Introduction
Reducing maternal mortality is one of the important goals of the United Nations Millennium Development Goals (MDG) and Sustainable Development Goals (SDG).1,2 According to the most recent estimates, near 295,000 women died worldwide in 2017 during and following pregnancy and childbirth, wherein most of the deaths could have been avoided.3 A systematic analysis by the World Health Organization (WHO) reported that obstetric hemorrhage remained the top cause of maternal mortality worldwide, accounting for 27.1% of all maternal deaths, especially in developing countries.4 However, almost three-quarters of maternal deaths caused by obstetric hemorrhage, especially postpartum hemorrhage (PPH), were considered preventable.5 Therefore, reducing maternal deaths caused by obstetric hemorrhage plays an important role in achieving the MDGs and SDGs.
Efforts to reduce maternal deaths due to obstetric hemorrhage are ongoing worldwide; these include measures being taken at three levels: governments, health facilities, and patients.5 Countries such as Italy have achieved great improvement, with the maternal mortality ratio (MMR) due to obstetric hemorrhage having significantly decreased from 2.49 per 100,000 live births in 2007–2013 to 0.77 per 100,000 live births in 2014–2018.6 However, in other countries such as Turkey, the MMR due to obstetric hemorrhage remained unchanged from 2012 to 2015.7 One study published 10 years ago in China reported that the MMR due to obstetric hemorrhage reduced dramatically from 1996 to 2005, and the average annual decline rate was faster in rural areas than in urban areas.8 However, there is a lack of recent nationally representative study on the temporal trends of MMR caused by obstetric hemorrhage in China . In addition, few studies have reported trends in MMR caused by various specific causes of obstetric hemorrhage. Evaluation of MMR due to obstetric hemorrhage and the proportions of underlying death causes is important with respect to carrying out further interventions in maternal mortality.
In this study, we aimed to analyse the temporal trends of MMR due to obstetric hemorrhage and its specific causes in Chinese mainland from 2000 to 2019, to identify whether the rate of change has accelerated or slowed down during this period, and to confirm the causes of obstetric hemorrhage that need further focused intervention in the future.
Methods
Data sources
Data used in the present study were collected from the National Maternal and Child Health Surveillance System (NMCHSS) between 2000 and 2019. The NMCHSS was established by the Ministry of Health of China in 1996 and includes three surveillance systems: maternal mortality, under-5 child mortality, and birth defects. Ninety-seven urban districts and 79 rural counties were stratified and randomly sampled into the NMCHSS based on 17 socioeconomic strata, covering 31 provinces and 60 million residents in Chinese mainland.8–10 See the list of surveillance sites in the Supplemental Digital Content (https://links.lww.com/MFM/A16 ). Given the annual decrease of maternal and child deaths and to ensure the national representation, surveillance sites in the NMCHSS were expanded to 336 urban districts and rural counties in 2006.11 Specialists at the county-level maternal and child health hospitals were responsible for collecting the number of live births and maternal deaths, as well as the case report cards of maternal deaths. Data were reported through the national web-based registration system to municipal maternal and child health hospitals, provincial maternal and child health hospitals, and the National Office for Maternal and Child Health Surveillance. Each maternal death was reviewed by the maternal death review committee at the county level, municipal level, provincial level, and national level according to the WHO-recommended method.12–14 The final underlying cause of death was confirmed by the national review and was coded per the International Classification of Diseases (ICD)-10.8,11
To investigate the underreporting of live births and maternal deaths in the NMCHSS, a set of strict quality control measures were established. The surveillance staff at each level of maternal and child health hospital visited the other departments that also collected maternal mortality information, such as the National Disease Surveillance Points system of the Chinese Center for Disease Control, Household Registration Department of the Ministry of Public Security, and death registration of civil affairs departments (such as crematoria) to verify the numbers and causes of maternal deaths. Finally, based on the results of quality control, the underreporting of deaths and misdiagnosis of causes were corrected.
This study was approved by the ethics committee of the West China Second University Hospital (protocol ID: 2010015). Because the NMCHSS is part of the national data survey system, informed consent is not required.
Definitions
Maternal death was defined according to the WHO criteria: death of a woman while pregnant or within 42 days of termination of pregnancy, irrespective of the duration and the site of pregnancy, from any cause related to or aggravated by pregnancy or its management, but not from accidental or incidental cause.15 The causes of antepartum hemorrhages (APH) included placenta previa and placenta abruption. The causes of PPH included postpartum uterine atony, retained placenta, soft birth canal laceration, uterine rupture, uterine inversion, and late PPH. The definitions of the abovementioned causes of obstetric hemorrhage are based on the ninth edition of Obstetrics and Gynecology textbook.16 We used the National Bureau of Statistics of China 's official definitions of urban districts and rural counties.17 The definitions of eastern, central, and western regions are consistent with those in the National Maternal and Child Health Surveillance Manual.18
Statistical analysis
The characteristics, i.e., distribution of age, education, ethnicity, parity, and region, of maternal deaths due to obstetric hemorrhage were described in four discrete 5-year periods (2000–2004, 2005–2009, 2010–2014, and 2015–2019) and for the first and last years of the study (i.e., 2000 and 2019). Linear trends for changes in characteristics were assessed using linear or logistic models with year treated as a continuous variable. Analyses were based on maternal characteristics with non-missing values. Pie charts were used to show changes in the composition of the causes of obstetric hemorrhage from 2000 to 2019. The MMR and 95% confidence intervals (95% CI ) for regions or causes were estimated by Poisson's distribution. Joinpoint regression (also known as change point analysis) was used to assess the accurate temporal patterns by detecting points of deviation from a linear slope.19 Joinpoint Regression Program version 4.9.0.0 (http://surveillance.cancer.gov/joinpoint/ ) from the National Cancer Institute was used for this analysis.20 As maternal death is a rare event, it is difficult to maintain an annual variation according to an absolute value, but more likely to vary according to a relative value (i.e. percentage). Therefore, the annual percent change (APC) was used to describe the rate of change, and log-linear model was chosen based on the software manual's recommendations.20 All other analyses were performed using Stata version 16.1 (Stata Corp., College Station, TX, USA). A two-tailed P value of <0.05 was considered to indicate statistical significance.
Results
The national MMR due to obstetric hemorrhage was 18.4 per 100,000 live births (95% CI : 15.0–22.2) in 2000. It peaked in 2001 (22.1 per 100,000 live births, 95% CI : 18.3–26.4) and fell to the lowest in 2019 (1.6 per 100,000 live births, 95% CI : 1.0–2.3). Regional MMR experienced similar trends, with all figures peaking in 2001, except for the western region. In the western region, the MMR peaked in 2002 (65.1 per 100,000 live births, 95% CI : 49.5–84.2). The trends of MMR (95% CI ) due to obstetric hemorrhage across different areas of China are presented in Figure 1 .
Figure 1: Trends of MMR (95% CI ) due to obstetric hemorrhage across different areas of Chinese mainland, 2000–2019. CI : Confidence interval; MMR: Maternal mortality ratio.
For a long time, the national MMR caused by obstetric hemorrhage was at a low level, peaking at around 2.0 per 100,000 live births for specific causes of obstetric hemorrhage. However, the national MMR caused by PPH experienced a substantial reduction process and decreased from 17.0 per 100,000 live births (95% CI : 13.8–20.7) in 2000 to 1.3 per 100,000 live births (95% CI : 0.9–2.0) in 2019. The national MMR caused by postpartum uterine atony and retained placenta decreased most noticeably. The trends of national MMR (95% CI ) due to obstetric hemorrhage specified by different causes are presented in Figure 2 .
Figure 2: Trends of national MMR due to obstetric hemorrhage specified by different causes in Chinese mainland, 2000–2019. APH: Antepartum hemorrhages; CI: Confidence interval; MMR: Maternal mortality ratio; PPH: Postpartum hemorrhages.
Joinpoint analysis of national MMR due to obstetric hemorrhage by year showed no change points: significantly declined by 13.0% (95% CI : 11.5–14.5, P < 0.001) per year from 2000 to 2019 (Fig. 3 ). There were also no change points in urban areas and the eastern region: the APC was −11.2% and −10.4%, respectively. However, there were two changes in rural areas: from 2000 to 2003, the APC was 3.3% but not statistically significant (P = 0.715); whereas, from 2003 to 2011, the MMR significantly declined by 18.7% (95% CI : 14.3–22.9, P < 0.001) per year, and from 2011 to 2019, the APC fell to −9.1% (P = 0.004). A similar situation was noted in the western region: from 2000 to 2003, the APC was 1.7% but not statistically significant (P = 0.865); whereas, from 2003 to 2009, the MMR significantly declined by 24.3% (95% CI : 16.6–31.3, P < 0.001) per year; and from 2009 to 2019, the APC fell to −11.7% (P < 0.001). Although there were two change points in the central region, the APC was not statistically significant in the first two time periods (P = 0.071 for 2000–2007 and P = 0.102 for 2007–2010). The MMR significantly declined by 7.8% (95% CI : 2.2–13.0, P = 0.011) per year only between 2010 and 2019.
Figure 3: Annual percent change (APC) of MMR due to obstetric hemorrhage in different regions, A National; B Urban; C Rural; D East; E Central; F West. ∗Indicates that the APC is significantly different from zero at the α = 0.05 level. If the APC is significantly different from zero, it means that MMR increases year by year if APC is positive, on the contrary, MMR decreases year by year if APC is negative. MMR: Maternal mortality ratio.
There were no change points in joinpoint analysis of national MMR caused by APH, placenta previa, postpartum uterine atony, and retained placenta (Fig. 4 ); the respective APCs were −8.7% (P < 0.001), −12.0% (P < 0.001), −10.5% (P < 0.001), and −21.0% (P < 0.001). There were two change points in PPH and uterine rupture. The MMR caused by PPH significantly declined by 8.0% (95% CI : 1.9–13.6, P = 0.015) per year from 2000 to 2007. The APC of MMR caused by PPH accelerated further to −25.0% (P = 0.010) between 2007 and 2011 and then decreased to −7.8% (P = 0.026) between 2011 and 2019. However, the MMR caused by uterine rupture decreased significantly by 27.8% (95% CI : 10.3–41.8, P = 0.007) per year only in the middle period (2005–2011).
Figure 4: Annual Percent Change (APC) of national MMR due to obstetric hemorrhage by different causes, A APH; B PPH; C Placenta previa; D Postpartum uterine atony; E Retained placenta; F Uterine rupture. ∗Indicates that the APC is significantly different from zero at the α = 0.05 level. If the APC is significantly different from zero, it means that MMR increases year by year if APC is positive, on the contrary, MMR decreases year by year if APC is negative. APH: Antepartum hemorrhages; MMR: Maternal mortality ratio; PPH: Postpartum hemorrhages.
The proportion of maternal deaths due to APH increased from 7.6% (8/105) in 2000 to 14.3% (4/28) in 2019 (χ 2 =1.20, P = 0.274). For maternal deaths due to PPH, the proportion of postpartum uterine atony increased from 39.0% (41/105) in 2000 to 60.7% (17/28) in 2019 (χ 2 = 4.22, P = 0.040); moreover, the proportion of uterine rupture also increased from 12.3% (13/105) in 2000 to 14.3% (4/28) in 2019 (χ 2 =0.07, P = 0.789). However, the proportion of retained placenta decreased from 37.1% (39/105) in 2000 to 7.1% (2/28) in 2019 (χ 2 =9.33, P = 0.002). The changes in the composition of specific cause of maternal deaths due to obstetric hemorrhage are presented in Figure 5 .
Figure 5: Changes in the composition of specific cause of maternal deaths due to obstetric hemorrhage. Note: Red is antepartum hemorrhages and blue is postpartum hemorrhages.
From 2000 to 2019, 1831 maternal deaths caused by obstetric hemorrhage were collected in the NMCHSS database (Table 1 ). The mean age of maternal deaths increased from 28.6 in 2000 to 32.9 in 2019 (P for trend < 0.001). There was a statistically significant increase in the proportion of maternal deaths in mothers aged ≥35 years (P for trend < 0.001) from 2000 to 2019. Meanwhile, the proportion of maternal deaths in those who were educated to junior middle school and higher also increased significantly (P for trend < 0.001). In contrast, differences in proportions by ethnicity (Han vs. Non-Han), parity (primipara vs. multipara), region, or urban vs. rural were not statistically significant (the P for trend were 0.932, 0.400, 0.128, and 0.170, respectively).
Table 1 -
Characteristics for maternal deaths due to obstetric haemorrhage in Chinese mainland, 2000–2019.
Characteristics
Total(n = 1831)
2000(n = 105)
2019(n = 28)
2000-2004(n = 524)
2005-2009(n = 612)
2010-2014(n = 443)
2015-2019(n = 252)
Statistics
P value for linear Trend∗
Age (year), mean ± SD
†
30.5 ± 6.0
28.6 ± 5.7
32.9 ± 6.7
29.4 ± 5.5
30.7 ± 6.1
31.2 ± 6.5
31.3 ± 6.0
5.35‡
<0.001
Age group, n (%)†
<35 years
1321 (72.3)
93 (88.6)
17 (63.0)
428 (81.7)
432 (70.6)
288 (65.3)
173 (68.9)
5.42§
<0.001
≥35 years
507 (27.7)
12 (11.4)
10 (37.0)
96 (18.3)
180 (29.4)
153 (34.7)
78 (31.1)
Education, n (%)†
Primary school and below
813 (44.6)
63 (61.2)
11 (39.3)
302 (57.9)
305 (49.8)
157 (35.8)
49 (19.7)
10.38§
<0.001
Junior middle school or above
1009 (55.4)
40 (38.8)
17 (60.7)
220 (42.1)
307 (50.2)
282 (64.2)
200 (80.3)
Ethnicity, n (%)
Han
1396 (76.2)
74 (70.5)
19 (67.9)
386 (73.7)
498 (81.4)
315 (71.1)
197 (78.2)
−0.08§
0.932
Non-Han
435 (23.8)
31 (29.5)
9 (32.1)
138 (26.3)
114 (18.6)
128 (28.9)
55 (21.8)
Parity, n (%)†
Primipara
114 (6.2)
10 (9.5)
2 (7.1)
41 (7.8)
32 (5.2)
21 (4.7)
20 (7.9)
0.84§
0.400
Multipara
1714 (93.8)
95 (90.5)
26 (92.9)
482 (92.2)
578 (94.8)
422 (95.3)
232 (92.1)
Region, n (%)
East
275 (15.0)
4 (3.8)
4 (14.3)
61 (11.6)
90 (14.7)
75 (16.9)
49 (19.4)
−1.52
0.128||
Central
583 (31.8)
34 (32.4)
8 (28.6)
168 (32.1)
211 (34.5)
126 (28.5)
78 (31.0)
West
973 (53.2)
67 (63.8)
16 (57.1)
295 (56.3)
311 (50.8)
242 (54.6)
125 (49.6)
Urban and Rural, n (%)
Rural
1506 (82.3)
91 (86.7)
23 (82.1)
430 (82.1)
516 (84.3)
365 (82.4)
195 (77.4)
1.37§
0.170
Urban
325 (17.7)
14 (13.3)
5 (17.9)
94 (17.9)
96 (15.7)
78 (17.6)
57 (22.6)
∗ The P value for linear trend was for 2000–2019.
† Three maternal deaths had missing value for age, nine had missing value for education, and three had missing value for parity.
‡ t value.
§ z values.
|| Comparison between the proportion of maternal deaths that occurred in the western region and other regions.
Discussion
The main finding of our study is that the MMR due to obstetric hemorrhage declined significantly during the years 2000–2019. Maternal deaths due to retained placenta showed a considerable decline. However, although MMR due to postpartum uterine atony also declined and is now at a low level, it remained the most common cause of maternal death due to obstetric hemorrhage in 2019, followed by rupture. With respect to specific regions, MMR due to obstetric hemorrhage was most pronounced in rural areas and western regions, with both having a slight rise, then a quick fall, then a moderate decline. With respect to specific causes, APH changed little and stayed low, while PPH decreased significantly, particularly for postpartum uterine atony and retained placenta. The rate of decline in MMR due to retained placenta was the fastest, reaching almost twice the rate due to postpartum uterine atony.
A study covering 7 million births showed that the MMR due to obstetric hemorrhage in the USA was 2.3 per 100,000 births between 2003 and 2011.21 Donati et al. reported that MMR due to obstetric hemorrhage in Italy was 2.9 per 100,000 live births during the period 2000–2007.22 Two studies described the MMR due to obstetric hemorrhage in France at around 1.0 per 100,000 live births after 2010.23,24 Blagoeva Atanasova et al. 25 reported that this ratio was <1.0 per 100,000 live births in Spain between 1999 and 2015. Overall, the MMR due to obstetric hemorrhage in high-income countries was already at a very low level 10 years ago. In contrast, the MMR due to obstetric hemorrhage was substantially greater in low- and middle-income countries. One recent study from ten low- and middle-income countries, including sub-Saharan Africa, India, and Haiti showed that the average MMR due to obstetric hemorrhage in these regions was 67.0 per 100,000 deliveries.26 Gulumser et al. 7 reported that the MMR due to obstetric hemorrhage was 4.1 per 100,000 live births in Turkey from 2012 to 2015. A previous study reported that the MMR due to obstetric hemorrhage was 16.6 per 100,000 live births in China in 2005.8 Our study confirmed that China 's recent MMR due to obstetric hemorrhage was approaching that of a high-income country.
The vast majority of studies have focused on maternal mortality over a certain time period. There is very little literature that focuses specifically on temporal trends in maternal mortality due to obstetric hemorrhage. One study showed that the overall MMR in the USA remained stable between 2003 and 2011, but the proportion of obstetric hemorrhage that caused maternal death increased significantly from 8.2% to 22.0%.21 Based on this result, we could infer that the MMR due to obstetric hemorrhage was on the rise in the USA. Some countries, such as Turkey, have not changed in recent years.7 A few countries, such as Italy, reported that the MMR due to obstetric hemorrhage significantly decreased.6 Li et al. 8 reported that the average annual decline rate of MMR due to obstetric hemorrhage was 6.93% in China from 1996 to 2005. However, this study did not report temporal trends for each specific cause of obstetric hemorrhage. Our study found that the MMR due to obstetric hemorrhage declined even faster in the period 2000–2019 than in the 10-year period from 1996 to 2005. In addition, we found that the rate of decline in MMR due to obstetric hemorrhage varied by region and cause, with some (eg, rural areas and PPH) declining more rapidly initially and then becoming slower, and others (eg, uterine rupture) experiencing an initial rapid decline and then stagnating or perhaps even rebounding in recent years.
The Chinese government has invested heavily in maternal and child health, particularly in reducing maternal mortality.27 In 2000, obstetric hemorrhage accounted for 40.5% of maternal deaths in China (mainly retained placenta and postpartum uterine atony),28 and most of them were preventable. To ensure the achievement of MDG5, the “Reducing maternal mortality and eliminating neonatal tetanus” program (one of the best known maternal and child health intervention program) was implemented by the State Council Committee for Women and Children together with the Ministry of Health and the Ministry of Finance since 2000.14 This program began to expand in 2004, reached the maximum number of counties in 2010, ended in 2013, and was then integrated into the National Essential Public Health Programs in 2014.14,29,30 The program covered rural populations in the central and western regions, established hospital delivery subsidy for low-income mothers to encourage hospital delivery, assisted in the establishment of obstetric emergency centers and “green channel” (Green channel refers to a simple, safe and fast way or channel, such as simplifying some procedures of reception, admission, referral, multidisciplinary consultation and rescue.) express referral networks, and provided training for grass root-level clinicians to improve their service of midwifery skills, such as manual removal of the placenta, repairing vaginal laceration, and other first aid skills.14 Most of these basic skills trainings were aimed at obstetric hemorrhage, the major cause of maternal deaths. As a result, an extremely rapid decrease in the MMR due to obstetric hemorrhage was observed in our results for the central and western regions, as well as for the MMR due to retained placenta. It is worth noting that MMR due to obstetric hemorrhage in rural and western areas or that caused by PPH experienced an accelerated decline around 2004–2010 (significantly faster than other time periods), and these change points also coincided highly with the time points for the expansion of coverage of counties in the “Reducing maternal mortality and eliminating neonatal tetanus” program. In addition, some economically developed provinces, such as Beijing and Shanghai, achieved significant reductions in maternal deaths due to PPH by strengthening the management of delivery sites for floating populations, as well as the network management of maternal near miss.31,32
Although our study shows that the MMR in China is currently low, obstetric hemorrhage remains the leading cause of maternal mortality in China .11 In particular, it should be noted that there are significant differences in the decline rate of MMR due to obstetric hemorrhage in different regions or because of different causes. With the change of national fertility policy and the implementation of the “two-child” and “three-child” policies, the proportion of mothers of advanced age or with a history of cesarean section has increased significantly,33 and the risk of obstetric hemorrhage has also consequently increased. Reduction of maternal mortality due to obstetric haemorrhage remains an important challenge to ensure maternal safety in China , despite the current low mortality level. Maybe we can learn from the experience of high-income countries. A study from Italy suggests that improving the quality of care through the development of evidence-based and carefully selected research and training bundle set designed specifically for health professionals involved in pregnancy and delivery assistance to enhance maternal mortality surveillance system may help reduce maternal deaths due to obstetric hemorrhage.6 Clinicians need to be actively involved in maternal near miss and maternal death reviews, providing long-term feedback on the bundles of interventions developed through these reviews, improving actions, and enhancing training on effective measures to create a cycle that will significantly decrease in maternal deaths due to obstetric hemorrhage. In addition, given the particular context of China 's new fertility policy, the “three-child” policy, we should pay particular attention to pregnant women who are older or have a history of cesarean sections. It is important not only to provide adequate prenatal care, but also to carefully assess the mode of delivery for this population. Continuous, careful, and whole-process monitoring is critical for women who have had a previous cesarean section and opt for vaginal delivery. Clinicians should anticipate uterine rupture and be prepared for emergency cesarean section and blood transfusion at any moment to limit the risk of maternal mortality from uterine rupture.
The strength of our study is that the data were collected based on the national maternal death surveillance network and the underlying causes of all cases were determined by the national maternal death review committee, making the MMR due to obstetric hemorrhage and cause-specific MMR accurate, reliable, and nationally representative. However, our study also has some limitations. First, because the MMR in China has been at a low level in recent years, a larger population needs to be included and evaluated to ensure data accuracy. The population covered by the NMCHSS needs to be expanded in the future. Second, data from surveillance systems inevitably suffer from underreporting and therefore should be adjusted according to the underreporting rate to obtain more accurate data. Given the lack of a specific underreporting rate for maternal deaths due to obstetric hemorrhage over the past years, it is not possible to adjust the observed data from the surveillance system in this study. Hence, there is a potential underestimation of the MMR due to obstetric hemorrhage, but this does not affect the estimation of trends in rates.
In conclusion, the intervention practice in China in the past 20 years has proven that it is possible to quickly reduce the MMR due to obstetric hemorrhage. Clinicians and caregivers need to be aware that the MMR due to some specific causes, such as uterine rupture, has been at a plateau and have started to rise. China needs to build on the experience of high-income countries to develop more effective interventions to reduce maternal deaths due to obstetric hemorrhage, especially because of postpartum uterine atony and uterine rupture.
Acknowledgments
The authors thank the institutions and staff of the National Maternal and Child Health Surveillance System for data collection, data entry, and data check.
Funding
This study was supported by the Key Research and Development Projects, Science & Technology Department of Sichuan Province (grant no. 2022YFS0042).
Author Contributions
Juan Liang had full access to all of the data in the study. Juan Liang and Xiaodong Wang designed the study with contribution from all authors. Yi Mu did the statistical analysis with support from Peiran Chen and Yanxia Xie. Yi Mu, Juan Liang, and Xiaodong Wang prepared the first draft and all authors contributed to critical interpretation of the results and revised the manuscript.
Conflicts of Interest
None.
Editor Note
Xiaodong Wang is an Editorial Board Member of Maternal-Fetal Medicine . The article was subject to the journal's standard procedures, with peer review handled independently of this editor and their research groups.
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