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Maternal mortality in China, 1996–2005
International Journal of Gynecology and Obstetrics 110 (2010) 93–96
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j g o
CLINICAL ARTICLE
Maternal mortality in China, 1996–2005 Juan Liang, Jun Zhu, Li Dai, Xiaohong Li, Mingrong Li, Yanping Wang ⁎ National Office for Maternal and Child Health Surveillance, West China Second University Hospital, Sichuan University, Chengdu, Sichuan, China
a r t i c l e
i n f o
Article history: Received 18 August 2009 Received in revised form 3 March 2010 Accepted 26 March 2010 Keywords: China Maternal mortality ratio Obstetric hemorrhage Surveillance Trend
a b s t r a c t Objective: To analyze the trend in maternal mortality ratio (MMR), characteristics and causes of maternal deaths, and factors influencing the MMR in China between 1996 and 2005. Methods: Data used in this study are based on the nationwide maternal mortality surveillance system. Trend in MMR and cause-specific mortality were analyzed using the Cochran-Armitage trend test. Results: From 1996 to 2005, MMR was higher in rural areas than in urban areas; and highest in remote areas followed by inner lands and coastal regions. The overall MMR in China decreased from 64.1 per 100 000 live births in 1996 to 47.6 per 100 000 live births in 2005. MMR in rural areas, remote areas, and coastal regions showed a decreasing trend. The leading causes of maternal death were obstetric hemorrhage, pregnancy-induced hypertension, and amniotic fluid embolism. The mortality ratio of obstetric hemorrhage in rural areas and remote areas reduced significantly (P b 0.001). Conclusion: The MMR in China displayed regional differences. Declines in rural areas and remote areas resulted from well-targeted programs by the Chinese government. Future interventions are recommended to target causes of maternal death. © 2010 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Maternal mortality ratio (MMR) is one of the most important indicators reflecting development of a country's economy, culture, and healthcare system, and is recognized globally. According to WHO, there are 500 000 maternal deaths worldwide each year, and 90% occur in low-resource countries [1]. China is one of the largest lowresource countries and has a high number of maternal deaths, accounting for 2% of all maternal deaths worldwide [2]. Twenty years ago, MMR data and information on influencing factors from China were inaccessible. The reports on MMR were mostly regional, and the MMR reported by WHO for China was an estimated figure [3]. Although the Chinese Vital Registration System has collected data on MMR since 1990, these data were based on statistical reports only and did not contain information on individual cases. Data on the causes of death and the influencing factors were also incomplete. The system played a limited role in health and medical policy-making and population interventions [4]. In 1989, the Chinese Ministry of Health established a maternal mortality surveillance system covering the 31 provinces, autonomous regions, and municipalities of the mainland to assess the changes in MMR, main causes of maternal death, and factors influencing MMR, and to provide evidence for policy-making. This system—taking a county (district) as the smallest sampling unit—is population-based, ⁎ Corresponding author. National Office for Maternal and Child Health Surveillance, West China Second University Hospital, Sichuan University, No 17, Section 3, Renmin Nan Lu, Chengdu, Sichuan, China. Tel./fax: +86 28 85501386. E-mail address: [email protected] (Y. Wang).
and the samples selected are representative of a specific region for geographic features and healthcare quality. The system is managed in different stratifications. Specially trained professionals collect information on live births and individual cases of maternal death. The accuracy of the data and the causes of death are guaranteed by a welldesigned data quality management system, investigation of each maternal death, and a strict review system. The surveillance results are released by the Ministry of Health every year. The data collected by the system are included in the National Health Statistics Year Book and cited by scientific studies [5,6]. The aim of the present study was to analyze the trend in maternal mortality ratio (MMR), characteristics and causes of maternal deaths, and factors influencing the MMR in China between 1996 and 2005. Based on these findings, interventions have been proposed to the government. 2. Materials and methods The areas under surveillance were classified according to residence as rural or urban areas, and according to geographic location and socioeconomic status as coastal region, inner land, or remote area [7,8]. A total of 176 surveillance districts/counties were selected across the 31 provinces, autonomous regions, and municipalities of China's mainland. There were 97 urban areas and 79 rural areas; and there were 62 costal regions, 54 inner lands, and 60 remote areas. Pregnant women included in the household registry in surveillance areas were surveyed. The official definition of a maternal death is the death of a woman while pregnant or within 42 days of termination of pregnancy, irrespective of the duration and the site of
0020-7292/$ – see front matter © 2010 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijgo.2010.03.013
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J. Liang et al. / International Journal of Gynecology and Obstetrics 110 (2010) 93–96
pregnancy, from any cause related to or aggravated by pregnancy or its management, but not from accidental or incidental cause. The causes of maternal death were classified as direct obstetric causes and indirect obstetric causes [9]. Data were collected and reported by trained professionals. The quarterly surveillance forms allow recording of the number of live births and maternal deaths, a death registry to list the deaths of women of reproductive age and the causes of death, and an investigation report into the cause of maternal death containing individual information on the case. The clinics of a village or neighborhood record and submit to the township level the numbers of live births and maternal deaths, the list of deaths of women of reproductive age, and the causes of death. The healthcare providers at the township hospitals check the data during the routine meetings with the physicians at township levels and correct errors. Data from a township are summarized quarterly into statistical forms recording the number of live births and deaths, and the forms are submitted to women and child healthcare institutions at the county or district level. The data submitted by townships are collected and summarized by county or district women and child healthcare institutions, and then submitted to healthcare institutions at the provincial level. Finally, data are sent to the National Office for Maternal and Child Health Surveillance, where they are checked and inputted quarterly, and then analyzed annually for compilation of a report to the Ministry of Health. If a maternal death or death of a woman of reproductive age is reported by a village clinic, the woman's family is visited within 3 days by an obstetrician from the township hospital to investigate the cause of death. If the death is confirmed or a new death is found, the information is reported to the institutions at the county or district level. Experienced obstetricians from hospitals at the county or district level interview (using standardized forms) the family members, midwife, insiders, fellow physicians, and nursing staff of the deceased woman, and photocopy the medical records. The investigative reports should be completed within 7 days and the cause of death ascertained. The investigation includes information on prenatal care, history of the pregnancy, course of delivery, the date of termination of pregnancy, and the date of maternal death. In accordance with the review method recommended by WHO [10], maternal deaths were reviewed by a committee at the county and province levels every 6 months. The results were submitted to the National Office for Maternal and Child Health Surveillance, which reviewed the data once a year to rectify possible errors made at the county and provincial levels. The data included in our study originate from the data finalized by the National Review Committee. Trained professionals at each level verified data collection, data accuracy, and cause of death according to the program manual to ensure high quality of data. In addition, before submitting data to higher levels, surveillance officers at the county, provincial, and national levels organized independent retrospective surveys to assess and rectify deficiencies and inaccuracies in data collection and reporting, and in investigation and review of maternal deaths. These data were checked against those recorded by the police office, statistical bureau, crematorium, and department of family planning for any missing live births or deaths. Errors in data were corrected before the issue of the state annual report. Maternal mortality ratio and trend for cause-specific mortality were tested using the Cochran-Armitage trend test (SAS version 9.0; SAS Institute, Carey, NC, USA) [11]. The statistical significance level for α was set at 0.05.
MMR was higher in rural areas compared with urban areas between 1996 and 2005. In rural areas, MMR ranged from 86.4 to 58.3 per 100 000 live births, while in urban areas it ranged from 38.2 to 22.2 per 100 000 live births. Although both areas showed a decrease in MMR, the reduction was statistically significant for rural areas (P b 0.001) (Fig. 1A). MMR also differed by geographic location. Remote areas had the highest MMR and coastal regions had the lowest. Over the study period, MMRs for remote areas, inner lands, and coastal regions ranged from 133.7 to 71.6 per 100 000 live births, 67.7 to 50.9 per 100 000 live births, and 33.6 to 13.3 per 100 000 live births, respectively. Although the MMRs of all 3 locations reduced over the study period, only the declines in remote areas and coastal regions were statistically significant (P b 0.001) (Fig. 1B). Different trends in MMR were observed between 1996 and 2005 (Table 1). Over the entire study period, the overall MMR decreased by 25.7%. The MMRs of urban and rural areas decreased by 5.5% and 31.5%, respectively; and the MMRs of remote areas, inner lands, and costal regions decreased by 34.7%, 24.8%, and 25.2% , respectively. The average annual reduction rate in remote areas was the highest. Changes in MMR differed by subgroup region over different time periods. Between 1996 and 2000, the reduction in MMR and the average annual reduction rate were highest in coastal regions (7.2%), followed by inner lands (6.8%), and remote areas (3.7%); only the reductions for coastal regions and inner lands were statistically significant (P b 0.05). However, between 2000 and 2005, the reduction in MMR and the average annual reduction rate were highest in remote areas, where MMR reduced significantly (P b 0.05). Direct obstetric complications were the leading causes of maternal death, the most common of which were obstetric hemorrhage, pregnancy-induced hypertension, and amniotic fluid embolism.
3. Results From 1996 to 2005, the MMR for China ranged from 43.3–64.1 per 100 000 live births, with the highest and lowest MMRs in 1996 (64.1 per 100 000 live births) and 2002 (43.3 per 100 000 live births). The overall MMR showed a declining trend (P b 0.001).
Fig. 1. Time trends in maternal mortality ratio in China (per 100 000 live births), 1996–2005: (A) Maternal mortality ratio by urban/rural area, 1996–2005; (B) Maternal mortality ratio by geographic location, 1996–2005.
J. Liang et al. / International Journal of Gynecology and Obstetrics 110 (2010) 93–96
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Table 1 Changes in China's maternal mortality ratio by location, 1996–2005. Location
Area classification Urban Rural Total Geographic location Coastal region Inner land Remote area
MMR (per 100 000 live births)
Reduction margin (%)
1996
2000
2005
1996–2000
2000–2005
1996–2005
Average annual reduction rate (%) 1996–2000
2000–2005
1996–2005
29.2 86.4 64.1
28.8 67.2 53.0
27.6 59.2 47.6
–1.4 –22.2 –17.3
–4.2 –11.9 –10.2
–5.5 –31.5 –25.7
–0.3 –6.1 –4.6
–0.8 –2.5 –2.1
–0.6 –4.1 –3.3
28.6 67.7 133.7
21.2 51.0 114.9
21.4 50.9 87.3
–25.9 –24.7 –14.1
0.9 –0.2 –24.0
–25.2 –24.8 –34.7
–7.2 –6.8 –3.7
0.2 0.0 –5.3
–3.2 –3.1 –4.6
Abbreviation: MMR, maternal mortality ratio.
Indirect obstetric causes of maternal death were primarily cardiac disorders and hepatic diseases. Obstetric hemorrhage was the leading cause of death irrespective of urban/rural area or geographic location (Table 2). In 1996, obstetric hemorrhage was the cause of death in 55.8% and 62.9% of cases in rural and remote areas respectively; this
decreased to 49.2% and 45.3%, respectively, in 2005. In both areas, maternal mortality due to obstetric hemorrhage reduced significantly (P b 0.001). However, the reductions observed for other causes of mortality, including cardiac disorders, hepatic diseases, and amniotic fluid embolism, were not significant (P N 0.05). 4. Discussion
Table 2 Primary causes of maternal death in China, 1996–2005. Area and cause of death
Urban/rural Urban Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Rural Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Geographic location Coastal region Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Inner land Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Remote area Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other
Relative proportion (%)
Cause-specific mortality (per 100 000 live births)
1996
2000
2005
1996
2000
2005
P value
19.1 8.8
19.4 10.5
27.5 11.8
5.6 2.6
5.6 3.0
6.6 2.8
0.31 0.20
13.3 4.4 14.7 8.8 30.9
16.4 4.4 10.5 8.0 30.8
7.8 3.9 13.7 3.9 31.4
3.9 1.3 4.3 2.6
4.7 1.3 3.0 2.2
1.9 0.9 3.3 0.9
0.002 0.54 0.004 0.15
55.8 13.8
46.7 16.2
49.2 8.7
48.2 11.9
31.4 10.9
26.2 4.6
b0.001 b0.001
5.4 4.2 6.7 2.6 11.5
9.2 5.2 7.9 4.4 10.4
9.3 3.1 9.2 0.0 20.5
4.7 3.6 5.8 2.2
6.2 3.5 5.3 2.9
4.9 1.6 4.9 0.0
0.81 b0.001 b0.001 0.004
23.5 8.8
21.7 10.9
26.7 4.3
6.7 2.5
4.5 2.3
5.3 0.9
0.15 0.008
19.1 3.0 8.8 5.9 30.9
13.0 0.0 15.2 8.8 30.4
6.7 0.0 8.9 6.7 46.7
5.5 0.8 2.5 1.7
2.7 0.0 3.2 1.8
1.3 0.0 1.8 1.3
b0.001 0.03 0.002 0.07
48.3 15.7
38.5 15.6
42.9 7.9
33.7 11.0
20.7 8.4
19.9 3.7
b0.001 0.002
4.7 4.1 11.0 3.5 12.7
14.1 3.7 7.4 6.7 14.0
11.1 4.8 11.9 0.8 20.6
3.3 2.8 7.7 2.4
7.6 2.0 4.0 3.6
5.2 2.2 5.5 0.4
0.27 0.21 0.16 0.01
62.9 11.4
50.4 15.7
45.3 16.0
84.1 15.3
57.9 18.0
35.0 12.3
b0.001 0.07
3.6 5.0 4.2 2.9 10.0
6.1 8.7 7.0 1.7 10.4
6.7 5.3 6.7 0.0 20.0
4.8 6.7 5.7 3.8
7.0 10.0 8.0 2.0
5.1 4.1 5.1 0.0
0.25 0.003 0.46 0.16
For the decade spanning 1996–2005, MMR in China ranged from 43.3–64.1 per 100 000 live births—lower than the average MMR of other low-resource countries but higher than that of high-income countries [12]. The MMR has declined and the reduction rate is greater than the average rate of both low- and high-income countries [13]. These changes can be attributed primarily to China's fast-developing economy and healthcare services. Similar to other countries [14], MMR in China displays regional differences: a higher MMR in rural areas than in urban areas, and a higher MMR in remote areas than in coastal regions. The large differences between rural and urban areas and among different regions in China may be attributed to the unbalanced development in economy and inequity of healthcare services in these areas [15]. Rural areas in China, especially those in remote areas, are usually poverty-stricken, lacking in resources, and hard to reach. These factors affect the availability and accessibility of healthcare services in such areas. Our study showed that the overall MMR and its trends have marked regional differences. The reductions in MMR from 1996 to 2005 in rural, coastal, and remote areas were statistically significant, whereas the changes in urban and inner areas were not. The trends differed over different time periods. From 1996 to 2000, MMR reduced the most and fastest in coastal and inner areas compared with remote areas, most likely resulting from better economic and healthcare facilities in the former. In these areas, the routine healthcare programs that aim to improve quality of obstetric care and encourage prenatal care significantly reduced local MMR, whereas remote areas did not respond as well to such programs. In view of this, the Chinese government focused on the reduction of MMR in remote areas by initiating the program “Reducing maternal mortality and eliminating newborn tetanus” in 1000 counties in mid-western regions in 2000. Covering 70% of the counties in remote areas [16], this program aimed to eliminate traditional home delivery—adopted by rural women because of its low cost. To encourage hospital deliveries among rural women and therefore lower the risk of maternal death, the program waived inpatient charges for hospital deliveries, improved the quality of local obstetric services, and conducted health education among rural women. As a result, the average rate of hospital delivery in these areas increased by 17% between 2001 and 2005 [17,18]. The MMR in remote areas reduced by 24%, with an annual reduction rate of 5.3%—both figures were higher than those for 1996–2000 in the same areas and those of coastal regions and inner lands. These results proved that well-targeted programs could yield specific effects. Our results also revealed the leading causes of maternal death, occurrence, and the changes in cause-specific mortality—all of which are
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essential for designing interventions and evaluating their effects. The first 3 leading causes of maternal death in China between 1996 and 2005 were direct obstetric causes: obstetric hemorrhage, pregnancy-induced hypertension, and amniotic fluid embolism. As in other Asian countries [19], obstetric hemorrhage was the most common cause of maternal death, and its proportion among all causes was higher in rural areas than in urban areas, and higher in remote areas than in coastal regions. Occurrence of obstetric hemorrhage in rural areas and remote areas was 55.8% and 62.9%, respectively. The figures are high, even though most of the deaths from obstetric hemorrhage are avoidable [20]. Women in rural and remote areas preferred to deliver at home and were typically attended by local midwives not skilled in manual removal of the placenta or use of oxytocin, which often resulted in a retained placenta or uterine inertia that consequently caused obstetric hemorrhage and finally death [21]. The program of “Reducing maternal mortality and eliminating newborn tetanus” was therefore launched to encourage hospital delivery, improve quality of healthcare services at the grassroots level, and ultimately reduce death due to obstetric hemorrhage. In 2005, the occurrence of obstetric hemorrhage in remote areas decreased to 45.3%, and the mortality ratio of obstetric hemorrhage in rural and remote areas reduced significantly. Meanwhile, the mortality ratios of pregnancy-induced hypertension and puerperal infection also reduced, which contributed to the overall reduction in national MMR. It is worth mentioning that the proportions of medical complications such as cardiac disorders and hepatic diseases increased in remote and inner areas. In conclusion, the MMR in China showed a declining trend from 1996 to 2005, and the decreased maternal mortality from obstetric hemorrhage was decisive. Although women who migrated into the surveillance areas were not included, women who migrated out of the areas were followed-up and any cases of death were investigated individually. Therefore, MMR data in the present study are the most reliable for China's health information system. The results of the present study will help medical workers, the government, and international organizations understand the current status and factors influencing maternal deaths in China. More importantly, our study demonstrated that interventional measures targeted at the leading cause of maternal death were highly effective. The study also suggests that efforts to lower MMR should continue to focus on remote areas in the future. Meanwhile, MMR in inner lands and urban areas should also receive further attention. Cause-specific interventions for maternal health should be designed to deal with the primary causes of death, such as obstetric hemorrhage and medical complications.
Acknowledgments This work was supported and funded by the Chinese Ministry of Health. Conflict of Interest None to disclose. References [1] Yayla M. Maternal mortality in developing countries. J Perinat Med 2003;31(5): 386–91. [2] WHO, UNICEF, UNFPA. Maternal mortality in 2000: estimates developed by WHO, UNICEF, UNFPA. Geneva: WHO; 2004. [3] Hill K, AbouZahr C, Wardlaw T. Estimates of maternal mortality for 1995. Bull World Health Organ 2001;79(3):182–93. [4] Ministry of Health of The People's Republic of China. China health statistics yearbook. [In Chinese]. Beijing: Ministry of Health of the People's Republic of China; 2000. [5] Ministry of Health of The People's Republic of China. China health statistics yearbook. [In Chinese]. Beijing: Ministry of Health of the People's Republic of China; 2005. [6] Fang J, Kaufman J. Reproductive health in China: improve the means to the end. Lancet 2008;372(9650):1619–20. [7] Rao K, Chen Y, Tian M. Research on the classification of health status in China. [In Chinese]. Zhongguo Weisheng Tongji 1989;6:12–7. [8] Lin LM, Liu YL, Mi J, Liu JJ, Feng SY, Zhang S, et al. A survey of deaths of children under the age of 5 years in China. [In Chinese]. Chin J Pediatr 1994;32(3):149–52. [9] World Health Organization. International Statistical Classification of Diseases and Related Health Problem (ICD-10). 10th rev.Geneva: WHO; 1993. [10] World Health Organization. Beyond the numbers: reviewing maternal deaths and complications to make pregnancy safer. Geneva: WHO; 2004. [11] Agresti A. Categorical Data Analysis. New York: John Wiley and Sons; 1990. [12] Carrera JM. Maternal mortality in Africa. J Perinat Med 2007;35(4):266–77. [13] Hill K, Thomas K, AbouZahr C, Walker N, Say L, Inoue M, et al. Estimates of maternal mortality worldwide between 1990 and 2005: an assessment of available data. Lancet 2007;370(9595):1311–9. [14] Betran AP, Wojdyla D, Posner SF, Gulmezoglu AM. National estimates for maternal mortality: an analysis based on the WHO systematic review of maternal mortality and morbidity. BMC Public Health 2005;5:131. [15] UNICEF, WHO, UNFPA. Joint review of the maternal and child survival strategy in China. Beijing: UNICEF; 2006. [16] Liang J, Zhu J, Li MR, Wang YP, Dai L, He CH, et al. Analysis of epidemiological characteristics of maternal mortality in target counties in 2007. [In Chinese]. Mod Prev Med 2009;36(10):1851–60. [17] Liang J, Wang YP, Zhu J, Li MR. Analysis of the Relationship between Maternal Mortality Ratio and Support Indicators in China. [In Chinese]. Zhongguo Fu You Bao Jian 2008;23(21):2945–8. [18] Liang J, Wang YP, Zhu J, Li MR. Maternal mortality in 1000 counties in China. [In Chinese]. Sichuan Da Xue Xue Bao Yi Xue Ban 2009;40(2):341–3. [19] Khan KS, Wojdyla D, Say L, Gulmezoglu AM, Van Look PF. WHO analysis of causes of maternal death: a systematic review. Lancet 2006;367(9516):1066–74. [20] Berg CJ, Harper MA, Atkinson SM, Bell EA, Brown HL, Hage ML, et al. Preventability of pregnancy-related deaths: results of a state-wide review. Obstet Gynecol 2005;106(6):1228–34. [21] Liang J, Wang YP, Wu YQ, Zhou GX, Zhu J, Dai L, et al. Maternal mortality in rural areas in China. [In Chinese]. Sichuan Da Xue Xue Bao Yi Xue Ban 2004;35(2):258–60.
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j g o
CLINICAL ARTICLE
Maternal mortality in China, 1996–2005 Juan Liang, Jun Zhu, Li Dai, Xiaohong Li, Mingrong Li, Yanping Wang ⁎ National Office for Maternal and Child Health Surveillance, West China Second University Hospital, Sichuan University, Chengdu, Sichuan, China
a r t i c l e
i n f o
Article history: Received 18 August 2009 Received in revised form 3 March 2010 Accepted 26 March 2010 Keywords: China Maternal mortality ratio Obstetric hemorrhage Surveillance Trend
a b s t r a c t Objective: To analyze the trend in maternal mortality ratio (MMR), characteristics and causes of maternal deaths, and factors influencing the MMR in China between 1996 and 2005. Methods: Data used in this study are based on the nationwide maternal mortality surveillance system. Trend in MMR and cause-specific mortality were analyzed using the Cochran-Armitage trend test. Results: From 1996 to 2005, MMR was higher in rural areas than in urban areas; and highest in remote areas followed by inner lands and coastal regions. The overall MMR in China decreased from 64.1 per 100 000 live births in 1996 to 47.6 per 100 000 live births in 2005. MMR in rural areas, remote areas, and coastal regions showed a decreasing trend. The leading causes of maternal death were obstetric hemorrhage, pregnancy-induced hypertension, and amniotic fluid embolism. The mortality ratio of obstetric hemorrhage in rural areas and remote areas reduced significantly (P b 0.001). Conclusion: The MMR in China displayed regional differences. Declines in rural areas and remote areas resulted from well-targeted programs by the Chinese government. Future interventions are recommended to target causes of maternal death. © 2010 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Maternal mortality ratio (MMR) is one of the most important indicators reflecting development of a country's economy, culture, and healthcare system, and is recognized globally. According to WHO, there are 500 000 maternal deaths worldwide each year, and 90% occur in low-resource countries [1]. China is one of the largest lowresource countries and has a high number of maternal deaths, accounting for 2% of all maternal deaths worldwide [2]. Twenty years ago, MMR data and information on influencing factors from China were inaccessible. The reports on MMR were mostly regional, and the MMR reported by WHO for China was an estimated figure [3]. Although the Chinese Vital Registration System has collected data on MMR since 1990, these data were based on statistical reports only and did not contain information on individual cases. Data on the causes of death and the influencing factors were also incomplete. The system played a limited role in health and medical policy-making and population interventions [4]. In 1989, the Chinese Ministry of Health established a maternal mortality surveillance system covering the 31 provinces, autonomous regions, and municipalities of the mainland to assess the changes in MMR, main causes of maternal death, and factors influencing MMR, and to provide evidence for policy-making. This system—taking a county (district) as the smallest sampling unit—is population-based, ⁎ Corresponding author. National Office for Maternal and Child Health Surveillance, West China Second University Hospital, Sichuan University, No 17, Section 3, Renmin Nan Lu, Chengdu, Sichuan, China. Tel./fax: +86 28 85501386. E-mail address: [email protected] (Y. Wang).
and the samples selected are representative of a specific region for geographic features and healthcare quality. The system is managed in different stratifications. Specially trained professionals collect information on live births and individual cases of maternal death. The accuracy of the data and the causes of death are guaranteed by a welldesigned data quality management system, investigation of each maternal death, and a strict review system. The surveillance results are released by the Ministry of Health every year. The data collected by the system are included in the National Health Statistics Year Book and cited by scientific studies [5,6]. The aim of the present study was to analyze the trend in maternal mortality ratio (MMR), characteristics and causes of maternal deaths, and factors influencing the MMR in China between 1996 and 2005. Based on these findings, interventions have been proposed to the government. 2. Materials and methods The areas under surveillance were classified according to residence as rural or urban areas, and according to geographic location and socioeconomic status as coastal region, inner land, or remote area [7,8]. A total of 176 surveillance districts/counties were selected across the 31 provinces, autonomous regions, and municipalities of China's mainland. There were 97 urban areas and 79 rural areas; and there were 62 costal regions, 54 inner lands, and 60 remote areas. Pregnant women included in the household registry in surveillance areas were surveyed. The official definition of a maternal death is the death of a woman while pregnant or within 42 days of termination of pregnancy, irrespective of the duration and the site of
0020-7292/$ – see front matter © 2010 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijgo.2010.03.013
94
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pregnancy, from any cause related to or aggravated by pregnancy or its management, but not from accidental or incidental cause. The causes of maternal death were classified as direct obstetric causes and indirect obstetric causes [9]. Data were collected and reported by trained professionals. The quarterly surveillance forms allow recording of the number of live births and maternal deaths, a death registry to list the deaths of women of reproductive age and the causes of death, and an investigation report into the cause of maternal death containing individual information on the case. The clinics of a village or neighborhood record and submit to the township level the numbers of live births and maternal deaths, the list of deaths of women of reproductive age, and the causes of death. The healthcare providers at the township hospitals check the data during the routine meetings with the physicians at township levels and correct errors. Data from a township are summarized quarterly into statistical forms recording the number of live births and deaths, and the forms are submitted to women and child healthcare institutions at the county or district level. The data submitted by townships are collected and summarized by county or district women and child healthcare institutions, and then submitted to healthcare institutions at the provincial level. Finally, data are sent to the National Office for Maternal and Child Health Surveillance, where they are checked and inputted quarterly, and then analyzed annually for compilation of a report to the Ministry of Health. If a maternal death or death of a woman of reproductive age is reported by a village clinic, the woman's family is visited within 3 days by an obstetrician from the township hospital to investigate the cause of death. If the death is confirmed or a new death is found, the information is reported to the institutions at the county or district level. Experienced obstetricians from hospitals at the county or district level interview (using standardized forms) the family members, midwife, insiders, fellow physicians, and nursing staff of the deceased woman, and photocopy the medical records. The investigative reports should be completed within 7 days and the cause of death ascertained. The investigation includes information on prenatal care, history of the pregnancy, course of delivery, the date of termination of pregnancy, and the date of maternal death. In accordance with the review method recommended by WHO [10], maternal deaths were reviewed by a committee at the county and province levels every 6 months. The results were submitted to the National Office for Maternal and Child Health Surveillance, which reviewed the data once a year to rectify possible errors made at the county and provincial levels. The data included in our study originate from the data finalized by the National Review Committee. Trained professionals at each level verified data collection, data accuracy, and cause of death according to the program manual to ensure high quality of data. In addition, before submitting data to higher levels, surveillance officers at the county, provincial, and national levels organized independent retrospective surveys to assess and rectify deficiencies and inaccuracies in data collection and reporting, and in investigation and review of maternal deaths. These data were checked against those recorded by the police office, statistical bureau, crematorium, and department of family planning for any missing live births or deaths. Errors in data were corrected before the issue of the state annual report. Maternal mortality ratio and trend for cause-specific mortality were tested using the Cochran-Armitage trend test (SAS version 9.0; SAS Institute, Carey, NC, USA) [11]. The statistical significance level for α was set at 0.05.
MMR was higher in rural areas compared with urban areas between 1996 and 2005. In rural areas, MMR ranged from 86.4 to 58.3 per 100 000 live births, while in urban areas it ranged from 38.2 to 22.2 per 100 000 live births. Although both areas showed a decrease in MMR, the reduction was statistically significant for rural areas (P b 0.001) (Fig. 1A). MMR also differed by geographic location. Remote areas had the highest MMR and coastal regions had the lowest. Over the study period, MMRs for remote areas, inner lands, and coastal regions ranged from 133.7 to 71.6 per 100 000 live births, 67.7 to 50.9 per 100 000 live births, and 33.6 to 13.3 per 100 000 live births, respectively. Although the MMRs of all 3 locations reduced over the study period, only the declines in remote areas and coastal regions were statistically significant (P b 0.001) (Fig. 1B). Different trends in MMR were observed between 1996 and 2005 (Table 1). Over the entire study period, the overall MMR decreased by 25.7%. The MMRs of urban and rural areas decreased by 5.5% and 31.5%, respectively; and the MMRs of remote areas, inner lands, and costal regions decreased by 34.7%, 24.8%, and 25.2% , respectively. The average annual reduction rate in remote areas was the highest. Changes in MMR differed by subgroup region over different time periods. Between 1996 and 2000, the reduction in MMR and the average annual reduction rate were highest in coastal regions (7.2%), followed by inner lands (6.8%), and remote areas (3.7%); only the reductions for coastal regions and inner lands were statistically significant (P b 0.05). However, between 2000 and 2005, the reduction in MMR and the average annual reduction rate were highest in remote areas, where MMR reduced significantly (P b 0.05). Direct obstetric complications were the leading causes of maternal death, the most common of which were obstetric hemorrhage, pregnancy-induced hypertension, and amniotic fluid embolism.
3. Results From 1996 to 2005, the MMR for China ranged from 43.3–64.1 per 100 000 live births, with the highest and lowest MMRs in 1996 (64.1 per 100 000 live births) and 2002 (43.3 per 100 000 live births). The overall MMR showed a declining trend (P b 0.001).
Fig. 1. Time trends in maternal mortality ratio in China (per 100 000 live births), 1996–2005: (A) Maternal mortality ratio by urban/rural area, 1996–2005; (B) Maternal mortality ratio by geographic location, 1996–2005.
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Table 1 Changes in China's maternal mortality ratio by location, 1996–2005. Location
Area classification Urban Rural Total Geographic location Coastal region Inner land Remote area
MMR (per 100 000 live births)
Reduction margin (%)
1996
2000
2005
1996–2000
2000–2005
1996–2005
Average annual reduction rate (%) 1996–2000
2000–2005
1996–2005
29.2 86.4 64.1
28.8 67.2 53.0
27.6 59.2 47.6
–1.4 –22.2 –17.3
–4.2 –11.9 –10.2
–5.5 –31.5 –25.7
–0.3 –6.1 –4.6
–0.8 –2.5 –2.1
–0.6 –4.1 –3.3
28.6 67.7 133.7
21.2 51.0 114.9
21.4 50.9 87.3
–25.9 –24.7 –14.1
0.9 –0.2 –24.0
–25.2 –24.8 –34.7
–7.2 –6.8 –3.7
0.2 0.0 –5.3
–3.2 –3.1 –4.6
Abbreviation: MMR, maternal mortality ratio.
Indirect obstetric causes of maternal death were primarily cardiac disorders and hepatic diseases. Obstetric hemorrhage was the leading cause of death irrespective of urban/rural area or geographic location (Table 2). In 1996, obstetric hemorrhage was the cause of death in 55.8% and 62.9% of cases in rural and remote areas respectively; this
decreased to 49.2% and 45.3%, respectively, in 2005. In both areas, maternal mortality due to obstetric hemorrhage reduced significantly (P b 0.001). However, the reductions observed for other causes of mortality, including cardiac disorders, hepatic diseases, and amniotic fluid embolism, were not significant (P N 0.05). 4. Discussion
Table 2 Primary causes of maternal death in China, 1996–2005. Area and cause of death
Urban/rural Urban Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Rural Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Geographic location Coastal region Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Inner land Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other Remote area Hemorrhage Pregnancy-induced hypertension Amniotic fluid embolism Puerperal infection Cardiac disorders Hepatic diseases Other
Relative proportion (%)
Cause-specific mortality (per 100 000 live births)
1996
2000
2005
1996
2000
2005
P value
19.1 8.8
19.4 10.5
27.5 11.8
5.6 2.6
5.6 3.0
6.6 2.8
0.31 0.20
13.3 4.4 14.7 8.8 30.9
16.4 4.4 10.5 8.0 30.8
7.8 3.9 13.7 3.9 31.4
3.9 1.3 4.3 2.6
4.7 1.3 3.0 2.2
1.9 0.9 3.3 0.9
0.002 0.54 0.004 0.15
55.8 13.8
46.7 16.2
49.2 8.7
48.2 11.9
31.4 10.9
26.2 4.6
b0.001 b0.001
5.4 4.2 6.7 2.6 11.5
9.2 5.2 7.9 4.4 10.4
9.3 3.1 9.2 0.0 20.5
4.7 3.6 5.8 2.2
6.2 3.5 5.3 2.9
4.9 1.6 4.9 0.0
0.81 b0.001 b0.001 0.004
23.5 8.8
21.7 10.9
26.7 4.3
6.7 2.5
4.5 2.3
5.3 0.9
0.15 0.008
19.1 3.0 8.8 5.9 30.9
13.0 0.0 15.2 8.8 30.4
6.7 0.0 8.9 6.7 46.7
5.5 0.8 2.5 1.7
2.7 0.0 3.2 1.8
1.3 0.0 1.8 1.3
b0.001 0.03 0.002 0.07
48.3 15.7
38.5 15.6
42.9 7.9
33.7 11.0
20.7 8.4
19.9 3.7
b0.001 0.002
4.7 4.1 11.0 3.5 12.7
14.1 3.7 7.4 6.7 14.0
11.1 4.8 11.9 0.8 20.6
3.3 2.8 7.7 2.4
7.6 2.0 4.0 3.6
5.2 2.2 5.5 0.4
0.27 0.21 0.16 0.01
62.9 11.4
50.4 15.7
45.3 16.0
84.1 15.3
57.9 18.0
35.0 12.3
b0.001 0.07
3.6 5.0 4.2 2.9 10.0
6.1 8.7 7.0 1.7 10.4
6.7 5.3 6.7 0.0 20.0
4.8 6.7 5.7 3.8
7.0 10.0 8.0 2.0
5.1 4.1 5.1 0.0
0.25 0.003 0.46 0.16
For the decade spanning 1996–2005, MMR in China ranged from 43.3–64.1 per 100 000 live births—lower than the average MMR of other low-resource countries but higher than that of high-income countries [12]. The MMR has declined and the reduction rate is greater than the average rate of both low- and high-income countries [13]. These changes can be attributed primarily to China's fast-developing economy and healthcare services. Similar to other countries [14], MMR in China displays regional differences: a higher MMR in rural areas than in urban areas, and a higher MMR in remote areas than in coastal regions. The large differences between rural and urban areas and among different regions in China may be attributed to the unbalanced development in economy and inequity of healthcare services in these areas [15]. Rural areas in China, especially those in remote areas, are usually poverty-stricken, lacking in resources, and hard to reach. These factors affect the availability and accessibility of healthcare services in such areas. Our study showed that the overall MMR and its trends have marked regional differences. The reductions in MMR from 1996 to 2005 in rural, coastal, and remote areas were statistically significant, whereas the changes in urban and inner areas were not. The trends differed over different time periods. From 1996 to 2000, MMR reduced the most and fastest in coastal and inner areas compared with remote areas, most likely resulting from better economic and healthcare facilities in the former. In these areas, the routine healthcare programs that aim to improve quality of obstetric care and encourage prenatal care significantly reduced local MMR, whereas remote areas did not respond as well to such programs. In view of this, the Chinese government focused on the reduction of MMR in remote areas by initiating the program “Reducing maternal mortality and eliminating newborn tetanus” in 1000 counties in mid-western regions in 2000. Covering 70% of the counties in remote areas [16], this program aimed to eliminate traditional home delivery—adopted by rural women because of its low cost. To encourage hospital deliveries among rural women and therefore lower the risk of maternal death, the program waived inpatient charges for hospital deliveries, improved the quality of local obstetric services, and conducted health education among rural women. As a result, the average rate of hospital delivery in these areas increased by 17% between 2001 and 2005 [17,18]. The MMR in remote areas reduced by 24%, with an annual reduction rate of 5.3%—both figures were higher than those for 1996–2000 in the same areas and those of coastal regions and inner lands. These results proved that well-targeted programs could yield specific effects. Our results also revealed the leading causes of maternal death, occurrence, and the changes in cause-specific mortality—all of which are
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essential for designing interventions and evaluating their effects. The first 3 leading causes of maternal death in China between 1996 and 2005 were direct obstetric causes: obstetric hemorrhage, pregnancy-induced hypertension, and amniotic fluid embolism. As in other Asian countries [19], obstetric hemorrhage was the most common cause of maternal death, and its proportion among all causes was higher in rural areas than in urban areas, and higher in remote areas than in coastal regions. Occurrence of obstetric hemorrhage in rural areas and remote areas was 55.8% and 62.9%, respectively. The figures are high, even though most of the deaths from obstetric hemorrhage are avoidable [20]. Women in rural and remote areas preferred to deliver at home and were typically attended by local midwives not skilled in manual removal of the placenta or use of oxytocin, which often resulted in a retained placenta or uterine inertia that consequently caused obstetric hemorrhage and finally death [21]. The program of “Reducing maternal mortality and eliminating newborn tetanus” was therefore launched to encourage hospital delivery, improve quality of healthcare services at the grassroots level, and ultimately reduce death due to obstetric hemorrhage. In 2005, the occurrence of obstetric hemorrhage in remote areas decreased to 45.3%, and the mortality ratio of obstetric hemorrhage in rural and remote areas reduced significantly. Meanwhile, the mortality ratios of pregnancy-induced hypertension and puerperal infection also reduced, which contributed to the overall reduction in national MMR. It is worth mentioning that the proportions of medical complications such as cardiac disorders and hepatic diseases increased in remote and inner areas. In conclusion, the MMR in China showed a declining trend from 1996 to 2005, and the decreased maternal mortality from obstetric hemorrhage was decisive. Although women who migrated into the surveillance areas were not included, women who migrated out of the areas were followed-up and any cases of death were investigated individually. Therefore, MMR data in the present study are the most reliable for China's health information system. The results of the present study will help medical workers, the government, and international organizations understand the current status and factors influencing maternal deaths in China. More importantly, our study demonstrated that interventional measures targeted at the leading cause of maternal death were highly effective. The study also suggests that efforts to lower MMR should continue to focus on remote areas in the future. Meanwhile, MMR in inner lands and urban areas should also receive further attention. Cause-specific interventions for maternal health should be designed to deal with the primary causes of death, such as obstetric hemorrhage and medical complications.
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