Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana.

BACKGROUND: Maternal and Child health remains at the core of global health priorities transcending the Millennium Development Goals into the current era of Sustainable Development Goals. Most low and middle-income countries including Ghana are yet to achieve the required levels of reduction in child and maternal mortality. This paper analysed the trends and the associated risk factors of stillbirths in a district hospital located in an impoverished and remote region of Ghana.
METHODS: Retrospective hospital maternal records on all deliveries conducted in the Navrongo War Memorial hospital from 2003-2013 were retrieved and analysed. Descriptive and inferential statistics were used to summarise trends in stillbirths while the generalized linear estimation logistic regression is used to determine socio-demographic, maternal and neonatal factors associated with stillbirths.
RESULTS: A total of 16,670 deliveries were analysed over the study period. Stillbirth rate was 3.4% of all births. There was an overall decline in stillbirth rate over the study period as stillbirths declined from 4.2% in 2003 to 2.1% in 2013. Female neonates were less likely to be stillborn (Adjusted Odds ratio = 0.62 and 95%CI [0.46, 0.84]; p = 0.002) compared to male neonates; neonates with low birth weight (4.02 [2.92, 5.53]) and extreme low birth weight (18.9 [10.9, 32.4]) were at a higher risk of still birth (p<0.001). Mothers who had undergone Female Genital Mutilation had 47% (1.47 [1.04, 2.09]) increase odds of having a stillbirth compared to non FGM mothers (p = 0.031). Mothers giving birth for the first time also had a 40% increase odds of having a stillbirth compared to those who had more than one previous births (p = 0.037).
CONCLUSION: Despite the modest reduction in stillbirth rates over the study period, it is evident from the results that stillbirth rate is still relatively high. Primiparous women and preterm deliveries leading to low birth weight are identified factors that result in increased stillbirths. Efforts aimed at impacting on stillbirths should include the elimination of outmoded cultural practices such as FGM.

Background

Stillbirths are among the most common adverse pregnancy outcomes with accompanying long-lasting deep psychological effects on parents, care givers, health providers and the community at large [1-3]. Globally, over 2.6 million babies are stillborn annually and 98% of all these stillbirths are said to be occurring in low and middle income countries [4].

Due to the huge differences in prevalence of stillbirth between high and Low to Middle Income Countries (LMIC), stillbirth equally used as a global development indicator [5]. Stillbirth has a direct association with availability of obstetric care services and so it disproportionately affects the poor in resource-constraint countries more than high-resource countries [6] with a reported prevalence of 55% among rural families [7]. This pattern of distribution mirrors maternal deaths and correlates mainly with areas of low skilled birth attendants (SBA), inadequate health infrastructure and lack of emergency obstetric care service [8]. Currently, 77% of the 98% stillbirths recorded in LMIC occur mainly in South-East Asia and sub-Saharan Africa (SSA) [4, 8]. In SSA particularly, women are reported to be 24 and 50 times more at risk of having stillbirths during labour than women in North America and United Kingdom respectively [6, 9]. The Ghana Maternal Health Survey 2017 observed 68% of stillbirths occur in rural areas compared to urban areas [10]. Saleem et al (2018) observed a 3.0% annual decline in stillbirth rate globally with much lower rates of decline for countries in South-East Asia and Africa [9]. This the author observed will further result in the inability of these countries to achieve the Every Newborn Action Plan goal of 12 per 1000 births by the year 2030 [9].

The slow pace of decline in resource-constraint settings can be attributed to the lack of SBAs, inadequate emergency obstetric services and inadequate health infrastructure. For instance, districts hospitals in Ghana have an average of one Medical Officer at post, yet emergency Obstetric and Gynaecological surgeries have been previously reported to represent a substantial proportion of the clinical duties of Medical Officers. Particularly, obstetric complications often requiring caesarean section are the commonest cases encountered [11].

In addressing these challenges, Ghana, recently implemented a number of maternal and child health related initiatives with the core objective of improving universal access to comprehensive obstetric care through an increase in institutional deliveries, where births are attended to by SBAs and improving obstetric referrals [12]. The Upper East Region of Ghana has since seen a steady improvement in maternal and child health care service provision. Notable improvements include increase in institutional deliveries from 46% in 2008 to 77% in 2010 and improved obstetric and new-born referrals at all four levels of the health system: Community-based Health and Planning Services compounds to Health Centres through the District Hospitals and finally to the Regional Hospital [13].

However to date, little is documented about how the observed improvements in obstetric care services has impacted on pregnancy outcomes in the region. Few longitudinal studies exist in Ghana and SSA on stillbirth as a monitoring tool for improving obstetric care. Most of the epidemiological studies assessing pregnancy outcomes use perinatal mortality which combines both stillbirths and early neonatal deaths and are often based on complex statistical modelling methods, country-wide or community demographic health surveillance and community verbal autopsies [5]. The value of these estimates is limited because of etiological differences between stillbirths and early neonatal deaths [12, 14], especially that labour and delivery (intrapartum period) are the highest risk periods for stillbirths [15-18]. A major challenge to preventing or reducing the incidence of stillbirths is the paucity of context specific knowledge on the causes and risk factors associated with stillbirths especially in resource poor settings [2]. This paper provides a ten-year longitudinal analysis of the trend in stillbirth rate and examines the neonatal and maternal characteristics associated with stillbirths using data from a hospital located in a rural poor setting in northern Ghana.

Materials and methods

Study setting

This study used data collected from the Navrongo War Memorial Hospital (WMH) in the Kassena-Nankana Municipality of the Upper East Region of Northern Ghana. The WMH is located in Navrongo and is the only secondary referral facility in the Kassena-Nankana area offering emergency obstetric care, surgical and other public health services [19]. It is a 123 bed facility serving a population of about 165,000 people and receives referrals from the many primary level health facilities in the area including private clinics as well as referrals from neighbouring districts and neighbouring towns in Burkina Faso [20]. Unpublished data from the hospital shows an average yearly Out Patient Department attendance of about 55,000 with an average of 10,000 in-patient admissions of which maternal related conditions form part of the top ten causes of admissions. The annual Antenatal attendance is about 2,500 and annual deliveries are hovering around 1,500.

The Kassena-Nankana Municipality which is home to the WMH lies within the Guinea Savannah ecological zone in the extreme north-eastern part of Ghana and occupies an area of about 1,675 square kilometres. It borders the Bulisa and Sissala Districts to the South West and West respectively, Bongo and Bolgatanga Districts in East and North-East respectively, and Burkina Faso in the North-eastern corner. About 90% of the population live in rural communities, with a small suburban area within the capital town, Navrongo. Settlements are mainly sparse with closely knit extended families living in the same compound with average of 10 people per compound. There are two main climatic seasons: A short rainy season between June and September and a dry season between October and May with the harmattan winds peaking in January-February. The average rainfall is between 850-1000mm while temperatures range from 20°C to as high as 40°C during the dry season. The vast majority of residents in the Upper East region are engaged in subsistence rain-fed agriculture. However, over-cropping and increasingly erratic rainfall have diminished agricultural productivity, exacerbating pervasive poverty [21, 22]. As a consequence of these circumstances, the region ranks among Ghana’s three most impoverished regions with a poverty prevalence of 55% [21].

Data collection

Delivery records data was retrospectively assembled from the Navrongo WMH maternity ward record books. The hospital keeps record books that contain systematically documented information on each patient attending the hospital. These hospital record books includes a maternal register that is used to capture information on all maternal related cases, information captured includes maternal demographic characteristics, mode of delivery, delivery outcome (live, fresh and macerated stillbirths and birth weight), gestation at delivery, genital mutilation status of the mother, relevant previous obstetric history etc. A structured designed data capturing tool was used to extract all information needed for the study from delivery record books in the maternity ward. Extracted data span a ten year period (2003–2013). The information was extracted by four trained research assistants independently to eliminate bias and errors and to ensure reliability. The extracted data was vetted and confirmed by two physicians independently before data was entered electronically for analysis.

Data analysis

The main outcome of interest in this study was stillbirth. We applied the standard definition of stillbirth being any foetal loss after 28 weeks of gestation, and or a weight of 1000g (1kg) [4, 23]. The ICD-10 further states the foetus must be 35cm of length or more to qualify as a stillbirth [23]. We however had no information on the foetal length at birth. We also categorised Birth weight less than 2.5Kg as Low Birth weight (LBW) as recommended by WHO [24]. A fresh stillbirth was defined as the intrauterine death of a foetus during labour or delivery, and a macerated stillbirth was defined as the intrauterine death of a foetus before the onset of labour or 24 hours before delivery, where the foetus showed degenerative changes [24] as reported in the obstetric records by the attending physician or midwife. Primiparous woman refers to a pregnant woman who had not delivered before, with the index pregnancy being the first expected delivery. Multiparous woman has more than 1 delivery but less than five and a grand multiparous woman has greater than five deliveries. A termed pregnancy is defined as 37 completed weeks of gestation to 40 weeks while preterm pregnancy is defined as one less than 37 weeks gestation and post term pregnancy is greater than 40weeks gestation. The proportions of post term deliveries were so negligible and therefore had no statistical significance so were added these to term deliveries for the analysis. The data were entered in Epidata 3.1 and exported to STATA version 14.2 (Statacorp College Station, Texas 77845 USA) for analysis. Descriptive analyses were first used to summarise maternal and new-born characteristics such as maternal age, type of delivery, delivery outcome, sex of neonate, perineum, use of partograph, birth weight, gestational age, maternal parity and Female Genital Mutilation (FGM) status of mother. In addition, trends in stillbirth rate were presented over the ten year period using a line graph and reported as absolute counts with respective proportions. Next, we performed bivariate analysis of these maternal and neonatal factors with delivery outcome (either live birth or stillbirth) and report examined differences using Pearson’s Chi Squared (χ2) test.

To determine the maternal and neonatal factors associated with stillbirths, we employed the Generalized Estimation Equation (GEE) regression models. The GEE formulated by Liang and Zeger (1986) was found to be the best regression approach for estimating the relationship of factors associated with stillbirth because of the correlation in our data which is an important assumption for using GEE [25]. In addition the GEE is said to use the generalized linear regression models to provide more unbiased and efficient parameters as compared to the ordinary least squares approach because it permits specification of correlation matrix accounting for within subject correlation of responses on dependent variables of different distributions [26]. Variables from the bivariate analyses that were significant at a 10% significance level were included in the GEE regression models. Associations from the GEE are presented as unadjusted and adjusted odds ratios (AOR) with corresponding 95% confidence intervals and significance set at two-tailed p<0.05.

Ethical considerations

The Navrongo WMH administration and the Upper East Regional Health Directorate of the Ghana Health Service granted approval for the study. Additional ethics approval was obtained from the Navrongo Health Research Centres Institutional Review Board. Because secondary data was used, informed consent was waived. Further to this, we ensured confidentiality and anonymity in data extraction, processing/cleaning and analyses.

Results

Background characteristics of study participants

Presented in Table 1 are background characteristics of study participants.

Table 1

Maternal and New-born background characteristics.

Characteristics	Number (n)	Percentage (%)	95% CI
Type of delivery
Spontaneous Vaginal Delivery	13752	82.5	81.9, 83.1
Caesarean-Section	2080	12.5	12.0, 13.0
Assisted/Instrumental	838	5.0	4.7, 5.4
Birth outcome
Single Birth	16103	97.2	96.9, 97.4
Multiple Birth	468	2.8	2.6, 3.1
Sex of neonate
Male	8816	53.8	53.0, 54.6
Female	7572	46.2	45.4, 47.0
Delivery outcome
Alive birth	16084	96.6	96.3, 96.9
Fresh Stillbirth	373	2.2	2.0, 2.5
Macerated Stillbirth	192	1.2	1.0, 1.3
State of perineum
Intact	3198	47.4	46.2, 48.6
Laceration	1924	28.5	27.4, 29.6
Episiotomy	1628	24.1	23.1, 25.1
Use of Partograph
Yes	3280	69.0	67.6, 70.3
No	1472	30.9	29.6, 32.3
Birth weight (Kg)
Extreme LBW (<1.5)	248	1.5	1.3, 1.7
Low birth weight (>1.5–2.5)	2385	14.5	13.9, 15.0
Normal birth weight (>2.5)	13831	84.0	83.4, 84.6
Estimated Gestational age (weeks)
Preterm (<37 weeks)	8942	60.3	59.5, 61.1
Term pregnancy (38–40 weeks)	5615	37.9	37.1, 38.7
Post-term (> 40weeks)	264	1.8	1.6, 2.0
Maternal Age (years)
< 20 years	2444	15.1	14.6, 5.7
20–34 years	11836	74.1	73.4, 74.7
> 35 years	1720	10.8	10.3, 11.3
Maternal Parity
Primiparous	313	1.9	1.7, 2.1
Multiparous	15374	92.2	91.8, 92.6
Grand multiparous	983	5.9	5.5, 6.3
Female Genital Mutilation
Yes	1646	18.6	17.8, 19.4
No	7201	81.4	80.6, 82.2

A total of 16,670 maternal deliveries were recorded in the WMH over the study period out of which 53.8% of the neonates were males and 46.2% females. Out of the total deliveries, 96.6% were live births and 3.5% were stillbirths. Of the 565 stillbirths recorded, 2.2% were fresh stillbirths and 1.2% macerated stillbirths. Average maternal age was 26 years with 74.1% of mothers in the 20-34years age group and advanced maternal age of 35+ years being the least at 10.8% (see Table 1). About 15.1% of the participants were less than 20 years denoting teenage pregnancy.

Most deliveries were from multiparous women representing 58.8% followed by grand multiparous women with 39.3%, and the least was primiparous women (1.9%). The predominant mode of delivery was by spontaneous vagina delivery (82.6%) followed by caesarean section (12.5%) and assisted or instrumental deliveries (5.0%). Preterm deliveries were 60.3%, and term deliveries were 39.7%. Approximately 42.4% of mothers were unemployed and 5.1% were students. Of the employed group 5.7% were Government employees, 36.3% were self-employed engaging mostly in petty trading while 7.5% had farming as their main occupation.

About 69% of expectant mothers were monitored with the partograph while 31.0% were not. Of all the deliveries documented 18% of the mothers had undergone FGM. A total of 4,876 women were tested for Human Immunodeficiency Virus (HIV) as part of Prevention of Mother-To-Child Transmission, out of which 1.3% tested positive.

Trends in stillbirth rate

Fig 1 presents the trends in stillbirth rates from 2003 to 20013. Results suggest a general decline in trends of stillbirth over the entire 10 year period.

Fig 1

Trends in stillbirth rates from 2003–2013 expressed as percentage of the number of births per year.

The overall stillbirth rate was 4.2% in 2003 and this declined to 2.1% in 2013. Fresh stillbirths as at 2003 represented 2.8% and declined to 1.3% in 2013, and macerated stillbirths declined from 1.4% to 0.7% 2013 [Fig 1]. The highest rate of decline in stillbirth rate recorded was from 2010 (3.6%) to 2013 (2.1%), a period during which, institutional (hospital) deliveries were on the rise.

Bivariate and multivariate analysis of stillbirths

Results of bivariate analysis of the association of selected foetal and maternal factors with stillbirth status are presented in Table 2. At the bivariate level all neonatal and maternal factors had varied associations with stillbirth in the study population.

Table 2

Bivariate analysis of stillbirth and maternal and new born characteristics.

Maternal and foetal characteristics	Number of births	Proportion of Live births (%)	Proportion of Stillbirths (%)	P-value
Sex of neonate
Male	8781	8544 (97.3)	237 (2.7)	0.008
Female	7553	7397 (97.9)	156 (2.0)
Maternal age (years)
12–19	2514	2444 (97.2)	70 (2.8)	0.021
20–34	12253	11836 (96.6)	417 (3.4)
35+	1798	1720 (95.7)	78 (4.3)
Maternal parity				<0.0001
Primiparous	313	289 (92.3)	24 (7.7)
Multiparous	9704	9362 (96.5)	342 (3.5)
Grand multiparous	6512	6317 (97.0)	195 (3.0)
Maternal Occupation
Unemployed	6874	6553 (95.3)	321 (4.7)	<0.0001
Farmer	1225	1188 (97.5)	37 (3.0)
Self-employed	5880	5735 (97.5)	145 (2.5)
Student	833	815 (97.8)	18 (2.1)
Government employed	933	915 (98.1)	18 (1.9)
Other	434	420 (96.8)	14 (3.2)
Gestation
Preterm	8876	8530 (96.1)	346 (3.9)	<0.0001
Term	5571	5435 (97.6)	136 (2.4)
Post-term	261	257 (98.5)	4 (1.5)
Birth weight
Extreme LBW	243	179 (73.7)	64 (26.4)
LBW	2369	2216 (93.5)	153 (6.5)	<0.0001
Normal birth weight	13729	13413 (97.7)	316 (2.3)
Type of Delivery				0.098
SVD	13651	13215 (96.8)	436 (3.1)
Caesarean Section	2059	1975 (95.2)	84 (4.1)
Assisted/Instrumental delivery	835	810 (97.0)	25 (3.0)

For instance, male neonates (p = 0.008), mothers older than 35 years (p = 0.021), nulliparous women (p<0.0001), unemployed women (p<0.0001), neonates born preterm (p<0.0001) and extreme LBW neonates (p<0.0001) were more likely to be born still than the rest. More caesarean deliveries also had a trend towards stillbirth (p = 0.098) compared to SVDs.

Presented in Table 3 are the GEE regression analyses showing factors associated stillbirth.

Table 3

Association between maternal and new born characteristics and stillbirth GEE Model.

Risk factors	n	Unadjusted OR (95% CI)	P-value	Adjusted OR (95% CI)	P-value
Sex of neonate
Male	8781	1		1
Female	7553	0.76 (0.62, 0.93)	0.009	0.62 (0.46, 0.84)	0.002
Mothers age
< 20 years	2514	0.81 (0.63, 1.05)	0.022	0.66 (0.33, 1.29)	0.270
20–34 years	12253	1		1
≥ 35 years	1798	1. 28 (1.01, 1.65)		1.04 (0.66, 1.65)
Mother Occupation
Unemployed	6874	1		1
Farmer	1225	0.64 (0.45, 0.89)	<0.0001	0.82 (0.39, 1.71)	0.280
Self-employed	5880	0.52 (0.42, 0.63)		0.67 (0.47, 0.94)
Student	833	0.45 (0.28, 0.73)		1.06 (0.47, 2.39)
Government employed	933	0.40 (0.25, 0.65)		0.73 (0.31, 1.72)
Other	434	0.68 (0.39, 1.17)		1.19 (0.51, 2.81)
Birth weight
Normal birth weight	13729	1		1
Extreme LBW	243	15.2 (11.2, 20.6)	<0.0001	18.9 (10.9, 32.4)	<0.0001
LBW	2369	2.93 (2.40, 3.57)		4.02 (2.92, 5.53)
FGM status
Yes	7201	1		1
No	1646	1.56 (1.21, 1.99)	0.001	1.47 (1.04, 2.09)	0.031
Parity
Multiparous	9704	1		1
Primiparous	313	2.27 (1.48, 3.49)	<0.0001	1.40 (0.73, 2.67)	0.037
Grand multiparous	6512	0.85 (0.71, 1.01)		0.65 (0.46, 0.92)
Gestation
Preterm	8876	1.62 (1.33, 1.98)	<0.0001	1.19 (0.85, 1.66)
Term	5571	1		1	0.301
Post-term	261	0. 62 (0.23, 1.69)		0.84 (0.60, 1.17)

Female neonates had a lower risk of being stillborn compared to their male counterparts (Adjusted Odds Ratio, AOR = 0.62 95%CI [0.46, 0.84]); p = 0.002]. Although maternal age was significantly associated with delivery outcome in bivariate analysis and the unadjusted model, it was not significant in the adjusted regression analysis. Also maternal occupation turn out not to be significantly associated with birth outcome in multivariate analysis.

Neonates were extreme LBW (AOR = 18.9 [10.9, 32.4]) and LBW (AOR = 4.02 [2.92, 5.53]) were at a higher odds of been stillborn than those with normal weight.

Mothers who had some form of FGM had 47% odds of having stillbirths compared to those who have not undergone FMG (AOR = 1.47 [1.04, 2.09]). Nulliparous women were at a higher odds of having stillbirths (AOR = 1.40 [0.73, 2.67]) during delivery compared to multiparous women. On the contrary, grand multiparous women were however, less likely to have stillbirths (AOR = 0.65 [0.46, 0.92]). Gestational age of foetus was not significantly associated with stillbirth experience in multivariate analysis.

Discussion

Still births is a major problem in developing countries were about 98% of the incidence of stillbirths are said be occurring [4]. To achieve the required reductions in the global burden of stillbirths, proven strategic interventions that are anchored on a clear understanding of the causes and factors associated with the incidence of stillbirths are required [27]. However, there is paucity of such context specific evidence in most rural poor settings. In this study, we assess the trends in stillbirth rates over a ten year period and examine the maternal and neonatal factors associated with still births in a hospital located in a rural impoverished setting of northern Ghana.

Overall, we found a stillbirth rate of 34 per 1000 live births which is higher than the country rate of 14 per 1000 live births [28] Interestingly there was a decline in stillbirth rate from 42 per 1000 live births in 2003 to 21 per 1000 live births by the year 2013. This modest achievement notwithstanding, the reported rate remains high. However, these findings are lower than what has been reported in other developing countries like Nigeria which has an average of 42 per 1000 live births, Pakistan with 47 per 1000 live births and The Gambia with 156 per 1000 live births [7, 29]. General improvements in health care delivery across the Upper East Region [13] is said to have increased access to healthcare services resulting from the ever improving Community-based Health and Planning Services in the region could account for the low SB rate documented. The trends in SB rate over the period indicate an annual rate of decline of 0.2% far lower than the overall reported annual rate of decline for LMIC, high income countries and the global rate [30]. However, the peak of the decline in stillbirths for the study area was from 2010 to 2013 and this period coincides with increased institutional deliveries and improved emergency obstetric referrals in the area probably resulting from the implementation of the millennium accelerated framework for the achievement of the MDG 4 and 5 in Ghana.

Logistic regression analysis found that younger and advanced maternal ages did not confer an increased risk to SB and this is consistent with available literature that showed most SBs in Ghana occurred in the 20–29 year group [28]. However, a study in India identified younger and advanced maternal ages as important risk factors to stillbirths [31] suggesting that maternal age as a risk factor for stillbirth may be setting specific. Maternal occupation did not confer a significant risk to stillbirth in this study.

From the results, majority of the deliveries were by Spontaneous Vaginal Delivery followed by C-Section and assisted deliveries consistent with a study conducted in The Gambia which found that about four out of five births were by spontaneous vaginal delivery [29]. The C-section rate over the study period was 12.5% within the 10–15% proposed by the World Health Organization but far lower than the rates reported in the developed world.

Our study showed that three out of five stillbirths were due to preterm deliveries and this is consistent with studies conducted in Burkina Faso [32] and also by the Global Alliance to prevent stillbirths and prematurity which reported that majority of stillbirths involve preterm foetuses especially the extremely premature [33].

In bivariate analysis, sex of neonate, birth weight, FGM status of mother, maternal age, maternal occupation, gestation age, mode of delivery and parity were significantly associated with the birth outcome. However after adjusting for confounding factors in multivariable analyses, the risk factors for stillbirths in the district were sex of neonate, weight of the neonate, FGM, and parity. The effect of FGM on birth outcomes has previously been documented in the same area which found that babies from circumcised mothers were about two times more likely to be stillborn [19]. This is a significant finding as FGM has been part of the passage rite to adulthood for several decades in the study area [34, 35]. However due to culturally appropriate community interventions embarked upon by the Navrongo Health Research Centre in the past decade, prevalence of FGM has been declining in recent years [19]. This study showed a further drop in the prevalence of FGM from 9.0% to 0.4% over the study period.

We also found that primiparous women had increased risk of stillbirths which was similar to findings reported in Dublin, Ireland [36] and in Ghana [37]. Even though prevalence of HIV infection in pregnancy during the study period was low at 1.3%, it is discouraging to know that only a smaller proportion 28% of expectant mothers were counselled and tested. The study did not find any association between HIV and the risk of having a stillborn as reported by some studies in SSA [38].

Previous studies in Ghana and Angola have identified the use of partograph in monitoring labour as an appropriate tool for improving pregnancy outcomes through early referrals for interventions such as augmentation and emergency surgery when indicated [12, 39]. Our study found over half of the expectant mothers had their labour monitored on the partograph. This improvement can be attributed to continuous training of midwives by Upper East Regional Health Directorate as part of its audit of obstetric and new-born referrals in the region [12].

Study limitation (s)

The use of hospital based data is limited by deficiency in data collection and collation and as a retrospective study, some important obstetric outcomes and indications may not have been consistently documented and therefore could have not permitted further sub analysis. However, as an index study to assess the true burden of stillbirth and the trends at the facility level, the results do provide significant evidence for the prevailing situation and forms the basis for which future evaluation can be compared.

Conclusion

The study showed modest decline in stillbirth rate over the study period. It is evident from the study that stillbirth rate is still relatively high. Primiparous women and preterm deliveries leading to low birth weight are identified factors that result in increased stillbirths. Efforts aimed at impacting on stillbirths should include the elimination of outmoded cultural practices such as FGM. Health systems strengthening especially in the utilization of antenatal care services and skilled attendants at delivery are essential in improving foeto-maternal outcomes.

Data used for the analyses (Stillbirth data).

(XLS)

Click here for additional data file.

11 Nov 2019

PONE-D-19-24698

Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana

PLOS ONE

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The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: I Don't Know

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The present study has important findings and highlights the need of attention to heath conditions in LMIC, especially when considering obstetric care as a window of opportunity to social and economic development of a nation. In addition, the results signalize current alarming health issues, such as the presence of genital mutilation and high rates of stillbirth, revealing a gap in public politics in specific settings. Also, the discussion of possible connections between the stillbirth rate decrease and health care improvements reinforces the importance and the effectiveness of investments in health care.

The manuscript is well written overall. Yet, the language quality should be verify, since punctuation marks issues can be identified over the manuscript, compromising the structure, organization of the text, leading to ambiguity, doubts and demanding extra attention to interpret the information.

The high quality methodology used in the present study contributes to the credibility of the results. Both statistical analysis and data collection are detailed and well described in the text, listing the different variables and criteria considered to elaborate the GEE regression models. However, I recommend a revision of some topics before the manuscript can proceed due to some minor issues.

The introduction section brings great information about the topic and provides a contextualization of the subject to the reader. However, the given fact that “the rates of decline for South-East Asia and Africa are still very low” (page 5, 18th line) could be presented in a more reliable and solid manner if the “very low” numbers were introduced, according to the reference indicated.

At the beginning of the study setting section (page 7, 1st line), a retrospective study (Oduro et al, 2006) is used as a reference in order to describe the Navrongo War Memorial Hospital (WMH)’s services - emergency obstetric care, surgical and other public health services. However, the referred paper does not describe it, stating only that “WMH is a district health facility that offers secondary clinical and public health services” (Oduro, 2006). In addition, in the same paragraph (page 7, 10th line) the writer state that “The annual Antenatal attendance is about 2,500 and annual deliveries are hovering around 1,500”. Meantime, the paper to which this sentence refers to (Nonterah et al, 2019) informs that this data was collected from an unpublished WMH material. Thus, it would be preferable if this same consideration was made in the present study, since this material is not available to the external scientific community.

The applied definition of stillbirth as “any foetal loss after 28 weeks of gestation, and or a weight of 1000g (1kg)” (data analysis section – page 8, 1st line) is referring to a Lancet Global Health’s article (Blencowe et al, 2016). However, this is not the primary source of the stillbirth definition, but yes the International Classification of Diseases 10th revision (ICD-10). Also, according to the ICD-10, there is a third criterium to classify stillbirth: fetus of 35cm of length or more. If the writer decides not to include it, it is possible to justify the reasons for it (eg. absence of length data).

The table 1 is well presented but contains some minor issues. The variable “perineum” may not be self-explicative, demanding a more descriptive nomenclature, such as “perineum status”. Still in the table 1, the variable “maternal parity” presents 3 categories: P0, P1-P5 and >P5. Despite the explanation about the variable in the method section, the categories could be presented in a clearer manner if the 3 nominal classifications were included: primiparous, multiparous and grand multiparous. Also, the variable “gestational age” is presented with 3 categories: <37 weeks, 37 to 40 weeks and >40 weeks. However, the inclusion of the classification pre term and term (as previous presented in the text), with the corresponding intervals, may contribute to data understanding.

The results from the study are described in a very fine way. However, there are some important considerations in order to contribute to the quality of this section. The phrase “The proportion of teenage pregnancies (≤19 years) was relatively high at about 15.1%” (6th line, page 12) may be reformulated to follow the results section requirements. The use of expressions such as “high” is considered an interpretation, what is an attribute of the discussion section. In addition, to discuss if it is a high or low rate, it is important to compare the values with national/international references.

The discussion section highlights important previous findings, intertwining the existing literature and the risk factors associated with stillbirths from the presented study. However, in the discussion stablished about the C-section rate over the study period may be reconsidered in some aspects (page 18, 31st line). First, according to the text, the C-section rate of 12,5% is within the rate interval proposed by WHO (10 to 15%). Therefore, it may be considered as a positive result, providing discussions about the conditions of the Spontaneous Vaginal Delivery instead, which also requires skilled health personnel, good sanitary conditions and a satisfactory infrastructure environment. Second, the writers compare the C-section rate to the developed “world”, considering this last one as a “positive” parameter. However, developed countries usually present high C-section rates not only because of emergency obstetric care, but also due to many other factors that lead to unnecessary recommendations of this surgical procedure (eg. private health insurance interests; convenience of choosing the day of delivery). Therefore, when discussing about this specific result, it is important to conduct a careful discussion, considering all long-term benefits of the vaginal delivery.

The conclusions were drawn appropriately based on the presented data, which are fully available in the manuscript over the text, but also in tables and graphics. However, the affirmation “First time pregnant mothers and those carrying male foetus should strictly follow antenatal and prenatal services and recommendations as they are at a higher risk of stillbirths” may be reconsidered. Despite the study shows great findings, it is a retrospective e non controlled study, carrying some important limitations. Even though the literature supports many of the findings, it is essential to analyze carefully all results. For example, the correlation between pregnancies of boys and stillbirth can suggest a fact but it is not correct to stablish strong recommendations about it without a deep interpretation. The results from scientific studies may imply early actions and miss interpretations, generating negative consequences. Therefore, I suggest that the conclusion section be revised and based on solid evidenced and scientific findings.

Reviewer #2: The background section is well written. Authors started with high rates of stillbirths in the world. The authors explained how stillbirths are associated with poor health services and the availability of obstetric care services.

I will suggest updating reference 1. In line 13 of the background, I suggest abbreviating the word “Sub-Saharan Africa” in the first moment that it was presented. Also, through the paper, the authors used many abbreviations that they did not use after, I suggest to remove and only keep the abbreviations that have more the one citation.

The method section needs more work.

I think it was not clear if the author used a cross-sectional or longitudinal data. I understood that it was a cross-section study using trends.

I think would be important to describe more about the “systematically documented information”, on the second and third line of the data collection section.

Also, I would like to know more information about the “A structured designed data capturing tool”. Did the authors use a tool? Which tool was that?

The author did not specify which period the data was collected, this information should be clear.

The data was double coded but what is the reliability of the data? Could the author present a statistic measure for that?

In the analyzes section, I notice that in the GEE analyzes the authors used sometimes the groups of high risk as a reference, for example, mothers age “12-19 yrs”, mother occupation “Unemployed”, gestation >37 weeks and sometimes groups with fewer risks as normal birth weight, my suggestion is using the groups with less risk as reference “1” and establish a pattern in the analyzes.

Also, the author described what GEE means but they did not describe the assumption of the GEE.

I would like also the authors to discuss more the result's implications and recommendations.

In the last paragraph of the discussion they mentioned that the data is longitudinal, I am confused about that. Do you follow the patients between 2003-2013? if you did follow, this information should be more clear in the method section.

Please review the references for typos.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Reviewer #1: Yes: Isabel Giacomini Marques

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

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26 Nov 2019

Dear Sir/Madam,

Response to reviewers: Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana (PONE-D-19-24698)

We wish to thank the academic Editor and the Reviewers for the due diligence with our manuscript.

We do appreciate and acknowledge the comments which we believe will indeed improve the content of our paper.

Below is a point-by-point response to the editor’s and reviewer’s comments. Also attached is the tracked and clean version for your review

It is our fervent hope that you would consider the revised manuscript suitable for the wider reader population

Sincerely

Dr Engelbert A. Nonterah. MD, MSc.

Response to Editor’s Comments

Editors comments Response

Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at: We appreciate this important reminder by the editor and have now ensured that the entire manuscripts conforms to PLOS ONE style requirements

Please provide additional details regarding participant consent. If the need for consent was waived by the ethics committee, please include this information. If the data was accessed anonymously the lack of waiver will be acceptable: Thanks to the editor for this point. We have now clarified this in the below statement: “Because secondary data was used, informed consent was waived. Further to this, we ensured confidentiality and anonymity in data extraction, processing/cleaning and analyses.”

Please amend either the abstract on the online submission form (via Edit Submission) or the abstract in the manuscript so that they are identical.: We will do just this to ensure the abstract in the manuscript is identical to the online submission form

Response to Reviewers Comments

Reviewer #1

Comments Response

The manuscript is well written overall. Yet, the language quality should be verify, since punctuation marks issues can be identified over the manuscript, compromising the structure, organization of the text, leading to ambiguity, doubts and demanding extra attention to interpret the information.: We have edited the entire manuscript and to improve the language quality. We have also used “grammar check” to improve the manuscript where necessary

The high quality methodology used in the present study contributes to the credibility of the results. Both statistical analysis and data collection are detailed and well described in the text, listing the different variables and criteria considered to elaborate the GEE regression models. However, I recommend a revision of some topics before the manuscript can proceed due to some minor issues.: We acknowledge and appreciate the reviewers kind comments

The introduction section brings great information about the topic and provides a contextualization of the subject to the reader. However, the given fact that “the rates of decline for South-East Asia and Africa are still very low” (page 5, 18th line) could be presented in a more reliable and solid manner if the “very low” numbers were introduced, according to the reference indicated.: We have now revised this statement to read as “Saleem et al (2018) observed a 3.0% annual decline in stillbirth rate globally with much lower rates of decline for countries in South-East Asia and Africa. This the author observed will further result in the inability of these countries to achieve Every Newborn Action Plan goal of 12 per 1000births by 2030” this can be found in page 5 lines 91-95

At the beginning of the study setting section (page 7, 1st line), a retrospective study (Oduro et al, 2006) is used as a reference in order to describe the Navrongo War Memorial Hospital (WMH)’s services - emergency obstetric care, surgical and other public health services. However, the referred paper does not describe it, stating only that “WMH is a district health facility that offers secondary clinical and public health services” (Oduro, 2006). In addition, in the same paragraph (page 7, 10th line) the writer state that “The annual Antenatal attendance is about 2,500 and annual deliveries are hovering around 1,500”. Meantime, the paper to which this sentence refers to (Nonterah et al, 2019) informs that this data was collected from an unpublished WMH material. Thus, it would be preferable if this same consideration was made in the present study, since this material is not available to the external scientific community.: Thanks to the Reviewer for this observation. In our paper we have sought to expand or explain what Oduro et al 2006 meant by “secondary clinical and public health services”. These services include emergency obstetric care, surgical and other public health services as we observed. We were of the view that since we have captured this in a previous paper, it suffices to cite this. We have however rephrased this as suggested by the Reviewer. “Unpublished data from the hospital shows an average yearly Out Patient Department (OPD) attendance of about 55,000 with an average of 10,000 in-patient admissions of which maternal related conditions form part of the top ten causes of admissions. The annual Antenatal attendance is about 2,500 and annual deliveries are hovering around 1,500”

The applied definition of stillbirth as “any foetal loss after 28 weeks of gestation, and or a weight of 1000g (1kg)” (data analysis section – page 8, 1st line) is referring to a Lancet Global Health’s article (Blencowe et al, 2016). However, this is not the primary source of the stillbirth definition, but yes the International Classification of Diseases 10th revision (ICD-10). Also, according to the ICD-10, there is a third criterium to classify stillbirth: fetus of 35cm of length or more. If the writer decides not to include it, it is possible to justify the reasons for it (eg. absence of length data).: We appreciate the observation made by the Reviewer. We do agree that the primary source is ICD-10 and we have included this as a reference now. We have also justified the reason for non-exclusion of the third component of the definition in the following sentence: “The ICD-10 further states the foetus must be 35cm of length or more [23]. We however had no information on the foetal length at birth”. This can be found in page 9 lines 173-174.

The table 1 is well presented but contains some minor issues. The variable “perineum” may not be self-explicative, demanding a more descriptive nomenclature, such as “perineum status”. : Perineum corrected to “State of perineum”

Still in the table 1, the variable “maternal parity” presents 3 categories: P0, P1-P5 and >P5. Despite the explanation about the variable in the method section, the categories could be presented in a clearer manner if the 3 nominal classifications were included: primiparous, multiparous and grand multiparous. Also, the variable “gestational age” is presented with 3 categories: <37 weeks, 37 to 40 weeks and >40 weeks. However, the inclusion of the classification pre term and term (as previous presented in the text), with the corresponding intervals, may contribute to data understanding.: We have now amended this using the nominal classifications proposed by the Reviewer. “Primiparous” “multiparous” and “Grand multiparous”. We have similarly amended gestational age as Preterm (<37 weeks), Term (38-40 weeks) and Post-term (>40 weeks)

The results from the study are described in a very fine way. However, there are some important considerations in order to contribute to the quality of this section. The phrase “The proportion of teenage pregnancies (≤19 years) was relatively high at about 15.1%” (6th line, page 12) may be reformulated to follow the results section requirements. The use of expressions such as “high” is considered an interpretation, what is an attribute of the discussion section. In addition, to discuss if it is a high or low rate, it is important to compare the values with national/international references.: We indeed appreciate this observation and have made these amendments: The phrase “The proportion of teenage pregnancies (≤19 years) was relatively high at about 15.1%” has been edited to read “About 15.1% of the participants were less than 20 years of age denoting teenage pregnancy”

The discussion section highlights important previous findings, intertwining the existing literature and the risk factors associated with stillbirths from the presented study. However, in the discussion stablished about the C-section rate over the study period may be reconsidered in some aspects (page 18, 31st line). First, according to the text, the C-section rate of 12.5% is within the rate interval proposed by WHO (10 to 15%). Therefore, it may be considered as a positive result, providing discussions about the conditions of the Spontaneous Vaginal Delivery instead, which also requires skilled health personnel, good sanitary conditions and a satisfactory infrastructure environment. Second, the writers compare the C-section rate to the developed “world”, considering this last one as a “positive” parameter. However, developed countries usually present high C-section rates not only because of emergency obstetric care, but also due to many other factors that lead to unnecessary recommendations of this surgical procedure (eg. private health insurance interests; convenience of choosing the day of delivery). Therefore, when discussing about this specific result, it is important to conduct a careful discussion, considering all long-term benefits of the vaginal delivery.: We do appreciate the further explanation given by the Reviewer. We do not want to overemphasize the discussion on CS rates since the focus of the paper is stillbirth. We do agree with the Reviewer that there are several other reasons for high CS rates especially in high income countries.

The conclusions were drawn appropriately based on the presented data, which are fully available in the manuscript over the text, but also in tables and graphics. However, the affirmation “First time pregnant mothers and those carrying male foetus should strictly follow antenatal and prenatal services and recommendations as they are at a higher risk of stillbirths” may be reconsidered. Despite the study shows great findings, it is a retrospective non controlled study, carrying some important limitations. Even though the literature supports many of the findings, it is essential to analyze carefully all results. For example, the correlation between pregnancies of boys and stillbirth can suggest a fact but it is not correct to stablish strong recommendations about it without a deep interpretation. The results from scientific studies may imply early actions and miss interpretations, generating negative consequences. Therefore, I suggest that the conclusion section be revised and based on solid evidenced and scientific findings.: Thanks for this important point. We have now edited the conclusion and it reads: “The study showed modest decline in stillbirth rate over the study period. It is evident from the study that stillbirth rate is still relatively high and some neonatal and maternal characteristics are major contributors. Efforts aimed at impacting on stillbirths should include the elimination of outmoded cultural practices such as FGM. Health systems strengthening especially in the utilization of antenatal care services and skilled attendants at delivery are essential in improving foeto-maternal outcomes”.

Reviewer #2

I will suggest updating reference 1.: We believe the information contained in the reference is still relevant but we have added a current reference to it.

In line 13 of the background, I suggest abbreviating the word “Sub-Saharan Africa” in the first moment that it was presented.: We have now corrected this accordingly

Also, through the paper, the authors used many abbreviations that they did not use after, I suggest removing and only keeping the abbreviations that have more the one citation.: We have screened through and removed the abbreviations such as KNM, OPD, VA which were not repeated in the manuscript

I think it was not clear if the author used a cross-sectional or longitudinal data. I understood that it was a cross-section study using trends. Data were collected in serial cross-sectional manner

I think would be important to describe more about the “systematically documented information”, on the second and third line of the data collection section.: We have now expanded on this to read as: “The hospital keeps record books that contain systematically documented information on each patient attending the hospital. These hospital record books includes a maternal register that is used to capture information on all maternal related cases, information captured includes maternal demographic characteristics, mode of delivery, delivery outcome (live, fresh and macerated stillbirths and birth weight), gestation at delivery, genital mutilation status of the mother”

Also, I would like to know more information about the “A structured designed data capturing tool”. Did the authors use a tool? Which tool was that? This was a designed excel spread sheet

The author did not specify which period the data was collected, this information should be clear. We have now clarified that “data were collected between 2003 and 2013”

The data was double coded but what is the reliability of the data? Could the author present a statistic measure for that? We merged data and there was a complete match hence data were reliable

In the analyzes section, I notice that in the GEE analyzes the authors used sometimes the groups of high risk as a reference, for example, mothers age “12-19 yrs”, mother occupation “Unemployed”, gestation >37 weeks and sometimes groups with fewer risks as normal birth weight, my suggestion is using the groups with less risk as reference “1” and establish a pattern in the analyzes. We have re-analysed this. For age “20-34 years” is now the reference group while for gestational age “38-40 weeks (term)” is now the reference group

Also, the author described what GEE means but they did not describe the assumption of the GEE. We have now modified the below statement to capture the relevant assumptions for GEE that relates to our analyses.: “The GEE formulated by Liang and Zeger (1986) was found to be the best regression approach for estimating the relationship of factors associated with stillbirth because of the correlation in our data which is an important assumption for using GEE [25]”

I would like also the authors to discuss more the result's implications and recommendations. We have expanded the conclusion to include recommendations:

“The study showed modest decline in stillbirth rate over the study period. It is evidence from the study that stillbirth rate is still relatively high and some neonatal and maternal characteristics are major contributors. Efforts aimed at impacting on stillbirths should include the elimination of outmoded cultural practices such as FGM. Health systems strengthening especially in the utilization of antenatal care services and skilled attendants at delivery are essential in improving foeto-maternal outcomes”.

In the last paragraph of the discussion they mentioned that the data is longitudinal, I am confused about that. Do you follow the patients between 2003 and 2013? If you did follow, this information should be clearer in the method section. We have now clarified the cross-sectional nature of our study

Please review the references for typos. Thanks for the comment. We have now revised the relevant references thoroughly

Submitted filename: Response to reviewers_25 Nov 2019.pdf.docx

Click here for additional data file.

27 Dec 2019

PONE-D-19-24698R1

Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana

PLOS ONE

Dear Dr Nonterah,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The authors have made major improvements in the manuscript. However, there are minor points for revision based on reviewers´ recommendations.

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Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for all the responses for each one of the comments. There was a significant improvement of the manuscript, demonstrating the effort of the authors in order to develop a high quality research. However, I still have two considerations about the text.

First, I understand that the discussion about C-section is not the focus of this study. Yet, if the results about it are going to be included in the discussion, it is extremely important to conduct it carefully. In the line 304 you say that the C-section rate are within the 10-15% proposed by the World Health Organization. But then, in the next phrase, you make a statement about "This low C-section rate (...)". The sentence is not consistent since this "low" classification should not be based on developed countries rates. These countries, as I have already said in the previous review, have high C-section rates because of other elements and not only because of adequate emergency obstetric care services. Therefore, I reinforce that this discussion may be revised since C-section contributes to many short and long term negative effects in a child's life.

Second, the results in this study show the urgent need of female adequate care, mainly when discussing about FGM. Therefore, the conclusions do not show the potential of the results. I suggest that instead of the sentence "some neonatal and maternal characteristics are major contributors", the authors state the main findings, identifying these specific characteristics that contribute to neonatal and maternal health outcomes.

Overall, the quality of the writing improved, making the reading process more clear and less unambiguous.

Reviewer #2: The authors incorporated most of the suggestions and the article had an improvement. My suggestion is a review to fix minor errors.

Inline 92, there is a typo " 1000births" that need a space between the words.

Inline 106 the authors write an abbreviation for "Community-based Health and Planning Services (CHPS)" but they did not use this after through the text. I strongly recommend only to use abbreviations for words that are important for the text.

Inline 125 the authors wrote an abbreviation for "Navrongo War Memorial Hospital (WMH)", but inline 152 and 202 they used the whole name again, I recommend using only the abbreviation after the first reference in the text.

In table 1, line Estimated Gestational age (weeks), need a space between "40weeks".

In table 1, line Maternal Age (years), need a space between "< 20years".

Inline 229 they used an abbreviation for "Mother-To-Child Transmission (PMTCT)", as the authors did not use this abbreviation anymore through the text I suggest removing the abbreviation.

Please, check reference again for typos. For example, in the reference number 19 there are some dots after the first name of the author, different from the other references.

Thank you.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Isabel Giacomini Marques

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org. Please note that Supporting Information files do not need this step.

27 Dec 2019

Navrongo Health Research Centre

Ghana Health Service

P. O. Box 114

Navrongo

Mob:+233 (0) 505 989 986

E-mail: engelbert.nonterah@navrongo-hrc.org

Alternate email: drenanonterah@gmail.com

Skype: engelbert.nonterah4

December 27, 2019

Dear Sir/Madam,

Response to reviewers: Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana (PONE-D-19-24698R1)

We wish to thank the Reviewers for the second round of review and the comments.

We do appreciate and acknowledge the comments as useful to improve the content of our paper.

Below is a point-by-point response to reviewer’s comments. Also attached is the tracked and clean version for your review

It is our fervent hope that you would consider the revised manuscript suitable for publication

Sincerely

Dr Engelbert A. Nonterah. MD, MSc.

Response to Reviewers Comments

Reviewer #1

First, I understand that the discussion about C-section is not the focus of this study. Yet, if the results about it are going to be included in the discussion, it is extremely important to conduct it carefully. In the line 304 you say that the C-section rate are within the 10-15% proposed by the World Health Organization. But then, in the next phrase, you make a statement about "This low C-section rate (...)". The sentence is not consistent since this "low" classification should not be based on developed countries rates. These countries, as I have already said in the previous review, have high C-section rates because of other elements and not only because of adequate emergency obstetric care services. Therefore, I reinforce that this discussion may be revised since C-section contributes to many short and long term negative effects in a child's life.

We have now deleted this statement to avoid further ambiguity and inconsistency. “This low C-section rate in the study setting may be a reflection of the inadequate emergency obstetric care services including the lack of skilled health personnel to provide such services. Therefore, this may increase in future when access to emergency obstetric care and skilled personnel improves. Presently however, the increased institutional deliveries and obstetric referrals have seen no direct effect on C-section rate across the study area. Besides the study setting being rural, other prevailing factors that might account for the low rate as some observation seem to indicate, is the fear of caesarean section by the resident population and hence the preference for home delivery”.

Second, the results in this study show the urgent need of female adequate care, mainly when discussing about FGM. Therefore, the conclusions do not show the potential of the results. I suggest that instead of the sentence "some neonatal and maternal characteristics are major contributors", the authors state the main findings, identifying these specific characteristics that contribute to neonatal and maternal health outcomes.

We have now revised the conclusion by specifying the factors that contribute to stillbirths. The new sentence reads “Primiparous women and preterm deliveries leading to low birth weight are identified factors that result in increased stillbirths”.

Reviewer #2

Inline 92, there is a typo “1000births" that need a space between the words. We have now corrected “1000births” to “1000 births”.

Inline 106 the authors write an abbreviation for "Community-based Health and Planning Services (CHPS)" but they did not use this after through the text. I strongly recommend only using abbreviations for words that are important for the text: CHPS was used once in line 289 but we have decided to deleted the abbreviated “CHPS” and maintained the full name “Community-based Health and Planning Services” in both instances (line 106 and 289)

Inline 125 the authors wrote an abbreviation for "Navrongo War Memorial Hospital (WMH)", but inline 152 and 202 they used the whole name again, I recommend using only the abbreviation after the first reference in the text: We have now used the abbreviation “WMH” in lines 126, 152 and 202

In table 1, line Estimated Gestational age (weeks), need a space between "40weeks": We have now corrected “40weeks” to “40 weeks”.

In table 1, line Maternal Age (years), need a space between "< 20years": We have now corrected “<20years” to “< 20 years births”.

Inline 229 they used an abbreviation for "Mother-To-Child Transmission (PMTCT)", as the authors did not use this abbreviation anymore through the text I suggest removing the abbreviation. We have now deleted “PMTCT”

Please, check reference again for typos. For example, in the reference number 19 there are some dots after the first name of the author, different from the other references: The dots after the first name has been deleted and reference 19 now reads “Oduro A., Ansah P, Hodgson A, Afful T, Baiden F, Adongo P, et al. Trends in the prevalence of female genital muti-lation and its effect on delivery outcomes in the kassena-nankana district of northern Ghana. Ghana Med J. 2006;40. doi:10.4314/gmj.v40i3.55258”.

We have checked other references: References 11, 14, 15 have all been edited

29 Jan 2020

Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana

PONE-D-19-24698R2

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10 Feb 2020

PONE-D-19-24698R2

Trends and risk factors associated with stillbirths: A case study of the Navrongo War Memorial Hospital in Northern Ghana

Dear Dr. Nonterah:

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