Risk factors and causes of stillbirths among pregnant women in Pakistan

Background Globally 3 million stillbirths occur per year, and Pakistan is ranked 3rd among the countries having the highest burden. Despite being a major public health problem, efforts to reduce this figure are insufficient. Objective The aim of the study was to identify and measure the inequalities in stillbirth associated risk factors, causes and fertility risk behaviors. Methods Data were derived from the Pakistan Demographic and Health Surveys (PDHS) 1990–2013. Inequalities on determinants were evaluated using rate differences and rate ratios; time trends computed with annualized reduction rate (ARR). Results Overall ARR determined for stillbirth was −12.52 percent per annum. The high ARR were recorded for mothers age <20, urban areas, educated mothers and for highest wealth quintile. The relative inequalities were most pronounced for wealth quintiles, education and age of mothers. Stillbirth causes were unexplained antepartum (33%), unexplained intrapartum (21%), intrapartum asphyxia (21%) and antepartum maternal disorders (19%). The high fertility risk behavior was found in mothers with age >34 and birth order >3. Conclusion The study concluded that to achieve gain in child survival, there is need to promote antenatal care, birth spacing, and family planning programs in developing countries.


Introduction
Stillbirths represent a devastating outcome of pregnancy, and 3 million deaths occurred each year during intra-partum period, among these 98% of cases are from low and middle income countries. 1 In south Asia over a million of stillbirths occurred in 2008. 1 Stillbirths are mostly unseen in world health monitoring reports, millennium development goals (MDGs) and countdown to 2015 monitoring process. 2 Global burden of disease estimates did not include disability adjusted life-years for perinatal mortality. 3 The World Health Organisation's defines stillbirth as the numbers with birth weights of 1000g or more after 28 weeks of gestation in less developed countries. In developed countries more than third of stillbirths occurred after 22 and before 28 completed weeks of gestation. 4 but are hardly estimated in low-income countries. 1,5 In Pakistan, stillbirth rate is 32 per thousand deliveries, 6 with estimated number of 167,040 stillbirths in the year 2012 based on total population (180 million) of Pakistan and expected number of deliveries (2.9%). 7,8 The direct medical causes of stillbirths are documented as: congenital abnormalities, ante-partum haemorrhage, infection, prematurity, maternal accident, prolonged labour, cord prolapse and malpresentation. Some of these direct medical causes are indicative of poor quality of care of services, clinical error and medical negligence. 9 In Pakistan at the community level, nearly two-third of deliveries continue to take place at home with more than 62% of all deliveries assisted by untrained birth attendants. 10 Hence, in a substantial number of cases the exact cause of stillbirth remains unconfirmed with the communities explaining stillbirths according to socio-cultural and religious beliefs.
The governmental health departments in low and middle income countries do not record stillbirths; it is surely overlooked by funding bodies, policy makers, and local communities. In Pakistan, despite considerable initiatives undertaken over decades progress with respect to maternal and neonatal health indicators remains poor, and country remained clearly 'off track' to reach the set targets of MDGs 2015. 11 In post 2015 era to reduce the stillbirths new targets were set for the countries within the agenda of the Lancet Commission on Investing in Health and the Sustainable Development Goals (SDGs) to be met by 2035 and 2030. 12,13 These targets include less than 10 stillbirths per 1000 total births by 2035. 12 To complete the set targets and end the preventable perinatal deaths, considerable efforts are required.
In Pakistan, due to slow progress in child survival programs and to achieve new targets, there is need to comprehend the determinants of stillbirths. To determine the best performance scenario, we calculated the average annual rate of reduction for risk factors associated with stillbirths in Pakistan by using data from three national surveys. The objectives of this study are also to measure relative and absolute socio-economic and demographic inequalities in stillbirths over time.

Data source
Data used in present study were obtained from three national surveys conducted in 1990-1991, 2006-2007 and 2012-2013 to calculate perinatal mortality, its causes and high risk fertility behaviour across Pakistan. The registration system of Pakistan is incomplete and stillbirth rates were figured form household surveys (Pakistan Demographic and Health Surveys, PDHS). The study protocol does not raise any ethical issues; all data are freely avail-able from the MEASURE DHS website (www.measuredhs.com).
PDHS 1990-191 used three types of questionnaires, the Household Questionnaire, the Woman's Questionnaire and the Husband's Questionnaire, formatted on DHS Model B Questionnaire developed for countries with low contraceptive use. The two-stage stratified sampling technique was applied in survey and recorded response rate was 96% for women and 78% for men. In 2006-2007 PDHS six types of questionnaires were used namely: the Community, the Short Household, the Long household, the Women's, the Maternal Verbal Autopsy, and the Child Verbal Autopsy Questionnaires, formatted on model questionnaires developed by the Measure DHS program. A two stage-stratified cluster random sampling method was designed in the survey with a total response rate 98%. The PDHS 2012-2013 selected four types of questionnaires: Household Questionnaire, Woman's Questionnaire, Man's Questionnaire, and Community Questionnaire, with two-stage stratified sample design. The response rate recorded was 93% in women and 79% in men. In all three surveys verbally informed consent was taken and trained enumerators were selected to assemble information from households and respondents. The comprehensive detail on contents of questionnaires, sampling methodologies are available separately in three national PDHS.
The information on the causes of stillbirth was obtained from mothers of deceased children, doctors and from health care workers during the 1990-2013 PDHS. The standard infant and child verbal autopsy (VA) questionnaire 14 were used, and a panel consensus with computer allocation and manual assessments was applied to decide the ultimate cause of demise. The International Classification of Diseases (ICD 10) coding system was used to assign the final cause of death.

Model selection and uncertainty estimation
This study assess the determinants of stillbirths rates, represented as deaths per 1,000 live births. The variables evaluated in current study from above mentioned three surveys data were: place of residence, education of mothers, wealth quintiles and age of mothers at birth, maternal fertility behaviour in term of single and multiple risk African Health Sciences Vol 19 Issue 1, March, 2019 categories. Bivariate logistic regression analysis was performed and adjusted odds ratios (OR) with 95% CI were calculated. Level of significance was set at p<0.05.
To calculate the magnitude and trends in inequalities, rate differences (highest-lowest) as absolute measures of inequality and rate ratios (highest/lowest) as relative measures of inequality for 2006-2007and 2012-2013 PDHS were computed. The rate ratio is unit less and independent of average levels and scale, whereas the rate difference depends on both average levels and scale. [15][16][17] The annual rate of reduction is applied to calculate the trends in increase (e.g. improved coverage) or decrease (e.g. reduced rate) in mortality rates, and to create pro-jections of rates into the future. The annual rate of reduction (ARR) in perinatal mortality for this study was calculated as: Where LN is the natural logarithm, PMR is the perinatal mortality rate, and t0 and t1 correspond to base year and current year respectively. 18 The statistical analyses were calculated by using Microsoft Excel version 10 and SPSS V. 17.

Perinatal mortality rate
The change in perinatal mortality along its critical determinants age of mothers at birth, residence, education of mothers and wealth quintiles are given in table 1   The data on associated risk factors of stillbirth was not generated in 1990-1991 PDHS. The annual reduction rate in stillbirth is recorded -12.52 percent per annum. The progress in perinatal mortality was recorded for all associated risk factors from 2006-2013. The annual reduction rate recorded for mothers age <20 is -10.65 percent per annum, with 40-49 is -9.75 percent per annum. The annual reduction rate was recorded in urban (-20.36 percent per annum), rural (-9.80 percent per annum), uneducated mothers (-9.94 percent per annum), educated mothers (-22.76 percent per annum) and in lowest (-5.20 percent per annum), second (-12.12 percent per annum) and highest (-21.88 percent per annum) wealth quintiles. The rate difference (55)  High-risk fertility behaviour Several demographic reports have directed that the survival chances of children are dependent on fertility pattern of her mothers. In current analysis, the variables are defined as young mothers with age group <18,Old mothers with age more than 34, birth interval less than 24 months and birth order more than 3 children. The birth percentages in six year preceding the survey by various risk categories in three national surveys are shown in figure 2. The births fall into any single high risk category were found to be 55 % (1990-1991), 38% (2006)(2007) and 37% (2012-2013) for three national surveys. The major single high risk categories reported were age of mothers >34, birth order >3 and birth interval <24 months. Births fall in multiple risk category were recorded 19 %, 24% and 21% respectively for three surveys from 1990-2013 PDHS.
The birth percentages in currently married women along with risk category are shown in figure 2. The data collected during three national surveys identified sterilized women not being in any risk category, who were found engaged in family planning activities by using different contraceptive methods and with prolonged abstinence.  Figure 2: Birth percentages among women in six years preceding the survey and currently married women, who were to conceive a child at the time of survey by various risk categories from the data obtained from three national surveys.

Discussion
Stillbirth is a major but often neglected public health issue. The population based data derived from national surveys of country allowed us to assess risk categories of stillbirth that will require further investigation in future studies. The current findings indicated high stillbirth rates in Pakistan and identified the risk categories which were uneducated women, those who have lowest wealth quintiles, old age and those who are living in remote areas where they did not have access to any health services, as previously reported. [19][20][21][22][23] The development and implementation of number of maternal and child health programs at national level to date do not have significant role in increase or decrease of inequalities, and annualized reduction rate has not pronounced decline to reach the set targets for 2035.
Comparing stillbirth rates with risk factors shows that most of the variables did not significantly associated in 2006-2007 survey period, while for 2012-2013 survey these variables are significantly associated. One of the reasons of this contrary in the result of both surveys stillbirth rate may because of high degree of sampling variation and differences by background characteristics. The 2006-2007 PDHS did not include an event "calendar" for recording the pregnancy losses that had occurred in the five years preceding the survey, while it had been recorded for 2012-2013 PDHS.
The relative inequalities in perinatal mortality increases between wealth quintile and education of mothers for the 2012-2013 survey periods compared to 2006-2007. This increase leads to reduction in stillbirth with improvement in wealth quintiles and education of mother. The results showed that stillbirth rate significantly differ between lowest wealth quintiles, uneducated, older aged mothers and those living in deprived areas. The socio-economic status of mother is one of the major risk factor of stillbirth, reflects with reports from developing countries. 14,25-30 In India several studies had reported significant association of wealth status with stillbirth. 31,32 A study conducted in five developing countries recorded lack of formal education increases the relative risk of stillbirths. 33 Other studies in Nigeria, recorded statistically significant association between uneducated mothers and stillbirth. 34 A number of reports from Ghana and Brazil recorded signification association between uneducated poor mothers and stillbirth. 31,[35][36][37][38][39][40] The uneducated mother with lowest wealth quintiles has about two-fold risk of perinatal deaths as compared to educated mothers with high wealth quintiles. Existing evidence supports the fact that overall health seeking behavior of the more educated mother is much better than those of parturient with low levels of education or no formal education, as recorded in previous studies. [41][42][43] Education tends to minimize the challenges of low socioe-conomic status and lack of knowledge amongst the females. 41,44 The Government of Pakistan and many international donors have implemented various programs to improve mother and child health. Considerable policy change occurred in the last decade by adding newborns care into existing community-based maternal and child packages delivered by the Lady Health Worker Program. National Maternal, Newborns and Child Health (MNCH) Communication Strategy Framework were developed under the MNCH Program. 45 The U.S. Agency for International Development (USAID) funded project Pakistan Initiative for Mothers and Newborns (PAIMAN) results reported significant reductions instillbirth. 46 The implementation of these programs in the country by using large financial and personnel resources will be helpful to improve the newborns survival and will be important to sensibly assess their future performance in terms of coverage and effectiveness. A combination of challenges has prevented progress, such as humanitarian disaster and political instability, policy to programme gaps and demand/supply barriers like geographic and socio-cultural obstacles that prevent care seeking. 47 Despite the number of programs that have been initiated in the country to reduce stillbirth rate, Pakistan was reported as worst performer out of 186 countries having highest rate of stillbirths at the end of year 2015. 45 The perinatal deaths in Pakistan are 43.1 per 1,000 total births a rate higher than that compared to global rate (18.4 stillbirths per 1000 total births). 45 Although worldwide stillbirth rates have decreased slightly, the average annual rate of reduction (ARR) of stillbirths (2.0%) has been far slower than that for either maternal (3.0%) or post-neonatal mortality of children younger than 5 years (4.5%). 45 African Health Sciences Vol 19 Issue 1, March, 2019 The major causes of stillbirth identified in national surveys were unexplained antepartum (33%), unexplained intrapartum (21%), intrapartum asphyxia (21%) and antepartum maternal disorders (19%). The findings are in accordance with developed countries having high socio-economic status and health services. The risk factors for antepartum stillbirth reported in previous studies are absence of pre-birth care, hemorrhage, hypertensive disorder, and small-for-gestational age babies. [19][20][21]23 Several studies conducted to identify causes of perinatal deaths reported 3.1-25% were due to intrapartum and trauma. 48,49 In Tanzania asphyxia-related causes (25%), 49 intrauterine asphyxia (21%) in Thailand 50 and intrauterine asphyxia (16.7%) in West Bengal. 48 Similarly to present investigation, previous studies recorded 3.8-57.4% of perinatal mortality were unclassifiable with unknown causes. 51,52 In Bangladesh (49%)and Nepal (47%) half of the all perinatal mortalities are reported with unknown causes. 12, 53 Similarly in Nigeria (38.8%) 54 and India (18%) 25 causes of perinatal deaths were unidentified. A study conducted in Ghana recorded unexplained causes of antepartum (57.4%) and intrapartum (31.5%) deaths. 51 Nevertheless, the identification of causes of perinatal mortalities for number of cases are never been established. 51,55,56 Moreover, majority of these factors are preventable and focused efforts on part of health care providers are required. 57 The present results indicated mothers with birth interval less than 24 months, birth order more than 3, age of mothers >34 and<18 are at high risk category, which are in agreement with other reported studies. [58][59][60] Only a few studies have examined the risks of older maternal age on birth outcomes by parity. [61][62][63][64] In contrast to present findings no differential effect of parity on the risk of stillbirth in older mothers was recorded. [62][63]65 The healthy timings and spacing of pregnancies initiative 66 should be measured as a precedence in Pakistan because of its importance for mothers and newborns health; hence the role health care providers in promoting health interventions is needed. The areas with high stillbirths and poor health services strategies should target the peri-partum period for maximal reduction. 1 The current results can be useful for designing appropriate interventions that will improve obstetric practices and reduce the enormity stillbirth burden in Pakistan.

Conclusion
Stillbirths vary significantly by socio-demographic variables. The current results concluded that in order to achieve gain in child survival there is dare need to promote antenatal care, birth spacing and family planning programs. The development of clear guidelines, suitable classification system to assign causes of death, training of health care personnel to solve complications during parturition in developing countries is required.