Timely Attendance of the First Antenatal Care among Pregnant Women Aged 15–49 Living with HIV in Juba, South Sudan

Timely attendance of the first antenatal care (ANC) is the period in which pregnant women visit ANC less than four months of pregnancy. There is a paucity of data on timely first ANC attendance and its associated factors among pregnant women living with human immunodeficiency virus (HIV) in Juba. The aim of this study was to investigate timely attendance of the first ANC visit among pregnant women living with HIV. Institutional cross-sectional study was conducted in three public health facilities in Juba by convenience sampling from January 2019 to December 2019. Pearson’s chi-squared test was conducted for bivariate analysis and variables with probability values ( p values) less than 5% were considered as statistically significant for multivariable analyses using Fisher’s exact test. At the multivariate level, binary logistic regression analysis was conducted. Out of the 192 participants studied, 27 (14.1%) had timely first ANC attendance as recommended and 165 (85.9%) attended first ANC at four months and above. Distances (adjusted risk ratio [aOR], 7.14; 95% confidence interval [CI], 1.40–36.68), ANC card (aOR, 3.48; 95% CI, 1.17–10.40), waiting time ([aOR], 0.04; 95% CI, 0.01–0.75), and prevention of mother-to-child transmission (PMTCT) services (aOR, 0.12; 95% CI, 0.03–0.56) were the factors associated with timely first ANC attendance. Health education interventions targeting pregnant women attending ANC at health facilities should focus on increasing knowledge and awareness of the importance of timely first ANC attendance.


Introduction
Timely attendance of antenatal care (ANC) is the period in which pregnant women visit ANC less than four months of pregnancy [1]. Timely ANC visit connects pregnant women to the healthcare professionals where they are able to know the status of their pregnancy, estimated gestation age, and expected date of delivery (EDD) [2]. Timely ANC visit is an entry point for pregnant women to receive health education and preventive services such as PMTCT and identify other pregnancy-related complications at an early stage [3]. Timely ANC is very advantageous to pregnant women, and several studies have linked timely ANC attendance to skill birth attendants and increased opportunity of diagnosis and su cient perinatal care [4][5][6].Globally, approximately 830 women die every day from preventable causes related to pregnancy and childbirth of which the sub-Saharan African region accounts for 550 of this death compared with 5 in the developed countries [7]. In 2019, there were 36.8 million people living with HIV globally [8]. Sub-Saharan Africa recorded the highest number of incident cases at 83.3% of the global number of incident cases, 78.5% of the global number of deaths, and 74.1% of the global number of people living with HIV. Regional disparities in HIV incidence and mortality among people aged 15-49 shows that HIV incidence rate was recorded at 218.1 cases per 100,000 people living with HIV and 87.2 deaths per 100,000 people: at the national level, the HIV incidence ranged from 2.8 cases per 100,000 people to 1585.9 cases in Lesotho [9]. Mozambique had the highest HIV incidence with 2805.9 cases per 100,000 people, with HIV mortality of 1163.0 deaths per 100,000 people.
As part of sub-Saharan Africa, South Sudan has been considered among countries with the worst maternal mortality outcome of 789 deaths per 100,000 live births [10].
Studies conducted on timely ANC attendance and its associated factors revealed that the majority of women initiate their first ANC visit after 12 weeks of pregnancy [11,12]. Studies have identify many factors such as maternal age, level of educational, low monthly income level, ANC history, and parity as determinant of timely ANC visits [4,13,14]. In developing countries, a few studies have regarded maternal and husband education level, available ANC services, women's media exposure, obstetric history, and employment as factors affecting timely ANC attendance [12,15,16]. e World Health Organization (WHO) in 2016 promoted the antenatal care model to prevent perinatal death and improve women's experience of health care with a minimum number of eight ANC contact for all pregnant women with the first ANC visit schedule within the first 12 weeks of pregnancy [17].
ough the new WHO 2016 updated ANC visit has been recommend, South Sudan is still using the previous 4 ANC visit recommended by the WHO [18]. ere is scarcity of data on first ANC attendance among pregnant women living with HIV. ere is a paucity of data on timely first ANC attendance and its associated factors among pregnant women living with HIV in Juba. Studies have shown that poor timely attendance of the first ANC is associated with obstetric labor, stillbirth; poor PMTCT, maternal mortality, and increased government health expenditure. is has subsequently contributed to poor health conditions among women. It is from the above background that the study investigated the timely attendance of the first ANC and its associated factors.

Study Area and Period.
is study was conducted in three public health facilities in Juba during the period between January 2019 and December 2019.In Juba there are two public hospitals and numerous health centers.
is study was conducted in three public health facilities that included Juba Teaching Hospital (JTH), Gurie, and Munuki Primary Health Care Centres. ese public health facilities were selected purposively because the provided ANC and integrated HIV services. JTH is a national hospital and the only referral hospital within South Sudan that serves the ten states of South Sudan with a population of 9.8 million people [19]. e hospital has an inpatient and outpatient department that offers curative, preventive, and rehabilitative health services [20]. Gurie  e study participants were selected using convenience sampling technique for interviews based on their arrival time and readiness to consent.

Data Collection Tools and Procedures.
Quantitative data for this study were collected using a pretested structured questionnaire among all eligible pregnant mothers living with HIV who were enrolled in the ANC clinic. e questionnaire was designed in English, and a highly skilled and fluent specialist in Arabic was hired to translate to Arabic language and then back to English for consistency. e study involved three research assistants who were nurses and health educators and who had knowledge on HIV ,ANC and communication skills required for interviewing the respondents. e research assistants recruited were trained on research protocols focusing on key aspects of sampling, storage, handling of data, and ethical considerations. e research tools were pretested on 15% of the sample size and among respondents with similar characteristics as those of actual respondents. Pretest was conducted in a nearby health facility out of the actual population of the study to conform to the principle of validity and reliability of the tools before proceeding with data collection. Before the participant's enrollment, informed consent was obtained (the informed consent form was translated into the local language, Arabic Juba language).

Study Variables.
e outcome variable for this study was "timely attendance of the first ANC" defined as ANC visit within the first 12 weeks of pregnancy. e outcome variable was measured as yes or no using a binary scale. Independent variables in the study that was considered as potential factors to timely first ANC included maternal factors (number of children, ever diagnosed with complication in previous pregnancy, gravida, to acquire ANC card, and to ensure safe delivery) and health facility factors (distance from home to health facility in kilometers, distance affects timely ANC visit, transport cost to health facility in South Sudanese pounds, and waiting time at ANC in hour).

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Data Management and Analysis.
Data entry for this study was conducted by creating a data entry field in EpiData version 3.1 [21], and all categorical responses were put on check to eliminate errors and inconsistent data. Descriptive analysis was conducted for independent variables using frequencies and percentages. Pearson's chi-squared test was conducted for bivariate analysis, and variables with probability values (p values) less than 5% were considered as statistically significant for multivariable analyses using Fisher's exact test. At the multivariate level, binary logistic regression analysis was conducted to determine factors independently associated with the outcome by using the adjusted odds ratio. e variable age in this study was analyzed with mean. e age variable was categorized into groups to determine whether there was a relationship between age group and first ANC attendance.

Ethical Considerations
is study was approved by Clarke International University Research Ethics Committee, CIU-REC (reference # CIU-REC/0137) and an administrative approval from Ministry of Health, South Sudan (MOH/ERB 29/2019). All participants that participated in the study provided written informed consent and were free to withdraw at any stage of the interview if they so wished. Research codes were used instead of the respondent's name to ensure anonymity. Table 1 shows the socio-demographic characteristics of participants. Of the 192 participants, 75 (39.3%) were aged 25 to 29 and the mean age was 27.72 ± 4.49 years. 168 (87.5%) of the participants were married, 55 (28.6%) ended with a secondary level of education, 94 (49.0%) were Catholic, 164 (85.4%) lived in an urban setting, 102 (53.4%) were not employed, and 166 (86.5%) had married an employed spouse. Figure 1 is a bar graph that shows the timely attendance of the first ANC among the 192 participants. e results indicated that 27 (14.1%) participants had attended the first ANC timely.

Bivariate Analysis of Maternal Factors and Timely
Attendance of the First ANC. In Table 3, most participants who had attended the first ANC visits had 2 to 4 children (n � 16, 59.3%), had never been diagnosed with complications from previous pregnancies (n � 24, 88.9%), and were multigravida (n � 134, 81.2%). However, the participants differed on the reasons for starting ANC, namely, PMTCT services (p < 0.001) and acquisition of ANC cared (p < 0.001), as shown in Table 3.

Bivariate Analysis of Health Facility Factors and Timely
Attendance of the First ANC. In Table 4, most participants who had attended the first ANC lived within less than or equal to a 5-kilometer radius to the health facility (n � 20, 74.1%), reported distance had not affected them from attending ANC (n � 25, 92.6%), incurred a transport costs of between 100 and 500 South Sudanese pounds (n � 16, 59.3%), and had waited to receive ANC services for more      Note. ANC, antenatal care: PMTCT, prevention of mother-to-child transmission; n, number of samples.
receiving PMTCT service compared with receiving PMTCT service was associated with lower odds of first ANC attendance (adjusted odds ratio (aOR), 0.12; 95% CI, 0.03-0.56); attendance of timely ANC visits not to receive an ANC card relative to the need to receive an ANC card was associated with increased odds of first ANC visit (aOR, 3.48; 95% CI, 1.17-10.40); participants with distances that had no effect on ANC visit compared to those with distances that had effect on ANC visit had increased odds of first ANC attendance (aOR, 7.14; 95% CI, 1.40-36.68); and waiting at the ANC for 2 to 3 hours compared to 1 hour was associated with lower odds of first ANC visit (aOR, 0.04; 95% CI, 0.01-0.75).

Discussion
ANC is a key health intervention for reducing maternal morbidity and mortality. Considering South Sudan with one of the highest maternal mortality in the world associated with poor access to quality health and reproductive services [22], when ANC is conducted appropriately and timely by pregnant mothers, there is a potential to save lives by identifying and preventing pregnancy-related complications at an early stage and institute proper management [6]. e findings from this study revealed that timely attendance of the first ANC was by far very low (14.1%) in Juba. ese findings show that a substantial proportion (85.9%) of pregnant women are not benefiting from first ANC services as recommended by the WHO [23]. ese findings have important implications on maternal health and the outcome of pregnancy. Studies have shown that when women initiate first ANC visit late, the risk of maternal and neonatal mortality increases, and secondly, it becomes difficult for the health facility to implement ANC strategies effectively [24]. e findings of this study indicate a need for Ministry of Health to design health education interventions targeting pregnant mothers attending ANC at lower health facilities to change their mindset and increase knowledge and awareness on the importance of first ANC visit and its implications. e proportion of pregnant mothers adhering to the first ANC visit in this study is low compared with studies conducted in Pakistan (48%) [25], Ethiopia (35.4%) [26], and Rwanda (25%) [27]. Such a relatively high difference in these studies could be attributed to the socio-demographic characteristics of the study population, level of maternal knowledge on the importance of the first ANC visit, media coverage, and variation in study settings.  Note. * p < 0.05 , * * p < 0.01 , * * * p < 0.001 ; all odds ratios are exponentiated; 95%, unadjusted analysis (uOR), adjusted odds ratio (aOR), confidence interval (CI) for odds ratios are in brackets.
Advances in Public Health is study found that mothers who attended ANC clinics not to receive ANC cards were three times more likely to adhere to the first ANC visits compared to mothers who attended first ANC with the reason of getting ANC cards.
is finding differs from a study conducted in Uganda where pregnant women believed that having ANC cards was a guarantee for health facility delivery and this was the main reason for attending ANC visit [28]. ere is limited literature with regard to the association between first ANC visit and attending first ANC not to receive ANC card in previous studies. In this study, it could be attributed that pregnant mothers had poor knowledge on the importance of services such as receiving ANC cards during the first visit; furthermore, for these mothers, attending health services was not related to ANC cards, probably these mothers might have been aware of their HIV status. As a result, they were more concern with getting other health services such as antiretrovirals(ARVs); rather than ANC card, more ever women who even come after six months of pregnancy were given ANC card by the health facilities. ese findings suggest health promotion and education activities targeted at increasing maternal knowledge on the benefits of first ANC visit should be paramount.
In this study, the fact that distance was instrumental in affecting ANC visits among the respondents is worth noting. Pregnant mothers who reported having no effect of distance were almost eight times more likely to initiate first ANC within the first 12 weeks of pregnancy. is finding is supported by previous studies conducted in Cameroon [29], Ethiopia [13], and Uganda [30] where a positive association between distance to the health facilities and initiation of first ANC visit was found among pregnant women who lived within a shorter distance and travelled less than 30 minutes to one hour. is finding is supported by the fact that the longer the distance from home to the nearest health facility, the poor the utilization of healthcare services. is could be because distance affects the utilization of healthcare services in terms of cost of transport from one point to another, and distance limits easy access to such services. Furthermore, in this study the positive association between distance and timely attendance of the first ANC can be supported by the fact that the majority of the respondents lived in urban areas where these facilities were located within a distance of 5 km with a transport fare ranging between 100 and 500 South Sudanese pounds (SSP) that could be afforded by the majority of mothers. ese findings suggest that the Ministry of Health should design and implement policies that ensure the introduction of equitable, effective, and efficient healthcare delivery services closer to mothers, and hence, travel distances from home to the nearest health facility will be reduced.
In this study, pregnant women living with HIV who attended ANC clinics not to receive PMTCT services were less likely to adhere to the first ANC visits. Rigorous searches have been conducted on previous literature; however, no substantial studies have been found that explains the significant relationship between first ANC and PMTCT service uptake among pregnant women living with HIV. However, a few studies cited poor maternal knowledge and awareness, stigma, and discrimination as barriers of PMTCT utilization during ANC visit [31]. Another study cited confidentiality, dissatisfaction with health worker, and poor support from male partners [32]. In this study, poor utilization of PMTCT can be attributed to the HIV status of the mothers with majority (81.2%) being multigravida with parity of 2-4 (55.8%), and these mothers might be relying on their previous experience. Secondly, these findings suggested that mothers were already aware of their HIV status and they might have been receiving PMTCT services from other health facilities where they were comfortable; hence, they were attending ANC clinic only for routine follow-up and checking the status of pregnancy.
Waiting time before being attended by a healthcare worker acted as a serious barrier to first ANC utilization. Mothers who reported a waiting time of 2-3 hours were less likely to achieve the recommended timing of the first ANC visit. Findings from other studies found waiting time as a negative barrier for ANC utilization [33][34][35][36]. In Mozambique, client at the health facility added that waiting time acted as a barrier for seeking multiple ANC visits as well as increasing their direct cost through purchasing of food or packing food from home [37].
Waiting time of about 2-3 hours could be attributed to the fact that ANC service only begins after health education sessions have been conducted to a sizable number of pregnant mothers; as a result, mothers who reported earlier had to wait until a reasonable number of women are present in the health facility. is results in clients spending long hours in the health facility during ANC visit; hence, reducing the chances of the first ANC visit, pregnant mothers would rather attain to others household chores, then spending longer hours at the health facility. From a prospective of service delivery, this study suggests that ANC clinic should address waiting time at the facility by scheduling different ANC interventions.

Study Strengths and Limitations.
Considering the importance of first ANC visit, this study is one of the few and the first studies to investigate the timely attendance of a first ANC visit among pregnant women living with HIV. e findings of this study will be a good source of reference for other upcoming studies and will inform policies that may lead to policy formulation and implementation. However, the study had a number of limitations that might have affected the results. e data collected were self-reported by the respondents; as a result, there might have been recall bias on the exact weeks of pregnancy during the first ANC visit, which might have affected the result of the study. Lastly, this study was conducted at a point in time during pregnancy, so the pregnancy outcome could not be determined by the study.

Conclusion
Timely attendance of the first ANC in this study was low (14.1%). Distance to the health facilities and attending ANC not to receive ANC cards were positive influencers of timely 6 Advances in Public Health first ANC visit. Waiting time for 2-3 hours at the health facility and attending ANC not to receive PMTCT services were negatively associated with a timely first ANC visit. Ministry of Health should upgrade the timing of first ANC booking based on WHO 2016 recommendations. e low coverage of first ANC visit calls for a need to improve health education interventions targeting pregnant mothers attending ANC at the health facilities and communities with focus on increasing knowledge and awareness of the importance of timely attendance of the first ANC. e study recommends further qualitative study to explore the reasons for low timing of first ANC.

Abbreviation
ANC: Antenatal care HIV: Human immunodeficiency virus PMTCT: Prevention of mother-to-child transmission PHCC: Primary healthcare unit WHO: World Health Organization.
Data Availability e dataset used or analyzed for this manuscript is available in excel sheet that can be found by requesting the corresponding author.

Conflicts of Interest
e authors declare that they have no conflicts of interest.