Can clinical risk factors for late stillbirth in West Africa be detected during antenatal care or only during labour?

Martin Chalumeaua, Marie-Hélène Bouvier-Collea and Gérard Brearta and The MOMA Groupb

a Institut National de la Santé et de la Recherche Médicale. Unité 149 Recherches Epidémiologiques en Santé Périnatale et Santé des Femmes, Paris, France.
b Burkina Faso: Ouedraogo C, Sondo B, Testa J, Koné B; Ivory Coast: Barbé T, Berche T, Bohoussou MK, Eono P, Koffi AS, Ortiz P, Portal JL, Tano-Bian A, Touré-Coulibally K, Welffens-Ekra C, Zadi F; Mali: Decam C, Doucouré-Diallo A, Duponchel JL, Huguet D, Prual A; Mauritania: Cunin P, Ould El Joud D; Niger: Alfari D, Mounkaila N, Vangeenderhuysen C; Senegal: de Bernis L, Bouillin D, Dompnier JP, Gueye A; Ministère de la Coopération, France: Laure JM, Leloup M.

Marie-Hélène Bouvier-Colle, INSERM U149, 123 Boulevard de Port-Royal, 75014 Paris, France. E-mail: bouvier-colle{at}cochin.inserm.fr


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
Background Recent studies have shown that the most important risk factors for perinatal mortality in developing countries are not detectable during antenatal care but can be observed only shortly before or during labour. Although 60% of perinatal deaths in these countries are stillbirths, few epidemiological studies focus on them. We tested the hypothesis that the risk factors for late stillbirth in West Africa are detectable principally shortly before or during labour.

Methods Data came from a prospective population-based study (the MOMA survey) that collected information about 20 326 pregnant women in seven areas, primarily urban, in West Africa.

Results There were 19 870 singleton births. The stillbirth rate was 25.9 per 1000 total births (95% CI: 23.7–28.1). In the crude analysis, after adjustment and consideration of prevalence, the principal risk factors for late stillbirth were: late antenatal or intrapartum vaginal bleeding, intrapartum hypertension, dystocia, and infection. Other risk factors were: maternal height (<150 cm), maternal age (>35 years), previous stillbirths, hypertension at the 8-month antenatal visit and number of antenatal visits (<2).

Conclusions The principal risk factors for late stillbirth observed in our study could be detected only in the late antenatal and intrapartum period. These results highlight the potential benefits of partograph use. They need to be confirmed by studies incorporating continuous intrapartum fetal monitoring.

Keywords Developing countries, West Africa, fetal death, epidemiology, multivariate analysis

Accepted 17 December 2001


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
Stillbirths account for approximately 60% of all perinatal mortality in developing countries.1–24 We found that the most important risk factors for perinatal mortality in West Africa could not be detected during antenatal care but only during labour.16 Kusakio et al. reached the same conclusion in Bangladesh.15 We do not know, however, if this is the case for stillbirths or early neonatal deaths, or both. In developed countries, most stillbirths are related to antepartum causes (congenital malformations or intra-uterine growth retardation), and monitoring during labour is not helpful in detecting them.

In developing countries, methodological issues have limited or made controversial the results of the principal studies of risk factors for stillbirth.6–13,17–23 Voorhoeve et al.6 have demonstrated the substantial recruitment bias in hospital-based studies.8–12,17–21 Moreover, these studies are unable to take into consideration the real prevalence of risk factors in the population. On the other hand, some population-based studies have failed to analyse intrapartum risk factors22 or limited their analysis to antepartum fetal deaths.23 The three population-based studies that did consider risk factors detectable in antenatal visits and during labour unfortunately did not use statistical analysis to identify the risk factors that were significant.6,7,13

The present work is a part of a prospective populationbased inquiry in six West African countries (the MOMA study). It tested the hypothesis that the late antenatal and intrapartum risk factors for perinatal mortality that we have identified in West Africa are also risk factors for stillbirth. This study also allowed us to compare the potential contribution of antenatal care and monitoring during labour in their detection.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
The MOMA study
Study population
The MOMA study took place at seven study sites in six West African countries (Table 1Go).25–27 Five sites were capitals, one a big city (Saint-Louis, Senegal), and one a semi-urban area (Kaolack, Senegal). Geographical areas were chosen within each site to include the greatest possible range of social and demographic characteristics and of levels of health care. The study took place from December 1994 through June 1996. It included all pregnant women permanently living in each area. Women with miscarriages during the first or second trimester were not included.


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Table 1 Stillbirth rate by study site
 
Survey methodology
A door-to-door census of all women permanently living in the areas was carried out by specially-trained investigators. Women who were pregnant were seen at least three times: at a first antenatal visit before the end of the second trimester (inclusion), at a second visit around the eighth month of pregnancy and at delivery. Simple clinical signs were noted by the investigators at each home visit. Thorough interviews were performed for home deliveries, and hospital records were checked by a local physician when necessary.

Ethics
Every woman provided oral informed consent to study participation. The study was designed to avoid any interference with local health care and medical structures. When investigators detected unknown risk factors or conditions, they advised the women to consult their usual health provider.

Specific methods for this analysis
Definition of early and late stillbirths
A stillbirth was defined as a product of conception weighing >=500 g or with a gestational age >22 weeks without evidence of life at birth. Early and late stillbirths were distinguished clinically: early stillbirths were those for which active movements or heart sounds were absent at the 8-month antenatal visit, and late stillbirths were those that occurred after this visit.

Patient selection
The present study analyses only singleton births. Multiple pregnancies will be analysed separately to comply with international standardization recommendations28 and because they represent a special risk factor for stillbirth.18,29,30 Except for the calculation of overall stillbirth rates, the early stillbirths were excluded from analysis, to avoid studying variables that were collected after the death of the fetus.

Potentially viable fetuses
In developing countries, the main perinatal problem is not, as it is in industrialized nations, saving very low birthweight or premature or malformed neonates. For that reason, we have paid particular attention to the sub-group of fetuses that should not have died. We defined a potentially viable fetus as one weighing >2500 g, with a gestational age >36 weeks and no major malformations on clinical examination at birth. Within this group of potentially viable fetuses, we compared the late stillbirths and the live births. The study of this sub-group also allowed us to take into consideration potential confounding factors (e.g. prematurity and low birthweight) that are highly related to intrapartum risk factors (e.g. non-cephalic presentation, which is more frequent in pre-term births).

Statistical analysis
All analyses used either SAS (SAS Institute Inc., Cary, NC, USA) or BMDP (BMDP Statistical Software Inc., Los Angeles, CA, USA) software. Potential risk factors for late stillbirth were selected from all available variables if their prevalence in the study population was >0.5% and the rate of missing data was <15%. We performed a univariate analysis to determine the association between 29 simple clinical variables and late stillbirth and used logistic regression to examine the modifications after adjustment for study site. The Breslow-Day test assessed the potential interaction between the study site and the other risk factors. Subsequent multivariate analysis also used logistic regression (backward stepwise procedure). If the P-value of the Breslow-Day test was <0.05, an interaction term was included. The study site was forced into all regressions. The population-attributable risks were calculated from the adjusted odds ratios (OR) and the proportion of cases exposed to the risk factor.31


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
Census results and general health indicators
The census counted 21 577 pregnant women; 20 326 agreed to participate in the study and were followed at least until delivery (lost to follow-up: 1251–5.8%). There were 19 870 singleton and 456 multiple births to study participants. Vital status at birth of 61 (0.3%) of those singletons was unknown. The following results are therefore based on 19 809 singleton births.

The overall maternal mortality rate was 311 per 100 000 live births, and the perinatal mortality rate 41.8 per 1000 total births. Further details have been reported elsewhere.16,27 Stillbirths accounted for 62% of the overall perinatal deaths (range 55–71). The overall stillbirth rate was 25.9 per 1000 total births (95% CI: 23.7–28.1) and ranged from 19.6 in Niamey to 33.9 in Abidjan (Table 1Go). Eleven mothers of stillborns died: two before labour, two during labour, and seven after delivery. Of the 513 stillbirths, 18 (3.5%) were early, and 495 (96.5%) late. The following analysis is based on 19 296 live births and 495 late stillbirths.

Univariate analysis
A significant association was found with only two of the social, economic, and anthropometric risk factors: shortness (<150 cm) and age (>=35 years) (Table 2Go). No significant association was found with educational level (low), occupation (none), absence of a partner (i.e. widow, unmarried, or divorced), absence of a co-wife, or lameness. Of the risk factors related to obstetric history and status, grand multiparity (>6), previous stillbirth, previous postnatal death, more than three previous miscarriages and previous caesarean section were significantly associated with stillbirth (Table 3Go). No significant association was found with nulliparity, short interval between births (<18 months) or undesired pregnancy. Of the risk factors detectable at the 8-month antenatal visit, subsequent stillbirth was fairly significantly associated with vaginal bleeding at examination (OR = 3.4, 95% CI: 1.8–6.5). Further significant associations were also found with one or no antenatal visits, self-reported absence of malaria chemoprophylaxis, absence of tetanus immunization during this pregnancy, and hypertension (as defined by WHO32) (Table 4Go). No significant association was found with self-reported absence of iron supplementation.


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Table 2 Distribution of social, economic and anthropometric risk factors and crude relations to stillbirth (odds ratios [OR], 95% CI, P-value)
 

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Table 3 Distribution of risk factors related to past and current obstetric history and crude relations to stillbirth (odds ratios [OR], 95% CI, P-value)
 

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Table 4 Distribution of risk factors detectable at the 8-month antenatal visit and crude relations to stillbirth (odds ratios [OR], 95% CI, P-value)
 
All of the late antenatal and intrapartum risk factors were significantly and highly associated with subsequent stillbirth (Table 5Go). These risk factors were vaginal bleeding (late antenatal or intrapartum), infection (prolonged rupture of the membranes >24 hours and intrapartum fever >38°C), dystocia (non-cephalic presentation, labour duration >12 hours, intrapartum oxytocin administration), and intrapartum hypertension. None of the OR changed after adjustment for study site (data not shown).


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Table 5 Distribution of late antenatal and intrapartum risk factors and crude relations to stillbirth (odds ratios [OR], 95% CI, P-value)
 
Multivariate analysis
After adjustment for study site and all other risk factors, eight factors identified in the univariate analysis were no longer significantly associated with late stillbirth: grand multiparity, previous post-natal death, previous miscarriage, previous caesarean section, absence of malaria chemoprophylaxis, absence of tetanus immunization, vaginal bleeding at the 8-month antenatal visit and intrapartum fever. The adjusted OR were similar to the crude OR for the remaining variables assessed at inclusion and at the second antenatal visit (Table 6Go). On the other hand, the adjusted OR for the late antenatal and intrapartum risk factors were much lower than the crude OR because of the global correlations between these variables.


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Table 6 Adjusted relations to stillbirth (adjusted odds ratios [ORa], 95% CI)
 
Significant interactions (in both directions) were observed with the study site and the following risk factors: absence of malaria chemoprophylaxis, absence of iron supplementation, vaginal bleeding at the 8-month visit, intrapartum oxytocin administration, and non-cephalic presentation. Interaction terms were introduced into the regression for all these risk factors but, except for the latter, were removed from the model. The interaction with non-cephalic presentation was based on very few cases at one study site and was not taken into consideration for the analysis.

The adjusted population-attributable risks reveal that the three principal risk factors were intrapartum oxytocin administration (12%), non-cephalic presentation (11%), and prolonged labour (9%).

Results among potentially viable fetuses
At birth, the weight, gestational age, and presence of malformations were known for 85.6% of the 19 296 live births and 495 late stillbirths. Of the live births, 86.5% met the criteria defining a potentially viable fetus, and, of the late stillbirths, 55.8%. The associations between intrapartum risk factors and late stillbirths in this subgroup were in the same range as, or stronger than, those observed in the overall population (Table 6Go).


    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
Main results
The stillbirth rate observed in our survey was 26 per 1000. It was three to five times greater than the ratio observed in developed countries during the same period.24 The most important associations with late stillbirth involved risk factors that could be detected only during the late antenatal period or labour and not during early antenatal visits. This was the case regardless of the measure of association chosen: crude relations, adjusted relations, or population-attributable risks that take into account the prevalence of the risk factors in the population. These risk factors can be classed into four groups: vaginal bleeding, hypertension, dystocia, and infection. Of those that can be detected during antenatal visits, the most important were late antenatal vaginal bleeding, hypertension, short stature, maternal age, previous stillbirth, and less than two antenatal visits.

Because confounding factors such as prematurity or low birthweight might have caused the association between some of the intrapartum risk factors and late stillbirth, we performed a sub-group analysis of potentially viable fetuses to take these factors into account. The associations in this subgroup were still in the same range as or stronger than those for the overall population.

Intrapartum oxytocin administration was an important risk factor for stillbirth. This association remained strong after an overall adjustment for factors including prolonged labour, which is a major confounder. Oxytocin administration must be accompanied by close monitoring of fetal tolerance as suggested by Ellis et al.33 Prospective trials should reassess the safety of oxytocin in situations where this monitoring is not available, as is the case in most developing countries. Finally, non-cephalic presentation was a strong and frequent risk factor for stillbirth, even among full-term fetuses. This association, like the others involving intrapartum risk factors, may indicate sub-optimal intrapartum monitoring and care. One explanation for this inadequate intrapartum monitoring is that the partograph, a graphic record of the progress of labour, is not used in the study areas.

Internal validity
Approximately 5.8% of the 21 557 pregnant women counted in the census were not included in the study because they refused to participate or were lost to follow-up. It was not possible to determine the vital status at birth of 61 (0.3%) of the included singleton pregnancies, and we cannot be sure that the results were not biased by these missing data. There was not, however, any significant difference between the distribution of risk factors among the 61 women whose pregnancy outcome was unknown and the others (data not shown). We therefore assume that the potential bias is small.

The exhaustiveness of the study was assessed from local birth registers or a new door-to-door census at the end of the study period or both, depending on study site. We concluded that we had enrolled up to 93.9% of non-early-aborted pregnancies. As we enrolled women during the second trimester, we may have missed many late abortions or very early stillbirths. Accordingly, we have probably substantially underestimated the percentage of early stillbirths and the overall stillbirth rate. This selection bias, however, is present—and essentially inescapable—in all studies of stillbirths in developing countries. It does not modify the relations observed with late stillbirths.

Because of missing birthweight data, potential viability could not be determined for 40.6% of the late stillbirths. It is likely that many premature or growth-restricted stillbirths were not weighed. The selection bias may therefore have been less important among the potentially viable stillbirths, although this cannot be demonstrated. The relations observed between intrapartum risk factors and potentially viable stillbirths should thus be interpreted with caution.

We took several steps to avoid introducing any bias when we pooled data from the different study sites. Crude OR were compared with OR adjusted for sites; they did not differ. All regressions were adjusted for site, and the heterogeneity between sites was also taken into consideration.

The variables that we studied were primarily clinical signs, rather than risk factors in the strict sense of the term. Accordingly, a directly causal interpretation of the adjusted population-attributable risks is inappropriate; these risks simply reflect a combination of the level of association and the prevalence of the signs among patients.

External validity
The stillbirth rate we observed was in the same range (13–56) as those reported in other developing countries over the past 20 years.6–13,17–23 The strong associations between late stillbirths and intrapartum risk factors are consistent with those from previous studies in Brazil,17 India,7,19 Nepal10,13 and Zambia.21 The particularly adverse role of non-cephalic presentation and prolonged labour was also emphasized in these studies. The less important but still significant relations with short stature,20,22 maternal age,6,17,18,21 previous stillbirth,7,17,20 late antenatal vaginal bleeding,17,21 and minimal if any antenatal visits7,17,19,21 are also consistent with previous findings. Similarly, others have also found that stillbirth is not significantly associated with socio-economic status,17,20 schooling,17 marital status,6 short period between children17 or undesired pregnancy.17

Other issues
An initial question raised by our findings is whether the intrapartum clinical signs we examined are predictive of an ongoing stillbirth or simply associated with an already dead fetus. A definitive answer would necessitate continuous fetal monitoring. Although this may be feasible in hospital-based studies in developing countries,34 it was not compatible with the observational population-based design of our study. Two points support the hypothesis that these risk factors are predictive. First, other studies in developing countries indicate that an important portion of stillbirths occur during labour. Kunzel et al., in a survey of 3548 pregnancies in three countries in West Africa, found that 60% of the stillbirths were intrapartum deaths.35 In their population-based study of 10 527 pregnancies in Jamaica, Ashley et al. found approximately 56% of the stillbirths to be intrapartum deaths.36 Second, as Ellis et al.10 demonstrated in Nepal, intrapartum risk factors are related to both fetal death and neonatal encephalopathy; this indicates that these factors precede stillbirth rather than following it.

A second question necessarily follows: if these intrapartum clinical signs are predictive of stillbirth, what if any intervention could be helpful? Our results cannot answer this question. We think, however, that implementation of a definition of high risk based principally on late antenatal clinical and labour monitoring could be helpful. The elements in our definition of high risk are not very different from those used in the WHO partograph.37 Its introduction in four hospitals in Southeast Asia was associated with a 38% decline in intrapartum stillbirths. Similar results were obtained in a rural area of Gabon.38 Women with late antenatal vaginal bleeding and intrapartum risk factors should be referred promptly to structures where optimal care is available.


    Conclusion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
The stillbirth rate in the areas we studied in West Africa was high. The main risk factors that we observed for stillbirths were detectable only in the late antenatal and intrapartum periods: vaginal bleeding, hypertension, dystocia, and infection. These results point to the benefits that partograph use could provide. They need to be confirmed by studies incorporating continuous intrapartum fetal monitoring.


KEY MESSAGES

  • A prospective population-based study of 20 326 pregnant women was performed in West Africa. The stillbirth rate was 25.9 per 1000 total births.
  • The principal risk factors for late stillbirth could be detected only in the late antenatal and intrapartum period. They were: late antenatal or intrapartum vaginal bleeding, intrapartum hypertension, dystocia, and infection. These results point up the potential benefits of partograph use.

 


    Acknowledgments
 
To all those involved in the MOMA study for their participation. To PY Ancel, A Dumont and B Salanave for their help and their critical advice on the manuscript. To the French Ministère des Affaires Etrangères-Coopération et Francophonie for financial support to the MOMA study. To the Société Française de Pédiatrie for its grant to M Chalumeau.


    References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
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