Risk factors of stillbirth in Yemen

Abstract

BACKGROUND:

Yemen has the highest stillbirth rate among the Arab countries. However, the risk factors of this high rate are lacking. This study aimed to determine the maternal, newborn, and service related risk factors for stillbirths at the main maternity hospital in Sana’a city.

METHODS:

A case-control study was conducted in the main maternity hospital in Sana’a city, Yemen. Case and controls were selected prospectively during the study period. Cases were women who delivered stillbirths after 24 weeks of gestation. Risk factors data for mothers and their neonates were collected using face-to-face interview and data abstraction from medical records.

RESULTS:

The study included 101 women with stillbirths and 202 women with singleton live births. Mothers older than 35 years (Odds ratio (OR) = 4.9) and those with low level of education were significantly more likely to give stillbirths. Prolonged labor (OR = 5.8), mothers’ anemia (OR = 2.1), less than 4 antenatal visits (OR = 5.1) and meconium stained amniotic fluid (OR = 11.5) were significantly associated with increased odds of stillbirth. Prematurity (OR = 27), umbilical complications (OR = 6.4), low birth weight (OR = 17.7), and congenital complications (OR = 40.6) were significantly associated with higher odds of stillbirths.

CONCLUSIONS:

This study identified many risk factors of stillbirth that are amenable to intervention. Encouraging women to deliver at health facilities, providing better management of obstetrical complications, proper antenatal care, and prompt referral services are essential for reduction of stillbirths in Yemen.

Keywords

Stillbirth risk factors case-control study Field Epidemiology Training program Yemen

1 Introduction

Stillbirth has a high burden for women, families, communities, and health system. The estimated average global stillbirth rate in 2015 was 18·4 per 1000 births with an estimated 2.6 million babies were stillborn at 28 weeks or more in 2015 [1]. The Every Newborn Action Plan in 2014 set a target for national stillbirth rates of 12 or fewer stillbirths per 1000 births in all countries by 2030 [2]. About 98% of stillbirths occur in low and middle-income countries [1]. Stillbirth is closely related to maternal and neonatal mortality and with the care received during pregnancy and delivery [3].

The cause of fetal death is complex as there are many contributing and interacting factors. For many stillbirths it is difficult to determine the exact cause and therefore the cause of death is classified as “unexplained”. Previous studies reported different risk factors of stillbirth, including advanced maternal age [4, 5], high pre-pregnancy body mass index (BMI) [6], smoking [7], fewer than four antenatal visits [8], fetal growth restriction [9, 10] and low socio-economic status [11]. Other risk factors such as low birth weight [12], maternal anemia [13, 14], maternal malnutrition, poor antenatal care, grand multi-parity, maternal fever, antepartum hemorrhage and maternal infections [13] were reported by other studies.

Yemen’s health indicators are among the lowest in the region and reproductive health situation is one of the least favorable in the Arab world. Three hundred sixty five women per 100,000 live births die as a result of complications of pregnancy and childbirth, making maternal death the leading cause of death among women of reproductive age in Yemen [15]. The neonatal mortality rate in Yemen is estimated to be 37 per 1000 live births, accounting for nearly half of the under 5 mortality rate which is estimated at 75 per 1000 live births [15]. The stillbirth rate in Yemen is 23 per 1000 live birth which is the highest among the Arabic countries. Furthermore, only a quarter of all deliveries are attended by skilled personnel [15].

There is scarcity of data on stillbirth in countries of the Eastern Mediterranean region including Yemen. A study in 2005 in Yemen reported a stillbirth rate of 47.2 per 1000, where stillbirths accounted for 54% of perinatal deaths. While the study reported 13.3% reduction in perinatal deaths in 4-year period, authors reported 17% increase in stillbirth [16]. The same study reported that many women attended the hospitals as emergencies after failed delivery attempts at home and arrived to the labour ward in a critical condition which is well known contributing factor for stillbirth [10].

Although that Yemen has the highest stillbirth rate among the Arab countries, the underlying risk factors of this high rate were not fully investigated. This has negatively influenced the health policy plans in Yemen, where the reproductive health system has no indicators that target perinatal health at the community or health facility level. These appear to be neglected in terms of allocation of resources and research activities. Therefore, this study was conducted to determine the maternal, newborn, and service related risk factors of stillbirths at the main maternity hospital, in Sana’a city. Such information is necessary to design interventions to reduce stillbirth rate in Yemen.

2 Methods

2.1 Study design and study population

A case-control study was conducted in the main maternity hospital in Sana’a city, Al-Sabeen maternity hospital, over a period of four months in 2013–2014. Case and controls were selected prospectively during the study period. Cases were women who delivered stillbirths during the study period, defined as the delivery of a neonate after 24 weeks of gestation with no signs of life, such as heartbeat or spontaneous respiration, after delivery. For each selected case, two women who delivered a live-born singleton neonate after 24 weeks of gestation in the same hospital and in the same period were selected as controls. The two controls for each case were selected at random to match the cases on the day of delivery. Only women with singleton fetuses were included in the study. A total of 101 cases and 202 controls were selected. The power to detect a clinically significant association (Odds ratio of 2) between any of the independent variables and stillbirth at a confidence level of 95% using this sample size exceeded 80%. The power calculation was calculated using Epicalc 2000 assuming that 50% of controls are exposed. Ethical approval was obtained from the institutional review board in the Ministry of Public Health and Population, Yemen. A consent form was signed by all participants before conducting interviews.

Table 1
The socio-demographic characteristics of women according to the status of the birth (stillbirth or alive baby)

Demographic characteristics Stillbirth (n = 101) Live births (n = 202) p-value

n % n %

Maternal age 0.008

<18 years 6 5.9 11 5.4

18–35 years 84 83.2 186 92.1

>35 years 11 10.9 5 2.5

Mother’s education <0.005

Illiterate 52 51.5 72 35.6

Primary 33 32.7 80 39.6

Secondary and higher 16 15.8 50 24.8

Mother’s employment 0.302

Yes 8 7.9 10 5

No 93 92.1 192 95

Parity 0.986

None 28 27.7 57 28.2

1–4 59 58.4 116 57.4

≥5 14 13.9 29 14.4

Demographic characteristics	Stillbirth (n = 101)	Live births (n = 202)	p-value
Maternal age					0.008
<18 years	6	5.9	11	5.4
18–35 years	84	83.2	186	92.1
>35 years	11	10.9	5	2.5
Mother’s education					<0.005
Illiterate	52	51.5	72	35.6
Primary	33	32.7	80	39.6
Secondary and higher	16	15.8	50	24.8
Mother’s employment					0.302
Yes	8	7.9	10	5
No	93	92.1	192	95
Parity					0.986
None	28	27.7	57	28.2
1–4	59	58.4	116	57.4
≥5	14	13.9	29	14.4

2.2 Data collection

Necessary data for mothers and their neonates including socio-demographic, clinical, maternal, pregnancy, delivery and other risk factors were gathered through face-to-face interview using a semi-structured form and by abstraction of data from medical records. Data were collected by a trained nurse before mother’s discharge. The study form was used to collect data on demographic, medical, and maternal characteristics of mothers including age, parity, history of miscarriages, gestational age, smoking hookah, qat chewing, preterm labor, antepartum hemorrhage, obstructed labour, pregnancy induced hypertension, eclampsia, and prenatal visits. In addition, the study form was used to collect data on newborns’ characteristics including gender, weight, prematurity and congenital malformation. The completed questionnaires were checked on daily basis by the investigator before women discharge and any inconsistencies and inaccuracies were corrected.

2.3 Statistical analysis

Data were analyzed using the Statistical Package for Social Sciences (SPSS) version 20. Data were described using frequencies and percentages. The differences between proportions were analyzed using Chi-square test. Binary logistic regression analysis was used to determine the factors associated with stillbirth. A p-value of less than 0.05 was considered statistically significant.

3 Results

This study included a total of 101 stillbirths and 202 singleton live births. The age of their mothers ranged from 14 to 40 years with a mean (SD) of 26.3 (6.0) year. Table 1 shows their mothers’ socio-demographic characteristics. Stillbirths were more likely to be born to mothers older than 35 years and mothers of low educated level.

Table 2 shows the distribution of maternal and fetal risk factors for stillbirths among cases and controls. The majority (71%) of stillbirth deliveries and 17% of live birth deliveries were premature. Stillbirths were significantly more likely to be born to mothers who had prolonged labor, anemia, meconium stained amniotic fluid, and less than 4 antenatal visits. Umbilical complication, low birth weight and congenital malformation were significantly higher among the stillbirths than the controls (Table 2).

Table 2
Distribution of maternal and fetal risk factors for stillbirths and live births

Maternal and fetal variables Stillbirth (n = 101) Live births (n = 202) P-value

n % n %

Premature delivery 72 71% 17 8% 0.005

Prolonged labor 38 38% 19 9% 0.005

Mother’s anemia 27 27% 30 15% 0.013

Meconium stained amniotic fluid 19 19% 4 2% 0.005

Antenatal care visits 0.005

<4 visits 89 88% 120 59%

≥4 visits 12 12% 82 41%

Umbilical complications 21 21% 8 4% 0.005

Low birth weight 77 76% 31 15% 0.005

Congenital malformation 17 17% 1 1% 0.005

Maternal and fetal variables	Stillbirth (n = 101)	Live births (n = 202)	P-value
Premature delivery	72	71%	17	8%	0.005
Prolonged labor	38	38%	19	9%	0.005
Mother’s anemia	27	27%	30	15%	0.013
Meconium stained amniotic fluid	19	19%	4	2%	0.005
Antenatal care visits					0.005
<4 visits	89	88%	120	59%
≥4 visits	12	12%	82	41%
Umbilical complications	21	21%	8	4%	0.005
Low birth weight	77	76%	31	15%	0.005
Congenital malformation	17	17%	1	1%	0.005

Table 3 shows the multivariate analysis of factors associated with stillbirth. All studied factors were significantly associated with stillbirth except the working status of the mother and the parity. Mothers older than 35 years (Odds ratio (OR) = 4.9) compared to mothers aged 18–35 years and those with low level of education were significantly more likely to give stillbirths. Prolonged labor (OR = 5.8), mothers’ anemia (OR = 2.1), less than 4 antenatal visits (OR = 5.1) and meconium stained amniotic fluid (OR = 11.5) were significantly associated with increased odds of stillbirth. Prematurity (OR = 27), umbilical complications (OR = 6.4), low birth weight (OR = 17.7), and congenital complications (OR = 40.6) were significantly associated with higher odds of stillbirths.

Table 3

The multivariate analysis of factors associated with stillbirth*

Variables	Adjusted odds ratio	95% confidence interval
Maternal age
<18 years	1.2	0.4–3.4
18–35 years	Ref
>35 years	4.9	1.6–14.5
Mother’ education
Illiterate	1.8	1.02–3.0
Primary	2.3	1.2–4.4
Secondary and higher	Ref
Gestational age (Preterm vs. full term)	27.0	13.9–52.2
Prolonged labor	5.8	3.1–10.8
Mother’s anemia	2.1	1.2–3.8
Meconium stained amniotic fluid	11.5	3.8–34.8
Antenatal care visits
<4 visits	5.1	2.6–9.9
≥4 visits	Ref
Umbilical complications	6.4	2.7–14.9
Low birth weight	17.7	9.7–32.1
Congenital malformation	40.6	5.3–310.6

^*Employment of mother and parity were tested in the model and were found non-significant.

4 Discussion

There is scarcity of information on risk factors of stillbirth in Yemen. This study identified many risk factors including demographics, maternal and fetal, and health service related factors. The most common risk factors for stillbirths in developing countries include the lack of a skilled attendant at delivery, low socioeconomic status and poor nutrition, prior stillbirths, and advanced maternal age [17]. In many developing countries, one third or more of the women in labor are attended by skilled birth attendants and deliver at home [18]. In Yemen, only a quarter of all deliveries are attended by skilled personnel [15] and this finding explains the high stillbirth rate in Yemen because of the complications associated with lack of skilled care at delivery. Women who lack skilled care at delivery and who do not have access to emergency obstetrical care are among those at greater risk for stillbirth.

In most geographic areas, maternal age, low socioeconomic status and lack of education had been associated with increased stillbirth rates [19 –22]. This study showed that mothers older than 35 years and those with low level of education were significantly more likely to give stillbirths. This finding is consistent with previous studies that showed that advanced maternal age and maternal illiteracy were associated with adverse delivery outcome [4 , 22].

Many studies noted the association of several maternal and fetal risk factors with stillbirth. Consistent with the findings of other studies [4 , 23], this study demonstrated that preterm labor, prolonged labor, and anemia among mothers were associated with increased odds of stillbirths. Our finding of higher stillbirth rate among anemic women support the findings of previous studies that reported that anemic mothers and those with poor antenatal care had 8 times higher risk to have stillbirth compared to non-anemic mother and those with adequate antenatal care [4 , 13]. The relationship with prolonged labor was not unexpected, since it is well known that in many developing countries, prolonged and obstructed labor and associated asphyxia, is a major cause of stillbirth [23].

Umbilical cord pathology includes prolapse, true knots, stricture, and strangulation of the fetus. Umbilical cord pathology (OR = 6.4) was significantly associated with higher odds of stillbirths. It has been reported that the risk of umbilical cord pathology increases as the pregnancy continues and may lead to more fetal demise outcomes in late pregnancy [24]. The risk of cord problems result in vessel compression and cessation of blood flow as well as fetal perfusion in the third trimester [25, 26]. Because most cord accidents are sudden and unpredictable, pregnant women need to pay attention to subjective fetal movement to prevent delayed diagnosis. Fortunately, the prognosis for future pregnancies is believed to be favorable.

Congenital complications were significantly associated with higher odds of stillbirths. Fetuses born with an abnormal anatomy are at high risk of infection and have genetic abnormalities [27]. About 10–20% of stillbirths are attributed to intrinsic fetal anomalies [28, 29]. One study determined that the risk of major congenital anomaly among stillbirths was 20-fold higher compared to that among live births, and most anomalies were anencephaly [30]. There are other important factors that were not investigated in our study such as smoking [31] and other maternal medical illnesses [32, 33]. There is about 10% of all stillbirths being related to maternal medical illnesses [32]. Among these diseases, hypertension and diabetes mellitus are the most common [33].

Stillbirth prevention does not need a separate set of intervention programmes from antenatal and intrapartum care. An improved and strengthened perinatal care system must bring together evidence-based medicine, modern medical technology, and family-centered care. Improving care for both mothers and children requires that all main pillars of the health system are in place, since improved care and outcomes cannot be ensured if there are major deficiencies in key components such as organization and delivery of services, health system financing, information systems and human resources creation and management. The current system of maternal and perinatal and in Yemen needs to be better organized and coordinated among different levels of care with clearly defined competencies and volume of services, staff and equipment, and referral practices. An efficient referral system which directs high risk pregnancies to institutions with optimum facilities and equipment and personnel technical skills will improve perinatal outcomes and survival. Moreover, there are broad opportunities in Yemen to improve and achieve better quality of maternal and perinatal health care and health outcomes. Low-cost and evidence-based interventions that reduce mortality in preterm and low birthweight babies need immediate attention. Interventions directed towards improving the provision of advanced antenatal care (e.g. detection and management of hypertensive disorders during pregnancy, maternal-fetal infections, timely detection and management of fetal growth restriction, etc) and quality of comprehensive emergency obstetric care have to be targeted simultaneously to substantially reduce major proportions of stillbirths. The interventions of top action priority in Yemen include periconceptional folic acid fortification, iron supplementation, detection and management of maternal diseases in pregnancy, detection and management of fetal growth restriction, basic emergency obstetric care and comprehensive emergency obstetric care and health education. One of the central recommendations for reducing perinatal and neonatal mortality is the use of and compliance with clinical practice guidelines. Improved compliance with guidelines can be achieved through the establishment of a system of periodic criterion-based clinical audits. Case reviews should be used to investigate causes of fetal, neonatal and perinatal mortality. They should focus on identifying preventable deaths that are caused by health system failure or insufficient quality of care. Audit results have to be used to develop recommendations for improving processes of care, ensuring feedback to clinicians and identifying actions required to improve quality of care. In addition, improving the quality of maternal and neonatal health services requires a competent health workforce and effective policies to address human resources challenges faced by the health care system in Yemen.

In conclusion, the main risk factors for stillbirths in Sana’a include mothers’ age > 35 years, low level of education, prolonged labor, mothers’ anemia, less than 4 antenatal visits, meconium stained amniotic fluid, prematurity, umbilical complications, low birth weight and congenital complications. Many of these risk factors are amenable to intervention. There is an urgent need to educate pregnant women about risk factors for stillbirths during antenatal visits. Encouraging women to deliver at health facilities and providing better management of obstetrical complications may help to reduce the burden of stillbirths. Proper antenatal care, prompt referral services and availability of emergency obstetric care will provide a pivotal role for reduction of stillbirths in Yemen.

Disclosure statements

- All authors have no conflict of interest.

- Authors affirm that this research was conducted in accordance with the ethical standards of all applicable national and institutional committees and the World Medical Association’s Helsinki Declaration.

Footnotes

Acknowledgments

Authors would like to acknowledge the Training Programs in Epidemiology & Public Health Interventions Network (TEPHINET) and Yemen Field Epidemiology Training Program for their technical support.

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