most pregnant women post level (the lowest level), health centre level and at the in resource-poor settings are unable to meet the recom- level one (district), two and three (tertiary) hospitals. In the mended four ANC visits, largely because of the distances selected sites, women had a choice to attend ANC from ei- to the health facilities and the poor road conditions [3], ther the health post or health centre closest to them. delayed initiation of ANC, lower education and income levels [16–19]. These barriers to focused ANC expose Study design women to increased risk of maternal deaths and other The present research uses a qualitative case study design pregnancy-related complications [11]. conducted between August and October 2014. Jacobs et al. BMC Health Services Research (2018) 18:409 Page 3 of 9 Participants and recruitment tools were piloted in a similar facility not included in the Triangulation of different participant groups was used study. The average duration of FGDs and KIIs was for cross verification and complementary purposes. Women 45 min. The interviews were delivered at the health facil- of reproductive age, community healthcare workers, trad- ities on a face-to-face basis, and were intended to gather itional birth attendants, neighbourhood health committee information on the perceptions of the respondents regard- members, and healthcare providers were identified and re- ing ANC visits by women, including the frequency of care cruited for participating in the study. They were from one and reasons why a single visit from a skilled provider seem health facility in each of the districts that showed the worst more common among women than four ANC visits. For outcomes of maternal health indicators. In each of the four this study, a skilled healthcare provider was defined as an districts, a medical officer, a clinical care expert and a mater- accredited health professional, such as a midwife, doctor nal and child health coordinator were purposively selected or nurse who has been “trained to proficiency in the skills as key informants at district health office level. Within each needed to manage normal (uncomplicated) pregnancies, of the selected health centres, a health centre-in-charge was childbirth and the immediate postnatal period, and in the purposively sampled for in-depth interviews. Women of re- identification, management and referral of complications productive age, with children under one year old and living in women and newborns” [21]. An Interview Guide that within the study community during their most recent preg- directed FGDs and KIIs is shown in the Additional file 1. nancy, were included for focus group discussions (FGDs) All interviews were digitally recorded after obtaining in- from each health facility. Community health volunteers that formed consent from the participants. No repeat inter- have been actively working for more than six months within views were conducted. the communities under study were purposively sampled and included for FGDs with the help of healthcare workers at Data management and analysis the facility level. A total of 84 participants were interviewed The recordings were transcribed and translated from within 24 interviews, which included eight FGDs with Bemba into English. Six of the 24 transcripts, randomly women (4) and community health volunteers (4). Sixteen selected, were verified by back translation into Bemba key informant interviews (KIIs) (4 from each district) were for accuracy. Transcripts that were not back translated also conducted. None of the participants approached refused were also reviewed by listening to the original voice re- to participate. Table 1 summarises the list of interviews and cordings to ensure that they retained the original mean- instruments that were used to collect information. ings after translation. The transcripts were not returned to the participants for review because of logistical con- Data collection straints. The transcribed documents in Microsoft Word Focus group discussions and KIIs were conducted in were then exported into NVIVO 10 software (QSR Inter- English and/or in a local language, Bemba, by trained re- national, Melbourne, Australia) for coding. The authors (CJ search assistants experienced in qualitative research. Each and MM) generated the codes/themes. An inductive FGD was conducted by a pair of research assistants, who thematic analysis was used through an iterative process, were of the same gender and were conversant with the whereby themes were continuously generated, revised, local language. One research assistant facilitated the ses- and re-examined to discover and make explicit why sions, while the other one managed the audio recordings women predominantly attend only one ANC visit dur- and took field notes. The research assistants underwent a ing pregnancy. Triangulation of the different sources, one-day training prior to data collection and were super- FGs, KIIs, and field notes were employed to validate vised by one of the co-authors (CJ). The data collection thedatabyusing cross-referencing. Table 1 List of the respondents who participated in the qualitative study Type of Tool Respondents Number of Interviews (Key Informat Number of participants Total number of Interviews) per interview participants Key Informat Interviews Medical Officers, Clinical Care Experts and 12 (3 in each of the 4 districts) 1 12 Maternal and Child Health Cordinator Health Facility in-charge 4 (1 in each of the 4 districts) 1 4 Focus Group Discussions Mothers of children below one year 4 (1 in each of the health facilities 8–10 38 from each district) Community Health Volunteers (CHWs, 4 (1 in each of the health facilities 6–830 NHC, TBAs) from each district) Total 24 84 CHW Community Health Workers, NHC Neighbourhood Health Committee, TBAs Traditional Birth Attendants Jacobs et al. BMC Health Services Research (2018) 18:409 Page 4 of 9 Results areas due to a limited number of visits made overall. Characteristics of the participants Nearly all the respondents reported that most women The age range of the participating mothers varied from 18 sought ANC from the health facility at least once. to 45 years. Nearly all the mothers were married (36 out Attendance of ANC by most women was characterised of 38) and unemployed (35 out of 38). About two-thirds by delayed entry for ANC. Most healthcare workers and of the mothers (27 out of 40) had either not attended community health volunteers explained that initiation school before or completed primary school education. for ANC visits was delayed because most women were Parity for mothers varied between two and 12 children. quite silent about their pregnancies until it was visible. Only nine out of the 28 community health volunteers Most pregnant women agreed that their ANC booking interviewed were male. All healthcare workers interviewed was delayed due to a shared reluctance to prematurely had worked in the study sites for over one year preceding disclose a pregnancy. One of the community health vol- the interviews; 11 out of 16 were female. The age range unteers had this to say: for healthcare providers was between 28 and 49 years. In this study, we aimed at understanding why attend- Most of these women will be quiet about their ance of one ANC visit with a skilled provider seemed pregnancy, and they wait until it [pregnancy] shows more common than the recommended four ANC visits. (FGD, Mungwi, female, NHC). The following themes as shown in Table 2,emerged from the data: factors that affect the timing of the first ANC ap- pointment, factors that affect failure to return for subse- Uncertainty in the timing of ANC initiation quent appointments, factors that affect both timing and Women’s uncertainty in the timing of ANC initiation, return for subsequent appointments, and opportunities largely indicative of a tension between the health provider for the intervention to modify the different factors. messages and individual preferences, also explained why timing for the first ANC appointment was delayed. A Factors that affect timing of the first ANC appointment 26-year-old woman from Chiengi said: Delayed initiation of ANC A single ANC visit by a skilled provider was more com- Some go at four months, others at six and even at mon than four ANC visits for women in the remote seven, but it is not very clear the exact month but I Table 2 Reasons why one antenatal care visit with a skilled provider seemed more common than four ANC visits among women in remote and poorest districts of Zambia Theme Sub-Themes Mothers Community Health volunteers Healthcare Provider 1. Factors that affect timing of the � Uncertainty in the timing � Waiting for elderly women � Waiting for elderly women to first ANC appointment of ANC initiation to confirm pregnancy confirm pregnancy � Lack of transport 2. Factors that affect failure to return � Unavailability/Low quality services � Low quality services at � Unavailable and Poor-quality for subsequent appointments at health posts closest to women health posts services in the health posts º Inadequate supplies at the � Inadequate supplies health facilities � Unavailable/Inadequate skilled º Inadequate health personnel health care providers � Lack of awareness and education about the services 3. Factors that affect both timing of � Livelihoods as a priority � Denied subsequent care � Nomadic lifestyles the first ANC appointment and return Nomadic lifestylesBusy schedules for ANC � Seasonal migration to places for subsequent appointments with house chores house chores � Nomadic lifestyles where they might be no � Long distances to the health facilities � Long distances to the health centres health facilities � Lack of transport � Lack of money for transport 4. Opportunities for the intervention to � Assessment of Health Status � Assessment of Health Status � Assessment of Health Status modify factors affecting timing of the � To confirm if really pregnant º To check the health of the º To confirm if really pregnant first ANC appointment and failure to � Check the health of the unborn mother and their unborn � Access for services such as return for subsequent appointments. baby baby mosquito nets, folic acid and � Need to get tested for HIV � To obtain ANC cards test for HIBV � Need to receive medication such � Incentives provided by NGO � Incentives provided by NGO as IPTp � Protection for the unborn baby � To obtain ANC cards � Financial charges imposed on women for late booking Jacobs et al. BMC Health Services Research (2018) 18:409 Page 5 of 9 think it depends on how you feel in the body (FGD, (un) availability/poor quality of services Mungwi, mother, 20-34 years). Most women failed to return for subsequent appointments because the services provided at the health posts were of low quality because of inadequate services provided to Waiting for confirmation of pregnancy by elderly women women, often provided by inadequately trained personnel. The fear of ‘bad luck’ held by women also led to women’s On the whole, most health posts were not managed by preference to wait until the pregnancy was visible before skilled health facility staff. talking to others, including healthcare providers, about their pregnancy. Most of the women waited for elderly For some of us, the clinic is far from where we come women they trusted to confirm the pregnancy. Both from and to be honest what you are saying does not healthcare providers and community health volunteers happen for some of us ... Those tests are just for held similar perspectives and indicated that most preg- others who live close to the clinic (FGD, Mungwi, nant women waited for elderly women to confirm a mother, 35-49 years). pregnancy before ANC booking, with the consequence of late initiation into ANC visits. One of the healthcare Further, the quality of health services was also reported providers had this to say: to be poor at the health posts due to inadequate supplies. A midwife from Chiengi had this to say: Most of the women in this place start going for ANC very late, most of them after the second trimester. This The antenatal care we provide at the health post is is because most of them traditionally believe that they also questionable because you know, we usually lack will only come for antenatal care after an elderly certain things, you know the focused ANC we provide woman such as an auntie or grandmother confirms should be really focused antenatal, but you find that that they are pregnant (In-depth interview [IDI], sometimes you do not have everything (IDI, Chiengi, Chiengi, midwife, 35-49 years). midwife, 35-49 years). As a result, women were compelled to go to the health Factors that affect failure to return for subsequent centres for ANC only once. appointments Long distances to the facility Factors that affect both delayed timing of the first ANC Women had an option of attending ANC at a health and return for subsequent appointments post nearer to them, or a health centre further away. In Livelihoods as a priority most communities, women were reported to visit the Women’s livelihoods among these remote communities health posts for ANC to avoid traveling long distances were also another challenge for attendance of adequate to the clinics. ANC visits. Most women and their families were reported to be mobile due to fishing, the major source of their live- ... most women go to the health post, but very few lihood. This came out more particularly in Samfya and come to the health facilities because many of them Mungwi where it was reported that many women only cannot walk to the health facility (IDI, Luwingu, came once for ANC and did not have regular ANC visits healthcare worker, 35-49 years). due to their nomadic lifestyles The long distance to the health facilities influenced … a large population is mobile due to seasonal whether women could return for subsequent ANC ap- migration of people, when you consider the fishing pointments. There was a general perception among all period where men and women and their families move the categories of respondents that the long distances to the fishing camp, and also once they discover that rendered attendance of all four recommended visits for ‘my pregnancy is fine and I’ve been checked and okay, ANC difficult for women, as stated below by a mother: all is fine’, women think they are fine, they do not see any need to come back for ANC, and they disappear What I can say is that the distance from here to the (IDI, Samfya, healthcare worker, 35- 49 years). hospital [clinic] is very far, the four times they tell us to come for antenatal care is not easy, again walking back there, especially when you are almost due, the Busy schedules with house chores clinic is very far, for me most times I fail to keep The discussions with the women also revealed that the coming back because of distance (FGD, Samfya, busy schedules with house chores could barely allow mother, 35-49 years). women to return to the health facility for subsequent Jacobs et al. BMC Health Services Research (2018) 18:409 Page 6 of 9 ANC visits, given the distances and the time it took to [HIV] they will tell you and put you on medication so visit the clinic. Women could not afford not to keep up that you protect the baby from having the disease with their daily house chores. (FGD, Samfya, mother, 20-34 years). Sometimes we get very busy at home such that leaving This behaviour was also reported by healthcare workers all the work for the clinic becomes a problem. To be as well as a community health volunteer. honest for my situation at home, without someone to take care of the children at home and others, it Promotion of antenatal care through punishment/incentives becomes hard to abandon the work (FGD, Chiengi, In some facilities, attendance of ANC was enforced mother, 35-49 years). through financial charges imposed on women for late bookings. This was reported by most women and the community health volunteers. For instance, a 20-year Opportunities for the intervention to modify the different old woman reported that her ANC booking after three factors months of pregnancy invoked a fee charged by their Need to confirm pregnancy clinic, which necessitated her to book early for ANC to As soon as the pregnancy showed, the women sought avoid the charge. care from a skilled healthcare provider to confirm that they were indeed carrying a baby. The need for most Yes, like my friend has said, we are charged for women to confirm pregnancy with a skilled provider delaying to start ANC ... they say if you come after was perceived as an important driver of ANC bookings. three months you should pay 15 kwacha (FGD, Once the women were convinced that they were indeed Chiengi, mother, 20-34 years). pregnant, most of them did not return for the subse- quent visits. This health behaviour was reported by most We also found that in some facilities, some women women in nearly all group discussions. sought ANC from a skilled provider, even if it was only once, for fear of being denied subsequent care such as We go for ANC because we want to know what is in skilled attendance at delivery, if they did not obtain an the abdomen ..., because sometimes you may think you ANC card. are carrying a baby when in fact you are not (FGD, Mungwi, mother, 20-34 years). We fear not being attended to well or being chased away when we come back because if you have no ANC card, they know for sure that one missed ANC. So, we Assessment of health status have to come even if it is once so that at least you get The women viewed ANC attendance as an opportunity a card (FGD, Samfya, Mother, 35-49 years). to confirm if they were really pregnant and to check their own health status and that of the baby. Where health A community healthcare worker had this to say: problems are identified, women would welcome the ne- cessary health care to ensure their own health and the They know that if they do not attend ANC, they will well-being of their unborn baby. not get the ANC card, and without the card it becomes a problem at the clinic for delivery ... that is why they Like for me [number 7] why I come here I would want make sure they come even if it is once (FGD, Luwingu, the nurse to tell me and just to know how the baby is CHW, 35-49 years). and to know my health because if you are just at home you can’t know whether the baby is healthy or Furthermore, incentives provided during antenatal clinics not (FGD Mungwi, woman 20-34 years). through skilled personnel from the nongovernmental or- ganisation partners, which included provision of mother Furthermore, we also found that most women attended and baby packs, baby nappies, soap and mosquito nets, ANC mainly to test for HIV and to know their status. motivated women to attend ANC. Women believed that once they came to the facility, were tested and found they are HIV positive, they would receive We have seen the numbers of women attending ANC medication and their unborn baby would be protected. increase when we distribute incentives, although once, especially with the coming in of partners like MSF, Even me that’s what I know, that a woman who is they give out Chitenge materials and baby packs, and pregnant should go to the clinic, so that they test your that acts also like a motivator to the women (IDI, blood [and] if they find that you have the disease Luwingu, healthcare worker, 35-49 years). Jacobs et al. BMC Health Services Research (2018) 18:409 Page 7 of 9 Discussion these factors reported by both women and community This study sought to explain why one visit with a skilled health volunteers suggests the need to appreciate complex provider was more common than four visits among mechanisms involved in ANC utilisation, and to co-design women in the remote and poorest populations in the se- strategies together with the women that would improve lected remote and poorest districts of Zambia. Attend- continuity of care for maternal and neonatal health. ance of ANC provided by skilled personnel, often once, Specific to these rural and remote communities is the by mothers was to confirm pregnancy and check their value attached to the livelihoods and instrumental activities own health and that of their unborn child. Attendance of daily living, as well as their nomadic lifestyles, which of ANC by most women was characterised by delayed make both initiation and return visits inconvenient, entry for ANC booking, uncertainty in the timing of considering the long travel distances involved. Accord- ANC booking and due to waiting for confirmation of ing to Killewo and colleagues [33], daily chores tend to the pregnancy by elderly women. In this study, it seems distract women’s health-seeking behaviours through delay that most women in remote areas in Zambia found it in- in seeking help, particularly among poorer women. Also, convenient to revisit ANC once pregnancy, fetal health research in developing countries has shown that liveli- and their well-being were confirmed. The study has also hoods may supersede women’s motivation to visit ANC revealed that, although facilities in these communities, clinics [34–37]. Socially sensitive and appropriate health- such as health posts, were available close to the women’s care services, considerate of livelihoods and sociocultural homes, inadequate staff and low quality of services in practices, with adequate and effective patient-centred these facilities hindered women from attending adequate communication strategies by healthcare providers [34], ANC visits from skilled personnel. Women’s livelihoods, could also help modify health-seeking behaviours. such as nomadic lifestyles and household chores, led to Consistent with the findings reported in prior studies their preference for a single visit with a skilled provider. [38, 39], the perceived need for services by women found Furthermore, and consistent with other studies [22, 23], in this study, including the need for HIV testing and the due to punitive measures imposed on women by health- need to confirm the health of the mother and baby, pro- care providers and/or incentives provided by nongovern- vide an important opportunity for health promotion strat- mental organisation partners, some women attended egies such as the provision of information, education and ANC only once and did not return for subsequent visits. communication for creating awareness of the importance The observations pertaining to women’s inclination to of other pregnancy-related services. Women’s ability to at- attend a single ANC visit with a skilled provider are per- tend ANC, even if it was once in marginalised and haps the most important contribution of this study. hard-to-reach areas, suggests the need for the provision of Consistent with other qualitative studies in the rural comprehensive services as a ‘one-stop-shop’ where as parts of countries in sub-Saharan Africa, it was not sur- many services as possible are provided during the one prising that most women from the rural and remote visit, as subsequent visits for these women may not be communities of Zambia have minimum ANC visits with guaranteed [40]. Although this argument may seem to skilled personnel due to delays in entry to ANC [24–26]. contradict the WHO’s ideal focused ANC visits, now to The persisting uncertainty and confusion about timing become eight ANC visits [1], the findings generated from for ANC commencement expressed by most women this study demonstrated that for these women, their envir- have also been echoed in other similar studies and have onment (remoteness) was complex and it dictated their been explained as being due to limited awareness and ability to use maternal and neonatal health services. information about the importance of ANC [27], a pos- Our findings must be interpreted in light of some limi- sible indication of health system failures. tations. First, the interviews were conducted at the On the one hand, women recognise the need to confirm health centres. Therefore, the opinions of the women pregnancy with skilled health providers at the clinic, in- could have been influenced by some power relations at cluding their own well-being as well as that of their un- the health centres. Second, the study population was ex- born children. However, healthcare providers in health tremely rural and poor, and may be limited to similar centres further away from the women’shomesare using contexts due to differential contextual contrasts that punitive techniques to coerce women into ANC enrolment may have existed. Third, recall bias was a possibility be- and attendance, as well as using occasional incentives to cause participants were asked to describe situations as induce women into ANC. Furthermore, services at health far back as one year. posts closest to the women’s homes are inadequate However, although we thought that these limitations [28, 29], and often provided by inadequately trained could have been present, we do not think they were im- personnel, culminating in the by-pass phenomenon portant in explaining the findings. First, the finding and [30, 31], a behaviour in which women travel farther than explanation are based on different perspectives that are necessary to obtain health care [32]. A combination of also in agreement, through triangulation of different Jacobs et al. BMC Health Services Research (2018) 18:409 Page 8 of 9 sources, healthcare workers, community health volun- Acknowledgements We are grateful to the Ministry of Health, Zambia, particularly the District teers and the women themselves. Second, this paper Management Teams in Luwingu, Samfya, Chiengi and Samfya for authorising brings out the ‘voices’ of the most marginalised women the study, the neighbourhood health committees, health facility workers and who are not only poor and living in remote and limited mothers for participating in the study. resourced areas but are also from less researched areas. Funding An understanding of the poorest and hard-to-reach This study was not funded. communities is fundamental in achieving universal ac- Availability of data and materials cess to care and should not be ignored if universal access The datasets used and/or analysed during the current study are available to focused ANC is to be achieved. Lastly, this study pro- from the corresponding author on reasonable request. vides timely insight to the most developing countries, Authors’ contributions particularly Zambia, which is transitioning from the CJ, MM and CM contributed towards the study design. CJ and CM carried out WHO policy of ‘ideal four ANC visits’, now to become the data collection. CJ and MM analysed the data. CJ drafted the manuscript ‘ideal eight ANC visits’, on some factors that limit the and all authors contributed towards revision of the manuscript. All authors read and approved the final manuscript. numbers of ANC visits among the remote and poorest populations of Zambia. Targeted interventions aimed at Authors’ information reaching the poor and the marginalised remote women CJ, the corresponding author, is a PhD candidate at the University of KwaZulu-Natal. This paper is part of her doctoral project on utilisation of need to be co-designed by policymakers and programme maternal and neonatal health services among the remote and poorest implementers, including women themselves, if the new population of Zambia. WHO ‘ideal eight ANC visits’ is to be achieved. Ethics approval and consent to participate We obtained ethical clearance from the research ethics committees at the Tropical Disease Research Centre (Ref No. TRC/C4/07/2015) in Zambia and Conclusion the University of KwaZulu-Natal Biomedical Research Ethics (Ref No. BE363/15) In these remote and poorest populations of Zambia, a in South Africa. Informed written or thumbed print consent was obtained from minimum of one ANC visit to a skilled provider seemed all participants. more popular and feasible for these women due to mul- Competing interests tiple unavoidable contextual factors, creating an environ- The authors declare that they have no competing interests. ment of social exclusion that pushes the populations further away from the health system. The findings in this Publisher’sNote study reflect the interplay of structural constraints and Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. social exclusion of the poorest and remote populations [41]. These findings are suggestive of the need to repack- Author details age maternal and neonatal health services based on the School of Nursing and Public Health, University of KwaZulu-Natal, Durban, South Africa. School of Public Health, Department of Epidemiology & available opportunities. In the meantime, it is vital that Biostatistics, Section for Surveillance & Disease Control, University of Zambia, the single ANC visits women spent with skilled health- Lusaka, Zambia. Strategic Centre for Health Systems Metrics and Evaluations care workers are maximised as they may very likely be (SCHEME), School of Public Health, University of Zambia, Lusaka, Zambia. Africa Health Research Institute, Durban, Kwa-Zulu Natal, South Africa. the only one a rural woman may attend. The findings of this study also call for a rethink in the stated WHO pol- Received: 4 August 2017 Accepted: 17 May 2018 icies of ‘ideal four ANC visits’, now to become ‘ideal eight ANC visits’, without consideration of the women’s References financial, geographical and social factors that dictate levels 1. World Health Organization WHO. WHO recommendations on antenatal care of access and participation in health care. In addition to for a positive pregnancy experience. In.; 2016. 2. World Health Organization WHO. The world health report 2005: make every current community-based strategies, local women groups mother and child count: World Health Organization; 2005. who work with policymakers could be used to remodel 3. Titaley CR, Hunter CL, Dibley MJ, Heywood P. 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Why do rural women in the most remote and poorest areas of Zambia predominantly attend only one antenatal care visit with a skilled provider? A qualitative inquiry

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Medicine & Public Health; Public Health; Health Administration; Health Informatics; Nursing Research
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Abstract

Background: While focused antenatal care (ANC) has served as an entry point in the continuum of care for both mothers and children, fewer than a third of pregnant women in the most remote and poorest communities of Zambia achieve the four ANC visits recommended by the World Health Organization. Current evidence suggests that attending ANC provided by a skilled healthcare worker at least once is common and associated with skilled birth attendance. The aim of this study was to explain why one ANC visit with a skilled provider seemed more common than four ANC visits among women in the remote and poorest districts of Zambia. Methods: A qualitative case study design was conducted in 2012 among 84 participants in the selected remote and poorest districts of Zambia. Focus group discussions were conducted with mothers and community health volunteers, while key informant interviews were conducted with healthcare providers. Thematic analysis was conducted. Results: Most women delayed starting antenatal care visits due to uncertainties about the timing for initiation of ANC and due to waiting for confirmation of the pregnancy by an elderly woman. Attendance of ANC once with a skilled provider was due to the need to assess their health status and that of their baby. In some facilities, attendance of ANC at least once was enforced by financial charges imposed on women for late ANC initiation, and/or incentives provided by nongovernmental organisations. Unavailability of services at health posts closest to these remote communities led to failure to return for subsequent ANC visits. Women’s livelihoods such as nomadic lifestyles made it harder for them to initiate and make additional ANC visits. Conclusion: The popularity of ANC attendance once by a skilled provider among the remote and poorest women of Zambia was explained through perceived unavoidable social and economic barriers to care, and the punitive and incentive procedures implemented by health services. Maximising comprehensive care by skilled healthcare workers in the one visit a woman makes at the health facility, may lead to optimal utilisation of quality focused ANC. Enhancing community-based interventions may increase the potential to reach the vulnerable populations. Keywords: Antenatal care, Appreciative inquiry, Access to care, Healthcare utilisation, Rural, Remote, Zambia * Correspondence: choolwe2003@yahoo.com School of Nursing and Public Health, University of KwaZulu-Natal, Durban, South Africa School of Public Health, Department of Epidemiology & Biostatistics, Section for Surveillance & Disease Control, University of Zambia, Lusaka, Zambia Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Jacobs et al. BMC Health Services Research (2018) 18:409 Page 2 of 9 Background Since 2016, the WHO released new guidelines for fo- The World Health Organization (WHO) recommends cused ANC, recommending a minimum of eight visits focused antenatal care (ANC) as an essential approach during pregnancy from four ANC visits [1]. Zambia is to the care of pregnant women [1]. The main goal of the currently transitioning from four ANC visits to eight ANC WHO’s focused ANC is to facilitate early detection and visits forfocused ANC. In acountry wherefour visitsare treatment of pregnancy-related complications with the difficult to meet, eight visits will likely be even harder to minimum number of visits [2]. Each visit includes care achieve for these pregnant women. There was, however, a that is appropriate to the woman’s overall condition and promising observation from our recent survey of the most stage of pregnancy and facilitates preparation for birth remote and poorest women in Zambia, in that attendance and care of the newborn. According to the WHO [2], of ANC with one visit provided by a skilled healthcare antenatal care provides a platform for important health- worker was more common at 69%, and a significant pre- care functions, including health promotion, screening dictor for skilled birth attendance and postnatal care [15]. and diagnosis, and disease prevention. There was no explanation found in our survey as to why a When utilised, focused ANC can improve women’s single visit with a skilled provider seemed common and likelihood of accessing skilled birth attendance [3] and positively associated with outcomes among women in the postnatal care [4], and improve maternal and newborn remote and poorest areas. We therefore embarked on an health outcomes [5, 6]. For instance, some studies have in-depth qualitative study to explain why one ANC visit with shown that receiving focused ANC from a skilled health a skilled provider seemed more common than four ANC attendant is associated with better infant care practices, visits among women in the remote and poorest districts of increased use of postnatal check-ups and decreased risk Zambia. Such understanding may help policymakers and of both maternal and neonatal mortality [7–9]. Conversely, implementers in designing appropriate ANC services with a women who attend fewer than four ANC visits were less limited number of visits in remote and poverty-stricken likely to receive skilled attendance at delivery [10, 11]. In communities, without compromising desired outcomes of Egypt, a study among high-risk women (pre-eclamptic) skilled birth attendance and postnatal care. who did not attend the WHO-recommended four ANC visits had a 12-times greater risk of poor maternal out- Methods come, a 53-times greater risk of poor fetal outcome, and a Study setting significantly high risk of neonatal mortality, compared to Thestudy wasconducted in four of themostrural and women who attended the recommended four antenatal poorest districts of Zambia: Chiengi and Samfya districts visits [11]. from Luapula province, and Mungwi and Luwingu from the Zambia, like many developing countries, adopted the northern provinces of Zambia. The selection of these dis- WHO model of focused ANC in 2003 which entails that tricts was purposive representing the districts classified as the expectant woman visits the health facility a minimum poorest, inhabited by the most marginalised people in the of four times, at 16 weeks, between 24 and 28 weeks, at country, and with the highest maternal and child mortality 32 weeks and the last one at 36 weeks, for women whose rates [20]. Most people are peasant farmers, engaged in crop pregnancies were progressing normally [12]. Focused and livestock production as well as fishing. Due to fishing as ANC also requires that for each visit a woman makes she the main livelihood for many households, most women and should be attended by a skilled healthcare provider [13]. their families are usually away for extended periods of time While focused ANC has served as an entry point in the and only return home occasionally. Most of the surface continuum of care for both mothers and children [14], the areas in these districts have poor terrain and are covered by achievement of ANC at least four times is not common lakes, rivers and hills. For instance, in the Samfya district, in many low- and middle-income countries, including approximately 40% of the surface area is covered by wet- Zambia [12–15]. It was demonstrated in a recent survey lands. The total estimated population size of these four dis- that less than a third of pregnant women in the most tricts is 580,090 inhabitants. In Zambia, the health system is remote and poorest communities of Zambia achieved organised into different levels of health facilities for service the WHO-recommended four ANC visits, 53% lower provision. Maternal health services are provided at health than the national estimates [15]. Most pregnant women post level (the lowest level), health centre level and at the in resource-poor settings are unable to meet the recom- level one (district), two and three (tertiary) hospitals. In the mended four ANC visits, largely because of the distances selected sites, women had a choice to attend ANC from ei- to the health facilities and the poor road conditions [3], ther the health post or health centre closest to them. delayed initiation of ANC, lower education and income levels [16–19]. These barriers to focused ANC expose Study design women to increased risk of maternal deaths and other The present research uses a qualitative case study design pregnancy-related complications [11]. conducted between August and October 2014. Jacobs et al. BMC Health Services Research (2018) 18:409 Page 3 of 9 Participants and recruitment tools were piloted in a similar facility not included in the Triangulation of different participant groups was used study. The average duration of FGDs and KIIs was for cross verification and complementary purposes. Women 45 min. The interviews were delivered at the health facil- of reproductive age, community healthcare workers, trad- ities on a face-to-face basis, and were intended to gather itional birth attendants, neighbourhood health committee information on the perceptions of the respondents regard- members, and healthcare providers were identified and re- ing ANC visits by women, including the frequency of care cruited for participating in the study. They were from one and reasons why a single visit from a skilled provider seem health facility in each of the districts that showed the worst more common among women than four ANC visits. For outcomes of maternal health indicators. In each of the four this study, a skilled healthcare provider was defined as an districts, a medical officer, a clinical care expert and a mater- accredited health professional, such as a midwife, doctor nal and child health coordinator were purposively selected or nurse who has been “trained to proficiency in the skills as key informants at district health office level. Within each needed to manage normal (uncomplicated) pregnancies, of the selected health centres, a health centre-in-charge was childbirth and the immediate postnatal period, and in the purposively sampled for in-depth interviews. Women of re- identification, management and referral of complications productive age, with children under one year old and living in women and newborns” [21]. An Interview Guide that within the study community during their most recent preg- directed FGDs and KIIs is shown in the Additional file 1. nancy, were included for focus group discussions (FGDs) All interviews were digitally recorded after obtaining in- from each health facility. Community health volunteers that formed consent from the participants. No repeat inter- have been actively working for more than six months within views were conducted. the communities under study were purposively sampled and included for FGDs with the help of healthcare workers at Data management and analysis the facility level. A total of 84 participants were interviewed The recordings were transcribed and translated from within 24 interviews, which included eight FGDs with Bemba into English. Six of the 24 transcripts, randomly women (4) and community health volunteers (4). Sixteen selected, were verified by back translation into Bemba key informant interviews (KIIs) (4 from each district) were for accuracy. Transcripts that were not back translated also conducted. None of the participants approached refused were also reviewed by listening to the original voice re- to participate. Table 1 summarises the list of interviews and cordings to ensure that they retained the original mean- instruments that were used to collect information. ings after translation. The transcripts were not returned to the participants for review because of logistical con- Data collection straints. The transcribed documents in Microsoft Word Focus group discussions and KIIs were conducted in were then exported into NVIVO 10 software (QSR Inter- English and/or in a local language, Bemba, by trained re- national, Melbourne, Australia) for coding. The authors (CJ search assistants experienced in qualitative research. Each and MM) generated the codes/themes. An inductive FGD was conducted by a pair of research assistants, who thematic analysis was used through an iterative process, were of the same gender and were conversant with the whereby themes were continuously generated, revised, local language. One research assistant facilitated the ses- and re-examined to discover and make explicit why sions, while the other one managed the audio recordings women predominantly attend only one ANC visit dur- and took field notes. The research assistants underwent a ing pregnancy. Triangulation of the different sources, one-day training prior to data collection and were super- FGs, KIIs, and field notes were employed to validate vised by one of the co-authors (CJ). The data collection thedatabyusing cross-referencing. Table 1 List of the respondents who participated in the qualitative study Type of Tool Respondents Number of Interviews (Key Informat Number of participants Total number of Interviews) per interview participants Key Informat Interviews Medical Officers, Clinical Care Experts and 12 (3 in each of the 4 districts) 1 12 Maternal and Child Health Cordinator Health Facility in-charge 4 (1 in each of the 4 districts) 1 4 Focus Group Discussions Mothers of children below one year 4 (1 in each of the health facilities 8–10 38 from each district) Community Health Volunteers (CHWs, 4 (1 in each of the health facilities 6–830 NHC, TBAs) from each district) Total 24 84 CHW Community Health Workers, NHC Neighbourhood Health Committee, TBAs Traditional Birth Attendants Jacobs et al. BMC Health Services Research (2018) 18:409 Page 4 of 9 Results areas due to a limited number of visits made overall. Characteristics of the participants Nearly all the respondents reported that most women The age range of the participating mothers varied from 18 sought ANC from the health facility at least once. to 45 years. Nearly all the mothers were married (36 out Attendance of ANC by most women was characterised of 38) and unemployed (35 out of 38). About two-thirds by delayed entry for ANC. Most healthcare workers and of the mothers (27 out of 40) had either not attended community health volunteers explained that initiation school before or completed primary school education. for ANC visits was delayed because most women were Parity for mothers varied between two and 12 children. quite silent about their pregnancies until it was visible. Only nine out of the 28 community health volunteers Most pregnant women agreed that their ANC booking interviewed were male. All healthcare workers interviewed was delayed due to a shared reluctance to prematurely had worked in the study sites for over one year preceding disclose a pregnancy. One of the community health vol- the interviews; 11 out of 16 were female. The age range unteers had this to say: for healthcare providers was between 28 and 49 years. In this study, we aimed at understanding why attend- Most of these women will be quiet about their ance of one ANC visit with a skilled provider seemed pregnancy, and they wait until it [pregnancy] shows more common than the recommended four ANC visits. (FGD, Mungwi, female, NHC). The following themes as shown in Table 2,emerged from the data: factors that affect the timing of the first ANC ap- pointment, factors that affect failure to return for subse- Uncertainty in the timing of ANC initiation quent appointments, factors that affect both timing and Women’s uncertainty in the timing of ANC initiation, return for subsequent appointments, and opportunities largely indicative of a tension between the health provider for the intervention to modify the different factors. messages and individual preferences, also explained why timing for the first ANC appointment was delayed. A Factors that affect timing of the first ANC appointment 26-year-old woman from Chiengi said: Delayed initiation of ANC A single ANC visit by a skilled provider was more com- Some go at four months, others at six and even at mon than four ANC visits for women in the remote seven, but it is not very clear the exact month but I Table 2 Reasons why one antenatal care visit with a skilled provider seemed more common than four ANC visits among women in remote and poorest districts of Zambia Theme Sub-Themes Mothers Community Health volunteers Healthcare Provider 1. Factors that affect timing of the � Uncertainty in the timing � Waiting for elderly women � Waiting for elderly women to first ANC appointment of ANC initiation to confirm pregnancy confirm pregnancy � Lack of transport 2. Factors that affect failure to return � Unavailability/Low quality services � Low quality services at � Unavailable and Poor-quality for subsequent appointments at health posts closest to women health posts services in the health posts º Inadequate supplies at the � Inadequate supplies health facilities � Unavailable/Inadequate skilled º Inadequate health personnel health care providers � Lack of awareness and education about the services 3. Factors that affect both timing of � Livelihoods as a priority � Denied subsequent care � Nomadic lifestyles the first ANC appointment and return Nomadic lifestylesBusy schedules for ANC � Seasonal migration to places for subsequent appointments with house chores house chores � Nomadic lifestyles where they might be no � Long distances to the health facilities � Long distances to the health centres health facilities � Lack of transport � Lack of money for transport 4. Opportunities for the intervention to � Assessment of Health Status � Assessment of Health Status � Assessment of Health Status modify factors affecting timing of the � To confirm if really pregnant º To check the health of the º To confirm if really pregnant first ANC appointment and failure to � Check the health of the unborn mother and their unborn � Access for services such as return for subsequent appointments. baby baby mosquito nets, folic acid and � Need to get tested for HIV � To obtain ANC cards test for HIBV � Need to receive medication such � Incentives provided by NGO � Incentives provided by NGO as IPTp � Protection for the unborn baby � To obtain ANC cards � Financial charges imposed on women for late booking Jacobs et al. BMC Health Services Research (2018) 18:409 Page 5 of 9 think it depends on how you feel in the body (FGD, (un) availability/poor quality of services Mungwi, mother, 20-34 years). Most women failed to return for subsequent appointments because the services provided at the health posts were of low quality because of inadequate services provided to Waiting for confirmation of pregnancy by elderly women women, often provided by inadequately trained personnel. The fear of ‘bad luck’ held by women also led to women’s On the whole, most health posts were not managed by preference to wait until the pregnancy was visible before skilled health facility staff. talking to others, including healthcare providers, about their pregnancy. Most of the women waited for elderly For some of us, the clinic is far from where we come women they trusted to confirm the pregnancy. Both from and to be honest what you are saying does not healthcare providers and community health volunteers happen for some of us ... Those tests are just for held similar perspectives and indicated that most preg- others who live close to the clinic (FGD, Mungwi, nant women waited for elderly women to confirm a mother, 35-49 years). pregnancy before ANC booking, with the consequence of late initiation into ANC visits. One of the healthcare Further, the quality of health services was also reported providers had this to say: to be poor at the health posts due to inadequate supplies. A midwife from Chiengi had this to say: Most of the women in this place start going for ANC very late, most of them after the second trimester. This The antenatal care we provide at the health post is is because most of them traditionally believe that they also questionable because you know, we usually lack will only come for antenatal care after an elderly certain things, you know the focused ANC we provide woman such as an auntie or grandmother confirms should be really focused antenatal, but you find that that they are pregnant (In-depth interview [IDI], sometimes you do not have everything (IDI, Chiengi, Chiengi, midwife, 35-49 years). midwife, 35-49 years). As a result, women were compelled to go to the health Factors that affect failure to return for subsequent centres for ANC only once. appointments Long distances to the facility Factors that affect both delayed timing of the first ANC Women had an option of attending ANC at a health and return for subsequent appointments post nearer to them, or a health centre further away. In Livelihoods as a priority most communities, women were reported to visit the Women’s livelihoods among these remote communities health posts for ANC to avoid traveling long distances were also another challenge for attendance of adequate to the clinics. ANC visits. Most women and their families were reported to be mobile due to fishing, the major source of their live- ... most women go to the health post, but very few lihood. This came out more particularly in Samfya and come to the health facilities because many of them Mungwi where it was reported that many women only cannot walk to the health facility (IDI, Luwingu, came once for ANC and did not have regular ANC visits healthcare worker, 35-49 years). due to their nomadic lifestyles The long distance to the health facilities influenced … a large population is mobile due to seasonal whether women could return for subsequent ANC ap- migration of people, when you consider the fishing pointments. There was a general perception among all period where men and women and their families move the categories of respondents that the long distances to the fishing camp, and also once they discover that rendered attendance of all four recommended visits for ‘my pregnancy is fine and I’ve been checked and okay, ANC difficult for women, as stated below by a mother: all is fine’, women think they are fine, they do not see any need to come back for ANC, and they disappear What I can say is that the distance from here to the (IDI, Samfya, healthcare worker, 35- 49 years). hospital [clinic] is very far, the four times they tell us to come for antenatal care is not easy, again walking back there, especially when you are almost due, the Busy schedules with house chores clinic is very far, for me most times I fail to keep The discussions with the women also revealed that the coming back because of distance (FGD, Samfya, busy schedules with house chores could barely allow mother, 35-49 years). women to return to the health facility for subsequent Jacobs et al. BMC Health Services Research (2018) 18:409 Page 6 of 9 ANC visits, given the distances and the time it took to [HIV] they will tell you and put you on medication so visit the clinic. Women could not afford not to keep up that you protect the baby from having the disease with their daily house chores. (FGD, Samfya, mother, 20-34 years). Sometimes we get very busy at home such that leaving This behaviour was also reported by healthcare workers all the work for the clinic becomes a problem. To be as well as a community health volunteer. honest for my situation at home, without someone to take care of the children at home and others, it Promotion of antenatal care through punishment/incentives becomes hard to abandon the work (FGD, Chiengi, In some facilities, attendance of ANC was enforced mother, 35-49 years). through financial charges imposed on women for late bookings. This was reported by most women and the community health volunteers. For instance, a 20-year Opportunities for the intervention to modify the different old woman reported that her ANC booking after three factors months of pregnancy invoked a fee charged by their Need to confirm pregnancy clinic, which necessitated her to book early for ANC to As soon as the pregnancy showed, the women sought avoid the charge. care from a skilled healthcare provider to confirm that they were indeed carrying a baby. The need for most Yes, like my friend has said, we are charged for women to confirm pregnancy with a skilled provider delaying to start ANC ... they say if you come after was perceived as an important driver of ANC bookings. three months you should pay 15 kwacha (FGD, Once the women were convinced that they were indeed Chiengi, mother, 20-34 years). pregnant, most of them did not return for the subse- quent visits. This health behaviour was reported by most We also found that in some facilities, some women women in nearly all group discussions. sought ANC from a skilled provider, even if it was only once, for fear of being denied subsequent care such as We go for ANC because we want to know what is in skilled attendance at delivery, if they did not obtain an the abdomen ..., because sometimes you may think you ANC card. are carrying a baby when in fact you are not (FGD, Mungwi, mother, 20-34 years). We fear not being attended to well or being chased away when we come back because if you have no ANC card, they know for sure that one missed ANC. So, we Assessment of health status have to come even if it is once so that at least you get The women viewed ANC attendance as an opportunity a card (FGD, Samfya, Mother, 35-49 years). to confirm if they were really pregnant and to check their own health status and that of the baby. Where health A community healthcare worker had this to say: problems are identified, women would welcome the ne- cessary health care to ensure their own health and the They know that if they do not attend ANC, they will well-being of their unborn baby. not get the ANC card, and without the card it becomes a problem at the clinic for delivery ... that is why they Like for me [number 7] why I come here I would want make sure they come even if it is once (FGD, Luwingu, the nurse to tell me and just to know how the baby is CHW, 35-49 years). and to know my health because if you are just at home you can’t know whether the baby is healthy or Furthermore, incentives provided during antenatal clinics not (FGD Mungwi, woman 20-34 years). through skilled personnel from the nongovernmental or- ganisation partners, which included provision of mother Furthermore, we also found that most women attended and baby packs, baby nappies, soap and mosquito nets, ANC mainly to test for HIV and to know their status. motivated women to attend ANC. Women believed that once they came to the facility, were tested and found they are HIV positive, they would receive We have seen the numbers of women attending ANC medication and their unborn baby would be protected. increase when we distribute incentives, although once, especially with the coming in of partners like MSF, Even me that’s what I know, that a woman who is they give out Chitenge materials and baby packs, and pregnant should go to the clinic, so that they test your that acts also like a motivator to the women (IDI, blood [and] if they find that you have the disease Luwingu, healthcare worker, 35-49 years). Jacobs et al. BMC Health Services Research (2018) 18:409 Page 7 of 9 Discussion these factors reported by both women and community This study sought to explain why one visit with a skilled health volunteers suggests the need to appreciate complex provider was more common than four visits among mechanisms involved in ANC utilisation, and to co-design women in the remote and poorest populations in the se- strategies together with the women that would improve lected remote and poorest districts of Zambia. Attend- continuity of care for maternal and neonatal health. ance of ANC provided by skilled personnel, often once, Specific to these rural and remote communities is the by mothers was to confirm pregnancy and check their value attached to the livelihoods and instrumental activities own health and that of their unborn child. Attendance of daily living, as well as their nomadic lifestyles, which of ANC by most women was characterised by delayed make both initiation and return visits inconvenient, entry for ANC booking, uncertainty in the timing of considering the long travel distances involved. Accord- ANC booking and due to waiting for confirmation of ing to Killewo and colleagues [33], daily chores tend to the pregnancy by elderly women. In this study, it seems distract women’s health-seeking behaviours through delay that most women in remote areas in Zambia found it in- in seeking help, particularly among poorer women. Also, convenient to revisit ANC once pregnancy, fetal health research in developing countries has shown that liveli- and their well-being were confirmed. The study has also hoods may supersede women’s motivation to visit ANC revealed that, although facilities in these communities, clinics [34–37]. Socially sensitive and appropriate health- such as health posts, were available close to the women’s care services, considerate of livelihoods and sociocultural homes, inadequate staff and low quality of services in practices, with adequate and effective patient-centred these facilities hindered women from attending adequate communication strategies by healthcare providers [34], ANC visits from skilled personnel. Women’s livelihoods, could also help modify health-seeking behaviours. such as nomadic lifestyles and household chores, led to Consistent with the findings reported in prior studies their preference for a single visit with a skilled provider. [38, 39], the perceived need for services by women found Furthermore, and consistent with other studies [22, 23], in this study, including the need for HIV testing and the due to punitive measures imposed on women by health- need to confirm the health of the mother and baby, pro- care providers and/or incentives provided by nongovern- vide an important opportunity for health promotion strat- mental organisation partners, some women attended egies such as the provision of information, education and ANC only once and did not return for subsequent visits. communication for creating awareness of the importance The observations pertaining to women’s inclination to of other pregnancy-related services. Women’s ability to at- attend a single ANC visit with a skilled provider are per- tend ANC, even if it was once in marginalised and haps the most important contribution of this study. hard-to-reach areas, suggests the need for the provision of Consistent with other qualitative studies in the rural comprehensive services as a ‘one-stop-shop’ where as parts of countries in sub-Saharan Africa, it was not sur- many services as possible are provided during the one prising that most women from the rural and remote visit, as subsequent visits for these women may not be communities of Zambia have minimum ANC visits with guaranteed [40]. Although this argument may seem to skilled personnel due to delays in entry to ANC [24–26]. contradict the WHO’s ideal focused ANC visits, now to The persisting uncertainty and confusion about timing become eight ANC visits [1], the findings generated from for ANC commencement expressed by most women this study demonstrated that for these women, their envir- have also been echoed in other similar studies and have onment (remoteness) was complex and it dictated their been explained as being due to limited awareness and ability to use maternal and neonatal health services. information about the importance of ANC [27], a pos- Our findings must be interpreted in light of some limi- sible indication of health system failures. tations. First, the interviews were conducted at the On the one hand, women recognise the need to confirm health centres. Therefore, the opinions of the women pregnancy with skilled health providers at the clinic, in- could have been influenced by some power relations at cluding their own well-being as well as that of their un- the health centres. Second, the study population was ex- born children. However, healthcare providers in health tremely rural and poor, and may be limited to similar centres further away from the women’shomesare using contexts due to differential contextual contrasts that punitive techniques to coerce women into ANC enrolment may have existed. Third, recall bias was a possibility be- and attendance, as well as using occasional incentives to cause participants were asked to describe situations as induce women into ANC. Furthermore, services at health far back as one year. posts closest to the women’s homes are inadequate However, although we thought that these limitations [28, 29], and often provided by inadequately trained could have been present, we do not think they were im- personnel, culminating in the by-pass phenomenon portant in explaining the findings. First, the finding and [30, 31], a behaviour in which women travel farther than explanation are based on different perspectives that are necessary to obtain health care [32]. A combination of also in agreement, through triangulation of different Jacobs et al. BMC Health Services Research (2018) 18:409 Page 8 of 9 sources, healthcare workers, community health volun- Acknowledgements We are grateful to the Ministry of Health, Zambia, particularly the District teers and the women themselves. Second, this paper Management Teams in Luwingu, Samfya, Chiengi and Samfya for authorising brings out the ‘voices’ of the most marginalised women the study, the neighbourhood health committees, health facility workers and who are not only poor and living in remote and limited mothers for participating in the study. resourced areas but are also from less researched areas. Funding An understanding of the poorest and hard-to-reach This study was not funded. communities is fundamental in achieving universal ac- Availability of data and materials cess to care and should not be ignored if universal access The datasets used and/or analysed during the current study are available to focused ANC is to be achieved. Lastly, this study pro- from the corresponding author on reasonable request. vides timely insight to the most developing countries, Authors’ contributions particularly Zambia, which is transitioning from the CJ, MM and CM contributed towards the study design. CJ and CM carried out WHO policy of ‘ideal four ANC visits’, now to become the data collection. CJ and MM analysed the data. CJ drafted the manuscript ‘ideal eight ANC visits’, on some factors that limit the and all authors contributed towards revision of the manuscript. All authors read and approved the final manuscript. numbers of ANC visits among the remote and poorest populations of Zambia. Targeted interventions aimed at Authors’ information reaching the poor and the marginalised remote women CJ, the corresponding author, is a PhD candidate at the University of KwaZulu-Natal. This paper is part of her doctoral project on utilisation of need to be co-designed by policymakers and programme maternal and neonatal health services among the remote and poorest implementers, including women themselves, if the new population of Zambia. WHO ‘ideal eight ANC visits’ is to be achieved. Ethics approval and consent to participate We obtained ethical clearance from the research ethics committees at the Tropical Disease Research Centre (Ref No. TRC/C4/07/2015) in Zambia and Conclusion the University of KwaZulu-Natal Biomedical Research Ethics (Ref No. BE363/15) In these remote and poorest populations of Zambia, a in South Africa. Informed written or thumbed print consent was obtained from minimum of one ANC visit to a skilled provider seemed all participants. more popular and feasible for these women due to mul- Competing interests tiple unavoidable contextual factors, creating an environ- The authors declare that they have no competing interests. ment of social exclusion that pushes the populations further away from the health system. The findings in this Publisher’sNote study reflect the interplay of structural constraints and Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. social exclusion of the poorest and remote populations [41]. These findings are suggestive of the need to repack- Author details age maternal and neonatal health services based on the School of Nursing and Public Health, University of KwaZulu-Natal, Durban, South Africa. School of Public Health, Department of Epidemiology & available opportunities. In the meantime, it is vital that Biostatistics, Section for Surveillance & Disease Control, University of Zambia, the single ANC visits women spent with skilled health- Lusaka, Zambia. Strategic Centre for Health Systems Metrics and Evaluations care workers are maximised as they may very likely be (SCHEME), School of Public Health, University of Zambia, Lusaka, Zambia. Africa Health Research Institute, Durban, Kwa-Zulu Natal, South Africa. the only one a rural woman may attend. The findings of this study also call for a rethink in the stated WHO pol- Received: 4 August 2017 Accepted: 17 May 2018 icies of ‘ideal four ANC visits’, now to become ‘ideal eight ANC visits’, without consideration of the women’s References financial, geographical and social factors that dictate levels 1. World Health Organization WHO. WHO recommendations on antenatal care of access and participation in health care. In addition to for a positive pregnancy experience. In.; 2016. 2. World Health Organization WHO. The world health report 2005: make every current community-based strategies, local women groups mother and child count: World Health Organization; 2005. who work with policymakers could be used to remodel 3. Titaley CR, Hunter CL, Dibley MJ, Heywood P. 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BMC Health Services ResearchSpringer Journals

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