Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-15T12:27:19.128Z Has data issue: false hasContentIssue false

Adequacy of antenatal care services utilisation and its effect on anaemia in pregnancy

Published online by Cambridge University Press:  21 September 2022

Ferguson Saapiire*
Affiliation:
Ministry of Health, St. Joseph Nursing Training College, Jirapa, Ghana
Richard Dogoli
Affiliation:
Jhpiego Ghana, PMB 18, Legon Accra, Ghana
Saaka Mahama
Affiliation:
Department of Nutritional Sciences, University for Development Studies, Tamale, Ghana
*
*Corresponding author: Ferguson Saapiire, email saapiireferguson@yahoo.com

Abstract

Anaemia in pregnancy remains a critical public health concern in many countries including Ghana and it poses severe consequences in the short to long-term for women and their unborn babies. Although antenatal care (ANC) is largely provided for pregnant women, the extent its utilisation protects against anaemia in pregnancy remains largely understudied. The study assessed the adequacy of ANC services utilisation and its effect on anaemia among pregnant women in the Wa Municipality of Ghana. A facility-based cross-sectional survey was conducted. Probability proportionate to size sampling and systematic random sampling were used to select the facilities and 353 respondents. While 80⋅2 % of the pregnant women reported having received a sufficient number of ANC services provided, the prevalence of the overall ANC adequacy was only 44⋅2 %. After adjusting for potential confounders, pregnant women who could not achieve adequate ANC attendance were 2⋅3 times more likely to be anaemic in the third trimester of gestation AOR = 2⋅26 (95 % CI 1⋅05, 4⋅89), compared to their counterparts who maintained adequate ANC attendance. Adequate ANC attendance was a consistent and significant predictor of anaemia in pregnancy in the third trimester. Health and nutrition education on the need for early initiation of ANC attendance and support for the consumption of diversified diets are two possible interventions that can help contain anaemia in pregnancy.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

Introduction

Maternal anaemia remains a serious global public health threat that affects over 38 % of pregnant women globally with 18 % in high-income countries and 35–75 % in low- and middle-income countries(1). The World Health Organization (WHO) defines pregnancy anaemia as those expectant mothers with haemogloblin (Hb) concentration lesser than 11⋅0 g per deciliter when at sea level or when the total volume ratios of the red blood cells to blood is less than 33⋅0 %, irrespective of gestation(Reference Benoist, McLean and Egll2,3) .

According to the Ghana Demographic Health Survey, anaemia prevalence among pregnant women in Ghana was 45 % which has not seen much improvement over the years(4). In the Wa Municipality of Ghana where the present study was conducted, the prevalence of anaemia at 36 weeks gestation in 2016 was 35⋅4 %(5).

Anaemia in pregnancy account for 20 % of maternal mortality worldwide(1) and it is a major nutritional disorder that poses severe consequences in the short to long-term for women and their unborn babies(Reference Zerfu, Umeta and Baye6). It has been established from several studies that anaemic expectant women stand a higher chance of having premature births and delivery of low-birth-weight babies and preterm delivery(Reference Figueiredo, Gomes-Filho and Silva7Reference Allen9).

The major determinant of pregnancy anaemia worldwide is known to be iron deficiency(Reference Stevens, Finucane and De-Regil10). However, poor antenatal care (ANC) quality and nutrition might also possibly explain the observed high prevalence of anaemia during pregnancy(Reference Obai, Odongo and Wanyama11) especially in developing countries(12). There has been an increase in the utilisation of antenatal services in low- and middle-income countries (LMICs) following the WHO recommended focused antenatal care (FANC) practice. FANC involves client-centered individualised care, disease detection and care by a skilled provider(13).

Despite the general increase in the frequency of ANC attendance, timely initiation remains problematic in many settings. In Northern Ghana, a study reported that although 75⋅0 % of pregnant women made at least four ANC visits in their last pregnancy, late initiation of ANC services was widespread(Reference Gudu and Addo14). Poor quality and inadequate ANC visits during pregnancy can increase the risk of anaemia. This is because, timely initiation and regular ANC visits give health personnel an opportunity to provide a variety of services including prophylaxis and micronutrient supplementation(Reference Simkhada, van Teijlingen and Porter15,Reference Magadi and Madise16) , which are preventative measures against anaemia. It has also been established that a combination of interventions may yield a stronger effect compared to one type of intervention(17). ANC, therefore, presents a unique opportunity for the prevention and management of concurrent diseases through integrated service delivery(18).

The persistent high prevalence of anaemia in many settings suggests that the most important risk factors have not been addressed yet and so many healthcare systems continue to seek for appropriate and effective measures to manage this situation. One of such measures is the promotion of ANC which serves as a platform for the delivery of protective health and nutrition interventions during pregnancy. Even though timely initiation and frequent ANC attendance as recommended by the WHO are the major strategies available to improve maternal health outcomes, limited evidence exists on the independent contribution of adequate ANC in protecting against pregnancy anaemia. The study assessed the adequacy of ANC services utilisation and its effect on anaemia among pregnant women in the Wa Municipality of Ghana.

Materials and methods

Study area

Wa Municipality is sited in the northern savannah part of Ghana between Latitudes 8°30″–10° N and Longitude 0°30″–2°30″W but lies in the Southwestern part of the Region between Longitudes 9°32″W and 10°20″W and Latitudes 1°40″N and 2°45″N. The Wa Municipality is subdivided into six (6) sub-municipals with a total of twenty-six government health facilities including community-based health planning and services (CHPS) and four private facilities(19). However, data from 2017 showed the total number of health facilities in the Municipality to be forty-five(5).

The Wa Municipal has 132 communities with one paramountcy, four area councils and one urban council(20). The municipality has an estimated total land area of 579⋅86 km2 and a projected population of 107 214 comprising of 52 996 males and 54 218 females.

Study design, study population and sampling

A facility-based cross-sectional survey was conducted. The study population comprised all women who had attended ANC in the municipality, delivered within the past 12 months preceding the study in a health facility and possessed a maternal health records booklet for the index pregnancy.

The minimum sample size was calculated using single population proportion formula:

$$n = \displaystyle{{t^2 \times p( {1-p} ) } \over {m^2}}$$

where n is the required sample size, t is the confidence level at 95 %, P represents the population proportion of anaemia (35⋅6 %)(21) and m is the margin of error at 5 %. Considering a 2 % contingency to take care of incomplete/damaged questionnaires, a total of 353 mothers were required for the study.

Health facilities for the study were selected from all six sub-districts in the Wa Municipality using probability proportionate to size sampling technique based on the total ANC registrants.

The study participants were selected using systematic random sampling to draw respondents from ANC registers. Women were excluded if they were referred from other district's ANC facilities but came to deliver in the Wa Municipality or attended ANC elsewhere for the most part of their pregnancy. Women without maternal health records or booklet for their index pregnancy were also excluded.

Data collection methods

A pre-tested structured questionnaire was used to collect information on socio-demographic characteristics, maternal behaviours and health status during last pregnancy, household wealth index, gravidity and parity. Information extracted from the ANC booklet included timing of ANC initiation, gestational age and Hb concentration levels.

Data for the present study were collected in 2019 by trained nurses and midwives with a minimum qualification of Diploma. ANC registers were major sources of data. Permission was granted by the health authorities of the institutions to have access to the ANC registers where data were extracted.

Measurement of independent and dependent variables

The main outcome (dependent) variable of interest was anaemia in the third trimester of pregnancy. The WHO's definition and categorisation were applied whereby women with haemoglobin (Hb) concentration levels more than or equal to 11 and <11 g/dl were classified as ‘not anaemic’ and ‘anaemic’, respectively(Reference Benoist, McLean and Egll2).

The Hb levels were determined using a portable HemoCue301 photometer. Trained laboratory technicians drew capillary blood samples from the finger prick with a lancet after taking all aseptic precautions. The first drop of blood was wiped away using alcohol sterile wipes, and the next drop was placed into the HemoCue cuvette for immediate testing of Hb.

The main exposure variable was the adequacy of ANC utilisation which was measured using a modified version of the adequacy of prenatal care utilisation (APNCU) index(Reference Kotelchuck22). The APNCU index is used for precise and comprehensive measurement of prenatal care(Reference Sahu and Mishra23). To be considered having adequate ANC attendance, a mother must have initiated ANC before gestational age (GA) week 12, and subsequent visits must be attended at recommended intervals throughout the pregnancy. The ultrasound technology was used to determine gestational age on first booking at the ANC. In the absence of ultrasound facility, gestational age was assessed using the last menstrual period (LMP) approach.

The WHO recommends at least four antenatal visits to healthcare facility during pregnancy(20). Adequacy of ANC attendance in this study was therefore measured as having made the first visit in the first trimester of pregnancy and attended ANC at least four times during pregnancy.

To assess ANC service content, participants were asked about the basic ANC services received as recommended by the WHO for all pregnant women at the first visit to ANC clinics(24).

The content of ANC services received during antenatal period was assessed included height and weight measurements, blood pressure and blood sugar, deworming, toxoid immunisation, malaria testing and treatment, health and nutrition education, blood and urine testing, iron and folic acid supplementation. A score of ‘1’ was assigned to receiving any of the services and ‘0’ for non-receipt. The total score for each respondent was categorised as low, if that score was below the median score and high, if it was at least the median score.

Another important exposure variable measured was a composite indicator that reflects an overall ANC adequacy. This was constructed using the three ANC utilisation indicators (that is, first ANC visit made during first trimester, making at least four ANC visits and receipt of adequate ANC core services(24). Thus, a woman was classified as having adequate overall ANC, if the woman had attended prenatal care early plus enough visits and sufficient services; otherwise, she was classified as having inadequate ANC.

Based on the literature, the other potential predictor/covariate variables included were socio-demographic factors such as age, maternal education, occupation, marital status, religion, whether the women received health and nutrition education, child vaccinations and immunisations, the number of tetanus toxoid (TT) and sulphadoxine pyrimethamine (SP) received, household wealth index, as well as maternal dietary intake. Details of some of these variables are given below:

The minimum dietary diversity for women (MDD-W) was used as measure of overall dietary quality since it has been shown to indicate adequate nutrient intake and can be used as a proxy indicator for measuring nutrient adequacy among pregnant women(Reference Martin-Prével, Allemand, Wiesmann, Arimond, Ballard and Deitchler25,26) . The dietary assessment was made by asking the women to recall all foods and drinks consumed in the past 24 h prior to the study(26).

The women's dietary diversity scores (WDDSs) were calculated by adding the values of all the food groups consumed by each participant. The ten food groups used to calculate WDDS were starchy staple foods, beans, peas, nuts, seeds, dairy, flesh foods, eggs, vitamin A-rich dark green leafy vegetables, other vitamin A-rich vegetables and fruits, other vegetables, and other fruits.

The consumption of a food item from any of the groups was assigned a score of ‘1’ and a score of ‘0’ if the food was not consumed. The WDDSs were used to categorise the women into high (WDDS ≥ 5) and low (WDDS < 5).

Also assessed was the household wealth index, which is a proxy indicator for socio-economic status (SES) of households. The principal component analysis (PCA) was used to quantify it from information collected on household assets and housing quality (floor, walls and roof material), source of drinking water, type of toilet facility, the presence of electricity, type of cooking fuel and ownership of modern household durable goods and livestock (e.g. bicycle, television, radio, motorcycle, sewing machine, telephone, cars, refrigerator, mattress, bed, computer and mobile phone)(Reference Vyas and Kumaranayake27Reference Howe, Hargreaves and Huttly30).

Statistical data analysis

The data were cleaned and coded for analysis using the Statistical Package for Social Science (SPSS) version 22 (SPSS Inc, Chicago). Data were cleaned by running preliminary frequencies of all the variables to check for entry inaccuracies. All incorrectly coded data were double-checked with the questionnaire after which all wrong entries were corrected.

Bivariate analysis was performed using Chi-square test of independence to assess the association between the dependent variable anaemia, and categorical independent variables. The variables in the bivariate analysis with P < 0⋅10 were included in the multivariable binary logistic regression to control for possible confounding and the independent effect of each independent variable on the outcome variable. Forward stepwise LR (likely hood ratio) method was used for entering variables.

The adjusted odds ratio (AOR) and 95 % confidence intervals were used to assess the strength of association at P-value < 0⋅05.

Multicollinearity was checked using variance inflation factor (VIF) and no collinearity existed between the independent variables.

Ethics consideration

The study protocol was approved by the School of Allied Health Sciences, University for Development Studies, Ghana. Ethical approval was obtained from the Kwame Nkrumah University of Science and Technology ethics committee (Reference no. CHRPE/AP/472/21). Permission was also granted by the Regional Health Directorate and District Director for Health Services of Wa Municipal to carry out the survey. Informed consent was obtained from the study participants prior to data collection. Confidentiality and anonymity of the study participants was also maintained by using identity numbers on the questionnaires other than participant's names.

Results

Socio-demographic characteristics of respondents

Out of a total of 353 study respondents, an overwhelming majority (85⋅0 %) were Waala/Dagaaba tribe. The predominant religion was Islam (84⋅4 %). In terms of marital status, almost all the respondents (91⋅2 %) were duly married. More than a third of the study participants (36⋅3 %) never had any formal education while (23⋅8 %) were able to attain at least a second cycle education (senior high and tertiary levels). It was also observed that about 38⋅0 % of the respondents were unemployed and a few on apprenticeship in various vocations including hairdressing, dressmaking or weaving. Aside 8⋅2 % that were engaged as government/private employees, 53⋅8 % were into self-occupation either as a farmer or as a trader in cooking/brewing and selling, buying and selling of commodities. With regard to household wealth index, 56⋅1 % of the respondents were above the median (Table 1).

Table 1. Socio-demographic characteristics of the respondents (N = 353)

Content of ANC services received during antenatal period

In the study sample, majority (60⋅3 %) had adequate requisite information. Most of the women (73⋅1 %) received less than two doses of tetanus toxoid (TT) for their most recent pregnancy. For sulphadoxine pyrimethamine (SP) intake, a vast majority of the women (82⋅4 %) had received at least two doses as stipulated by WHO for the minimum protection prophylaxis against malaria (Table 2).

Table 2. Content of ANC services received during antenatal period

Utilisation of antenatal care services

Adequacy of ANC attendance as measured by at least four ANC visits during pregnancy and making the first visit in the first trimester of pregnancy was low at 49⋅9 %.

More than half (51⋅3 %) of the ANC attendees-initiated ANC attendance in the first trimester of pregnancy and 80⋅7 % of the women had four or more ANC visits during the last pregnancy as recommended by the WHO. While 80⋅2 % of the pregnant women reported having received a sufficient number of ANC services provided, the prevalence of the overall ANC adequacy was only 44⋅2 % (Table 3).

Table 3. Utilisation of antenatal care services (N = 353)

Relationship between anaemia in the third trimester of pregnancy and selected factors

Table 4 shows the relationship between selected factors including the three main components of adequacy of ANC services utilisation and anaemia (Hb less than 11 g/dl) at 36 weeks of gestation. Adequacy of ANC attendance negatively associated with the prevalence of anaemia but the number of ANC services received (content) did not associate significantly with anaemia in the third trimester.

Table 4. Relationship between anaemia in the third trimester of pregnancy and selected factors (bivariate analysis)

Predictors of anaemia in the third trimester of pregnancy

After adjusting for potential confounders, adequacy of ANC attendance was a consistent significant predictor of anaemia in the third trimester (Table 5). Pregnant women who could not achieve adequate ANC attendance were 2⋅3 times more likely to be anaemic in the third trimester of pregnancy AOR = 2⋅26 (95 % CI 1⋅05, 4⋅89), compared with their counterparts who maintained adequate ANC attendance.

Table 5. Predictors of anaemia at 36 weeks of gestation among pregnant women (multiple logistics regression)

The potential confounding variables adjusted for included age of mother, gravidity, maternal educational level, early pregnancy BMI, weight gain during pregnancy, place of residence, the number of ANC services received (content), household wealth index, women's dietary diversity score (WDDS), whether anaemic in early pregnancy and gestational age at first ANC visit.

Lower BMI in early pregnancy was associated with 1⋅2-fold increase in the odds of anaemia, AOR = 1⋅16 (95 % CI 1⋅08, 1⋅25) whereas a unit increase in gestational weight gain led to 12 % protection against anaemia AOR = 0⋅88 (95 % CI 0⋅08, 0⋅95). A unit increase in women's dietary diversity score (WDDS) was associated with 56 % protection against anaemia AOR = 0⋅44 (95 % CI 0⋅25, 0⋅79). Women resident in the rural areas were 2⋅1 times more likely of being anaemic in the third trimester, compared with their counterparts in the urban settings AOR = 2⋅09 (95 % CI 1⋅19, 3⋅69).

The set of factors accounted for 23⋅7 % of the variance in anaemia at 36 weeks gestation (Nagelkerke R square = 0⋅237).

Discussion

The study assessed the adequacy of ANC services utilisation and its effect on anaemia among pregnant women in Ghana. The key finding was that adequacy of ANC attendance was low at 49⋅9 %. Pregnant women who could not achieve adequate ANC attendance were 2⋅3 times more likely to be anaemic in the third trimester of pregnancy compared with their counterparts who maintained adequate ANC attendance.

Adequacy of prenatal care services utilisation

The adequacy of ANC attendance as measured by at least four ANC visits during pregnancy and making the first visit in the first trimester of pregnancy was low at 49⋅9 %. Though more than 80 % of the pregnant women had four or more ANC visits during the last pregnancy, only 51⋅3 % of them initiated ANC attendance in the first trimester of pregnancy. At least 80 % of the women received sufficient ANC services but the overall ANC adequacy was only 44⋅2 %. As pointed out by Sumankuuro and colleagues, the barriers for adequate utilisation of ANC services include long distance to ANC facilities, transport difficulties, cultural influence and social reasons(Reference Sumankuuro, Crockett and Wang31). Several other studies have reported that in some cases, women might just not feel the need to seek professional care when there is nothing wrong with their pregnancy(Reference Atuyambe, Mirembe and Annika32Reference Mrisho, Obrist and Schellenberg34).

In order to derive maximum benefits from ANC services, it is critically important that every pregnant woman makes the first ANC visit during the first 3 months of pregnancy (timeliness), achieving a minimum of four, most recently at least eight contacts for ANC (frequency) and adequate services (ANC content)(Reference Tuncalp, Pena-Rosas and Lawrie35,36) . Generally, the content, timing and frequency of ANC services are inadequate in low- and middle-income countries (LMICs)(Reference Austin, Langer and Salam37Reference Smith, Portela and Marston39). In our sample, the late initiation of ANC attendance appears to be a major limitation to attaining the overall ANC adequacy. The focused ANC model recommends a minimum of four prenatal care visits and content of the packages that comprise physical examinations, laboratory investigations, preventive procedures and counselling on signs of pregnancy complications and measures to be taken by the mother(40). As observed in our study sample, the timely initiation of ANC should be a focus to reap the desired effect of ANC services since the other pre-requisites were met by most pregnant women.

Relationship between ANC services utilisation and pregnancy anaemia in the third trimester

After adjusting for potential confounders, inadequate ANC attendance positively associated with the prevalence of anaemia in the third trimesters. This finding is consistent with some studies(Reference Nonterah, Adomolga and Yidana41,Reference Stephen, Mgongo and Hussein Hashim42) . This finding may be explained by the fact that women who initiate ANC late in either the second or third trimester will definitely miss many of the interventions and services routinely offered to pregnant women at ANC clinics to prevent anaemia in pregnancy. Some of these routine preventive measures include iron-folic acid (IFA) supplementation, provision of long-lasting insecticide nets (LLINs) and sulphadoxine pyrimethamine (SP) dosing, as well as laboratory investigations to diagnose early anaemia in pregnancy. Indeed, early initiation of ANC is critical in preventing anaemia in pregnancy and other pregnancy outcomes. In particular, mothers with early signs of pregnancy anaemia who seek ANC services in the first trimester will be timely managed(Reference Gravett, Gravett and Martin43,Reference Satti, Motsamai and Chetane44) . This points to the urgent need for both health facility and community-based interventions to educate women and community members on the importance of early ANC initiation.

From our results, both timing and frequency of ANC attendance associated negatively with anaemia but the sufficiency of ANC services received did not. The lack of association between ANC services and anaemia may possibly be due to the limited variability of services among the study participants. When the content of ANC services provided to groups of women does not vary very much, it is the adequacy of ANC attendance that makes the difference. A woman who timely and frequently utilise ANC will benefit more from whatever quality services that are provided.

Other significant predictors of anaemia in the third trimester were early pregnancy BMI, weight gain during pregnancy, dietary diversity score and rural residence. These factors should also be considered when planning for interventions to improve the anaemia in pregnant women. For example, nutrition education on the consumption of diversified and iron-enriched foods during pregnancy should routinely be delivered in all ANC clinics.

Pregnant women who reported of high dietary diversity scores had 56 % protection against anaemia, compared with those with a low dietary diversity score. This finding is consistent with other studies(Reference Teshome, Meskel and Wondafrash45,Reference Tadesse, Seid and Mariam46) . Pregnant women on diversified diets are more likely to meet their micronutrients requirements such as iron, vitamin A and vitamin C all of which are necessary for blood formation. Improved consumption of iron-rich foods before and during pregnancy can therefore prevent anaemia. Unfortunately, foods of pregnant women in less developed countries are mostly carbohydrate-based with very little of micronutrient-rich vegetables, fruits and animal source foods(Reference Darnton-Hill and Mkparu47,Reference Lee, Talegawkar and Merialdi48) . The literature has it that the prevalence of anaemia is highest in the third trimester of pregnancy(Reference Tadesse, Seid and Mariam46,Reference Karaoglu, Pehlivan and Egri49Reference Dim and Onah51) because of the high nutrient requirement for the growing foetus which will reduce the maternal iron reserves. This problem can be minimised through dietary diversification.

Pregnant women living in a rural area were two times more likely to be anaemic than those who live in urban areas. This is consistent with a number of studies(Reference Teshome, Meskel and Wondafrash45,Reference Ebuy, Alemayehu and Mitiku52) and the relative high prevalence of anaemia in the rural areas might be due to several factors including socio-economic deprivations, cultural differences and a lack of information about adequate nutrition(Reference Grum, Brhane and Hintsa53).

In our study sample, lower BMI in early pregnancy was positively associated with increased risk of anaemia in the third trimester. This finding is consistent with a study that assessed the association between early pregnancy BMI and anaemia at first ANC visit in Indonesian and Ghanaian women which showed that higher BMI in early pregnancy associated with higher haemoglobin levels at antenatal booking and with a reduced risk of anaemia(Reference Mocking, Savitri and Uiterwaal54).

Several other studies have earlier reported that low BMI in pre- or early pregnancy increases the risk of anaemia(Reference Gedefaw, Ayele and Asres55Reference Agrawal and Singh58). Low early pregnancy BMI may be due to poor diets that lack various micronutrients that are essential for haematopoiesis(Reference Balarajan, Ramakrishnan and Özaltin59). Additionally, low BMI could result from chronic illness or parasitic infections such as malaria, which can cause anaemia(Reference Gedefaw, Ayele and Asres55,Reference Sifakis and Pharmakides60) .

Conclusion

While 80⋅2 % of the pregnant women reported having received a sufficient number of ANC services provided, the prevalence of the overall ANC adequacy was only 44⋅2 %. After adjusting for potential confounders, adequate ANC attendance was a consistent and significant predictor of anaemia in pregnancy in the third trimester. Health and nutrition education on the need for early initiation of ANC attendance and support for the consumption of diversified diets are two possible interventions that can help contain anaemia in pregnancy.

Acknowledgements

The authors wish to thank their research assistants for their committed work. Our sincerest thanks goes to Ghana Health Service (the regional director, District Directors and sub-municipal In-charges) and the community leaders for the permission to carry out the present study.

S. F., D. R. and M. S. conceived, planned and designed the study. M. S. drafted and wrote the manuscript. All authors contributed to the data interpretation, critical revision of the manuscript, read and approved the final manuscript.

No funding of any sort was received for the execution of the study.

All authors declare that they have no conflict of interests.

Relevant data has been added in the manuscript from which all logical conclusions were driven. Do not hesitate to contact the corresponding author for the dataset.

The scientific review committee of the University for Development Studies approved the study protocol.

The participated youth were asked to duly sign a consent form after obtaining the informed concern from them during the administration of the instrument. The purpose of the study was explained to them. Youth were assured of confidentiality of their information and they were also made to understand that participation was voluntarily and respondents could opt out at any stage of the study.

References

WHO (2020) Global Anaemia Reduction Efforts Among Women of Reproductive Age: Impact, Achievement of Targets and the Way Forward for Optimizing Efforts. Geneva: World Health Organization.Google Scholar
Benoist, BD, McLean, E, Egll, I, et al. (2008) Worldwide Prevalence of Anemia 1993–2005: WHO Global Database on Anemia. Geneva: World Health Organization.Google Scholar
WHO (2011) Hemoglobin Concentrations for the Diagnosis of Anemia and Assessment of Severity. Geneva: World Health Organization. (WHO/NMH/NHD/MNM/11.1) 2011. https://www.who.int/vmnis/indicators/haemoglobin.pdf :Google Scholar
Ghana Statistical Service (GSS), Ghana Health Service (GHS), ICF International (2015) Ghana Demographic and Health Survey 2014. Rockville, MD, USA: GSS, GHS, and ICF International.Google Scholar
Upper West Regional Health Directorate (2016) Annual Health Report for the Upper West Region. Wa, Ghana: Ghana Health Service.Google Scholar
Zerfu, TA, Umeta, M & Baye, K (2016) Dietary diversity during pregnancy is associated with reduced risk of maternal anemia, preterm delivery, and low birth weight in a prospective cohort study in rural Ethiopia. Am J Clin Nutr 103, 14821488.CrossRefGoogle Scholar
Figueiredo, ACMG, Gomes-Filho, IS, Silva, RB, et al. (2018) Maternal anemia and low birth weight: a systematic review and meta-analysis. Nutrients 10, 601.CrossRefGoogle ScholarPubMed
Rahman, MM, Abe, SK, Rahman, MS, et al. (2016) Maternal anemia and risk of adverse birth and health outcomes in low-and middle-income countries: systematic review and meta-analysis. Am J Clin Nutr 103, 495504.CrossRefGoogle ScholarPubMed
Allen, LH (2000) Anemia and iron deficiency: effects on pregnancy outcome. Am J Clin Nutr 71, 1280S1284S.CrossRefGoogle ScholarPubMed
Stevens, GA, Finucane, MM, De-Regil, LM, et al. (2013) Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995–2011: a systematic analysis of population-representative data. Lancet Glob Health 1, e16e25.CrossRefGoogle ScholarPubMed
Obai, G, Odongo, P & Wanyama, R (2016) Prevalence of anaemia and associated risk factors among pregnant women attending antenatal care in Gulu and Hoima regional hospitals in Uganda: a cross sectional study. BMC Pregnancy Childbirth 16, 76.CrossRefGoogle ScholarPubMed
WHO (2001) WHO | Archived: Iron Deficiency Anaemia: Assessment, Prevention and Control - A Guide for Programme Managers. Geneva: World Health Organization.Google Scholar
World Health Organization (2002) WHO Antenatal Care Randomized Trial: Manual for the Implementation of the new Model. Geneva: WHO.Google Scholar
Gudu, W & Addo, B (2017) Factors associated with utilization of skilled service delivery among women in rural northern Ghana: a cross sectional study. BMC Pregnancy Childbirth 17, 159.CrossRefGoogle ScholarPubMed
Simkhada, B, van Teijlingen, ER, Porter, M, et al. (2008) Factors affecting the utilization of antenatal care in developing countries: systematic review of the literature. J Adv Nurs 61, 244260.CrossRefGoogle ScholarPubMed
Magadi, MA & Madise, NJ (2000) Frequency and timing of antenatal care in Kenya: explaining the variations between women of different communities. Soc Sci Med 51, 551561.CrossRefGoogle ScholarPubMed
(2015) Health System and Community Level Interventions for Improving Antenatal Care Coverage and Health Outcomes [Database on the Internet]. Science and Education.Google Scholar
WHO (2009) WHO Recommended Interventions for Improving Maternal and Newborn: Integrated Management of Pregnancy and Childbirth (IMPAC) Clinical Guidelines. Geneva, Switzerland: World Health Organization. Contract No.: WHO/MPS/07.05.Google Scholar
Wa Municipal Health Directorate (2014) Annual Performance Report of Wa Municipality. Wa: Ghana Health Service.Google Scholar
WHO (2016) WHO Recommendations on Antenatal Care for A Positive Pregnancy Experience. Geneva, Switzerland: WHO.Google Scholar
SPRING, Ghana Health Service (2016) Ghana: Landscape Analysis of Anemia and Anemia Programming. Arlington, VA: Strengthening Partnerships, Results, and Innovations in Nutrition Globally (SPRING) Project.Google Scholar
Kotelchuck, M (1994) An evaluation of the Kessner adequacy of prenatal care index and a proposed adequacy of prenatal care utilization index. Am J Public Health 84, 14141420.CrossRefGoogle Scholar
Sahu, JP & Mishra, N (2017) Correlations of APNCU index and fetomaternal out come in tribal area of Chhattisgarh. Int J Multidiscip Curr Res 5, 320324.Google Scholar
WHO (2002) WHO Antenatal Care Randomized Trial. Manual for the Implementation of the New Model. Geneva: World Health Organization.Google Scholar
Martin-Prével, Y, Allemand, P, Wiesmann, D, Arimond, M, Ballard, T, Deitchler, M, et al. Moving Forward on Choosing a Standard Operational Indicator of Women's Dietary Diversity. Rome, Italy: Food and Agriculture Organisation of the United Nations; 2015.Google Scholar
FAO, FHI 360 (2016) Minimum Dietary Diversity for Women: A Guide for Measurement. Rome: FAO.Google Scholar
Vyas, S & Kumaranayake, L (2006) Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan 21, 459468.CrossRefGoogle ScholarPubMed
Filmer, D & Pritchett, LH (2001) Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography 38, 115132.Google ScholarPubMed
Rutstein, SO & Johnson, K (2004) DHS Comparative Reports 6: The DHS Wealth Index. Calverton, MD, USA: ORC Macro, MEASURE DHS.Google Scholar
Howe, LD, Hargreaves, JR & Huttly, SRA (2008) Issues in the construction of wealth indices for the measurement of socio-economic position in low-income countries. Emerg Themes Epidemiol 5, 3.CrossRefGoogle ScholarPubMed
Sumankuuro, J, Crockett, J & Wang, S (2017) The use of antenatal care in two rural districts of upper west region, Ghana. PLoS ONE 12, e0185537.CrossRefGoogle ScholarPubMed
Atuyambe, L, Mirembe, F, Annika, J, et al. (2009) Seeking safety and empathy: adolescent health seeking behavior during pregnancy and early motherhood in central Uganda. J Adolesc 32, 781796.CrossRefGoogle ScholarPubMed
Chapman, RR (2003) Endangering safe motherhood in Mozambique: prenatal care as pregnancy risk. Soc Sci Med 57, 355374.CrossRefGoogle ScholarPubMed
Mrisho, M, Obrist, B, Schellenberg, JA, et al. (2009) The use of antenatal and postnatal care: perspectives and experiences of women and health care providers in rural southern Tanzania. BMC Pregnancy Childbirth 9, 10.CrossRefGoogle Scholar
Tuncalp, Ӧ, Pena-Rosas, JP, Lawrie, T, et al. (2017) WHO recommendations on antenatal care for a positive pregnancy experience—going beyond survival. BJOG 124, 860862.CrossRefGoogle ScholarPubMed
WHO (2018) WHO Recommendations on Antenatal Care for a Positive Pregnancy Experience: Summary of Highlights and Key Messages from the World Health Organization's 2016 Global Recommendations for Routine Antenatal Care. Geneva, Switzerland: World Health Organization.Google Scholar
Austin, A, Langer, A, Salam, RA, et al. (2014) Approaches to improve the quality of maternal and newborn health care: an overview of the evidence. Reprod Health 11, 1.CrossRefGoogle Scholar
Benova, L, Tunçalp, Ö, Moran, AC, et al. (2018) Not just a number: examining coverage and content of antenatal care in low-income and middle-income countries. BMJ Global Health 3, e000779.Google ScholarPubMed
Smith, HJ, Portela, AG & Marston, C (2017) Improving implementation of health promotion interventions for maternal and newborn health. BMC Pregnancy Childbirth 17, 280.CrossRefGoogle ScholarPubMed
WHO (2016) World Health Statistics 2016: Monitoring Health for the SDGs, Sustainable Development Goals. Geneva: World Health Organization.Google Scholar
Nonterah, EA, Adomolga, E, Yidana, A, et al. (2019) Descriptive epidemiology of anaemia among pregnant women initiating antenatal care in rural northern Ghana. Afr J Prim Health Care Fam Med 11, e1e7.CrossRefGoogle ScholarPubMed
Stephen, G, Mgongo, M, Hussein Hashim, T, et al. (2018) Anaemia in pregnancy: prevalence, risk factors, and adverse perinatal outcomes in northern Tanzania. Anemia 2018, 1846280.CrossRefGoogle ScholarPubMed
Gravett, CA, Gravett, MG, Martin, ET, et al. (2012) Serious and life-threatening pregnancy-related infections: opportunities to reduce the global burden. PLoS Med 9, e1001324.CrossRefGoogle ScholarPubMed
Satti, H, Motsamai, S, Chetane, P, et al. (2012) Comprehensive approach to improving maternal health and achieving MDG 5: report from the mountains of Lesotho. PLoS One 7, e42700.CrossRefGoogle ScholarPubMed
Teshome, MS, Meskel, DH & Wondafrash, B (2020) Determinants of anemia among pregnant women attending antenatal care clinic at public health facilities in Kacha Birra district, southern Ethiopia. J Multidiscip Healthc 13, 10071015.CrossRefGoogle ScholarPubMed
Tadesse, SE, Seid, O, Mariam, YG, et al. (2017) Determinants of anemia among pregnant mothers attending antenatal care in Dessie town health facilities, northern central Ethiopia, unmatched case-control study. PLoS ONE 12, e0173173.CrossRefGoogle Scholar
Darnton-Hill, I & Mkparu, UC (2015) Micronutrients in pregnancy in low- and middle-income countries. Nutrients 7, 17441768.CrossRefGoogle ScholarPubMed
Lee, SE, Talegawkar, SA, Merialdi, M, et al. (2013) Dietary intakes of women during pregnancy in low- and middle-income countries. Public Health Nutr 16, 13401353.CrossRefGoogle ScholarPubMed
Karaoglu, L, Pehlivan, E, Egri, M, et al. (2010) The prevalence of nutritional anemia in pregnancy in an east Anatolian province, Turkey. BMC Public Health 10, 1.CrossRefGoogle Scholar
Obse, N, Mossie, A & Gobena, T (2013) Magnitude of anemia and associated risk factors among pregnant women attending antenatal care in Shalla Woreda, West Arsi zone, Oromia region, Ethiopia. Ethiop J Health Sci 23, 165173.Google ScholarPubMed
Dim, CC & Onah, HE (2007) The prevalence of anemia among pregnant women at booking in Enugu, south eastern Nigeria. Med Gen Med 9, 11.Google ScholarPubMed
Ebuy, Y, Alemayehu, M, Mitiku, M, et al. (2017) Determinants of severe anemia among laboring mothers in Mekelle city public hospitals, Tigray region, Ethiopia. PLoS One 12, e0186724.CrossRefGoogle ScholarPubMed
Grum, T, Brhane, E, Hintsa, S, et al. (2018) Magnitude and factors associated with anemia among pregnant women attending antenatal care in public health centers in central zone of Tigray region, northern Ethiopia: a cross sectional study. BMC Pregnancy Childbirth 18, 433.CrossRefGoogle ScholarPubMed
Mocking, M, Savitri, AI, Uiterwaal, CSPM, et al. (2018) Does body mass index early in pregnancy influence the risk of maternal anaemia? An observational study in Indonesian and Ghanaian women. BMC Public Health 18, 873.CrossRefGoogle ScholarPubMed
Gedefaw, L, Ayele, A, Asres, Y, et al. (2015) Anemia and associated factors among pregnant women attending antenatal care clinic in Wolayita Sodo town, southern Ethiopia. Ethiop J Health Sci 25, 155162.CrossRefGoogle ScholarPubMed
Liu, X, Du, J, Wang, G, et al. (2011) Effect of pre-pregnancy body mass index on adverse pregnancy outcome in north of China. Arch Gynecol Obstet 283, 6570.CrossRefGoogle ScholarPubMed
Sebire, NJ, Jolly, M, Harris, J, et al. (2001) Is maternal underweight really a risk factor for adverse pregnancy outcome? A population-based study in London. Br J Obstet Gynaecol 108, 6166.Google Scholar
Agrawal, S & Singh, A (2015) Obesity or underweigh: what is worse in pregnancy? J Obstet Gynecol India 66, 448452.CrossRefGoogle ScholarPubMed
Balarajan, Y, Ramakrishnan, U, Özaltin, E, et al. (2011) Anaemia in low-income and middle-income countries. Lancet 378, 21232135.CrossRefGoogle ScholarPubMed
Sifakis, S & Pharmakides, G (2000) Anemia in pregnancy. Ann N Y Acad Sci 900, 125136.CrossRefGoogle ScholarPubMed
Figure 0

Table 1. Socio-demographic characteristics of the respondents (N = 353)

Figure 1

Table 2. Content of ANC services received during antenatal period

Figure 2

Table 3. Utilisation of antenatal care services (N = 353)

Figure 3

Table 4. Relationship between anaemia in the third trimester of pregnancy and selected factors (bivariate analysis)

Figure 4

Table 5. Predictors of anaemia at 36 weeks of gestation among pregnant women (multiple logistics regression)