SEARCH

SEARCH BY CITATION

Keywords:

  • Early neonatal death;
  • fetal death;
  • maternal complications;
  • perinatal mortality

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information

Objective

We aimed to determine the prevalence and risks of late fetal deaths (LFDs) and early neonatal deaths (ENDs) in women with medical and obstetric complications.

Design

Secondary analysis of the WHO Multicountry Survey on Maternal and Newborn Health (WHOMCS).

Setting

A total of 359 participating facilities in 29 countries.

Population

A total of 308 392 singleton deliveries.

Methods

We reported on perinatal indicators and determined risks of perinatal death in the presence of severe maternal complications (haemorrhagic, infectious, and hypertensive disorders, and other medical conditions).

Main outcome measures

Fresh and macerated LFDs (defined as stillbirths ≥ 1000 g and/or ≥28 weeks of gestation) and ENDs.

Results

The LFD rate was 17.7 per 1000 births; 64.8% were fresh stillbirths. The END rate was 8.4 per 1000 liveborns; 67.1% occurred by day 3 of life. Maternal complications were present in 85.6, 86.5, and 88.6% of macerated LFDs, fresh LFDs, and ENDs, respectively. The risks of all three perinatal mortality outcomes were significantly increased with placental abruption, ruptured uterus, systemic infections/sepsis, pre-eclampsia, eclampsia, and severe anaemia.

Conclusions

Preventing intrapartum-related perinatal deaths requires a comprehensive approach to quality intrapartum care, beyond the provision of caesarean section. Early identification and management of women with complications could improve maternal and perinatal outcomes.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information

Despite enormous global progress in child survival since the 2000 Millennium Declaration, only 23 of the 75 ‘Countdown to 2015’ priority countries are on track to meet Millennium Development Goal 4 (MDG4) targets.[1] The last decade has seen a 2.5% annual reduction in child mortality, but only a 2.1% reduction in neonatal mortality. Newborn deaths now account for over 40% of all deaths in children under the age of 5 years.[1, 2] An estimated 2.6 million stillbirths occur worldwide every year, of which over 40% are intrapartum related.[3-5] Stillbirths are likely to be underestimated, because of the lack of vital registration in many countries, the lack of consistent definitions and classification systems, as well as poor reporting as a result of cultural taboos and social stigma.[5-7]

Perinatal survival is intimately linked to effective maternal and newborn care throughout the continuum of pregnancy, labour, and the postpartum period.[8, 9] Stillbirth risk factors include short interpregnancy interval, low socio-economic status, lower education, no antenatal care, history of stillbirth, smoking, alcohol use, multiple pregnancy, obesity, hypertension, diabetes, HIV, fetal growth restriction and post-term pregnancy.[10-12] In many low- and middle-income countries (LMICs) with high stillbirth rates and inadequate access to diagnostic tools and quality maternal care, these risk factors can go untreated. Preventing antepartum stillbirths requires improved maternal health and antenatal care,[13] whereas intrapartum interventions (such as caesarean section) can reduce the number of intrapartum stillbirths.[13-15] Approximately 85% of neonatal deaths can be attributed to preterm birth complications, infections, and intrapartum-related causes.[1] The majority of these can be prevented without high-cost interventions like intensive care.[16, 17] A South African study by Pattinson et al. identified suboptimal obstetric care and critical staff shortages as being associated with early neonatal mortality,[8] whereas Lawn et al.[9] identified prevention via antenatal care, skilled birth attendance, and emergency obstetric care as the most effective interventions to reduce intrapartum-related newborn deaths.

The risk of perinatal mortality associated with maternal complications has been well described in high-income countries with the capacity to diagnose and manage obstetric complications.[18, 19] These findings cannot necessarily be extrapolated to lower-resource settings, with significant restrictions in human resources, diagnostic capacity, and availability of obstetric interventions, however. The existing studies of perinatal mortality in LMICs have generally been limited in size (single or few institutions) and power (unable to consider stillbirth and early neonatal death as separate outcomes),[20-23] despite accounting for 98% of the global burden. Previous large epidemiological surveys of perinatal deaths in LMICs have not captured data on maternal complications.[2, 24] Such studies are necessary to understand the epidemiological patterns of these conditions and their effect on perinatal mortality, and to prioritise interventions in low-resource settings. We described the prevalence and risks of macerated and fresh stillbirth and early neonatal death in women with severe medical and obstetric complications in 29 countries, using the WHO Multicountry Survey on Maternal and Newborn Health (WHOMCS) data set.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information

Survey methodology

The WHOMCS is a cross-sectional survey of deliveries at 359 participating institutions in 29 countries, conducted from May 2010 to December 2011, and included 314,692 women. This survey collected data on maternal deaths and ‘near-miss’ cases (women who experience severe complications of pregnancy or delivery, and who nearly die but survive), irrespective of gestational age and site of pregnancy. The methodological details of the WHOMCS have been described previously,[25, 26] building on the existing network from the WHO Global Survey.[27] In brief, a stratified, multistage cluster sampling approach was used to obtain a global sample of countries from Africa, Asia, Latin America, and the Middle East. Two randomly selected provinces and the capital city were sampled from within each country. From these, seven institutions with over 1000 deliveries per year and caesarean section capacity were randomly selected. Data were collected for 2 months in institutions with ≥6000 annual deliveries, and for 3 months in institutions with <6000 annual deliveries. In countries where less than 3000 annual deliveries were anticipated, the data collection period was extended to 4 months.

All women giving birth and all women with a severe maternal outcome (death or near miss) associated with pregnancy or childbirth in participating institutions during the data collection period were the study population (including women that had a severe maternal outcome as a result of an abortion or ectopic pregnancy). Data were captured on all eligible participants from presentation to the institution until discharge or day 7 postpartum, whichever came first. Consequently, adverse outcomes occurring before admission, after discharge/day 7, or during a postpartum referral were not captured. Trained data collectors reviewed medical records during the study period and used this to complete the data form at hospital discharge, transfer, or death. There was no contact between data collectors and the admitted women; however, data clarification was occasionally sought from institutional staff. Data were then entered onto a web-based data management system. In addition, an institutional data form was completed by the data collector in consultation with the head of the obstetrics department on facility characteristics, including infrastructure, obstetric and intensive care services, as well as their capacity to identify a range of laboratory, clinical, and management severity indicators for mothers and newborns.

Variables and definitions

We used three perinatal mortality outcomes: (1) macerated late fetal deaths; (2) fresh late fetal deaths; and (3) early neonatal deaths (definitions summarised in Appendix S1). The tenth edition of the International Classification of Diseases (ICD-10) describes stillbirth as death prior to complete expulsion or extraction from the mother, indicated by the absence of any evidence of life.[28] The WHO recommends reporting on late fetal deaths, defined as stillbirths of birthweight ≥ 1000 g, or if birthweight is unknown stillbirths at ≥28 weeks of gestation, for international comparison.[29] When the timing of birth is not known, the absence of skin maceration (‘fresh’) in a fetus that died <12 hours before delivery is generally used as a proxy for intrapartum death.[2] This is an imprecise measure (delays in delivering an intrapartum stillbirth can cause maceration), and can underestimate the true number of intrapartum-related stillbirths[30]; however, it is of practical use in resource-limited settings where fetal status at the onset of labour is often not known. The reference group for both was liveborn neonates with the same birthweight/gestational age restrictions. Early neonatal death was defined as a death occurring by day 7 postpartum or prior to discharge in a liveborn neonate (the reference group was liveborn neonates who were alive at discharge/day 7). This definition slightly underestimates the true early neonatal mortality, as deaths occurring after discharge or during a subsequent readmission were not captured. Gestational age was based on the best obstetric estimate: the method used was not recorded, but varied between institutions. We elected to use these three outcomes separately, as they have different (yet often overlapping) patterns of prevalence, risk factors, and causal pathways. Despite this, few multicountry studies of perinatal mortality in LMICs have considered these outcomes individually, potentially confounding the results. The exposure variables considered were 16 maternal antepartum and intrapartum complications (categorised as haemorrhage disorders, infections, hypertensive disorders, and other complications or diseases) available in the WHOMCS data set as part of the WHO maternal near-miss criteria (described in Appendix S2). Dystocia/prolonged labour was not captured in the WHOMCS and postpartum haemorrhage was not included for this analysis, as it is not temporally related to perinatal deaths.

Statistical analysis

We included all women (including those experiencing a severe maternal outcome) with singleton deliveries of ≥500 g or, if the birthweight was missing, at ≥22 weeks of gestation. Multiple pregnancies were excluded, as their underlying mortality risk is higher and they may be more susceptible to the effect of maternal complications, potentially distorting risk estimates. Amongst 308,392 singleton deliveries, there were 5462 late fetal deaths and 2528 early neonatal deaths (Figure 1). We reported on the proportions of maternal, newborn, and delivery characteristics and conditions in perinatal mortality groups, and tested significance using chi-square tests. Rates of perinatal morbidity and mortality indicators were reported by country. As health facilities were the primary sampling unit of the WHOMCS, individual-level analyses may be affected by clustering. All estimates of association (chi-square tests) were corrected for the cluster effects (health facilities as sampling units, countries as strata) and P < 0.05 was regarded as significant.

image

Figure 1. Study flow chart.

Download figure to PowerPoint

To determine the relationship between maternal complications and perinatal mortality, we reported prevalences for the three outcome groups and calculated odds ratios. The complications as described in Appendix S2 were considered predictors in separate multilevel, multivariate logistic regression models of macerated and fresh late fetal death and early neonatal death. Using the genlinmixed procedure in spss 20, the model accounted for the clustering of mothers within facilities and facilities within countries, as well as adjusting for confounding factors at the maternal (maternal age, marital status, maternal education, number of previous births, and number of previous caesarean sections), perinatal (fetal presentation, congenital malformation, gestational age, and infant sex), and facility level (facility capacity index). The onset of labour and mode of delivery were not considered as confounding factors, as they lie in the causal pathway for several maternal conditions. Missing data were excluded from all modelling. We developed and applied a facility complexity index (FCI) to adjust for the level of services available in each facility, based on a similar index used in the WHO Global Survey.[31] The development and application of the FCI is described in Appendix S3. FCI scores were available for 295 facilities, and ranged from 12 to 57 points (only facilities with no missing data were included in the index).

Statistical analyses were conducted using spss 20.0.0.[32] The article was prepared in accordance with Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines.[33] The WHOMCS was approved by the World Health Organization Ethical Review Committee and relevant ethical clearance bodies in participating countries. This study was supported by the UNDP/UNFPA/UNICEF/WHO/World Bank Special Programme of Research, Development and Research Training in Human Reproduction (HRP), World Health Organization (WHO), United States Agency for International Development (USAID), the Ministry of Health, Labour and Welfare of Japan, and Gynuity Health Projects.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information

In these 308 392 singleton deliveries, the prevalence of late fetal death was 1.8% (64.8% were fresh) and early neonatal mortality was 0.8% (Figure 1). There was a higher prevalence of maternal age >35 years, education of 0 or 1–5 years, more than previous births, male gender, non-cephalic presentation, induced labour, and vaginal delivery in pregnancies resulting in late fetal death (Table 1). Comparatively, the early neonatal mortality group had a higher prevalence of mothers who were <20 years of age, without partners, with education of ≤9 years, with a history of more than one caesarean section, male gender, non-cephalic presentation, no labour, and delivery by caesarean section. Both late fetal and early neonatal deaths had a higher prevalence of low birthweight and preterm birth, and 72.9% of liveborn neonates that died were admitted to a neonatal intensive care unit (NICU; Table 2). Of early neonatal deaths, 67.1% had occurred by day 3 of life, and nearly 33% occurred on the first day (Figure 2). At the country level (Table S1), the median late fetal death rate was 6.6 per 1000 deliveries (interquartile range 4.2–26.8 per 1000 deliveries), and the median early neonatal death rate was 7.5 per 1000 live births (interquartile range 4.5–10.7 per 1000 live births). The overall rates of maternal morbidities by country are described in Table S2. Hypertensive disorders were the most common (2.7%), followed by other complications/diseases (2.5%), haemorrhagic disorders (1.1%), and infective disorders (0.6%).

Table 1. Maternal, neonatal, delivery, and institutional characteristics in all births and perinatal mortality groups
 All birthsPerinatal mortality
n (%)Late fetal deathscLiveborn neonatescAdjusted χ2, PcEarly neonatal deathdInfants alive at discharge/day 7dAdjusted χ2, Pe
n (%)n (%)n (%)n (%)
  1. a

    Late fetal deaths, defined as fetal death of birthweight ≥ 1000 g or, if birthweight unknown, at ≥28 weeks of gestation. Reference group is liveborn neonates with same birthweight/gestational age restrictions.

  2. b

    Adjusted chi-square P value for comparison of late fetal deaths with liveborn neonates only.

  3. c

    Early neonatal deaths, defined as death of a liveborn neonate by discharge/day 7 of life (deaths occurring after discharge were not captured). Reference group is liveborn neonates alive at discharge/day 7. Denominator is liveborn neonates only.

  4. d

    Adjusted chi-square P value for comparison of early neonatal deaths with liveborn neonates only. Denominator is liveborn neonates only.

Total deliveries 308,392 (100.0)5462 (1.8)301,473 (97.8) 2528 (0.8)298,912 (99.2) 
Maternal
Maternal age
<20 years31,896 (10.3)517 (9.5)31,170 (10.3)<0.001320 (12.7)30,839 (10.3)0.010
20–34 years238,679 (77.4)3952 (72.4)233,713 (77.5)1895 (75.0)231,788 (77.5)
≥35 years36,907 (12.0)974 (17.8)35,707 (11.8)305 (12.1)35,415 (11.8)
Missing910 (0.3)19 (0.3)883 (0.3)8 (0.3)870 (0.3)
Marital status
Without partner31,214 (10.1)536 (9.8)30,487 (10.1)0.793344 (13.6)30,176 (10.1)0.002
With partner273,572 (88.7)4853 (88.9)267,473 (88.7)2162 (85.5)265,259 (88.7)
Missing3606 (1.2)73 (1.3)3513 (1.2)22 (0.9)3477 (1.2)
Education
0 years46,580 (15.1)1855 (34.0)44,464 (14.7)<0.001421 (16.7)43,899 (14.7)0.002
1–6 years39,964 (13.0)876 (16.0)38,867 (12.9)368 (14.6)38,505 (12.9)
7–9 years58,190 (18.9)912 (16.7)57,008 (18.9)555 (22.0)56,501 (18.9)
10–12 years88,799 (28.8)1002 (18.3)87,427 (29.0)741 (29.3)86,744 (29.0)
>12 years49,616 (16.1)340 (6.2)49,092 (16.3)247 (9.8)48,884 (16.4)
Missing25,243 (8.2)477 (8.7)24,615 (8.2)196 (7.8)24,379 (8.2)
Previous births
0130,675 (42.4)1874 (34.3)128,203 (42.5)<0.0011066 (42.2)127,142 (42.5)0.105
1 or 2127,637 (41.4)1929 (35.3)125,123 (41.5)1007 (39.8)124,157 (41.5)
>249,465 (16.0)1648 (30.2)47,550 (15.8)451 (17.8)47,023 (15.7)
Missing615 (0.2)11 (0.2)597 (0.2)4 (0.2)590 (0.2)
Any previous caesarean section
0266,845 (86.5)4783 (87.6)260,816 (86.5)0.0582150 (85.0)258,585 (86.5)<0.001
128,768 (9.3)444 (8.1)28,197 (9.4)243 (9.6)27,987 (9.4)
>18606 (2.8)145 (2.7)8407 (2.8)110 (4.4)8309 (2.8)
Missing4173 (1.4)90 (1.6)4053 (1.3)25 (1.0)4031 (1.3)
Neonatal
Sex of neonate
Male157,891 (51.2)2940 (53.8)154,256 (51.2)<0.0011418 (56.1)152,867 (51.1)<0.001
Female150,077 (48.7)2463 (45.1)146,921 (48.7)1102 (43.6)145,798 (48.8)
Missing424 (0.1)59 (1.1)296 (0.1)8 (0.3)247 (0.1)
Delivery
Presentation
Cephalic294,479 (95.5)4609 (84.4)288,795 (95.8)<0.0012138 (84.6)286,534 (95.9)<0.001
Breech10,359 (3.4)611 (11.2)9497 (3.2)307 (12.1)9265 (3.1)
Other2960 (1.0)209 (3.8)2676 (0.9)74 (2.9)2629 (0.9)
Missing594 (0.2)33 (0.6)505 (0.2)9 (0.4)484 (0.2)
Labour
Spontaneous238,558 (77.4)3971 (72.7)233,606 (77.5)<0.0011846 (73.0)231,660 (77.5)<0.001
Induced32,513 (10.5)1021 (18.7)31,221 (10.4)262 (10.4)30,953 (10.4)
No labour36,883 (12.0)451 (8.3)36,242 (12.0)415 (16.4)35,907 (12.0)
Missing438 (0.1)19 (0.3)404 (0.1)5 (0.2)392 (0.1)
Mode of delivery
Vaginal delivery220,836 (71.6)4139 (75.8)215,616 (71.5)0.0011525 (60.3)213,963 (71.6)<0.001
caesarean Section87,137 (28.3)1253 (22.9)85,531 (28.4)992 (39.2)84,635 (28.3)
Missing419 (0.1)70 (1.3)326 (0.1)11 (0.4)314 (0.1)
Institutional
Location of facility
Urban242,545 (78.6)4059 (74.3)237,272 (78.7)0.3822073 (82.0)235,304 (78.7)0.246
Peri-urban29,436 (9.5)588 (10.8)28,743 (9.5)175 (6.9)28,463 (9.5)
Rural14,635 (4.7)308 (5.6)14,274 (4.7)108 (4.3)14,154 (4.7)
Missing21,776 (7.1)507 (9.3)21,184 (7.0)172 (6.8)20,991 (7.0)
Level of facility
Primary16,846 (5.5)205 (3.8)16,578 (5.5)0.128112 (4.4)16,461 (5.5)0.001
Secondary96,905 (31.4)1948 (35.7)94,633 (31.4)634 (25.1)93,838 (31.4)
Tertiary133,262 (43.2)2106 (38.6)130,365 (43.2)1394 (55.1)129,183 (43.2)
Other referral level37,017 (12.0)667 (12.2)36,164 (12.0)196 (7.8)35,912 (12.0)
Missing24,362 (7.9)536 (9.8)23,733 (7.9)192 (7.6)23,518 (7.9)
Table 2. Prevalence of neonatal conditions in all births and perinatal mortality groups
 All birthsPerinatal mortality
Late fetal deathLiveborn neonates
n (%)Late fetal deathcLiveborn neonatescAdjusted χ2, PcEarly neonatal deathdNeonates alive at discharge/day 7dAdjusted χ2, Pe
n (%)n (%)n (%)n (%)
  1. a

    Late fetal deaths, defined as fetal death of birthweight ≥ 1000 g or, if birthweight unknown, ≥28 weeks of gestation. Comparator group is liveborn neonates with same birthweight/gestational age restrictions.

  2. b

    Adjusted chi-square P value for comparison of late fetal deaths with liveborn neonates only.

  3. c

    Early neonatal deaths, defined as death of a liveborn neonate by discharge/day 7 of life (deaths occurring after discharge were not captured). Reference group is liveborn neonates alive at discharge/day 7.

  4. d

    Adjusted chi-square P value for comparison of early neonatal deaths with liveborn neonates only.

  5. e

    Denominator is liveborn neonates only.

Total deliveries 308,392 (100.0)5462 (1.8)301,473 (97.8) 2528 (0.8)298,912 (99.2) 
Birthweight
Low birthweight, <2500 g32,547 (10.6)2390 (43.8)28,896 (9.6)<0.0011530 (60.5)27,873 (9.3)<0.001
2500–3999 g261,843 (84.9)2531 (46.3)259,234 (86.0)944 (37.3)258,121 (86.4)
≥4000 g13,177 (4.3)194 (3.6)12,976 (4.3)54 (2.1)12,918 (4.3)
Missing birthweight825 (0.3)347 (6.4)367 (0.1)0 (0.0)0 (0.0)
Gestational age
All preterm births (<37 weeks)22,222 (7.2)2117 (38.8)18,849 (6.3)<0.0011320 (52.2)17,950 (6.0)<0.001
Term birth (37–42 weeks)278,290 (90.2)3196 (58.5)274,934 (91.2)1135 (44.9)273,350 (91.4)
Post-term birth (≥42 weeks)4860 (1.6)85 (1.6)4768 (1.6)46 (1.8)4714 (1.6)
Missing gestational age3020 (1.0)64 (1.2)2922 (1.0)27 (1.1)2898 (1.0)
Apgar score f
Apgar score <7 at 5 minutes7798 (2.5)   1457 (57.6)6255 (2.1)<0.001
Apgar score ≥7 at 5 minutes293,023 (95.0)  1010 (40.0)291,636 (97.6)
Neonatal ICU f
Admitted to NICU19,519 (6.3)   1842 (72.9)17,578 (5.9)<0.001
Not admitted to NICU282,390 (91.6)  684 (27.1)281,291 (94.1)
image

Figure 2. Distribution of early neonatal mortality by day of life. *Missing information on the date of birth/death for the remaining 8.6% of early neonatal deaths.

Download figure to PowerPoint

The prevalence of all maternal complications was significantly higher in macerated and fresh late fetal deaths and early neonatal deaths, except for placenta accreta/increta/percreta (= 0.071), influenza-like illness (= 0.819), and coincidental conditions (= 0.457) in macerated late fetal deaths, pyelonephritis (= 0.581) and coincidental conditions (= 0.149) in fresh late fetal deaths, and influenza-like illness (= 0.801) in early neonatal deaths (Tables 3 and 4). Figure 3 shows the prevalence of categories of maternal complications in perinatal mortality groups: only 14.4% of macerated late fetal deaths; 13.5% of fresh late fetal deaths; and 11.4% of early neonatal deaths did not have a maternal complication present. The risks of macerated late fetal death, fresh late fetal death, and early neonatal death were consistently increased in mothers with placental abruption, ruptured uterus, systemic infections/sepsis, pre-eclampsia, eclampsia, and severe anaemia (Table 5). Figures 4–6 use logarithmic scales to graph the prevalence of maternal complications against the point estimates for adjusted odds ratios (95% confidence intervals not displayed). The complications plotted towards the upper right corner of these graphs are of higher prevalence and risk.

Table 3. Prevalence of maternal complications in perinatal mortality groups
 All birthsLate fetal deathscLiveborn neonates
n (%)Macerated late fetal deathsbAdjusted χ2, PcFresh late fetal deathsdAdjusted χ2, Pe
n (%)n (%)n (%)
  1. a

    Late fetal deaths, defined as fetal death of birthweight ≥ 1000 g or, if birthweight unknown, at ≥28 weeks of gestation.

  2. b

    Macerated late fetal deaths, defined as late fetal death (birthweight ≥ 1000 g or, if birthweight unknown, at ≥28 weeks of gestation) with signs of maceration. Reference group is liveborn neonates with same birthweight/gestational age restrictions.

  3. c

    Adjusted chi-square P value for comparison of macerated late fetal deaths to liveborn neonates only.

  4. d

    Fresh late fetal deaths, defined as late fetal death (birthweight ≥ 1000 g or, if birthweight unknown, ≥28 weeks of gestation), with no signs of maceration. Reference group is liveborn neonates with same birthweight/gestational age restrictions.

  5. e

    Adjusted chi-square P value for comparison of fresh late deaths to liveborn neonates only.

  6. f

    Medical disease, defined as any one or more of: embolic disease (thromboembolism, amniotic fluid embolism, or air embolism); cancer; heart disease; lung disease; renal disease; or hepatic disease.

All deliveries 308,392 (100.0)1925 3537 301,473 (97.8)
Haemorrhage disorders
Placenta praevia1234 (0.4)23 (1.2)<0.00169 (2.0)<0.0011112 (0.4)
Placenta accreta/increta/percreta465 (0.2)6 (0.3)0.07113 (0.4)0.005435 (0.1)
Placental abruption1045 (0.3)74 (3.8)<0.001245 (6.9)<0.001674 (0.2)
Ruptured uterus297 (0.1)17 (0.9)<0.001128 (3.6)<0.001145 (0.0)
Other obstetric haemorrhage597 (0.2)18 (0.9)<0.00135 (1.0)<0.001523 (0.2)
Infections
Pyelonephritis471 (0.2)11 (0.6)0.0037 (0.2)0.581443 (0.1)
Influenza-like illness225 (0.1)0 (0.0)0.8196 (0.2)0.022216 (0.1)
Other systemic infections/sepsis1081 (0.4)63 (3.3)<0.00157 (1.6)<0.001923 (0.3)
Hypertensive disorders
Chronic hypertension1244 (0.4)31 (1.6)<0.00141 (1.2)<0.0011122 (0.4)
Pre-eclampsia6607 (2.1)129 (6.7)<0.001244 (6.9)<0.0016063 (2.0)
Eclampsia902 (0.3)23 (1.2)<0.001101 (2.9)<0.001738 (0.2)
Other complications or diseases
HIV+/AIDS/HIV wasting syndrome1268 (0.4)24 (1.2)<0.00130 (0.8)<0.0011206 (0.4)
Severe anaemia4385 (1.4)147 (7.6)<0.001320 (9.0)<0.0013840 (1.3)
Malaria/dengue344 (0.1)19 (1.0)<0.00146 (1.3)<0.001268 (0.1)
Medical diseasesf1590 (0.5)31 (1.6)<0.00150 (1.4)<0.0011477 (0.5)
Coincidental conditions645 (0.2)7 (0.4)0.45714 (0.4)0.149605 (0.2)
Table 4. Prevalence of maternal complications in liveborn neonates
 All birthsLiveborn neonatesAdjusted χ2, Pe
n (%)Early neonatal deathdNeonates alive at discharge/day 7
n (%)n (%)
  1. a

    Early neonatal deaths, defined as death of a liveborn neonate by discharge/day 7 of life (deaths occurring after discharge were not captured). Reference group is liveborn neonates alive at discharge/day 7.

  2. b

    Adjusted chi-square P value for comparison of early neonatal deaths with liveborn neonates only.

  3. c

    Medical disease, defined as any one or more of: embolic disease (thromboembolism, amniotic fluid embolism, or air embolism); cancer; heart disease; lung disease; renal disease; or hepatic disease.

All deliveries 308,392 (100.0)2528298,912 
Haemorrhage
Placenta praevia1234 (0.4)52 (2.1)1074 (0.4)<0.001
Placenta accreta/increta/percreta465 (0.2)14 (0.6)427 (0.1)<0.001
Placental abruption1045 (0.3)76 (3.0)607 (0.2)<0.001
Ruptured uterus297 (0.1)12 (0.5)133 (0.0)<0.001
Other obstetric haemorrhage597 (0.2)23 (0.9)509 (0.2)<0.001
Infection
Pyelonephritis471 (0.2)16 (0.6)431 (0.1)<0.001
Influenza-like illness225 (0.1)0 (0.0)216 (0.1)0.801
Other systemic infections/sepsis1081 (0.4)51 (2.0)883 (0.3)<0.001
Hypertensive disorders
Chronic hypertension1244 (0.4)35 (1.4)1103 (0.4)<0.001
Pre-eclampsia6607 (2.1)183 (7.2)5957 (2.0)<0.001
Eclampsia902 (0.3)64 (2.5)674 (0.2)<0.001
Other complications or diseases
HIV+/AIDS/HIV wasting syndrome1268 (0.4)18 (0.7)1190 (0.4)0.022
Severe anaemia4385 (1.4)122 (4.8)3730 (1.2)<0.001
Malaria/dengue344 (0.1)13 (0.5)253 (0.1)<0.001
Medical diseases1590 (0.5)46 (1.8)1436 (0.5)<0.001
Coincidental conditions645 (0.2)22 (0.9)593 (0.2)<0.001
Table 5. Crude and adjusted odds of perinatal mortality groups with maternal complications
 Macerated late fetal deathsaFresh late fetal deathsbEarly neonatal mortalityc
Crude ORAdjusted ORd95% CICrude ORAdjusted ORd95% CICrude ORAdjusted ORd95% CI
  1. a

    Macerated late fetal deaths, defined as late fetal death (birthweight ≥ 1000 g or, if birthweight unknown, at ≥28 weeks of gestation) with signs of maceration. Reference group is liveborn neonates with same birthweight/gestational age restrictions.

  2. b

    Fresh late fetal deaths, defined as late fetal death (birthweight ≥ 1000 g or, if birthweight unknown, at ≥28 weeks of gestation) with no signs of maceration. Reference group is liveborn neonates with same birthweight/gestational age restrictions.

  3. c

    Early neonatal deaths, defined as the death of a liveborn neonate by discharge/day 7 of life (deaths occurring after discharge were not captured). Reference group is liveborn neonates alive at discharge/day 7.

  4. d

    Logistic regression adjusted for: maternal age; marital status; maternal education; number of previous births; number of previous caesarean sections; fetal presentation; congenital malformation; infant sex; gestational age category and facility capacity index. Also adjusted for facility and country as random effects.

  5. e

    Medical disease, defined as any one or more of: embolic disease (thromboembolism, amniotic fluid embolism, or air embolism); cancer; heart disease; lung disease; renal disease; or hepatic disease.

  6. Bold values indicate adjusted ORs where the 95% CI does not excede 1 and are therefore significantly different.

Haemorrhage
Placenta praevia3.271.390.74–2.645.371.190.78–1.815.821.170.84–1.63
Placenta accreta/increta/percreta2.160.900.25–3.162.550.540.05–5.513.891.080.53–2.23
Placental abruption17.84 9.44 6.22–14.34 33.2112.38 8.17–18.75 15.23 4.00 2.74–5.86
Ruptured uterus18.52 7.48 4.02–13.91 78.0345.25 23.22–88.17 10.71 4.18 1.85–9.45
Other obstetric haemorrhage5.43 1.72 1.02–2.88 5.751.470.88–2.485.38 3.16 1.84–9.45
Infection
Pyelonephritis3.91 2.24 1.04–4.82 1.351.200.16–9.134.411.650.91–3.01
Influenza-like illnessNo casesNo casesNo cases2.370.990.42–2.31No casesNo casesNo cases
Other systemic infections/sepsis11.02 6.64 3.57–12.34 5.33 2.72 1.85–3.99 6.95 2.29 1.31–4.01
Hypertensive disorders
Chronic hypertension4.38 2.37 1.60–3.50 3.141.300.97–1.743.790.860.47–1.56
Pre-eclampsia3.50 3.27 2.10–5.07 3.61 2.25 1.80–2.81 3.84 1.72 1.36–2.19
Eclampsia4.93 1.74 1.36–2.23 11.98 3.27 2.30–4.63 11.49 4.84 3.24–6.21
Other complications or diseases
HIV+/AIDS/HIV wasting syndrome3.141.010.79–1.302.131.170.84–1.621.79 0.70 0.51–0.95
Severe anaemia6.41 2.46 1.80–3.36 7.71 2.64 2.23–3.11 4.01 1.37 1.07–1.77
Malaria/dengue11.20 2.08 1.57–2.76 14.81 1.97 1.48–2.62 6.101.680.45–6.32
Medical diseasese3.32 1.78 1.00–3.17 2.911.410.87–2.273.84 1.55 1.08–2.22
Coincidental conditions1.822.840.82–9.841.98 2.08 1.06–4.09 4.422.240.65–7.65
image

Figure 3. Prevalence of maternal complications in macerated and fresh late fetal deaths and early neonatal deaths. †Macerated late fetal deaths, defined as late fetal death (birthweight ≥ 1000 g or, if birthweight unknown, at ≥28 weeks of gestation) with signs of maceration. ‡Fresh late fetal deaths, defined as late fetal death (birthweight ≥ 1000 g or, if birthweight unknown, ≥28 weeks of gestation) with no signs of maceration. *Early neonatal deaths, defined as the death of a liveborn neonate by discharge/day 7 of life (deaths occurring after discharge were not captured). The reference group is liveborn neonates alive at discharge/day 7.

Download figure to PowerPoint

image

Figure 4. Prevalence and adjusted odds ratios of macerated late fetal deaths in maternal complications. The area of each bubble is proportional to the prevalence of these complications among all women; 95% confidence intervals are not displayed. Medical diseases: any one or more of embolic disease (thromboembolism, amniotic fluid embolism, or air embolism); cancer; heart disease; lung disease; renal disease; or hepatic disease.

Download figure to PowerPoint

image

Figure 5. Prevalence and adjusted odds ratios of fresh late fetal deaths in maternal complications. The area of each bubble is proportional to the prevalence of these complications among all women; 95% confidence intervals are not displayed. Medical diseases: any one or more of embolic disease (thromboembolism, amniotic fluid embolism, or air embolism); cancer; heart disease; lung disease; renal disease; or hepatic disease.

Download figure to PowerPoint

image

Figure 6. Prevalence and adjusted odds ratios of early neonatal deaths in maternal complications. The area of each bubble is proportional to the prevalence of these complications among all women; 95% confidence intervals are not displayed. Medical diseases: any one or more of embolic disease (thromboembolism, amniotic fluid embolism, or air embolism); cancer; heart disease; lung disease; renal disease; or hepatic disease.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information

Main findings

We conducted an analysis of the relationship between 16 maternal complications and perinatal mortality in 308 392 singleton deliveries at facilities in 29 countries, the largest such analysis conducted using consistent definitions of maternal morbidities and able to distinguish types of perinatal mortality. The vast majority of perinatal deaths in participating facilities occurred in the presence of a maternal complication, and two-thirds were fresh (i.e. were likely to be intrapartum-related). These relationships are critical in settings where maternal morbidities are often common, under-diagnosed, and/or under-treated, and where perinatal mortality is high. The late fetal death rate (17.7 per 1000 births) was significantly higher than that of higher-income countries – Cousens et al.[3] estimated 3.9 per 1000 births (with a relative uncertainty range of –1.6 to 6.3%) for high-income regions – but was comparable with the rate of 22 per 1000 births reported by McClure et al. in a study of 200 000 community deliveries in low-income countries.[2] Although recent global estimates suggested only 45% of stillbirths are intrapartum,[13] our facility data (64.8% fresh late fetal deaths) and McClure et al.'s community data (only 17.2% were macerated) strongly suggest that intrapartum stillbirths account for a greater proportion than has been previously thought.

Strengths and limitations

This analysis had several strengths. The WHOMCS was conducted in 29 countries, using trained data collectors and a standardised methodology that was refined from our experiences with the previous WHO global survey. We used a validated tool developed through an international collaborative process to assess maternal complications consistently.[34] To the best of our knowledge, it is the biggest international data set linking maternal complications with late fetal and early neonatal deaths. Some limitations must be acknowledged, however. We lacked information on several variables known to contribute to fetal and neonatal mortality, such as diabetes, obesity, malnutrition, syphilis, smoking, length and difficulty of labour, and birth spacing. We were therefore unable to include obstructed labour as a maternal complication, despite its contribution to intrapartum-related stillbirths and early neonatal deaths. The temporality and severity of maternal complications was also not known. As the primary data source was routine medical records, erroneous or absent documentation of complications in the records could have affected data quality, diluting risk estimates; however, we believe this bias was minimised as much as possible by training provisions prior to the commencement of the study (building on our experiences in the WHO global survey) and by data collectors consulting with clinical staff to complement the information obtained from the records, where necessary. The facility-based sampling frame may have led to an over-representation of maternal complications and perinatal deaths, as more complicated cases are referred to these facilities. Similarly, the focus of the survey was on women experiencing severe maternal morbidity and mortality, who are more likely to experience adverse perinatal outcomes. Whereas we have reported on perinatal indicators at the country level to benefit national efforts, our data are not representative of the population and can only be extrapolated to similar settings. As data collection was only conducted for the duration of the admission, we acknowledge that perinatal deaths occurring in the community or post-discharge were not captured by this survey.

Interpretation

Aside from a few lower-income countries with a lower proportion of fresh late fetal deaths (such as Sri Lanka, 39.0%, and Kenya, 49.6%), we were surprised that the proportion of intrapartum-related stillbirths was so high when all participating facilities had the capacity to perform caesarean section: many (if not most) of these fresh stillbirths should have been preventable. Several factors may explain this pattern. Our research group previously reported that coverage of essential maternal interventions (such as uterotonics for the prevention and management of postpartum haemorrhage, magnesium sulfate for eclampsia, and intravenous antibiotics for maternal infections) in the WHOMCS data set was generally high, yet care performance and rates of adverse maternal outcomes were variable between countries.[26] We hypothesised that aspects of obstetric care other than coverage of essential interventions alone, such as delays or obstacles in implementation, or a lack of comprehensive supportive care (such as shock management in postpartum haemorrhage), are equally important to maternal survival. Similarly, although the availability of caesarean section is critical to prevent intrapartum-related stillbirths and early neonatal deaths, so is the early identification of at-risk pregnancies, close supervision during labour, timely access to safe caesarean section, and appropriate postpartum care for mother and baby. The very low late fetal death rates in Vietnam, China, and Paraguay are likely to represent outliers, but the misclassification or under-documentation of stillbirths in some settings may be a factor. Similarly, Vietnam, Thailand, and Afghanistan had very low rates of early neonatal death – this could be related to early neonatal deaths occurring at home post-discharge, which may be increased if women are discharged very soon after delivery. The high rate of low Apgar scores (57.6%) amongst early neonatal deaths is suggestive of the contribution of prolonged labour; however, we lacked data on difficulties during labour and were therefore unable to estimate its impact.

Whereas only 7% of women in the WHOMCS had a potentially life-threatening complication,[26] 85.6% of macerated late fetal deaths, 86.5% of fresh late fetal deaths, and 88.6% of early neonatal deaths occurred in the presence of at least one of these complications. Although our sampling frame was based on larger facilities (and therefore was likely to have an over-representation of complicated pregnancies), this is significantly higher than the 50, 75, and 80% reported by Lawn et al. in a South African perinatal audit data set.[13] This implies that the continuum between maternal complications and perinatal mortality in facility deliveries is more important than previously thought. The early identification of these complications could permit prevention of a greater proportion of perinatal deaths. Although the risk of all types of perinatal mortality in women with complications was consistently high (for placental abruption, ruptured uterus, other systemic infections/sepsis, pre-eclampsia, eclampsia, and severe anaemia), combining information on prevalence and risks (Figures 4–6) implicates pre-eclampsia and severe anaemia as important targets for action. These conditions can be identified in the antenatal period, highlighting the need for improving the continuum of care between community-based antenatal identification of maternal complications and managing these at-risk deliveries and neonates in facilities to prevent perinatal deaths.

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information

The majority of late fetal deaths in deliveries at the participating facilities with access to caesarean section were fresh (i.e. likely to occur in the intrapartum period). Preventing intrapartum-related perinatal deaths goes beyond the provision of caesarean section, requiring a comprehensive approach including the early identification of at-risk pregnancies and universal access to safe, timely caesarean section. The vast majority of perinatal deaths occur in women with a medical or obstetric complication: the early identification and management of these women could yield benefits for improving maternal outcomes, but could also reduce perinatal mortality rates. Maternal complications that can be detected and managed during the antenatal period (such as pre-eclampsia and severe anaemia) are of moderate prevalence and also moderately increase the risks of all types of perinatal mortality. Improving the continuum of care between community-based antenatal identification of maternal complications and managing these at-risk deliveries and neonates in facilities is essential in preventing perinatal deaths.

Disclosure of interests

The authors declare that they have no competing interests or conflicts of interest.

Contribution to authorship

JPV and JPS conceptualised the article and analysis plan. JPV performed the analysis. JPV wrote the draft article, and JPS, RM, NM, PL, ML, JEOP, BH, RPC, MR, SM, JGC, OT, and AMG contributed to the interpretation of the results, development of the article, and approved the final version of the article. This article gives the views of the named authors only.

Details of ethics approval

The Special Programme of Research, Development and Research Training in Human Reproduction (HRP) Specialist Panel on Epidemiological Research reviewed and approved the study protocol for technical content. This study was approved by the World Health Organization Ethical Review Committee and the relevant ethical clearance mechanisms in all countries (protocol ID, A65661; date of approval, 27 October 2009).

Funding

This study was financially supported by: the UNDP/UNFPA/UNICEF/WHO/World Bank Special Programme of Research, Development and Research Training in Human Reproduction (HRP); World Health Organization; United States Agency for International Development (USAID); Ministry of Health, Labour and Welfare of Japan; and Gynuity Health Projects. The sponsors had no role in data collection, analysis, or interpretation of the data, the writing of the report, or the decision to submit for publication. All authors had access to the analysis plan, the outputs of that analysis, and could see the data if they wished to do so. All authors participated in the final discussion and approved the submission. JPV is supported by the Australian Postgraduate Award and the A&A Saw Scholarship.

Acknowledgements

The authors wish to thank all members of the WHO Multicountry Survey on Maternal and Newborn Health Research Network, including regional and country co-ordinators, data collection co-ordinators, facility co-ordinators, data collectors, and all staff of the participating facilities who made the survey possible.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information
  • 1
    Lawn JE, Kinney MV, Black RE, Pitt C, Cousens S, Kerber K, et al. Newborn survival: a multi-country analysis of a decade of change. Health Policy Plan 2012;27(Suppl 3):iii6ii28.
  • 2
    McClure EM, Wright LL, Goldenberg RL, Goudar SS, Parida SN, Jehan I, et al. The global network: a prospective study of stillbirths in developing countries. Am J Obstet Gynecol 2007;197:247.e15.
  • 3
    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;377:131930.
  • 4
    Lawn JE, Gravett MG, Nunes TM, Rubens CE, Stanton C, GAPPS Review Group. Global report on preterm birth and stillbirth (1 of 7): definitions, description of the burden and opportunities to improve data. BMC Pregnancy Childbirth 2010;10(Suppl 1):S1.
  • 5
    Lawn JE, Yakoob MY, Haws RA, Soomro T, Darmstadt GL, Bhutta ZA. 3.2 million stillbirths: epidemiology and overview of the evidence review. BMC Pregnancy Childbirth 2008;9(Suppl 1):S2.
  • 6
    Frøen JF, Cacciatore J, McClure EM, Kuti O, Jokhio AH, Islam M, et al. Stillbirths: why they matter. Lancet 2011;377(9774):135366.
  • 7
    Korteweg FJ, Gordijn SJ, Timmer A, Erwich JJ, Bergman KA, Bouman K, et al. The Tulip classification of perinatal mortality: introduction and multidisciplinary inter-rater agreement. BJOG 2006;113:393401.
  • 8
    Pattinson RC, Makin J, Shaw A. The value of incorporating avoidable factors into perinatal audits. S Afr Med J 1995;85:1457.
  • 9
    Lawn J, Kerber K, Enweronu-Laryea C. 3.6 Million neonatal deaths – what is progressing and what is not? Semin Perinatol 2010;34:37186.
  • 10
    Flenady V, Koopmans L, Middleton P, Frøen JF, Smith GC, Gibbons K, et al. Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis. Lancet 2011;377:133140.
  • 11
    Fretts R. Stillbirth epidemiology, risk factors, and opportunities for stillbirth prevention. Clin Obstet Gynecol 2010;53:58896.
  • 12
    Temmerman M, Chomba EN, Ndinya-Achola J, Plummer FA, Coppens M, Piot P. Maternal human immunodeficiency virus-1 infection and pregnancy outcome. Obstet Gynecol 1994;83:495501.
  • 13
    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;377:144863.
  • 14
    Barros FC, Bhutta Z, Batra M, Hansen TN, Victora CG, Rubens CE. Global report on preterm birth and stillbirth (3 of 7): evidence for effectiveness of interventions. BMC Pregnancy Childbirth 2009;10(Suppl 1):S3.
  • 15
    Victora CG, Rubens CE, GAPPS Review Group. Global report on preterm birth and stillbirth (4 of 7): delivery of interventions. BMC Pregnancy Childbirth 2009;10 (Suppl 1):S4.
  • 16
    Lawn JE, Kerber K, Enweronu-Laryea C, Bateman O. Newborn survival in low resource settings–are we delivering? BJOG 2009;116(Suppl 1):4959.
  • 17
    Knippenberg R, Lawn JE, Darmstadt GL, Begkoyian G, Fogstad H, Walelign N, et al. Systematic scaling up of neonatal care in countries. Lancet 2005;365:108798.
  • 18
    Gardosi J, Madurasinghe V, Williams M, Malik A, Francis A. Maternal and fetal risk factors for stillbirth: population based study. BMJ 2012;346:f108.
  • 19
    Stillbirth Collaborative Research Network Writing Group. Association between stillbirth and risk factors known at pregnancy confirmation. JAMA 2011;306:246979.
  • 20
    Olagbuji BN, Ezeanochie MC, Igbaruma S, Okoigi SO, Ande AB. Stillbirth in cases of severe acute maternal morbidity. Int J Gynecol Obstet 2012;119:536.
  • 21
    Bayou G, Berhan Y. Perinatal mortality and associated risk factors: a case control study. Ethiop J Health Sci 2012;22:15362.
  • 22
    Olamijulo JA, Olaleye OO. Perinatal mortality in Lagos University Teaching Hospital: a five year review. Nig Q J Hosp Med 2010;21:25561.
  • 23
    Fawole AO, Shah A, Tongo O, Dara K, El-Ladan AM, Umezulike AC, et al. Determinants of perinatal mortality in Nigeria. Int J Gynecol Obstet 2011;114:3742.
  • 24
    McClure EM, Pasha O, Goudar SS, Chomba E, Garces A, Tshefu A, et al. Epidemiology of stillbirth in low-middle income countries: a Global Network Study. Acta Obstet Gynecol Scand 2011;90:137985.
  • 25
    Souza JP, Gülmezoglu AM, Carroli G, Lumbiganon P, Qureshi Z, WHOMCS Research Group. The world health organization multicountry survey on maternal and newborn health: study protocol. BMC Health Serv Res 2011;11:286.
  • 26
    Souza JP, Gülmezoglu AM, Vogel J, Carroli G, Lumbiganon P, Qureshi Z, et al. Moving beyond essential interventions for reduction of maternal mortality (the WHO Multicountry Survey on Maternal and Newborn Health): a cross-sectional study. Lancet 2013;381:174755.
  • 27
    Souza J, Gülmezoglu A, Lumbiganon P, Laopaiboon M, Carroli G, Fawole B, et al. Caesarean section without medical indications is associated with an increased risk of adverse short-term maternal outcomes: the 2004–2008 WHO Global Survey on Maternal and Perinatal Health. BMC Med 2010;8:71.
  • 28
    World Health Organization. International Classification of Diseases and Related Health Problems, 10th Revision. Geneva, Switzerland: World Health Organization, 1993.
  • 29
    World Health Organization. Neonatal and Perinatal Mortality: Country, Regional and Global Estimates. Geneva, Switzerland: World Health Organization, 2006.
  • 30
    Lawn J, Shibuya K, Stein C. No cry at birth: global estimates of intrapartum stillbirths and intrapartum-related neonatal deaths. Bull World Health Organ 2005;83:40917.
  • 31
    Villar J, Valladares E, Wojdyla D, Zavaleta N, Carroli G, Velazco A, et al. Caesarean delivery rates and pregnancy outcomes: the 2005 WHO global survey on maternal and perinatal health in Latin America. Lancet 2006;367:181929.
  • 32
    IBM Corporation. PASW Statistics 20 [Internet], 20 edn. Chicago, IL, USA: IBM. Available from: https://www.ibm.com/software/analytics/spss/
  • 33
    von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 2008;61:6.
  • 34
    Souza JP, Cecatti JG, Haddad SM, Parpinelli MA. The WHO maternal near-miss approach and the Maternal Severity Index model (MSI): tools for assessing the management of severe maternal morbidity. PLoS ONE 2012;7:e44129.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
  9. Supporting Information
FilenameFormatSizeDescription
bjo12633-sup-0001-appendixs1final.pdfapplication/PDF214KAppendix S1. Key definitions.
bjo12633-sup-0002-appendixs2final.pdfapplication/PDF142KAppendix S2. Definitions of maternal complications of pregnancy and delivery.
bjo12633-sup-0003-appendixs3final.pdfapplication/PDF161KAppendix S3. Development of the Facility Capacity Index (FCI) for the WHO Multicountry Survey.
bjo12633-sup-0004-tables1final.pdfapplication/PDF306KTable S1. Prevalence of perinatal mortality and morbidity indicators, by country.
bjo12633-sup-0005-tables2final.pdfapplication/PDF187KTable S2. Prevalence of categories of maternal complications, by country.

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.