Rise in maternal mortality in the Netherlands - Wiley Online Library

Maternal medicine

DOI: 10.1111/j.1471-0528.2009.02382.x www.bjog.org

Rise in maternal mortality in the Netherlands JM Schutte,a EAP Steegers,b NWE Schuitemaker,c JG Santema,d* K de Boer,e M Pel,f G Vermeulen,g W Visser,b J van Roosmalen,h,i the Netherlands Maternal Mortality Committee a

Department of Obstetrics and Gynaecology, Isala Klinieken Zwolle, Zwolle, the Netherlands b Department of Obstetrics and Gynaecology, Division of Obstetrics and Prenatal Medicine, Erasmus University Medical Center Rotterdam, Rotterdam, the Netherlands c Diakonessenhuis Utrecht, Utrecht, the Netherlands d Department of Obstetrics and Gynaecology, Medical Center Leeuwarden, Leeuwarden, the Netherlands e Department of Obstetrics and Gynaecology, Rijnstate Hospital Arnhem, Arnhem, the Netherlands f Department of Obstetrics and Gynaecology, Amsterdam Medical Center, Amsterdam, the Netherlands g Department of Obstetrics and Gynaecology, Diaconessenhuis Meppel, the Netherlands h Department of Obstetrics and Gynaecology, Leiden University Medical Center, Leiden, the Netherlands i Department of Obstetrics and Gynaecology, VU University Medical Center, Amsterdam, the Netherlands Correspondence: Dr JM Schutte, Department of Obstetrics and Gynaecology, Isala Klinieken Zwolle, Dr Van Heesweg 2, PO Box 10400, 8025 AB Zwolle, the Netherlands. Email [email protected] Accepted 3 August 2009. Published Online 26 November 2009.

Objective To assess causes, trends and substandard care factors in

maternal mortality in the Netherlands. Design Confidential enquiry into the causes of maternal mortality. Setting Nationwide in the Netherlands. Population 2,557,208 live births. Methods Data analysis of all maternal deaths in the period 1993–

2005. Main outcome measures Maternal mortality. Results The overall maternal mortality ratio was 12.1 per 100 000 live births, which was a statistically significant rise compared with the maternal mortality ratio of 9.7 in the period 1983–1992 (OR 1.2, 95% CI 1.0–1.5). The most frequent direct causes were (pre)eclampsia, thromboembolism, sudden death in pregnancy, sepsis, obstetric haemorrhage and amniotic fluid embolism. The number

of indirect deaths also increased, mainly caused by an increase in cardiovascular disorders (OR 2.5, 95% CI 1.4–4.6). Women younger than 20 years and older than 45 years, those with high parity or from nonwestern immigrant populations were at higher risk. Most substandard care was found in women with preeclampsia (91%) and in immigrant populations (62%). Conclusions Maternal mortality in the Netherlands has increased

since 1983–1992. Pre-eclampsia remains the number one cause. Groups at higher risk for complications during pregnancy should be better identified early in pregnancy or before conception, in order to receive preconception advice and more frequent antenatal visits. There is an urgent need for the better education of women and professionals concerning the danger signs, and for the training of professionals in order to improve maternal health care. Keywords Immigrant populations, maternal mortality, pre-

eclampsia, safe motherhood, substandard care.

Please cite this paper as: Schutte J, Steegers E, Schuitemaker N, Santema J, de Boer K, Pel M, Vermeulen G, Visser W, van Roosmalen J, the Netherlands Maternal Mortality Committee. Rise in maternal mortality in the Netherlands. BJOG 2010;117:399–406.

Introduction In high-income countries, relatively few women die as a result of pregnancy, childbirth or puerperium. However, next to perinatal mortality, the maternal mortality ratio (maternal mortality per 100 000 live-born children, MMR) reflects the quality of obstetric care, and can be used for international comparisons. Although the absolute numbers are small, maternal death is just the tip of the iceberg of serious maternal morbidity. *Deceased.

The Dutch Maternal Mortality Committee (MMC), instituted by the Netherlands Society of Obstetrics and Gynaecology in 1981, published its first report in 1998, covering the years 1983–1992.1 The only two other countries performing periodical nationwide confidential enquiries are the UK2 and South Africa,3 although other countries publish reports on maternal mortality using vital statistics or regional data, which often results in underreporting.4 The MMR in the period 1983–1992 in the Netherlands was 9.7 per 100 000 live births. The level of substandard care in women with pre-eclampsia (93%) and the 20% underreporting to the enquiry indicated goals for improve-

ª 2009 The Authors Journal compilation ª RCOG 2009 BJOG An International Journal of Obstetrics and Gynaecology

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ment in the following decade. Recommendations were made to improve care, especially for immigrant populations, and to report cases to the MMC to lower the percentage of underreporting. This paper contains a nationwide analysis of maternal deaths during the period 1993–2005, examining trends in maternal mortality and evaluating the level of implementation of the recommendations of the previous report.

Methods All maternal deaths reported to the MMC during pregnancy or within 1 year after pregnancy between January 1993 and December 2005 in the Netherlands were included in the study. The MMC is made up of eight obstetricians and one internal medicine specialist working in the field of maternal medicine, appointed by the Dutch Society of Obstetrics and Gynaecology. The members are from both university and peripheral hospitals. Maternal mortality cases were voluntarily reported to the MMC by obstetricians and, in some cases, by midwives and GPs. Additional cases were collected after a cross-check with the data collected by Statistics Netherlands, which collects all vital data from the Netherlands. Finally, a request to report every death during or within 1 year after pregnancy in the study period was submitted to all 98 obstetric departments in the Netherlands. Maternal death was defined and classified according to the World Health Organisation’s International Classification of Diseases, 10th revision (ICD-10).5 Deaths were classified as direct, indirect or fortuitous. The MMR is defined as the number of direct and indirect maternal deaths per 100 000 live births up to 42 days after the termination of pregnancy. A single underlying cause or mode of death was assigned to each case by the members of the MMC. The underlying cause of death is the disease or injury which results directly in death or initiates the chain of events leading directly to death. The mode of death is the disease or injury that ends life directly. Late maternal death was defined as the death of a woman from direct or indirect obstetric causes more than 42 days but 42 days) Duration of pregnancy (week) 37 Deliveries Mode of delivery Vaginal birth Spontaneous Caesarean section Home birth Death at home Antepartum Within 6 weeks postpartum After 6 weeks postpartum Death in nonwhite immigrants Preterm delivery Autopsy performed Admission to intensive care unit Perinatal mortality Fetal death 24 weeks of gestation

n (%)

151 136 2 173 131 22 20 68 221 96 35 67 23

General population* (%)

(52) (47) (1) (60) (76) (13) (12) (24) (76) (43) (16) (30) (10)

37 (13)

79.5 20.5

0.4 (20–24 weeks) 0.4 1.8 5.2 91.1

18 62 51 121 212

(6) (21) (18) (42) (73)

108 84 104 9 33 16 13 4 82 113 117 183 121 36

(51) (40) (49) (4) (11) (48) (39) (12) (28) (39) (40) (63) (42) (12)

84.8 74.9 15.1 23.2

86 (30)

1.1

14.6** 9.5

*Data from Perinatal Registration, the Netherlands.25 **Deliveries in nonwhite immigrants.


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Caesarean section had been performed in 49% of the women who died. Caesarean section in this study was often performed in haemodynamically nonstabilised women, because of maternal or fetal compromise. In four women, a complication of caesarean section was the only cause of maternal death. All of these caesarean sections were urgent procedures during labour. Three women had severe haemorrhage after the procedure, two caused by haemorrhage from an artery or vein. In one woman, haemorrhage during the procedure resulted in disseminated intravascular coagulopathy. There were 22 maternal deaths in twin pregnancies, seven of which occurred after in vitro fertilisation and one after ovulation induction. Ten pregnancies in total occurred after in vitro fertilisation. Substandard care was identified in 158 of all 289 cases (55%): the classification is given in Table 8. Most substandard care was identified in direct cases (63%), especially in those with mortality caused by pre-eclampsia (91%). Other characteristics are given in Table 9.

Discussion Maternal mortality in the Netherlands has shown an increase compared with the period 1983–1992. This is a matter for concern. The rise in maternal mortality may be caused partly by better reporting to the MMC. The percentage of cases not reported to the MMC is still significant, although it has improved compared with the period 1983–1992, in which 80% of cases were available for complete analysis. There is a remarkable difference in underreporting between direct (17%) and indirect (3%) cases. The underreporting to Statistics Netherlands did not improve over time: it was 26% in 1983–1992 and 33% in 1993–2005. Vital statistics reported by Statistics Netherlands are used for international comparison, but are not sufficiently accurate.12 In the Confidential Enquiry into Maternal Deaths in the UK in 2000– 2002, all but two cases were completely available for coding according to type, from a total of 391 deaths. Comparison of the death register with the birth register from Statistics Netherlands has now become possible in the Netherlands and, hopefully, we will have a higher percentage available for analysis in the next period. The methods used in the enquiry, however, remain unchanged, and it seems unlikely that the increase is caused by registration or classification bias. Furthermore, the same trend was seen in the UK.2 Both enquiries are audits on a nationwide level using the same definitions. The pregnancy-related mortality surveillance in the USA has also shown a rise in maternal mortality since 1982, with a mortality ratio of 13.2 in 1999.13 Demographic changes could partly explain this increase. The risk of death is influenced by both age and parity. In the

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general population, the percentage of mothers aged ‡35 years at delivery increased from 5.2% in 1980 to 20% in 2003 in the Netherlands.14 The mean total number of children (1.8) for each woman remained virtually unchanged in this period, and thus parity is less influential. Maternal age at birth was shown to be an important risk factor for all causes. In the first enquiry in the period 1983–1992, no maternal mortality was seen in women above 45 years, whereas three women in this age group died in the subsequent study period (MMR 115.5, OR 10.7, 95% CI 3.6–31.9). A higher maternal age may be associated with an increase in the need for assisted reproductive techniques. In vitro fertilisation is associated with a higher maternal mortality in Australia (MMR 25.7 versus MMR 10.9 in the general population).15 The increase in maternal deaths from cardiovascular disease is similar to the findings in the UK and may be associated with the increase in obesity, chronic hypertension and maternal age in the Netherlands. The statistically significant decrease in maternal death caused by genital tract trauma, such as uterine rupture, seems unusual in the light of the increase in the percentage of caesarean sections. It may be that more primary caesarean sections were performed after a previous caesarean section, but it may also have resulted from earlier anticipation by obstetricians of impending uterine rupture. The rise in maternal death caused by acute fatty liver of pregnancy and amniotic fluid embolism may be attributable to improved awareness of these diseases by obstetricians. A high index of suspicion of these diseases leads to more diagnostic tests to confirm the diagnosis. In a cohort in the UK Obstetric Surveillance System, a relationship was found between twin pregnancy and acute fatty liver of pregnancy (18%).16 We found a comparable percentage (one in six cases, 17%), but our numbers were too small to draw firm conclusions. The MMR of sub-Saharan African and Asian women was more than three times that of the native Dutch group. In contrast with our first enquiry, MMRs of Moroccan and Turkish women were similar to the MMRs of indigenous women. Twenty percent of all births in the Netherlands are in immigrant populations today, whose fertility rate is 40% higher than that of the native Dutch population.14 In our study, 29% of the women who died were immigrants, and substandard care was found to be more frequent in immigrant women. In one of ten cases, communication difficulties were mentioned in medical files, and this probably is an underestimation. The fact that MMRs in women from Morocco and Turkey were similar to those of native Dutch women could be interpreted as a result of increased health literacy within a multicultural context, as these groups have been in the Netherlands for a relatively long time. Changes in care could have contributed to the rise in maternal mortality. The percentage of caesarean sections in


Rise in maternal mortality in the Netherlands

the Netherlands increased in the study period from 8.1% to 13.6%.17 In only four cases did caesarean section contribute directly to death but, in unstable women, it can influence the chain of events leading to death. Differences in the quality of care could explain some of the changes in MMR. Substandard care, however, decreased from 78% of all direct cases in the period 1983–1992 to 63% in the period 1993–2005. In contrast, substandard care in pre-eclampsia did not show such a decline (93% versus 91%). Pre-eclampsia is the leading cause of maternal mortality in the Netherlands, showing a rising trend in the period 1983–2005 (OR 1.3, 95% CI 0.9–1.9). The MMR for gestational hypertensive disorders is markedly higher than in the UK (MMR 3.5 versus 0.9).2 Substandard care in the UK for hypertensive diseases was 72% in the period 2003–2005, in which 44% major substandard care was involved.2 In previous reports of the Confidential Enquiry into Maternal and Child Health, hypertensive diseases were also ranked higher in the UK. Specific recommendations were subsequently given, especially for better monitoring of blood pressure and control of fluid balance. This advice possibly contributed to the decline in maternal deaths caused by hypertensive diseases. Most substandard care in maternal mortality caused by hypertensive disease in pregnancy in the Netherlands concerned insufficient diagnostic testing where indicated, inadequate management of hypertension by obstetricians, no use or inadequate use of magnesium sulphate, inadequate stabilisation before transport to tertiary care centres and/or delivery and failure to consider timely delivery.18 In addition, fluid overload in women with pre-eclampsia dying as a result of adult respiratory distress syndrome is of serious concern. In the UK, the advice to limit the administration of intravenous fluids in women with pre-eclampsia led to a decline of mortality caused by adult respiratory distress syndrome in preeclampsia.2 All women who were eligible for thromboprophylaxis according to the Dutch guideline received this.10 In the UK, most direct deaths are caused by thromboembolism (MMR 1.94). This is slightly higher than the Dutch MMR (1.6), whereas the UK has a higher caesarean section rate (23% versus 15.1%). The number of deaths caused by postpartum embolism after caesarean section decreased over the years in the UK, probably as a result of increasing vigilance and better application of thromboprophylaxis protocols. Current guidelines in the UK advise that doses of low-molecular-weight heparin should be adjusted to the woman’s weight.2 This is also advised in the Dutch guideline, but not strongly. With the increasing number of morbid obese women, this may also be a factor in the smaller number of deaths caused by thromboembolism in the Netherlands. Obese women should be aware of the risks of

obesity, preferably before conception, and should be educated about the danger signs. Risk assessment for thromboembolism should be undertaken for every pregnant woman. In contrast with the UK, where suicide was the leading cause of maternal deaths when late deaths were included in the period 2000–2002, only nine cases of maternal death from suicide were reported in the Netherlands.19–21 Cases of suicide are classified as indirect death if the pregnancy is thought to have influenced the psychiatric state of the woman. If such a connection cannot be found, the case is classified as fortuitous. There may be underreporting in the Netherlands, because often these women die more than 42 days after delivery and are no longer under the care of an obstetrician. In the period 2003–2005, the number of maternal deaths as a result of suicide declined in the UK, which may indicate that the recommendations to identify women most at risk and the application of appropriate management are having a preventative effect. We recommend that women at increased risk for complications during pregnancy, such as pre-eclampsia, thromboembolism and heart disease, should be recognised better through appropriate medical, obstetric and family history taking. When pre-existing risk factors are present, women should receive appropriate preconceptional advice and, when pregnant, should be seen more frequently than lowrisk pregnant women. If necessary, the woman should be referred to (university) hospital care. All pregnant women need to be educated about the danger signs associated with serious complications in pregnancy. Hopefully, this will lead to a decrease in the high percentage of delay in diagnosis. Special efforts should be directed towards nonwestern immigrant populations, especially sub-Saharan African women, because they face the highest risks.22 However, life-threatening complications are often unanticipated and occur suddenly. The rise in maternal deaths from hypertensive diseases and amniotic fluid embolism suggests that there is room for improvement in handling such emergencies in the Netherlands. There is evidence that simulation training programmes improve skills and thus reduce complications in emergency situations.23,24 Such programmes should also be incorporated in the education of obstetricians and midwives. In conclusion, the significant rise in maternal mortality and, especially, mortality from hypertensive diseases, as well as the high prevalence of substandard care involved in these cases, should lead to serious concern. Changing this situation must be a top priority for Dutch obstetrics.

Disclosure of interest There are no conflicts of interest.


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Contribution to authorship All authors contributed to the conception and design and/ or acquisition of data and the analysis of data. All authors contributed to the drafting or revising of the article and all approved of the final version to be published.

Details of ethics approval For this study, no ethics approval was needed, as it is a retrospective study of maternal mortality.

Funding No funding. j

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