Suboptimal distribution and utilization of antenatal care given bed Nets undermine pregnant women’s protection in Benin: a prospective field study

Abstract

Background

The World Health Organization (WHO) recommends that pregnant women in sub-Saharan Africa (SSA) receive a free long-lasting insecticidal net (LLIN) during their first antenatal care (ANC) visit to prevent malaria. This study, conducted in Benin, evaluates the distribution and utilization rates of LLINs provided at the first ANC visit among pregnant women.

Methods

Data were collected from 14 public and private health centers located in urban and rural areas across Southern, Central, and Northern Benin. Pregnant women were enrolled in the study during their initial ANC visit and were subsequently visited at home twice, where a questionnaire was administered. The study assessed the distribution and use of LLINs during the first ANC visit. After the second home visit, the LLIN found on the pregnant women’s sleeping unit was collected to evaluate its physical integrity and bio-efficacy. Chi-square tests were used to compare each indicator across three variables: region, urban/rural setting, and public/private status of health centers.

Results

A total of 718 pregnant women were included in the study. LLIN ownership and usage before the first ANC visit were 94% [89-97%] and 93% [85-97%], respectively. During the first ANC visit, 63% [40-80%] of the pregnant women received an LLIN, but only 11% [7-22%] installed it on their sleeping area. During the pregnancy period, 72% [64-78%] of the LLINs in use were found to be either physically damaged or not bio-effective.

Conclusion

The distribution of LLINs to pregnant women during their first ANC visit was inadequate, with only a small fraction of recipients actively using the net. This shortfall leads to suboptimal protection for this vulnerable population during pregnancy.

Background

Malaria persists as a major public health issue in Africa, despite significant financial support and the expansion of control tools since 2000 [1]. Globally, in 2020, there were an estimated 241 million cases and 627,000 deaths [2]. In Benin, malaria cases and deaths increased between 2014 and 2018, rising from 1,044,235 cases and 1,869 deaths to 1,768,450 cases and 2,138 deaths, respectively [2]. In 2018, malaria accounted for 46.8% of medical consultations, with an incidence rate of 185 cases per 1,000 inhabitants, particularly affecting pregnant women and children under five [3, 4]. Benin is divided into three malaria transmission zones: the Southern and Central regions have perennial transmission that intensifies during the rainy season, while the Northern region experiences seasonal transmission, peaking in the rainy season and ceasing during the dry season [5, 6]. Malaria infection poses significant risks during pregnancy, with pregnant women experiencing higher prevalence rates compared to non-pregnant women [7, 8]. This elevated risk is partly due to a weakened immune system and potentially more mosquito bites [9], but mainly due to the specific affinity of the infecting strain for the placenta [10, 11]. Furthermore, the impact of malaria during pregnancy varies significantly with transmission intensity [7, 12, 13]. In regions of stable endemicity, malaria during pregnancy increases the risk of low birth weight (LBW), maternal anemia, and perinatal mortality [7, 12–15].

To combat this issue, the World Health Organization (WHO) recommends the use of intermittent preventive treatment with sulfadoxine-pyrimethamine (SP) (IPTp), administered at least three times at monthly intervals starting from the second trimester, along with the use of Long-Lasting Insecticidal Nets (LLINs) throughout pregnancy [16]. In Africa, where malaria is endemic, using LLINs throughout pregnancy or from mid-pregnancy positively impacts pregnancy outcomes [17]. Currently, LLINs are the only preventive tool available for pregnant women during the first trimester [18].

Although there have been efforts to increase the proportion of people sleeping under LLINs in sub-Saharan Africa, the percentage has plateaued since 2015 [18]. A study assessing household LLIN use in the region found that higher LLIN use correlates with increased household ownership [19]. However, LLIN ownership does not necessarily ensure their use by household members [20]. In Africa, LLIN ownership and usage indicators among pregnant women vary between countries [21–23].

In Benin, the National Malaria Control Program distributes LLINs to the general population every three years across the entire country, just before the high malaria transmission season. In 2020, 14,423,998 people were registered, and 13,581,637 people received a total of 7,652,166 LLINs [4, 24]. LLINs are also routinely given to children and pregnant women during vaccination and antenatal care visits. The Demographic and Health Survey results indicate that LLIN ownership grew from 25% in 2006 to 92% in 2017, with use increasing from 15 to 71% in the general population and from 20 to 79% among pregnant women, largely due to mass distribution efforts [25]. A recent study in Sô-Ava, Southern Benin, showed that only 60% of pregnant women reported receiving an LLIN during their first trimester, and fewer than 10% of these LLINs met WHO bio-efficacy criteria [26].

This study aims to provide the first national-level estimate in Benin of the distribution and use of LLINs received by pregnant women during their initial antenatal care (ANC) visit.

Methods

Study area

This study was conducted from 2019 to 2021 across three regions of Benin: Southern, Central, and Northern. The Southern region has a sub-equatorial climate, with two dry seasons (August-September and December-March) and two rainy seasons (April-July and October-November). The Central and Northern regions experience a tropical climate with one rainy season (May to October) and one dry season (November to April), with a more pronounced contrast between the rainy and dry seasons in the Northern compared to the Central region [3]. Study sites were chosen in collaboration with the National Malaria Control Program of Benin and included both public and private health centers in rural and urban areas within these regions. Health districts were randomly selected in the Southern, Central, and Northern parts of Benin. The selection involved a random draw of stratified maternity clinics, requiring a minimum of 20 ANC visits per month. A total of 14 maternity clinics were stratified and selected based on their location in the Southern (five clinics), Central (five clinics), and Northern (four clinics) regions, as well as their status as public or private and their setting as rural or urban (see Fig. 1).

Fig. 1.

Map of the study area

Data collection

For this study, data were collected using the KoBo Toolbox platform. The survey was designed in XLSForm, a flexible tool that enabled us to create a structured, intuitive questionnaire incorporating skip logic and validation rules to minimize errors. Field teams were trained in using this data collection tool and subsequently collected data electronically with the KoBo Collect mobile app. This app facilitated real-time data entry, even in offline settings, and simplified secure data transfer for analysis.

The sample size was determined based on a previous study [26], which included approximately 240 women in the southern region of Benin. For this study, we targeted the same number of participants, around 240, for each of the three regions (Southern, Central, Northern), aiming for a total of 720 women. By the end of the recruitment period, 718 participants had been enrolled. Pregnant women were recruited at their first antenatal care visit at the maternity clinic and visited twice at home. All women attending their first antenatal care visit (ANC1) were invited to participate in the study. Those who agreed and signed the consent form were included in the study. The first home visit occurred 48 h after recruitment, and the second visit took place one month later. During the first home visit, data was collected on LLIN ownership by pregnant women prior to their first antenatal care (ANC) visit, as well as data on usage, including whether the pregnant woman slept under a bed net the previous night and the age of these LLINs if applicable. Information on LLIN distribution during ANC1 was also gathered. If the pregnant woman had received a LLIN at ANC1, it was noted whether she had installed it on her bed. Additionally, pregnant women were asked if they received sensitization during their ANC1 visit, which included instructions on proper LLIN use and the importance of using LLINs, especially during pregnancy. At the second home visit, the LLINs found on the sleeping area of each pregnant woman were collected for laboratory evaluation of physical integrity and bio-efficacy. These LLINs were then replaced with new ones provided by the study.

Physical integrity

The physical integrity of LLINs was assessed by counting and categorizing holes according to size on each side of the net:

Size 1: Smaller than a thumb (0.5–2 cm).

Size 2: Larger than a thumb but smaller than a fist (2–10 cm).

Size 3: Larger than a fist but smaller than a head (10–25 cm).

Size 4: Larger than a head (> 25 cm).

The area of each hole was calculated assuming circular holes, with the diameter equal to the midpoint of the size category (except for the largest category, which uses an arbitrary diameter of 30 cm). Estimated areas were weighted using the size 1 area as a reference. The hole index (HI) was calculated for each LLIN using:

HI = (A x no. of size-1 holes) + (B x no. of size-2 holes) + (C x no. of size-3 holes) + (D x no. size-4 holes) with A = 1, B = 23, C = 196, and D = 576 [27].

An LLIN with an HI between 0 and 64 is considered “good,” between 65 and 642 “acceptable,” and greater than 643 “bad” [28].

Bio-efficacy

Bio-efficacy of LLINs was evaluated using the standard WHO cone test. Twenty 2–5 day-old, non-blood-fed female Anopheles gambiae (Kisumu strain) mosquitoes were exposed to five pieces (25 cm x 25 cm each) of each LLIN for 3 min. As negative controls, 100 mosquitoes were exposed to non-insecticide-treated net pieces. Post-exposure, mosquitoes had access to a 10% sugar solution and were kept at 27 ± 2 °C with 75 ± 10% relative humidity. Knock-down (Kd) and mortality rates of mosquito were recorded at 1 and 24 h post-exposure, respectively. According to WHO criteria, an LLIN is bio-effective if the Kd rate is ≥ 95% or the mortality rate is ≥ 80% [27].

Statistical analysis

Statistical analysis was performed to estimate proportions and confidence intervals for each indicator, including LLIN ownership, distribution, use, physical integrity, Kd, and mortality rates. Chi-square tests compared these indicators across stratified variables: region, urban/rural status, and health center public/private status. STATA version 15 was used for all statistical analyses. All statistical analyses accounted for clustering induced by recruiting women from different maternity wards via STATA’s survey data analysis module, utilizing the svyset command to declare the survey design and svy commands to estimate robust standard errors, adjusted confidence intervals, and p-values.

Results

The women included in the study had an average age of 27 years (standard deviation 6.2 years), and 23% of them were primigravida with a median number of pregnancies of 3, including the current pregnancy. Almost all of them were married or in relationship (97.5%), and two-thirds of them were uneducated or had only primary-level education.

Ownership and use of LLINs by pregnant women before first antenatal care visit

During the study, 718 pregnant women were enrolled. Overall, the ownership and use rates of LLINs were 94% (95% CI [89-97%]) and 93% [85-97%], respectively, among pregnant women prior to their first antenatal care (ANC) visit (refer to Fig. 2). These indicators were fairly consistent across different health center statuses and regions. LLIN ownership and utilization rates remained above 90% and 88% respectively, regardless of the health center’s location, status, or site. Before the first ANC, approximately 57% [50-64%] of pregnant women used LLINs distributed during the 2017 mass campaign, and 21% [17-27%] used LLINs obtained from a health center during a previous pregnancy. Additionally, 67% [54-77%] of these women used LLINs that were over a year old, with minimal variation based on health center status and regional area.

Fig. 2.

LLIN ownership and use before ANC visit in Benin, 2019–2021

LLIN distribution and use during first antenatal care visit

The distribution and use of LLINs during the first ANC visit were analyzed, as shown in Fig. 3. Of the 718 pregnant women, 449 (63% [40-80%]) received an LLIN during their first ANC. Distribution proportions varied significantly with health center status and location. Only 35% [4-88%] of women in private health centers received an LLIN, compared to 76% [56-89%] in public centers (p = 0.07). Likewise, 74% [31-95%] of rural women received an LLIN, compared to 51% [23-78%] in urban areas (p = 0.27). Distribution also varied widely across sites: 81% [38-97%] in the Southern, 71% [52-85%] in the Central, and 34% [2-92%] in the Northern regions, respectively (p = 0.07).

Fig. 3.

LLIN distribution during first ANC visit and their use in Benin, 2019–2021

Among the 449 women who received an LLIN at their first ANC, only 19% [12-29%] placed it on their sleeping unit, equating to 11% [7-22%] of the overall sample. This usage differed significantly by health center status, regional area, and site, being higher in private centers than public ones (respectively 29% [17-46%]) vs. 16% [9-29%], p = 0.06), and higher in rural than urban settings (23% [13-38%] vs. 13% [4-31%], p = 0.16). Usage rates were 22% [11-38%], 12% [4-33%], and 26% [2-88%] in the Southern, Central, and Northern sites, respectively (p = 0.34).

As expected, among the 449 women who received a bed net at ANC1, 74% of those who did not own a bed net before the study installed the bed net they received at ANC1, compared to only 16% of women who already owned a bed net (p < 0.01).

More unexpectedly and interestingly, the use of bed nets received at the first prenatal visit (ANC1) was higher among younger women (< 27 years, the mean age) than among older women (respectively 16% [8-28%] vs. 8% [4-16%], p = 0.005), among primigravida or secundigravida compared to multigravida (respectively 16% [8-27%] vs. 10% [5-19%], p = 0.008), and among less educated women (uneducated or primary level) compared to more educated women (respectively 15% [8 − 27%] vs. 6% [3 − 13%], p = 0.02).

Pregnant women sensitization during first antenatal care visit

Out of 718 pregnant women, 395 (55% [36-72%]) reported receiving sensitization during their first ANC visit. This proportion varied by site (p = 0.09) but appeared consistent across health center statuses and areas. Sensitization rates were 31% [11-61%] in the Southern, 62% [16-93%]in the Central, and 71% [26-95%] in the Northern sites. Among those sensitized, 90% [78-96%] did not change the frequency of LLIN use during pregnancy following the session.

Physical integrity and Bio-efficacy of LLINs used by pregnant women

A total of 706 LLINs were collected from the pregnant women’s sleeping units. Overall, 434 LLINs (61% [55-68%]) were in good physical condition and 277 (39% [32-47%]) were bio-effective. The proportion of LLINs that were both bio-effective and in good condition was 28% [22-36%] (see Fig. 4). Physical integrity proportions were 71% [58-81%] in the Southern, 56% [40-71%] in the Central, and 58% [43-71%] in the Northern sites ((p = 0.06) but did not differ according to the health center status or area. Bio-efficacy did not differ across sites or health center status, but varied with area (44% [33-56%] rural vs. 34% [24-44%] urban, p = 0.10).

Fig. 4.

Physical integrity and bio-efficacy of LLINs used by pregnant women in Benin, 2019–2021

Bio-efficacy of LLINs in health center stocks

The bio-efficacy of 56 LLINs was tested, of which 51 achieved WHO efficacy criteria. Among the five that did not, four were from the same health center, an urban private center in the Southern region. Those not meeting criteria originated from an old stock (5 years old).

Discussion

To our knowledge, this study is the first to estimate, on a national level in an endemic malaria country in Africa, the proportion of LLIN distribution and usage received during the first antenatal care visit by pregnant women. The results revealed that LLIN ownership and use among pregnant women before their first antenatal care visit were very high. However, the distribution and subsequent use of LLINs obtained during this visit were notably suboptimal. Consequently, a majority of LLINs used on pregnant women’s sleeping areas were either not bio-effective or not in good physical condition.

The LLIN ownership rate observed in this study was higher than the 24% reported by Kinde-Gazard et al. in 2011 [29] for the Mono and Couffo departments in Southern Benin several years earlier. These authors also found high LLIN usage among those pregnant women who owned one, which aligns with our findings. The high LLIN ownership and usage rates in our study can likely be attributed to the successful mass free distribution efforts in Benin during 2014 and 2017. This is consistent with findings from studies conducted in Sô-Ava, Southern Benin [26], and other countries in sub-Saharan Africa, which also reported high levels of LLIN ownership and use [22, 30, 31].

Nonetheless, about 40% of pregnant women did not receive an LLIN during their first antenatal care visit, with variations across sites, health centers, and geographical areas. LLIN distribution rates were higher in public health centers than in private ones, possibly due to better stock availability of resources in public health centers that can be explained by simplified administrative access to malaria control tools, compared to private health facilities. Another noteworthy observation is the higher distribution and usage of LLINs in rural compared to urban areas. In rural areas, the relationship between the community and health workers tends to be closer, potentially leading to greater awareness and better usage of LLINs received in health centers.

A significant concern from our findings is that, despite receiving an LLIN during their first antenatal care visit, very few pregnant women actually used it throughout their pregnancy. Possible reasons for this low utilization rate could include inadequate sensitization during antenatal care visits or insufficient training of health care workers on malaria control strategies. Consequently, many pregnant women continued using LLINs they possessed before their first antenatal care visit, which were on average more than a year old. These factors are critical to consider in community malaria control strategies.

A majority of the LLINs collected from sleeping units were in good physical condition, which aligns with findings from Hounkonnou et al. (2018) [26]. However, the proportions of LLINs in good condition were different between sites, with the Southern site showing better LLIN maintenance. Despite this, most LLINs were not bio-effective according to WHO standards [27]. Our results show a better bio-efficacy rate (39%) compared to the 6% reported by Hounkonnou et al. (2018) [26], yet only a minority of LLINs used by pregnant women were both in good condition and bio-effective, indicating suboptimal protection against malaria during pregnancy.

One limitation of our study is that it is not representative of the entire diversity of all public and private maternity wards in the country. However, the aim was to position the study across three sites within different regions representative of the national territory (South, Center, North) to detect variations between these sites, being perfectly representative of the entire country was not the goal. The study provides numerous indicators that have not been thoroughly documented before. It highlights the variations across regions, public/private status, and rural/urban settings, which are valuable for understanding the complexities of implementing malaria control strategies among pregnant women. It can also be noted that the use of conservative tests accounting for the design clustering resulted in occasionally high p-values. Nonetheless, the observed differences are often substantial and likely indicate true differences, even if they are not significant in the strictest sense.

Conclusion

The study illustrates that LLIN ownership and use before the first antenatal care visit among pregnant women were highly satisfactory. Nevertheless, LLIN distribution at the first antenatal care visit was inadequate, and very few beneficiaries actually used the LLINs. Identifying factors that contribute to suboptimal LLIN distribution and use in pregnant women is crucial, as it affects malaria control in this vulnerable population. Potential factors could include inadequate training of healthcare workers, limited LLIN access in certain areas, lack of sensitization during antenatal visits, and issues with LLIN quality and maintenance. Addressing these root causes is essential to developing interventions that enhance LLIN distribution and use, thereby improving protection against malaria for pregnant women.

Abbreviations

ANC

Antenatal care

HI

Hole Index

IPTp

Intermittent Preventive Treatment

Kd

Knock-down

LBW

Low Birth Weight

LLIN

Long-Lasting Insecticidal Net

SP

Sulfadoxine-Pyrimethamine

SSA

Sub-Saharan Africa

WHO

World Health Organization

Author contributions

GC, AD, and AHO designed this study. GC, AD, and CS wrote this manuscript. CS and AB conducted laboratory tests. MF digitized the data and created the map of the study area. SE and CA contributed to the execution of this work. All authors reviewed and approved the final manuscript.

Funding

This study was supported by Initiative 5% [19SANIN827].

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Declarations

Ethics approval and consent to participate

Ethical clearance for the study was obtained from the Research Ethics Committee of the Institute of Applied Biomedical Sciences (CER-ISBA: n° 121 of 20 September 2019) which approved the methodology used. All methods were carried out in accordance with guidelines. In this study, no sample was collected from pregnant women. Any LLIN in use by the pregnant woman removed for laboratory testing with her consent was immediately replaced by a new LLIN. Before inclusion, free and informed consent was obtained from each pregnant women after that the study had been presented to them in the local language.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.