We captured delivery outcomes for almost 200 000 births in distinct, geographically defined clusters in seven countries, representing one of the largest studies of this kind to date. Although other studies have reported hospital-based stillbirth rates, few to date have examined hospital and community births to estimate the overall population rates for defined geographic areas (6
). The overall stillbirth rate of 22 per 1 000 births, with individual country rates ranging from 8 per 1 000 in the Argentinean clusters to 32 per 1 000 in the Pakistani clusters, closely approximates the estimated country rates reported for these countries in some modeling studies (1
). These rates are significantly greater than the rates of three to five per 1 000 reported from many high-income countries.
Stillbirth offspring weighing <1 000g, or those occurring at about 20–28 weeks, were not included in this study but are often included in reported USA and other high-income country rates. In the USA, for example, stillbirths occurring at 20–27 weeks account for almost half of the reported stillbirths and similar results have been reported in other high income countries (16
). Thus, the disparity between the stillbirth rates between high and low income countries may be even larger than suggested by our results.
When examining the socio-demographic and health care characteristics, the risk factors for stillbirth were consistent with previous studies from both low and high income countries (7
). Women >35 years of age, those who had no formal schooling, who received no prenatal care, and who were either primiparous or with grand-multiparity (≥5 prior pregnancies) were also at greater risk to experience a stillbirth.
Access to health care was of particular interest. For the entire study sample, 94% of the women had at least one antenatal care visit, 51% delivered at home, 16% had no health care provider available at delivery, and 34% had an unskilled attendant. Only 4% had a Cesarean delivery, with rates of less than 1% reported in several countries. Women who had no antenatal care had a higher risk for a stillbirth compared to those women with antenatal care. Although we did not formally test the association between stillbirth and Cesarean section due to the confounding factors reported elsewhere (21
), with one exception, the sites with the lowest Cesarean section rates tended to have the highest stillbirth rates. Of interest, in Nagpur, India, 17% of the births were delivered by Cesarean section, but the stillbirth rate was high (22 per 1 000 births). Rising Cesarean rates in low-resources settings are a topic of recent debate, especially as the Cesareans in these settings may be done for the wrong indications or may not improve outcome (23
). However, when performed on the appropriate patients, it remains clear that Cesarean section can save maternal and fetal lives and that a Cesarean section rate of at least 5% deliveries represents the minimal rate necessary to address preventable perinatal mortality, as recommended by a number of international organizations (24
The observation that among the providers, the physicians had the highest stillbirth rates, and that stillbirth rates did not differ markedly whether the delivery occurred in a home clinic or hospital, led us to speculate about the potential reasons for these observations. Most likely, women with high risk conditions such as bleeding or seizures may have been more likely to seek care with physicians in facilities. However, many facilities at our sites are characterized by limited equipment, few medicines, and long waits for life-saving interventions such as Cesarean section. Whether a physician was present or not, the lack of resources might explain the failure of facility or physician delivery to substantially reduce stillbirth rates.
This study had several strengths. First, it is one of the largest prospective studies to register women during pregnancy and to capture birth outcomes for a representative population-based sample. Because the study was conducted in geographic areas where a substantial proportion of the births occurred at home, data from this study are likely to be more representative of these geographic areas than many hospital-based studies. In addition, we used trained coordinators to supervise and evaluate the quality of the data collected, as well as a number of methods to ensure that data from all births were captured. Few low-income country studies of stillbirth in communities have captured birthweight or gestational age, often because of cultural or other barriers (1
). By repeated training, we worked very hard with our study staff to identify barriers to registering stillbirthsand,where applicable,to overcome their initial reluctance to handle or register stillbirth offspring.
One of the potential limitations of the study that may have resulted in reporting bias was our inability to ensure that all births were captured; however, in each site, our staff used several methods to determine who in each community was pregnant and who had delivered. In addition, the pregnancy outcomes obtained by our staff were compared with the available health records. Finally, the evaluation of delivery and stillbirth rates and inter-cluster variability ensured that large unexplained variations in either the birth or stillbirth rates were not occurring over time. Another potential limitation is the quality of the data collected for unattended births. To address this issue, our study coordinators interviewed each mother and other family members. Obtaining information on these home births is critical as they represent a substantial proportion of the live births and of the stillbirths in these geographic areas.
Still another potential limitation deals with the data regarding maceration. Despite training on this issue using graphic pictures and descriptions, it is possible that mild cases of maceration were misclassified. However, our results are in the same direction as other studies which have found that fewer than half of all stillbirths in low-income countries are macerated (2
). Signs of maceration have been used as one indicator to distinguish antepartum from intrapartum stillbirth (10
). However, we expect that an unknown proportion of the non-macerated stillbirths occurred prior to labor, and recognize that the concordance between ‘non-maceration’ and intrapartum death is not 100%. Finally, a potential limitation to the data relates to the estimates of gestational age. Because few of the sites had ultrasound to confirm LMP-derived gestational ages, we suspect that the actual percent of term births and especially term stillbirths may have been somewhat lower than the numbers reported here. Nevertheless, because the gestational age and birth-weight distributions paint a similar picture, we are confident that most stillborn offspring were born at or near term, and most were not macerated.
A primary gap in stillbirth research and policy planning has been the reliance on hospital studies to estimate stillbirth rates, especially as the majority of the stillbirths worldwide occur in home settings and are never registered, and thus no vital statistics are available (11
). The mean stillbirth rate of more than 22 per 1 000 births represents more than a five-fold increase compared to high-income country rates (1
). An important observation is that in the less developed communities, where most deliveries occurred in home settings without trained health providers, rates were as high as 32 per 1 000, compared to the stillbirth rates in Argentina of 8 per 1 000, where nearly all deliveries occurred in hospital settings. Of particular note, the majority of the stillbirths occurred at term and had no signs of maceration and almost half were ≥2 500g. Thus, if delivered before fetal death, most infants should not suffer the adverse effects of preterm birth and would likely survive. These results strongly suggest that the majority of stillbirths could be salvaged with access to appropriate obstetrical care. Although our data suggest that higher quality of health care at delivery, especially access to health care providers and appropriate Cesarean section, is associated with lower stillbirth rates, more research on the specific causes of these stillbirths would assist in defining appropriate interventions. Our findings suggest that the majority of stillbirths in these developing countries could be prevented.