Maternal, prenatal and traditional practice factors associated with perinatal mortality in Yemen

G Model WOMBI 825 No. of Pages 12

Women and Birth xxx (2018) xxx–xxx

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Maternal, prenatal and traditional practice factors associated with perinatal mortality in Yemen Ahmed H. Al-Shahethia , Rafdzah Ahmad Zakib,* , Abdul Wahed A. Al-Serouric , Awang Bulgibab a b c

Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia Julius Centre University of Malaya, Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia Department of Community Medicine, University of Medicine and Health Sciences, Sana’a, Yemen

A R T I C L E I N F O

A B S T R A C T

Article history: Received 28 December 2017 Received in revised form 14 May 2018 Accepted 25 June 2018 Available online xxx

Background: Perinatal mortality remains a major international problem responsible for nearly six million stillbirths and neonatal deaths. Objectives: To estimate the perinatal mortality rate in Sana’a, Yemen and to identify risk factors for perinatal deaths. Methods: A community-based prospective cohort study was carried out between 2015 and 2016. Ninehundred and eighty pregnant women were identified and followed up to 7 days following birth. A multistage cluster sampling was used to select participants from community households’, residing in the five districts of the Sana’a City, Yemen. Results: Total of 952 pregnant women were tracked up to 7 days after giving birth. The perinatal mortality rate, the stillbirth rate and the early neonatal mortality rate, were 89.3 per 1000, 46.2 per 1000 and 45.2 per 1000, respectively. In multivariable analysis older age (35+ years) of mothers at birth (Relative Risk = 2.83), teenage mothers’ age at first pregnancy (<18 years) (Relative Risk = 1.57), primipara mothers (Relative Risk = 1.90), multi-nuclear family (Relative Risk = 1.74), mud house (Relative Risk = 2.02), mothers who underwent female genital mutilation (Relative Risk = 2.92) and mothers who chewed khat (Relative Risk = 1.60) were factors associated with increased risk of perinatal death, whereas a positive mother’s tetanus vaccination status (Relative Risk = 0.49) were significant protective factors against perinatal deaths. Conclusion: Rates of perinatal mortality were higher in Sana’a City compared to perinatal mortality at the national level estimated by World Health Organization. It is imperative there be sustainable interventions in order to improve the country’s maternal and newborn health. © 2018 Australian College of Midwives. Published by Elsevier Ltd. All rights reserved.

Keywords: Perinatal mortality Risk factors Stillbirth Newborn Yemen

Statement of significance

Problem or issue Yemeni women have significantly higher rate of perinatal mortality including stillbirths and early neonatal mortality according to World Health Organization estimation. Perinatal mortality risk factors never studied before at community-based setting in Yemen.

What is already known Perinatal mortality rate and some of risk factors were estimated in one hospital as retrospective study in 2005 in Sana’a City, Yemen. What this paper adds Estimate the perinatal mortality rate and risk factors, especially traditional factors as female genital mutilation, water pipe and orange snuff smoking and chewer khat during pregnancy through community-based cohort study in Sana’a Capital City of Yemen.

* Corresponding author at: Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia. E-mail address: [email protected] (R.A. Zaki). https://doi.org/10.1016/j.wombi.2018.06.016 1871-5192/© 2018 Australian College of Midwives. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: A.H. Al-Shahethi, et al., Maternal, prenatal and traditional practice factors associated with perinatal mortality in Yemen, Women Birth (2018), https://doi.org/10.1016/j.wombi.2018.06.016

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1. Introduction The perinatal period is an extremely important phase of life. It is a sign of the quality of prenatal, obstetric, and early neonatal care that is given to mothers and newborns.1 Perinatal mortality remains a major public health challenge globally, which responsible for almost three million stillbirths and a similar number of neonatal deaths each year.2 Annually, babies die before they have reached one month of age owing to birth asphyxia conditions, for example, prematurity and serious infections.3 The World Health Organization estimates the perinatal mortality rate (PNMR) in the developed countries is about one percent of total births; this compares to under-developed countries with 5% of total births.4 The Eastern Mediterranean Region (EMR) PNMR is 49 per 1000 live births; the region shares 10.6% and 15.6% of the global burden of maternal and newborn deaths, respectively.5 In the EMR 910,000 newborn deaths take place in the region and the stillbirth rate is 27 per 1000 total births.6 Amazingly, there has been a great lack of realisation of the extent of perinatal conditions and their contribution in developing countries to both perinatal and early neonatal mortality. This is due to the preponderance of unregistered births and as a result, policymakers do not realise the extent of perinatal deaths. Yemen’s perinatal conditions are proving to be a major health problem. Two previous surveys have been conducted the country’s Indicators Multi-cluster Survey in 2006 and the Yemen National Health and Demographic Survey 2013.7,8 Neonatal mortality was reported to be 37 and 27 per 1000 live births respectively in those surveys. There was just a 27% reduction in neonatal mortality rate over a 7-year period.8 Neither survey yielded information about stillbirths or early neonatal mortality; each of these is a key indicator of prenatal services, birth care and early neonatal care. This has had a detrimental effect on healthcare policy plans in Yemen and as such the healthcare system does not have

programmes focused on perinatal health at the level of the community or health facility. It seems these are neglected in terms of allocation of resources and research activities. Yemen is a low-income country and in 2013 it had a population of 24.5 million. The most recent available information reveals that members of 37.3% of households live below the national poverty line8,9 and only 59% are using improved drinking water with fewer than 50% having adequate sanitation facilities. The mortality rate for children below the age of 5 is reported to be 53 out of 1000 live births with 39% of Yemeni children under the age of 5 years old being malnourished. Infant mortality is estimated to be 43 out of 1000 live births, with 44% of infants being born with a birth weight of less than 2500 g.8 A total of 43% of Yemeni women are illiterate with a total fertility rate of 4.4.8 Just 60% of pregnant women receive antenatal care (ANC) and consequently the maternal mortality ratio (MMR) is estimated at 148 per 100,000 live births.8 In Yemen, 30% of births take place at a health facility with just 45% of deliveries attended by skilled birth attendants. In order to plan effective interventions, it is crucial to estimate the rate and determine the risk factors linked with perinatal mortality via a community-based prospective study. Previous estimation of PNMR in Yemen were either from retrospective hospital-based study10 or by non-governmental organisation (NGO) household surveys; which have limitation with selection and recall bias. In addition, risk factors for perinatal mortality in Yemen were poorly recorded and not well understood. Therefore, the aim of this prospective follow up community-based study was to estimate the PNMR and identify the potential risk of perinatal death in Yemen’s communities. 2. Methods and analysis This is a prospective community-based cohort study, which was conducted in Sana’a City, the capital of Yemen from 1 August 2015 to

Fig. 1. Flow chart of participants selection (EA: Enumerations Area).

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31 December 2016. It was conducted among pregnant women of age 15 years to 49, residing in the five districts of the Sana’a City Governorate, Yemen. Sana’a City.11 All pregnant women were followed up to seven days post-delivery or 7 days following termination of their pregnancies (spontaneous or induced abortion). 2.1. Sample selection and study participants Sana’a City governorate has an estimated population of 2.35 million, with approximately 521,862 being in the reproductive age group, according to the national census.12 It is located in the centre of Yemen and subdivided into ten districts which contain 1619 enumeration areas (EAs) with 234,020 household. The EA is a specific geographical area with an average size of 144 households. This list of households was used as the study sampling frame. Therefore, each selected EA was a sampling cluster. A two-stage cluster sampling was used to choose study subjects (Fig. 1). In the first stage, five representative districts, Al-Safyah, AlThawrah, Shu’ub, Al-Tahreer and Ma’ain, were chosen at random from ten districts available in the governorate Sana’a City. In the second stage, proportionate sampling was conducted to select 49 EAs from a total of 863 EAs within the five districts. Each EA represents as one cluster in this study. A total of 20 households per cluster was chosen by systematic random sampling from a list of houses provided by the Sana’ city authority. The WHO recommended a sample of 20–30 household per cluster with absolute maximum of 50 respondents per primary sampling unit (PSU).13 All pregnant women (at any stage of pregnancy) reside in the study area between August 2015 to December 2016 in Sana’a city were included in this study. In the occasion where two or more eligible women discovered in a selected household; only one of the women chosen at random and included in this study. If there were no eligible women in the selected household, the next household was visited. All pregnant women must consented to participate in the studyand had no intention to leave the area up to 12 months of the study period. Womenwith severe illness, learning difficulties or psychiatric disorder were exclude in this study. Information gathered from respondents included socio-demographic, maternal reproductive characteristic, prenatal care of present pregnancy and traditional practices. 2.2. Sample size calculation Using the OpeEpi software for cohort study, the sample size was calculated. The minimum identifiable risk ratio for primary and secondary outcomes among those exposed to factors, was estimated 1.78 based on literature study in Tunisia.14 The proportion of perinatal mortality was estimated to be 6.5% based on the World Health Organisation (WHO) estimation.15 Power and two-sided α were set at 80% and 0.05, respectively. The sample size was then increased by 15% to overcome for any objection or dropout during the follow-up. The final sample size was 980 pregnant women. 2.3. Data collection and variables Thirteen midwives were chosen as interviewers; they had been trained in local cultures, languages, privacy belief confidentiality and instructed in how to build relationships. In addition, they were trained in how to use the questionnaires and conduct interview. The aim and reason of this study was made clear to the participant. Once the woman agreed to participate and fulfilled all the inclusion criteria, they were then asked to give their consent either by giving their signature or put their thumb impressions on the consent forms. Information on perinatal death was collected using a standard World Health Organization questionnaire that was translated to Arabic by qualified language lecturer and validated in a pilot study.16

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The questionnaire sought information concerning socio-demographic characteristics (age, residence, education, parity, etc.), along with past awareness of perinatal death, both prenatal and antenatal care, traditional practices, current birth methods, breastfeeding and condition of newborns soon after birth. Baseline information were collected at recruitment stage and follow up information were collected at monthly interval up to seven days post-delivery or 7 days following termination of their pregnancies (spontaneous or induced abortion). Information at baseline and after delivery were collected by face to face interview. All women were contacted by telephone during monthly follow up by the interviewers with the supervision of the principal investigators. Women were contacted within three to four days of the scheduled day and at least 5 attempts, at different times of the day and early evening, before they were considered to be lost-to follow-up from the study. This study aimed to estimate PNMR and look into the factors linked to perinatal deaths. Perinatal death was defined as: pregnancy loss taking place following (a) 7 completed months of gestation (stillbirth); or (b) death within the first 7 days of the birth of a live born neonate (early neonatal death). We also calculated the stillbirth rate (this is the number of babies born with no indication of life after 28 weeks or 7 months’ gestation per 1000 pregnancies) and early neonatal mortality rate (number of deaths in the first 7 days of life per 1000 live births). In addition, perinatal mortality rate was estimated as the number of deaths per 1000 births. Live births were identified by the mothers and defined as: any baby delivered after 28 weeks or 7 months of gestation with signs of life. 2.4. Data management and analysis Raw data were entered into SPSS Software (SPSS Inc., Chicago.II. USA, version 23.0) for data management. The data were checked prior to being analysed and cleaned; this involved surveying frequency tables along with logical errors and identifying outliers. Only subjects with complete information on variables included in the final analysis. The quantitative variables were handled in the analysis by grouped (e.g. age was grouped into less than 18 years, between 18 and 34 years and 35 years and more). Cleaned data were then transferred into Stata 11 (Stata-Corp, Texas 77845 USA) in order to estimate adjusted Relative Risk (RR) and 95% confidence intervals (CIs) of the independent variables on perinatal mortality which cannot be done using SPSS software. Adjusted RR was estimate using multivariable generalised linear models (GLMs) regression analysis with a log link and binomial distribution. All variables were initially included in the analyses. However, only variables associated with perinatal deaths giving a P-value < 0.25 were retained in the model, and as well as backward elimination the variables one by one was performed. No significant interaction was found for the variables tested in the model. Possible associated factors in the multivariable analysis model were examined for signs of collinearity. This was demonstrated in one of two ways: either by alterations in the direction of the effect between the univariate and multivariable analysis; or improbable standard mistakes for a given variable. 2.5. Ethical consideration Ethics approval was granted on 15/06/2015 from the Ethical Review Board of Ministry of Public Health and Population of Yemen (G 7/77). Approval also was obtained from the local district administrative and Sana’a City health offices. The mothers or guardians of those participating in the study gave their verbal consent. The respondent’s right to disengage from the interview or not to participate was informed and respected. The outcomes of the research were passed on to government offices. Most important of all, the outcomes were transmitted to the study subjects and

Please cite this article in press as: A.H. Al-Shahethi, et al., Maternal, prenatal and traditional practice factors associated with perinatal mortality in Yemen, Women Birth (2018), https://doi.org/10.1016/j.wombi.2018.06.016

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community members of the community via a health extension worker. 3. Results A total of 980 pregnant women were identified in the 49 clusters, but 8 women refused to participate (0.8%) in the study because did not get approval from their husbands for various reasons (lack of interest (3), health problems (2) and not satisfied with previous health surveys (3)). Two women were missing at follow up (0.2%) and 1 woman died and excluded. Of the nine hundred sixty-nine (969) pregnant women included, 6 had multiple births (all twins) and 11 spontaneous abortions were excluded from further follow-up as stipulated by the study protocol. The remaining nine hundred fifty-two (952) mothers with single birth completed the 7 days follow-up (Fig. 2). 3.1. Characteristics of mothers More than three quarters (85.3%) of the births in the sample were women aged 18–34. The mean age of women at recruitment was 26.3 years (SD 5.7). Only 3.3% of the births were to women less than 18 years. The proportion of mothers aged less than 18 years at first marriage was 36.1% while 27.8% was mothers aged less than 18 years at first pregnancy. Most mothers came from slum areas (59.3%), and the proportion of illiteracy was 18.3%. Only 26.3% of the women were nulliparous. Around 10% of multiparous mothers had previously experienced a perinatal death. The median gestational age of the women in the study at enrolment was 6.3 months. A total of 642 women (72%) went for antenatal care (ANC) prior to birth. ANC attendance differed

according to parity and 33.2% of nulliparous mothers completed in excess of four ANC visits. This compared to 66.8% among multiparous mothers. Among births whose mothers received ANC, nearly half (48.2%) received the initial visit during the first trimester of pregnancy, whereas 31.6% waited until the third trimester of pregnancy to seek care. In spite of high attendance at antenatal clinics, 41.3% (393) of births were delivered at home where 20.8% (198) of births were assisted by untrained health personnel. Nine percent of women were cigarettes smokers, while 20.2% were water pipe tobacco smokers. Around half of the women (50.0%) were khat chewers, and 3% of the women had a history of female genital mutilation. Detail of other characteristics are shown in Table 1. 3.2. Outcome of pregnancy The 969 pregnancies resulted in 952 singleton births, of which 44 were stillbirths (SBR = 46.2 per 1000 births, 95% CI: 32.7–59.3). There were 41 ENDs (ENMR = 45.2 per 1000 live births, 95% CI: 31.7–58.7), and one maternal deaths (MMR = 105 per 100,000 live births, 95% CI: 101.1–311.2). Thus, the PNMR was 89.3 per 1000 births (95% CI: 71.2–107.4) (Table 2). 3.3. Distribution of stillbirths There were 44 stillbirths that occurred in 27 out of 49 clusters. The highest observed risk in a cluster was 166.7 per 1000 births (Table 3). Twelve clusters had the highest stillbirths rate and represented 66% of the total stillbirths. Of these seven cluster could be classified as slum areas and accounted for around one third (32%) of the total stillbirths. There were no remarkable

Fig. 2. Flow chart of recruitment, follow up and outcome of the study.

Please cite this article in press as: A.H. Al-Shahethi, et al., Maternal, prenatal and traditional practice factors associated with perinatal mortality in Yemen, Women Birth (2018), https://doi.org/10.1016/j.wombi.2018.06.016

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Table 1 Distribution of respondents according to socio-demographic, prenatal and traditional practice among 952 pregnant, Sana’a City, Yemen, 8/2015–12/016. Variables/factors

Total births (n = 952)

n

%

Mother’s age (years) <18 18–34 35 or more

Mean: 26.25, a Sd: 5.70, min: 15, max: 45 31/952 3.3 812/952 85.3 109/952 31.7

6/31 56/812 23/109

19.4 6.9 21.1

Mother’s age at first marriage (years) <18 18–34 35+

Mean: 19.37, SD: 3.75, min: 10, max: 35 344/952 36.1 605/952 63.6 3/952 0.3

41/344 43/605 1/3

11.9 7.1 33.3

Mother’s age at first pregnancy (years) <18 18–34 35+

Mean: 20.13, SD: 3.87, min:12, max: 37 265/952 27.8 681/952 71.5 6/952 0.6

35/265 48/681 2/6

13.2 7.0 33.3

Parity Primipara 0 1 2–4 >/ = 5

250/952 231/952 387/952 84/952

Mean: 2.6, Sd: 1.65 26.3 24.3 40.7 8.8

25/250 13/231 36/387 11/84

10.0 5.6 9.3 13.1

Place of residence (district) Urban Slum

387/952 565/952

40.7 59.3

27/387 58/565

7.0 10.3

Mother’s level of education Illiteracy Primary/intermediate Secondary University and above

174/952 382/952 283/952 113/952

18.3 40.1 29.7 11.9

17/174 38/382 23/283 7/113

9.8 9.9 8.1 6.2

Mother's work Yes No

69/952 883/952

7.2 92.8

4/69 81/883

5.8 9.2

Number of family members 2–4 5–7 8 or more

372/952 297/952 283/952

39.1 31.2 29.7

30/372 31/297 24/283

8.1 10.4 8.5

Type of house Cement Mud

759/952 193/952

79.7 20.3

58/759 27/193

7.6 14.0

Family type Multi-nuclear Nuclear

427/952 525/952

44.9 55.1

48/427 37/525

11.2 7.0

Number of antenatal visit Not visit 4 5

32/952 682/952 238/952

3.4 71.6 25.0

4/32 59/682 22/238

12.5 8.7 9.2

Timing at first ANC visit (n = 917) First trimester Second trimester Third trimester

442/917 185/917 290/917

48.2 20.2 31.6

27/442 16/185 37/290

6.1 8.6 12.8

Use of contraception in preceding interval (n = 730) Yes No

517/730 213/730

70.8 29.2

41/517 21/213

7.9 9.9

Maternal Tetanus Toxoid vaccine Received Not received

747/952 205/952

78.5 21.5

52/747 33/205

7.0 16.1

Spacing (n = 730, primigravidae excluded) >24 months 24–60 months >60 months

302/730 298/730 130/730

Mean 36.10, Sd 28.98 41.4 40.8 17.8

21/302 25/298 16/130

7.0 8.4 12.3

Maternal Anaemia (g/dl)(n = 951) <12 g/dl 12 g/dl

207/951 744/951

Mean 12.46, Sd 1.35 21.8 78.2

24/207 61/744

11.6 8.2

n

Perinatal deaths (n = 85) %

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Table 1 (Continued) Variables/factors

Total births (n = 952)

Perinatal deaths (n = 85)

n

%

n

%

Maternal arm circumference (MUAC, cm) <21 cm (severe acute malnutrition) 21–22.9 cm (moderate acute malnutrition) 23 or more cm (normal)

15/951 41/951 895/951

Mean 26.85, Sd 3.01 1.6 4.3 94.1

1/15 3/41 81/895

6.7 7.3 9.1

Previous perinatal deaths Yes No

104/952 848/952

10.9 89.1

13/104 72/848

12.5 8.5

Female genital mutilation Yes No

24/952 928/952

2.5 97.5

6/24 79/928

25.0 8.5

Cigarette smoking Smoker Not smoker

81/952 871/952

8.5 91.5

9/81 76/871

11.1 8.7

Water pipe smoking (shisha) Yes No

192/952 760/952

20.2 79.8

20/192 65/760

10.4 8.6

Use orange snuff (smokeless tobacco) Yes No

16/952 936/952

1.7 98.3

4/16 81/936

25.0 6.7

Khat chewer during this pregnancy Yes No

476/952 476/952

50.0 50.0

54/476 31/476

11.3 6.5

Place of birth Home birth Health facility birth

393/952 559/952

41.3 58.7

33/393 52/559

8.4 9.3

Birth attendants Trained personnel Untrained personnel

752/952 200/952

79.0 21.0

62/752 23/200

8.2 11.5

a

Sd — standard deviation.

differences in proportion of stillbirths between urban (4.7%) and slum areas (4.6%). 3.4. Distribution of early neonatal deaths There were 867 single live births and 41 early neonatal deaths, a neonatal mortality rate of 45.2 per 1000 live births. These early neonatal deaths occurred in 26 clusters, which were mainly in the slum settings (51.2%) (see Table 3). Twenty out of the 41 babies who died within the first week were born at home (48.9%) and only 27 of them had a skilled birth attendant. 3.5. Socio-demographic variables (Table 4A) There is a highly significant association between perinatal mortality and mother age at birth. With regards to age at birth,

teenage mothers (aged <18) and older women (aged 35 and above) were observed to have higher perinatal deaths (RR 2.81; 95% CI: 1.31–6.01) and (RR 3.06; 95% CI: 1.97–4.76) respectively. Mother’s age at first marriage <18 years increased the risk of perinatal deaths (RR 1.68; 95% CI: 1.12–2.52) compared to other age groups, whereas mother’s age at first pregnancy (aged <18) and older women (aged 35 and above) increased the risk of perinatal deaths (RR 1.87; 95% CI: 1.1.24–2.83) and (RR 4.73; 95% CI: 1.48–15.15), respectively compare to other age groups. The result also indicates that mothers with higher parities (five and above) were 2.33 times more likely to experience a perinatal death (95% CI: 1.08–4.99). Babies who lived with a multi-nuclear family in a house were 1.60 times more likely to be died in perinatal period compared to those who live in a house with one nuclear family only (95% CI: 1.07–2.62). In addition, type of house was also associated with perinatal deaths, where those babies

Table 2 Outcome of pregnancy in a cohort of 952 births, Sana’a City, Yemen, 8/2015–12/2016. Pregnancy outcomes

Total number

Mortality rate

(95% confidence interval)

Total singletons births Total live singletons births Still births Early neonatal deaths Perinatal deaths Maternal deaths ratio

952 908 44/952 41/908a 85/952 1/952

46.2 per 1000 birth 45.2 per 1000 live births 89.3 per 1000 births 105 per 100,000 live births

(32.7–59.3) (31.7–58.7) (71.2–107.4) (101.1–311.2)

a

Only live births (908) were used in the denominator.

Please cite this article in press as: A.H. Al-Shahethi, et al., Maternal, prenatal and traditional practice factors associated with perinatal mortality in Yemen, Women Birth (2018), https://doi.org/10.1016/j.wombi.2018.06.016

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Table 3 Distribution of stillbirth rate (SBR), early neonatal mortality rate (ENMR) and perinatal mortality rate (PNMR) per clusters among 952 births, Sana’a City, Yemen, 8/2015–12/ 2016. No.

District

No. of clusters

Number of births/expected total birth (%)

SBR N(/1000)

ENMR N(/1000)

PNMR N(/1000)

1 2 3 4 5

Al-Safyah Al-Thawrah Shu’ub Al-Tahreer Ma’ain

6 10 13 4 16

118/120 (93.3) 194/200 (97.0) 253/260 (97.3) 75/80 (93.8) 312/320 (97.5)

6(50.8) 7 (36.1) 6 (23.7) 5 (66.7) 20 (64.1)

1 (8.9) 6 (32.1) 7 (28.3) 2 (28.6) 25 (85.6)

7 (59.3) 13 (67.0) 13 (51.4) 7 (93.3) 45(144.2)

Total

49

952/980 (97.1)

44/(46.2 per 1000 births)

41/(45.2 per 1000 live births)

85/(89.3 per 1000 births)

born in mud houses had 1.83 times higher risk (95% CI: 1.19–2.81) of having perinatal deaths compared to babies who were born in cement houses. 3.6. Prenatal factors (Table 4B) Those mothers who had their first visit in the third trimester of pregnancy were 2.09 times more likely than mothers who had their first visit in the first trimester to have perinatal deaths (95%

CI: 1.30–3.35). Furthermore, mothers who received tetanus toxoid vaccine had decreased risk of perinatal deaths by 57% relative to the mothers who had not received tetanus toxoid vaccine (RR 0.43; 95% CI: 0.29–0.65). Inter-pregnancy interval (p = 0.19), use of contraception in the preceding pregnancy interval (p = 0.39), history of previous perinatal deaths (p = 0.22), maternal anaemia (p = 0.13) and maternal arm circumference (p = 0.89) did not appear to be associated with perinatal deaths.

Table 4A Risk factors for perinatal mortality (PM) in bivariate analysis in a cohort of 952 births, Sana’a City, Yemen, 8/2015–12/2016. Variables/exposures

a

PM/total (%)

Unadjusted RRb

(95% CI)c

p-value

A. Socio-demographics: Mother’s age at birth (years) <18 18–34 35

6/31 (19.4) 56/812 (6.9) 23/109 (21.1)

2.81 1 3.06

1.31–6.01

0.008

1.97–4.76

<0.001

Mother’s age at first marriage (years) <18 18–34 35

41/344 (12.0) 43/605 (7.1) 1/3 (33.3)

1.68 1 4.69

1.12–2.52

0.013

0.92–23.84

0.062

Mother’s age at first pregnancy (years) <18 18–34 35

35/265 (13.2) 48/681 (7.0) 2/6 (33.3)

1.87 1 4.73

1.24–2.83

0.003

1.48–15.15

0.009

Place of residence (district) Urban Slum

27/387 (7.0) 58/565 (10.3)

1 1.47

0.95–2.28

0.084

Mother’s level of education Illiteracy Primary/intermediate Secondary University and above

17/174 (9.7) 38/382 (9.9) 23/283 (8.1) 7/113 (6.2)

1.58 1.61 1.31 1

0.68–3.68 0.74–3.50 0.58–2.97

0.292 0.233 0.515

Mother’s work Yes No

4/69 (5.8) 81/883 (9.2)

1 1.58

0.60–4.19

0.355

No. of family member 2–4 5–7 8

30/372 (8.1) 31/297 (10.4) 24/283 (8.5)

0.95 1.23 1

0.57–1.59 0.74–2.04

0.858 0.423

Family type Nuclear Multi-nuclear

37/525 (7) 48/427 (11)

1 1.6

1.07–2.62

0.025

Type of house Cement Mud

58/759 (7.6) 27/193 (14.0)

1 1.83

1.19–2.81

0.006

a b c

PM — perinatal mortality. (RR) — unadjusted Relative Risk. CI — confidence interval.

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3.7. Traditional practice factors (Table 4C)

4. Discussion

The unadjusted analysis showed that mothers who underwent female genital mutilation (RR 2.94; 95% CI: 1.42–6.06), who used orange snuff (smokeless tobacco) (RR 2.89; 95% CI: 1.21–6.92), and khat chewers (RR 1.74; 95% CI: 1.14–2.66) were factors associated with increased risk of perinatal deaths.

This study found a PNMR of 89.3 per 1000 births (95% CI: 71.2– 107.4) in the slums — urban area of Yemen which is higher than figures reported in the previous Yemeni hospital-based study (87.4 per 1000 births)10 and rate reported by WHO (65 per 1000 births). The PNMR found in this study also greater than that the wide range of rates reported in many studies from different developing countries (36–74 per 1000 births).17,18 Previous study in Yemen discovered that severity of condition at hospital admission was the strongest risk factor for maternal and neonatal mortality.10 A large number of women failed to seek medical care at an opportune time following signs of birth complications.19 Furthermore, the poor health system in Sana’a city could resulted in poor standard of healthcare throughout pregnancy and birth.20 In addition, a low education level among Yemen’s women may have significantly impacted the PNMR in Yemen.8 The risk factors identified in this study, were maternal age at birth, mother’s age at first marriage, mother’s age at first pregnancy, parity, family type, type of house, number of trimester pregnant at time of first ANC, mother being unimmunized for at

3.8. Multivariable analysis: predictors of perinatal deaths In the multivariate analysis, the risk of perinatal death was adjusted for socio-demographics factors, prenatal factors and some variables of traditional practices factors. Backward elimination of the variables one by one was done to obtain the final model (Table 5). In this model, the variables that are observed to significantly influence perinatal deaths are mother’s age at birth, mother’s age at first pregnancy, parity, multi-nuclear family, mud type of house, female genital mutilation and khat chewer. Maternal tetanus toxoid vaccine was found to be significant protective factors of perinatal deaths.

Table 4B Risk factors for perinatal mortality (PM) in bivariate analysis in a cohort of 952 births, Sana’a City, Yemen, 8/2015–12/2016. Variables/exposures

a

PM/total (%)

Unadjusted RRb

(95% CI)c

p-value

B. Prenatal care Antenatal care None 4 5

4/32 (12.5) 59/682 (8.7) 22/238 (9.2)

1.44 1 1.07

0.56–3.73

0.447

0.67–1.70

0.781

Parity Primipara 0 1 2–4 5

25/250 (10.3) 13/231 (5.6) 36/387 (9.3) 11/84 (13.1)

1.78 1 1.65 2.33

0.93–3.39

0.081

0.90–3.05 1.08–4.99

0.108 0.030

Timing at first ANC visit (n = 917) First trimester Second trimester Third trimester

27/442 (6.1) 16/185 (8.6) 37/290 (12.8)

1 1.42 2.09

0.78–2.56 1.30–3.35

0.251 0.002

Inter-pregnancy interval (n = 730) <24 months 24–60 months >60 months

22/317 (6.9) 24/283 (8.5) 16/130 (12.3)

1.00 1.22 1.77

0.70–2.13 0.96–3.27

0.480 0.066

Tetanus Toxoid Vaccine (at least one dose) Received Not received

53/763 (6.9) 32/189 (16.9)

0.43 1.00

0.29–0.65

<0.001

Use of contraceptive in proceeding interval (N = 730) Yes No

41/517 (7.9) 21/213 (9.9)

0.8 1.00

0.49–1.33

0.395

History of perinatal deaths Yes No

55/33 (15.2) 80/919(8.7)

1.74 1.00

0.76–4.10

0.202

Maternal anaemia Hb < 12 gm/dl Hb  12 gm/dl

14/118 (11.9) 71/833(8.5)

1.39 1.00

0.81–2.39

0.234

Maternal mid upper arm circumference (cm) <21 cm (severe acute malnutrition) 21–22.9 cm (moderate acute malnutrition) 23 cm (normal)

1/15 (6.7) 3/41 (7.3) 81/895 (9.1)

0.74 0.81 1

0.11–4.95 0.27–2.45

0.753 0.707

a b c

PM — perinatal mortality. (RR) — unadjusted Relative Risk. CI — confidence interval.

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Table 4C Risk factors for perinatal mortality (PM) in bivariate analysis in a cohort of 952 births, Sana’a City, Yemen, 8/2015–12/2016. a

Unadjusted RRb

(95% CI)c

p-value

6/24 (25.0) 79/928 (8.5)

2.94 1

1.42–6.06

0.004

Smoking cigarettes last 6 months before pregnancy Yes No

12/118 (10.2) 73/834 (8.8)

1.16 1

0.65–2.07

0.612

Smoking cigarettes during pregnancy Smoker Non smoker

9/81 (11.1) 76/871 (8.7)

1.27 1

0.66–2.45

0.468

Smoking Hubble-bubble (shisha) Yes No

20/192 (10.4) 65/760 (8.6)

1.22 1

0.76–1.96

0.416

Using orange snuff (smokeless tobacco) Yes No

4/16 (25.0) 81/936 (8.7)

2.89 1

1.21–6.92

0.017

Khat chewer Yes No

54/476 (11.3) 31/476 (6.5)

1.74 1

1.14–2.66

0.010

Variables/exposures C. Traditional practice Mothers underwent female genital mutilation Yes No

a b c

PM/total (%)

PM — perinatal mortality. (RR) — unadjusted Relative Risk. CI — confidence interval.

Table 5 Risk factors for perinatal deaths in a multivariable analysis in 952 births, Sana’a City, Yemen, 8/2015–12/2016. Variables/factors

Ba

Unadjusted RRb

Adjusted RR

(95% CId)

p-value

Mother’s age at birth (years) Mother age (1) <18 vs.18–34 Mother age (2) > = 35 vs.18–34

0.233

2.81

1.03

0.41–2.54

0.955

1.262

3.06

2.83

1.68–4.77

<0.001

Mother’s age at first pregnancy (years) Mother’s age (1) <18 vs. 18–34 Mother’s age (2) > = 35 vs.18–34

0.683

1.87

1.57

1.04–2.37

0.030

0.727

4.73

1.95

0.92–4.13

0.081

0.797

1.78

1.9

1.01–3.54

0.045

0.244

1.65

1.3

0.70–2.42

0.403

2.33

0.83

0.35–1.96

0.670

Parity Parity (1) Primipara vs. one child Parity (2) 2–4 child vs. one child Parity (3) >5 child vs. one child

0.308

Family type Multi-nuclear vs. Nuclear

0.612

1.6

1.74

1.18–2.55

0.005

Type of house Mud vs. cement

0.839

1.83

2.02

1.37–3.00

<0.001

0.43

0.49

0.33–0.72

<0.001

Tetanus Toxoid Vaccine (at least one dose) Received vs. not Received

1.075

Female genital mutilation Yes vs. no

0.877

2.94

2.92

1.85–4.60

<0.001

Khat chewer Yes vs. no

0.656

1.74

1.60

1.08–2.37

0.019

Ba — coefficient, RRb — Risk Ratio (Relative Risk), dCI — 95% confidence interval Adjusted for — maternal, prenatal and some of traditional practice with significant at 0.25 in bivariate level. Model includes: mother age at birth, mother age at first pregnancy, parity, family type, house type, maternal tetanus toxoid vaccine, female genital mutilation, Chewer khat.

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least two doses of tetanus toxoid vaccine, mothers underwent female genital mutilation, smoking orange snuff, and khat chewer. In 2013, the Yemen National Health and Demographic Survey (YNHDS) reported that it is a socio-cultural norm that most women in Yemen are married by the time they reach the age of 18 years.8 This study found that babies born to women younger than 18 years had a significantly increased risk of perinatal death (RR = 2.81). This finding is consistent with several other studies.21–25 The most obvious reason for this over risk is that young mothers have not given birth before and therefore carry a higher risk of obstructed labour.20 Obstructed labour often requires emergency obstetric care which is lacking in this area. On the other hand, maternal age 35 and above years had more than 3 times the risk of perinatal deaths compared with the reference group 18–34 years. This association remained statistically significant in the multivariable analysis adjusting for confounders (RR 2.83; 95% CI: 1.68–4.77). Myometrial under perfusion possibly due to sclerotic arterial lesions and aging endothelium of older women are thought to be responsible for perinatal complications.26 Multigravida women (parity > = 5) had an RR of 2.33 for perinatal deaths compared to those with 1-5 previous births. These findings have already been shown in other studies conducted in Morocco and Pakistan.18,27 The majority of this study’s semi-urban areas were slums; the majority of deaths took place here as opposed to urban areas. The rate of perinatal mortality was 70/1000 livebirths in urban areas; this compared to 103/1000 livebirths in slum areas. Women in the slums, therefore, were at a 1.47 times greater risk of losing their babies in the perinatal period compared to the ones in urban areas. A study of Nairobi’s urban slums yielded similar results28 and the same in Eastern Uganda.29 The population growth in slum areas, tradition, lack of education, and limited budgets may be a crucial factor in deterring women from using health services. In our study, we did not find any statistically significant association between perinatal deaths and primary or no education levels of mother. However, the perinatal mortality rate was highest (97.7/1000 total births) in the illiterate mothers and decreased with higher maternal education status (61.9/1000). Similar findings have been reported by several other authors in Nigeria,30 in Ethiopia31 as well as in India.32 Our study concurs with those from Ethiopia and India where the housewife mothers (92/1000) were more likely to experienced perinatal mortality compared to employed mothers (58/1000). However, the difference was not significant. Our findings emphasise the need for increased female literacy with its subsequent multiple benefits. Our findings show that mothers who started ANC follow-up in the first trimester of pregnancy had a lower risk of perinatal deaths compared to those who started ANC follow-up in the third trimester of pregnancy. Our findings are also consistent with the study in Nepal.33 A systematic review and meta-analysis by Hawkes et al. showed less incidence of any untoward results among women who had been given an intervention (screening and treatment) in the first and second trimesters of pregnancy compared to the third trimester.34 Mothers who received tetanus toxoid vaccines had decreased risk of perinatal deaths by 51% relative to the mothers who did not receive vaccine. These results were similar to published studies by Abdulhameed et al.35. The previous systematic and meta-analysis study also supported our findings, which indicated that immunization of pregnant women or women of childbearing age with at least two doses of tetanus toxoid is estimated to reduce mortality from neonatal tetanus by 94% (95% CI 80–98%).36 In this study, women living within multi-nuclear family, were found to be significantly associated with higher perinatal mortality. The large number of family members and increased economic requirements might results in pregnant women not having access to adequate health care during pregnancy and childbirth. The perinatal

mortality rate was higher in the mothers living in mud houses compared to those living in cement houses. In Sana’a city almost all of the houses in slum areas are built on earthen floors (made of dirt or clay) which does not provide adequate shelter from harsh weather conditions especially during the cold winter. Furthermore, the Yemeni dwellings have non-improved toilet facilities. Consequently, household waste water stagnates or remains in the open drainages around the house. Equally hazardous are the mud floors creating an environment conducive to malaria, diarrhoea, and a range of other infectious diseases. Twelve percent of the mothers had haemoglobin <12 gm/dl at time of current birth. They experienced higher perinatal mortality rate (118.6/1000) than those with haemoglobin 12 gm/dl and more (85.2/1000), but the difference was not statistically significant. Yemen is and has been experiencing a civil war and regional sanction for some years now. This critical situation may have some effect on maternal and newborn health, including the deterioration of nutritional status of women and health services especially in Sana’a, the Capital City of Yemen. Previous study in Yemen reported that twelve percent of women have severe acute malnutrition, and twenty percent have moderate acute malnutrition.8 Female genital mutilation (FGM) is a firmly held tradition practised by particular ethnic groups in Africa, Asia and the Middle East. The WHO defines FGM as “all procedures that involve partial or total removal of the external female genitalia or other injury to the female genital organs for non-medical reasons.”37 In the present study, mothers who underwent FGM were almost 3 times more likely to experience perinatal death. This is similar to finding from a systematic review in 2013, with greater number of participants, from Europe and the USA.38 A meta-analyses study revealed that women having experienced FGM have prolonged, difficult labour; this is accompanied by a greater rate of obstetric wounds, usually needing birth by instrument, and greater rates of obstetric haemorrhage. Indeed, evidence shows that more invasive techniques of FGM led to a greater amount of scarring and extensive delays in the second stage of labour.39 Smoking cigarettes is a concern for girls having reached reproductive age as many illness are attributable to maternal smoking during pregnancy; these effects include a greater risk of foetal growth restriction; preterm birth; stillbirth; perinatal death; sudden infant death syndrome, and placental abnormalities.40 Previous study in Yemen reported that the 7% of female age 15 and older are current smokers (i.e., they smoke regular or sometimes any other form of tobacco including water pipes).8 In our study, the rate of perinatal death was higher 111.1/1000 among smoking mothers compared to 87.3/1000 among those non-smoking mothers. However, in this study it did not appear to be a statistically significant association (p = 0.47). In the previous systematic review and meta-analysis conducted by Pineles et al.41 found that, smokers have risk increases of 46%, 33%, and 22% for stillbirth, perinatal death, and neonatal death, respectively. Our findings in this study showed that the rate of perinatal deaths was higher (104.2/1000 live births) among water pipe smokers’ mothers compared to 85.5/1000 among non-water pipe smoker mothers. However, there did not appear to be a statistically significant association (p = 0.42). In many parts of the world, usage of non-cigarette varieties of tobacco are prevalent or growing in popularity. In Yemen commonly used smokeless tobacco are orange snuff (or shamma) made of powdered tobacco, lime, ash, black pepper, oils and flavourings. In Yemen smoking prevalence is 11% of household members age 15 and older where 16% of men and 5.3% of women use smokeless tobacco in chewed form.8 In our study, the perinatal mortality rate was significantly higher among smokeless tobacco (orange snuff) mothers than among non-user mothers (25.0% vs. 8.7%). This is consistent with other studies that uncovered that

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snuff is associated with such conditions as immune dysfunction, reproductive impacts, e.g. perinatal mortality and preterm birth along with cardiovascular effects.42 In Yemen, it is common for both men and women and even children to engage in khat chewing. Khat chewing becoming a daily social habit. Khat (Catha edulis) is a plant which contains cathinone; this is a natural amphetamine. Khat leaf chewing is common in Yemen, and although is not considered addictive by WHO, there are physiological effects. These include increased heart rate and blood pressure, insomnia and low birth weight.43 In the current study, mothers who chewed khat during pregnancy had increased risk of perinatal deaths compared to mothers who did not chew khat. Our findings are in line with previous studies conducted in Yemen which showed that khat-chewing during pregnancy led to higher risk of foetal death44 with 6 times the risk of preterm labour and 3.83 times the risk of labour induction.45 5. Strengths and limitations Some of the deaths that occurred at home involved did not received death certificate and not recorded in any formal system. Therefore, many of these deaths would have been missed by facilitybased studies. The perinatal deaths of mothers dying during or shortly after birth would also have been missed. These retrospective surveys are the main sources of data concerning perinatal mortality in low and middle-income countries. All these factors were able to be taken into account in this prospective community-based cohort study and provide a thorough description of likely risk factors for perinatal death. This study has a relatively small sample size which is less able to identify a number of risk factors associated with small increases in perinatal death. In addition, we could not estimate accurate maternal mortality rates and ratios, which requires a large sample size. Maternal deaths are rare events, being far less common than childhood deaths and therefore more difficult to measure with small sample size. Nevertheless, in our study the proportion of stillbirth and early neonatal deaths is consistent with WHO estimates for the EMR region.5 In addition, literature suggests that in resource-limited almost two-thirds of stillbirths occur intrapartum and therefore include avoidable deaths.46 This study provides a useful insight on perinatal mortality which is still lacking in this country. Our findings might be generalized to women who deliver at Sana’a city governorate. 6. Conclusion In terms of public health, perinatal mortality is a major problem in both Yemen and other low-middle income countries. In this study, perinatal deaths were linked with older mother’s age at birth and mother’s age at first pregnancy (aged <18 years), parity, family type, type of house, history of previous perinatal deaths, maternal tetanus vaccination, female genital mutilation, smoking snuff and khat chewer. Our findings lend weight to arguments for sets the minimum age for marriage at 18 in accordance with the definition of a child in the convention on the Rights of the Child; ensuring that pregnant women have access to and use adequate birth facilities. This study confirms, there is a need for sexual and reproductive health awareness and education for both men and women inducting the health risks from FGM at the community, school, and university levels. Urgent action is necessary to be done by the local authority and NGOs to control khat cultivation and chewing by creating awareness and increasing knowledge on the harmful effects of khat chewing especially among women and the younger generations. There is an urgent need for sustainable interventions to significantly reduce neonatal mortality and help to achieve the

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sustainable development goals and improve maternal and newborn health in the country. Conflict of interest No conflict of interest, and the work was not supported or funded by any sponsor. Acknowledgment I would like to thank those who participated in the study. All the data collectors are recognised and thanked for their tremendous contribution during data collection. References 1. Zupan J.. Perinatal mortality in developing countries. N Engl J Med 2005;352 (20):2047–8. 2. Lawn JE, Blencowe H, Pattinson R, Cousens S, Kumar R, Ibiebele I, et al. Stillbirths: where? When? Why? How to make the data count?. Lancet 2011;377(9775):1448–63. 3. Spector JM, Daga S. Preventing those so-called stillbirths. Bull World Health Organ 2008;86(4):315–6. 4. WHO. Neonatal and perinatal mortality, 2004. Country, regional and global estimates. Geneva: World Health Organization; 2007. 5. WHO. Neonatal and perinatal mortality: country, regional & global estimates. Geneva, Switzerland: WHO; 2006. 6. Cousens S, Blencowe H, Stanton C, Chou D, Ahmed S, Steinhardt L, et al. National, regional, and worldwide estimates of stillbirth rates in 2009 with trends since 1995: a systematic analysis. Lancet 2011;377(9774):1319–30. 7. MoPHP of Yemen, UNICEF, PAPFAM. Yemen: monitoring the situation of children and women: multiple indicator cluster survey 2006. 2006 Sana’a, Yemen. 8. YMoPHP & CSO. National Demographic and Health Survey (YNDHS), 2013 Tech. Rep., MOPHP (Ministry of Public Health and Population) and CSO (Central Statistical Organization), Finally Report, Sana’a, Yemen, 2015, 2015. 9. World Bank Yemens’ Economic Outlook — Spring 2016, 2016. 10. Banajeh S, Al-Rabee A, Al-Arashi I. Burden of perinatal conditions in Yemen: a 12-year hospital-based study. East Mediterr Health J 2005;11(4):680–9. 11. Central Statistical Organization. Sana’a City Adminstrative Units. Sana’a,Yemen: Central Statistical Organization; 2004. 12. MoPHP of Yemen. Annual statistic health report 2014 Yemen. 2014. 13. WHO. The World Health Survey, sampling guidelines for participating countries. Geneva: WHO; 2002. 14. Nouaili EBH, Chaouachi S, Ayadi I, Said AB, Zouari B, Marrakchi Z. Risk factors for perinatal mortality in a Tunisian population. Int J Gynecol Obstet 2010;111 (3):265–6. 15. WHO. Neonatal and perinatal mortality country, regional and global estimates 2004. Geneva: World Health Organization, Department of Making Pregnancy Safer; 2007. 16. World Health Organization. Verbal autopsy standards: the 2012 WHO verbal autopsy instrument. 2012. 17. Ali AA, Elgessim ME, Taha E, Adam GK. Factors associated with perinatal mortality in Kassala, Eastern Sudan: a community-based study 2010–2011. J Trop Pediatr 2014;60(1):79–82. 18. Boubkraoui ME-M, Kabiri M, Mrabet M, El-hassani A, Barkat A. Perinatal morbidity and mortality at Souissi Maternity Hospital, Rabat, Morocco. Adv Res 2015;4(1):45–52. 19. Abdulghani N. Risk factors for maternal mortality among women using hospitals in North Yemen. A Thesis presented for the degree of PhD in the Faculty of Medicine University of London 1993. 20. Al Serouri AW, Al Rukeimi A, Afif MB, Al Zoberi A, Al Raeby J, Briggs C, et al. Findings from a needs assessment of public sector emergency obstetric and neonatal care in four governorates in Yemen: a human resources crisis. Reprod Health Matters 2012;20(40):122–8. 21. Al-Haddabi R, Al-Bash M, Al-Mabaihsi N, Al-Maqbali N, Al-Dhughaishi T, Abu-Heija A. Obstetric and perinatal outcomes of teenage pregnant women attending a tertiary teaching hospital in Oman. Oman Med J 2014;29 (6):399. 22. Benjamin AI, Paramita S, Shavinder S. Perinatal mortality and its risk factors in Ludhiana: a population-based prospective cohort study. Health Popul Perspect Issues 2009;32(1):12–20. 23. Diallo AH, Meda N, Zabsonré E, Sommerfelt H, Cousens S, Tylleskär T. Perinatal mortality in rural Burkina Faso: a prospective community-based cohort study. BMC Pregnancy Childbirth 2010;10(1):45. 24. Malabarey OT, Balayla J, Klam SL, Shrim A, Abenhaim HA. Pregnancies in young adolescent mothers: a population-based study on 37 million births. J Pediatr Adolesc Gynecol 2012;25(2):98–102. 25. Mukhopadhyay P, Chaudhuri R, Paul B. Hospital-based perinatal outcomes and complications in teenage pregnancy in India. J Health Popul Nutr 2010;28 (5):494.

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36. Blencowe H, Lawn J, Vandelaer J, Roper M, Cousens S. Tetanus toxoid immunization to reduce mortality from neonatal tetanus. Int J Epidemiol 2010;39(Suppl. 1):i102–9. 37. World Health Organization. Female genital mutilation. Fact sheet No 241, Updated February; 2014. 2014. 38. Berg RC, Underland V. The obstetric consequences of female genital mutilation/cutting: a systematic review and meta-analysis. Obstet Gynecol Int 2013;2013:. 39. Browning A, Allsworth JE, Wall LL. The relationship between female genital cutting and obstetric fistulas. Obstet Gynecol 2010;115(3):578. 40. Rogers JM. Tobacco and pregnancy. Reprod Toxicol 2009;28(2):152–60. 41. Pineles BL, Hsu S, Park E, Samet JM. Systematic review and meta-analyses of perinatal death and maternal exposure to tobacco smoke during pregnancy. Am J Epidemiol 2016kwv301. 42. Willis D, Popovech M, Gany F, Zelikoff J. Toxicology of smokeless tobacco: implications for immune, reproductive, and cardiovascular systems. J Toxicol Environ Health B 2012;15(5):317–31. 43. Al-Mugahed L. Khat chewing in Yemen: turning over a new leaf: Khat chewing is on the rise in Yemen, raising concerns about the health and social consequences. Bull World Health Organ 2008;86(10):741–3. 44. Masood Muhammed SA, AlMansoob MAK. The impact of chewing Khat during pregnancy on foetal death history. Int J Novel Res Healthc Nurs 2015;2(2):28–31. 45. Abdel-Aleem MA. Khat chewing during pregnancy: an insight on an ancient problem impact of chewing Khat on maternal and fetal outcome among Yemeni pregnant women. Ommega Int 2015;1(2):1–8. 46. Darmstadt GL, Yakoob MY, Haws RA, Menezes EV, Soomro T, Bhutta ZA. Reducing stillbirths: interventions during labour. BMC Pregnancy Childbirth 2009;9(1)S6.

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