Stillbirth in term and late term gestations in Stockholm during a 20-year period, incidence and causes.

INTRODUCTION: The incidence of stillbirth has decreased marginally or remained stable during the past decades in high income countries. A recent report has shown Stockholm to have a lower incidence of stillbirth at term than other parts of Sweden. The risk of antepartum stillbirth increases in late term and postterm pregnancies which is one of the factors contributing to the current discussion regarding the optimal time of induction of labor due to postterm pregnancy.
MATERIAL AND METHODS: This is a cohort study based on the Stockholm Stillbirth Database which contains all cases of stillbirth from 1998-2018 in Stockholm County. All cases were reviewed systematically and the cause of death was evaluated according to the Stockholm Stillbirth Classification. Stillbirths diagnosed between gestational week (GW) 37+0 and 40+6 n = 605 were compared to stillbirths diagnosed from GW 41+0 and onwards n = 157, according to the cause of stillbirth and pregnancy and maternal characteristics. The aim was to evaluate the incidence of stillbirth over time and the incidence of stillbirth diagnosed from GW 41+0.
RESULTS: In Stockholm County the overall incidence of stillbirth has decreased from 4.6/1000 births during the period 1998-2004 to 3.4/1000 births during the period 2014-2018, p-value <0.001. When comparing the same time periods, the incidence of stillbirth diagnosed from GW 41+0 and onwards has decreased from 0.5/1000 births to 0.15/1000 births, p-value <0.001. Among women still pregnant at GW 41+0 the incidence of stillbirth has decreased from 1.8/ 1000 to 0.5/ 1000. When comparing stillbirths diagnosed at GW 37+0-40+6 with stillbirths diagnosed from GW 41+0 and onwards infection was a more common cause of stillbirth in the latter group.
CONCLUSION: In Stockholm County there was a decreasing incidence of stillbirth overall and in stillbirths diagnosed from 41+0 weeks of gestation and onwards during the period 1998-2018. In stillbirths diagnosed from GW 41+0 and onwards infection was a more common cause of death compared to stillbirths diagnosed between GW 37+0 and 40+6.

Introduction

Approximately 2.6 million fetuses are stillborn every year [1]. Globally, the incidence of stillbirth is most prominent in low income parts of the world. However, stillbirth is also a public health problem in high income countries [1] and there has only been a marginal decrease during the past decades [2]. The incidence of neonatal death is decreasing faster than the incidence of stillbirth [1, 3] hence, stillbirth is the main contributor to perinatal death in high income countries [3]. In Sweden the incidence has been quite stable during the last 20 years, about 3-/1000 births, however according to a report from the National Board of Health and Welfare, stillbirth incidence differed significantly between regions in Sweden and pregnant women in Stockholm County had a lower risk compared to the rest of the country especially at term [3].

Approximately 20 percent of pregnant women have not gone into spontaneous labor at gestational week (GW) 41+0 [4]. In Sweden, postterm pregnancy is defined as a gestational age of ≥ 42+0 weeks. The frequency of women still pregnant at GW 42+0 was in 2018 approximately 9% among nulliparous and 5% among multiparous [5]. The risk of stillbirth increases in late term and postterm pregnancies [6]. Due to reports of increased risk of stillbirth in late term (GW 41+0-41+6) and postterm (GW ≥ 42+0) pregnancies the recommendations of surveillance of pregnancies and time of induction has changed in Stockholm County. In 2005 the recommended date for induction due to postterm pregnancy was changed from GW 43+0 to 42+0 in all delivery units in Stockholm County [7]. In 2014 the surveillance from GW 41+0 was standardized and extended at all delivery units [8].

A recent study comparing induction of labor at GW 41+0 to expectance and induction latest at GW 42+0 showed a lower risk of stillbirth in the former group [9]. These results and varying management policies between countries regarding postterm pregnancies have actualized the discussion regarding the optimal time of induction of labor due to prolonged pregnancy.

Fetal abnormalities, placental insufficiency, fetal growth restriction and infections are all common causes of stillbirth as is placental abruptio and umbilical cord complications [10, 11]. Main causes of stillbirth vary with gestational age [10, 12]. Pregnancies allowed to pass gestational week 41+0 are in general without risk factors and without known pregnancy complications.

The aim of this study was to investigate if the incidence of stillbirth diagnosed from 41 completed weeks and onwards as well as the overall incidence of stillbirth has changed over the past two decades in Stockholm County. And in addition, to investigate the specific causes of stillbirth among stillbirths diagnosed from GW 41+0 compared to stillbirths diagnosed between GW 37+0 and 40+6.

Material and methods

This is a cohort study based on the Stockholm Stillbirth Database. The Stockholm Stillbirth Database contains all stillbirths in Stockholm County 1998-2015. Since 2016, stillbirth cases are instead included in the Swedish Pregnancy Register, a certified national pregnancy register. Maternal characteristics, pregnancy complications, laboratory and microbiology findings, placental pathology, chromosomal analyses and fetal autopsy has been collected prospectively for each case All variates were collected in the same way over the whole time period although since 2016 saved in the Swedish Pregnancy Register. Each case was systematically reviewed by the Stockholm Stillbirth Group, consisting of obstetricians from all delivery units in Stockholm County and a senior perinatal pathologist. The cause of stillbirth was determined according to the Stockholm Stillbirth Classification [13] used since 2002. This classification defines seventeen different causes of stillbirth with clear definitions of necessary parameters for inclusion for each defined cause, Table 1. The primary and secondary cause of death as well as the degree of certainty of the cause according to classification criteria was decided by consensus during regular audits in the Stockholm Stillbirth Group [13]. The Stockholm Stillbirth Group has meeting for audit discussion approximately five times a year.

Table 1

Classification of stillbirth according to the Stockholm Stillbirth Classification.

Cause of stillbirth
Malformations and chromosomal abnormalities
Infection
Immunization
Feto-maternal transfusion
Twin-to-twin transfusion syndrome
Birth asphyxia
Intrauterine growth restriction/placental insufficiency
Umbilical cord complication
Placental abruptio
Preeclampsia
Diabetes mellitus
Intrahepatic cholestasis of pregnancy
Uterine complication
Coagulation disorders
Other causes related to stillbirth
Unknown
Unexplained

Cause of stillbirth according to the Stockholm Stillbirth Classification.

All singleton cases of stillbirth diagnosed at GW 37+0 or later were included in this study. Stillbirths diagnosed between GW 37+0 and 40+6 were compared with stillbirths diagnosed from GW 41+0 and onwards. Pregnancy and maternal characteristics have been prospectively gathered from antenatal records for all cases. Stillbirth was defined as fetal death from GW 22+0 according to the WHO and International Classification of Diseases (ICD-10) definition [14]. In Sweden the definition of stillbirth changed from fetal death from GW 28+0 to fetal death from GW 22+0 in 2008, but the Stockholm Stillbirth Group has been using the WHO and ICD-10 definition since 1998.

Gestational age was based on the routine screening ultrasound at GW 18-20. From 2015 gestational age was based on ultrasound in GW 11+0-13+6 if the woman had an ultrasound for nuchal translucency and biparietal diameter was over 21 mm. Body mass index was based on self-reported height and measured weight at the first antenatal visit during first trimester. Parity was handled as a categorical variable, nulliparous yes/no. Maternal age was handled as a continuous variable. Maternal country of birth was divided in six different regions of the world, i.e. Sweden, Europe/Australia/USA, Middle East, Asia, South America and Africa South of Sahara. All variables were collected from the antenatal medical records or the records from the delivery ward.

In 2005 the recommended time for induction due to postterm pregnancy was changed from GW 43+0 to 42+0 in all delivery units in Stockholm County. In 2014 the surveillance from GW 41+0 changed in Stockholm [8] and all women were opted for an ultrasound at GW 41+0 with the aim to identify fetuses small for gestational age and to detect oligohydramnios. Amniotic fluid was measured as single deepest pocket, > 20 mm was considered normal [15]. The fetal abdominal diameter was measured and was considered normal if ≥110 mm. When the abdominal diameter was < 110 mm fetal weight was estimated [16]. Women with fetuses with estimated weight ≤ 10th percentile were treated according to local guidelines with assessment of pulsatility index in the umbilical cord and the uterine arteries. Women with fetuses with estimated weight <- 2 standard deviations according to gestational age [17] or with abnormal Doppler findings were treated according to local guidelines and induction of labor was considered. The time periods 1998-2004, 2005-2013 and 2014-2018 were compared because of the change in recommendations in 2005 and 2014, mentioned above.

Statistics

Frequencies of maternal and pregnancy characteristics were compared between stillbirths diagnosed between GW 37+0 and 40+6 and stillbirths diagnosed from GW 41+0 and onwards. Maternal and pregnancy variates measured on a continuous scale were presented as means and standard deviations (SD) and categorical variates as numbers and proportions. Comparisons between the continuous variates were done with Wilcoxon ranksum test and with chi-square test for the categorical variates, comparing proportions.

The number of stillbirths diagnosed from GW 41+0 and onwards were counted per year of birth and in addition as a proportion of births per year.

The proportions of different causes of stillbirth and the degree of certainty according to the Stockholm Stillbirth Classification [13] were compared between stillbirths diagnosed between GW 37+0 and 40+6 and stillbirths diagnosed from GW 41+0 and onwards, with chi-square test.

The total incidence of stillbirth in Stockholm County was calculated as well as the incidence of stillbirths diagnosed from GW 41+0 and onwards. The total incidence of stillbirth as well as the incidence of stillbirth from GW 41+0 were compared between three chosen time periods (1998-2004, 2005-2013 and 2014-2018), with chi-square test, testing the difference in proportions between these three time periods. The incidence of stillbirth from GW 41+0 per 1000 women still pregnant at GW 41+0 was also compared between the same time periods. These time periods were chosen because time of induction due to prolonged pregnancy was changed in 2005 and surveillance from GW 41+0 were standardized and changed from 2014. All statistical analyses were done using R cran.

Ethical approval for this study was obtained from the Regional Research Ethics Committee at Karolinska Institute in Stockholm, Sweden Dnr 2020-01855. Data were fully anonymized before access. The Ethics Committee did not require written informed consent. The Ethics Committee prohibit data to be publicly available. However, data will be shared after an approval from the Regional Research Ethics Committee.

Results

The total number of births in the County has increased from 18 689 in 1998 to 28 672 in 2018. The number of women giving birth at GW 41+0 or later has increased from 4992 in year 1998 to 7015 in year 2018. During the period there were 605 singleton stillbirths diagnosed between GW 37+0 and 40+6 and 157 singleton stillbirths diagnosed from GW 41+0 and onwards. Maternal and fetal characteristics for these term stillbirths are described in Table 2. There was a significant higher proportion of nullipara among stillbirths diagnosed from GW 41+0 compared to stillbirths diagnosed between GW 37+0 and 40+6, Table 2. However, this difference was not significant when analyzing the time periods separately, S1A–S1C Table and it was not significant when the proportion of nullipara women still pregnant at GW 41+0 was taken into account.

Table 2

Maternal and fetal characteristics comparing term stillbirths at GW 37+0-40+6 with term stillbirths at GW 41+0 and onwards.

Maternal and fetal characteristics	Term Stillbirth before GW 41+0 n = 605	Stillbirth from GW 41+0 n = 157	P-value
Maternal age, years	31.81 (SD 5.22)	32.14 (SD 5.14)	0.478
Maternal age >35 (n, %)	181 (29.92%)	58 (36.94%)	0.111
BMI, kg/m2	25.21 (SD 4.83)	25.54 (SD 5.1)	0.491
Nullipara (n, %)	217 (41.57%)	73 (51.77%)	0.038
Born in Sweden (n, %)	255 (61.74%)	65 (61.9%)	1
Born in Africa (n, %)	27 (6.54%)	13 (12.38%)	0.072
Born in Middel East (n, %)	65 (15.74%)	13 (12.38%)	0.48
Born in South America (n, %)	4 (0.97%)	3 (2.86%)	0.306
Born in Asia (n, %)	23 (5.57%)	4 (3.81%)	0.632
Born in Euroupe/USA/Australia (n, %)	24 (5.81%)	5 (4.76%)	0.857
Smoking (n, %)	23 (4.57%)	4 (2.78%)	0.476
Assisted conseption (n, %)	21 (3.48%)	5 (3.18%)	1
Birthweight ≤10e percentilen (n, %)	180 (30.35%)	51 (32.9%)	0.607
Birthweight <-2 SD (n, %)	100 (16.86%)	26 (16.77%)	1

Stillbirths from 1998-2018, diagnosed GW 37+0-40+6 compared to stillbirths diagnosed from GW 41+0. BMI: body mass index; SGA: small for gestational age; LGA large for gestational age. Data are presented as mean and standard deviation (SD) or n (%).

The total incidence of stillbirth in the Stockholm County was 4.6/1000 births between 1998 and 2004, 3.9/1000 births between 2005 and 2013 and 3.4/1000 births between 2014 and 2018. The incidence changed significantly, p-value < 0.001 (Fig 1). The number of stillbirths diagnosed from GW 41+0 and onwards per year has decreased during the two past decades (Figs 1 and 2). Between 1998 and 2004 the incidence was 0.5/1000 births, between 2005 and 2013 0.3/1000 births and between 2014 and 2018 0.15/1000 births, p-value < 0.001 (Fig 2). The incidence of stillbirth from GW 41+0 has also significantly decreased between the three time periods when only including women still pregnant at GW 41+0 (1.8/1000, 1.1/1000 and 0.5/1000 respectively, p-value <0.001, Fig 2).

Fig 1

Total incidence of stillbirth in Stockholm county (violet).

Incidence of stillbirth in Sweden (black). Incidence of stillbirth among women still pregnant at GW 41+0 number/1000 pregnancies (red) and incidence of stillbirth diagnosed from GW 41+0/ 1000 births (blue). The decreased incidences, violet, red and blue were all significant with p-value <0.001. The incidence of stillbirth in Stockholm County has decreased comparing three time periods (1998-2004, 2005-2013 and 2014-2018).

Fig 2

Number of stillbirth cases diagnosed from GW 41+0.

Incidences compared between three time periods (1998-2004, 2005-2013 and 2014-2018). Dark grey indicates cases in GW 41 and light grey indicates cases in GW 42.

Main causes of stillbirth are described in Table 3, comparing causes of stillbirth between GW 37+0 and 40+6 with those diagnosed from GW 41+0. There was a significant higher proportion of infections as the cause of stillbirth diagnosed from GW 41+0 and onwards compared to those diagnosed between GW 37+0 and GW 40+6. This difference was significant during the first two time periods however, not significant during the last time period (S2A–S2C Table).

Table 3

Main cause of stillbirth according to the Stockholm Stillbirth Classification comparing term stillbirths at GW 37+0 -40+6 with term stillbirths at GW 41+0 and onwards.

Main Cause of Stillbirth	Term Stillbirth before GW 41+0 n = 605	Stillbirth from GW 41+0 n = 157	P-value
Malformation/chromosomal abnormalities (n, %)	45 (7.77%)	7 (4.6%)	0.226
Infection (n, %)	122 (21.07%)	65 (42.2%)	<0.001
Feto-maternal transfusion (n, %)	20 (3.45%)	1 (0.7%)	0.113
Placental insufficiency/IUGR (n, %)	169 (29.19%)	39 (25.3%)	0.398
Umbilical cord complications (n, %)	55 (9.5%)	7 (4.6%)	0.072
Placental abruptio (n, %)	43 (7.43%)	7 (4.6%)	0.28
Preeclampsia (n, %)	8 (1.38%)	2 (1.3%)	1
Diabetes mellitus (n, %)	11 (1.9%)	1 (0.7%)	0.466
Intrahepatic cholestasis (n, %)	4 (0.69%)	0 (0%)	0.675
Coagulation disorder (n, %)	1 (0.17%)	2 (1.3%)	0.217
Other causes related to stillbirth (n, %)	12 (2.07%)	3 (2.0%)	1
Cause of stillbirth un-known (n, %)	80 (13.82%)	18 (11.7%)	0.578

Cause of stillbirth among stillbirths diagnosed GW 37+0-40+6 compared to stillbirths diagnosed from GW 41+0 from 1998-2018. Data are presented as n (%).

During the whole period there was an increased proportion of infants small for gestational age among all term stillbirths (Table 2), also when analyzing the time periods separately there was an increased proportion of small for gestational age fetuses (S1A–S1C Table). Four fetuses small for gestational age, defined as < -2 standard deviations, were stillborn between 2014 and 2018 (S1C Table). Two of them would not have been helped by induction at GW41+0 (one had a known lethal fetal abnormality; one was found dead at the opted ultrasound at 41+0 GW).

Discussion

The incidence of stillbirth diagnosed from GW 41+0 and onwards has decreased from 0.5 to 0.15 /1000 births in Stockholm County between 1998 and 2018. Among women still pregnant at GW 41+0 the incidence of stillbirth has decreased from 1.8/1000 pregnancies to 0.5/1000 pregnancies. The total incidence of stillbirths from GW 22+0 in Stockholm County during the same time period has also decreased. However the incidence of stillbirth in all of Sweden has remained unchanged during this time period [3, 18]. Among stillbirths diagnosed from GW 41+0 and onwards there was an increased proportion of nullipara. However, comparing the proportion of nulliparas still pregnant at GW 41+0 and the proportion of nulliparas with stillbirth diagnosed from GW 41+0 the difference was not significant. There was an increased proportion of stillbirths caused by infections among those diagnosed from GW 41+0 compared to those diagnosed between GW 37+0 and 40+6. The altered surveillance policy of post term pregnancies after 2014 has not altered the proportion of small for gestational age infants among stillbirths compared to the period 1998-2013. Table 2 and S1A–S1C Table.

The strength of the present study is the large number of consecutive stillbirths over the period. All cases in the Stockholm County are included, scrutinized and diagnosed according to the same investigation protocol and classification. There are no cases of late abortions among the stillbirth cases. The limitation of the present study includes the observational design with its difficulties to pinpoint reasons behind the decreasing incidence of stillbirths diagnosed from GW 41+0 as well as reasons behind the overall decreased incidence of stillbirths in Stockholm County.

The decreasing incidence of stillbirth diagnosed from GW ≥ 41+0 may be a result of changes in policy. In 2005 the time of induction of labor due to postterm pregnancy was changed from GW 43+0 to 42+0 in the County. Neonatal mortality and morbidity decreased in Stockholm County when comparing the periods 2000-2004 and 2005-2007 [7]. In 2014 an additional ultrasound scan at GW 41+0 was introduced in all delivery units in Stockholm County with the aim to identify small for gestational age fetuses and detect oligohydramnios giving the possibility to induce labor because of these ominous signs [8]. However, the proportion of stillborn fetuses with birth weight <-2 standard deviations did not significantly change when comparing stillbirths before 2014 and stillbirths between 2014 and 2018. This is in line with results from a large randomized study showing that repeated ultrasound examinations during the third trimester resulted in a slightly increased proportion of known SGA fetuses at birth without any difference in neonatal outcome [19].

The incidence of stillbirth varies between European countries and there is a slightly decreasing trend at all gestational ages in Europe. This could suggest multifactorial causes behind the decrease [20]. Probably that is the case even in Stockholm County. The decreased incidence of stillbirths diagnosed ≥ 41+0 may be caused by changes in policy as described above together with causes affecting the overall stillbirth incidence. General obstetric care has evolved which could also affect the incidence [20]. Prenatal screening possibilities have evolved with a larger possibility to find fetal anomalies earlier in pregnancy leading to the possibility to terminate pregnancies at an earlier stage [21]. Doppler ultrasound has given possibility to surveil high-risk pregnancies more intricately. Third trimester ultrasound may have the possibility to identify a larger proportion of small for gestational age fetuses [19, 22, 23]. However, a third trimester ultrasound in a low risk population has not been shown to affect outcome for the infants [19, 22, 23]. Guidelines for the diagnosis and definition of gestational diabetes as well as preeclampsia and the recommended time of induction of labor due to preeclampsia have changed during the period [24-26]. During the past two decades the obstetric population has also changed which could affect the incidence of stillbirth. The prevalence of smoking during pregnancy has decreased [27], the prevalence of obesity has increased [18, 28] as well as maternal age [18]. Foreign-born women, especially those born in sub-Saharan Africa and the Middle East, are overrepresented in the group of women affected by stillbirth [29], Sweden has had an increasing group of women born outside Europe. During the first time period there was a very high proportion of women with unknown country of origin. The proportion of women with unknown country of origin is substantial also during the two later time periods, however much lower than during the first time period. Hence, un-known country of origin is not a substantial explanation of the decreasing number of women with stillbirth born in Sweden comparing the two later time periods. Changes in the obstetric population could affect the incidence of stillbirth.

There was an increased incidence of infection as primary cause of stillbirth among stillbirths diagnosed from GW 41+0. A histological diagnosis of chorioamnionitis is more common in term pregnancies than preterm pregnancies [30]. However, to be able to classify infection as a definite or probable cause of stillbirth, additional findings are needed according to the Stockholm Stillbirth Classification [13] such as vasculitis in the placenta or umbilical cord or funicitis or positive cultures from amnion fluid or fetal or maternal blood. To what degree the histological signs of chorioamnionitis are merely signs of infection with potential to harm the fetus or signs of inflammation associated with the delivery or the late GW in general is still unclear.

A decreasing incidence of stillbirth is observed in Stockholm County. However, to what degree induction of labor at GW 41+0 will contribute to the continuing declining incidence still is open for debate. Probably the answer is more complex, and induction of labor at an earlier gestational age will not solely solve the problem. Other parameters as body mass index, maternal country of birth, educational level and other socioeconomic factors are risk factors but the mechanisms behind these associations are largely unknown. More knowledge is still needed to make surveillance more focused on relevant risk factors.

Conclusion

There is a decreasing incidence of stillbirths diagnosed from GW 41+0 onwards in Stockholm County during the period 1998-2018. There is in addition, an overall decreasing incidence of stillbirths in Stockholm County during the same period. Infection was more common as a cause of death among stillbirths diagnosed from GW 41+0.

Due to the study design the underlying causes behind this decreasing incidence of stillbirth cannot be clearly identified in this study. The prevalence of risk factors in the pregnant population have changed over time and so has monitoring and mode of treatment. Further studies are needed to identify causes behind the reduced numbers of stillbirths.

a. Maternal and fetal characteristics comparing term stillbirths at GW 37+0-40+6 with term stillbirths at GW 41+0 and onwards between 1998-2004. b. Maternal and fetal characteristics comparing term stillbirths at GW 37+0-40+6 with term stillbirths at GW 41+0 and onwards between 2005-2013. c. Maternal and fetal characteristics comparing term stillbirths at GW 37+0-40+6 with term stillbirths at GW 41+0 and onwards between 2014-2018.

(DOCX)

Click here for additional data file.

a. Main cause of stillbirth according to the Stockholm Stillbirth Classification comparing term stillbirths at GW 37+0 -40+6 with term stillbirths at GW 41+0 and onwards between 1998-2004. b. Main cause of stillbirth according to the Stockholm Stillbirth Classification comparing term stillbirths at GW 37+0 -40+6 with term stillbirths at GW 41+0 and onwards between 2005-2013. c. Main cause of stillbirth according to the Stockholm Stillbirth Classification comparing term stillbirths at GW 37+0 -40+6 with term stillbirths at GW 41+0 and onwards between 2014-2018.

(DOCX)

Click here for additional data file.

3 Mar 2021

PONE-D-21-01718

Stillbirth in Stockholm during a 20-year period, incidence and causes with focus on term and late term gestations

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Reviewer #1: The topic is very interesting and it is quite orginal to focus on late stillbirth.

The manuscript is exclusively discribing late stillbirth so the title is ambiguous according to me, I would have chosen "Stillbirth in term or late gestation in Stockholm during a 20-year period..."

Discribing causes of stillbirth according to the gestational age gives relevant informations. But the comparison of maternal caracteristics between pregnancies before and after 41WG is obvioulsy related to the factors associated to late pregnancies such as primiparity. The authors discuss the fact that ultrasound performed at 41WG did not lead to reduce the rate of stillbirth due to SGA, though the performance of late ultrasound should here be discussed.

Comparison of very small group of patients in tables 2a and 3a can not be conclusive (n=22).

figure 2 why did the authors excluded late stillbirth while that is the subject of the mansucript, why not showing the rate /1000 birth of late stillbirth?

Reviewer #2: This paper from Stockholm Stillbirth Database reports stillbirth from the Stockholm county between 1998 and 2018. Not many countries have access to this kind of data.

Although purely descriptive as mentioned by authors in the discussion, and honestly not including very new data, this paper is arriving at the right time.

Since the publication of Grobman et al. study (Grobman WA, Rice MM, Reddy UM, Tita ATN, Silver RM, Mallett G, Hill K, Thom EA, El-Sayed YY, Perez-Delboy A, Rouse DJ, Saade GR, Boggess KA, Chauhan SP, Iams JD, Chien EK, Casey BM, Gibbs RS, Srinivas SK, Swamy GK, Simhan HN, Macones GA; Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal–Fetal Medicine Units Network. Labor Induction versus Expectant Management in Low-Risk Nulliparous Women. N Engl J Med. 2018;379(6):513-523) some teams around the world are thinking of inducing women at 39 weeks.

I would recommend to authors to try to analyze their data in order to look at data before and after 39 weeks.

I also would retrieve the cases with fetal malformations, TTS and immunization as independent factors and not considered as low risk pregnancies

Reviewer #3: I would like to thank the authors for this article, which studies the incidence of term and later stillbirths on a large period ( 1998-2018) in Stockholm County. The authors divided this period in three unequal laps of time ( 1998-200,/2005-2013, 2014-2018) due to changes in the management of late term pregnancies. More, the authors provided information on this etiology of each stillbirths.

However, it is difficult to have a correct overview of how the changes in the management of late term/ prolonged pregnancy have influenced the rate of stillbirths in this population?

Although the different curves are enough to understand the decrease in the incidence of stillbirths, Comparison groups were inadequate to understand if the population with stillbirths was also associated with different characteristics.

That being said, even though the overall is well written, there are sections that would benefit from rewriting, as the authors tend to lose sight of their objectives.

Here are some remarks I would like to share with the authors:

For the abstract:

The authors should state more clearly the objective of the study. ( to evaluate the incidence…)

The term of primipara should be avoided and nulliparous should be preferred. This modification should be done all along the manuscript.

Introduction :

There is a mistake in the incidence reported of stillbirths?. (wrong reference?)Reference 3 not available.

The third paragraph dealing with the etiologies of stillbirth is too long, and some sentences are inappropriate with the subject (etiologies of preterm births). The authors should focus on the etiologies of stillbirths in term and late-term pregnancies.

Material and methods :

The authors referred to two registers: one is the Stockholm Stillbirth database and the second one the Swedish Pregnancy Register. Did these two registers collected the same data? How the variables were recorded?

During this period of 20 years, was the cause of stillbirths always determined by two physicians ? (obstetrician and a perinatal pathologist)

The Stockholm Stillbirth Classification should be more detailed: how was it validated? Is there a good agreement between physicians in the determination of one etiology of the stillbirth. What is the proportion of stillbirths which remain unexplained? This information is important to validate the results presented afterwards. Since when this classification was used? This should be discussed.

What was the audit? how often is it?

I am doubtful with the description of the group 37+0 -40+6 weeks? To my point of view, the authors evaluate how modifications of late term/ prolonged pregnancies have influenced the incidence of stillbirths in this population. Therefore, description of this latest group ( ≥41 +0 ) is enough. If no, it should be interesting to provide information on the overall incidence of stillbirths.

The dating of the beginning of the pregnancy seemed to be based on routine ultrasound at 18-20 weeks. Was it the case during all the study? What about the first trimester scan? This should be discussed, as we could imagine that a better determination of the beginning of the pregnancy would have allowed to decrease the probability of a real prolonged pregnancy?

Maternal age seemed to be unchanged when it is described with means. However, it would be appreciated if maternal age was handled also a categorial variable ( to see if the proportion of women aged more than≥35 or 40 years was modified.)

If there is no information on the country of patients who were born out of Sweden , this variable should be removed.

Can the authors quote the reference which say that oligoamnios was related to as single deepest pool ≤20 mm? Same for AD≤110mm?

Results:

Were there 6 maternity units during all the period? If no , please remove this sentence.

The results presented referred to the description of maternal characteristics in the overall population study (1998-2018) and those related to women of the last period (2014-2018). There is no description of maternal characteristics of the two previous groups?

How the infectious cause was retained? What were the elements which were requested to keep this etiology?

A comparison of maternal characteristics for each period of time would be more adequate, than comparison between stillbirths occurring before and after 41 weeks of gestation.

The primary result (incidence of stillbirth) should be presented before the causes of stillbirth.

Table 3 reports only 12 different causes of stillbirths, whereas the classification used described 17 causes (table 1). How many stillbirths were unexplained between the three periods?

Discussion :

The discussion is difficult to read, as the ideas follow without order or hamony.

Legend 2 : evolution of stillbirths in Sweden should be removed.

The discussion should be

.

Reviewer #4: Your article titled Stillbirth in Stockholm during a 20-year period, incidence and causes with focus on term and late term gestations is submitted for publication in Plos One. My first remark should encourage you to explain to the reader why Stockholm is a good place to study the future of stillbirths.

-1- Do you consider Stockholm's rates to be among the lowest in the world? Is the question of continuing a long-term gestation beyond 41 GW or of interrupting labor at the 41th GW a priority question that arises or will arise in all countries? In other words, does the situation in Sweden, and in particular Stockholm, serve as an example for other countries?

We want to believe it, but the increase in the average age of women at the birth of their children, the heavy smoking during pregnancy, and the fight against social discrimination are also priorities for the countries even among the richest of the planet?

It seems to me that you should indeed give more arguments because other very recent publications relate exactly to the same subject (PLOS medicine 2020) and we would like your article to be able to both distinguish itself from it and also demonstrate that the subject is important for other countries, see reference (* from the Euro-Peristat Project) for example, but you mentioned an earlier reference [20].

-2- You seem to think that your statistical measurements of both gestational age and the number of stillbirths have not been affected by errors, of course, but when we know the statistical difficulties in certain countries in distinguishing abortions for therapeutic causes from stillbirths, the international reader would like to have a sentence to be enlightened on this point.

You could argue that to avoid the statistical problem of termination of pregnancy, you chose to primarily study long-term pregnancy of 40 GW to 42+ because the effect of termination of pregnancy is large only at short gestation times. However, this should affect the statistical measure of Sweden's stillbirth rate at the standard 36 GW threshold and you could mention this point.

-3- Your article, like other similar articles, does not frankly conclude on the benefit of inducing late pregnancy and your discussion is very interesting. But one wonders what would you need to be able to conclude and not just say that the woman must be informed of the risks incurred in each two cases of either termination or continuation of the pregnancy. And it seems from what you write that you need more statistical power, and you wonder why you do expand to the entire Sweden, or even why you do not prefer to do individual participant data meta-analyzes as of other colleagues. One of your main reference concerns a paper published in January 2019 in BMJ, but a paper published in December 2020 in Plos medicine should be mentioned.

-4- It is difficult to get a figure related to the title of your article: 20 years period of stillbirth in Stockholm? Figure 2, should be the place but there is no definition of stillbirths (22GW, 37GW ?). Stagnation of Sweden a whole since 10 years is not discussed.

-5- An important point that you do not discuss concerns the high proportion of women born outside Sweden (48% table 2) and how it is related to stillbirth rate.

-6- How a relatively higher proportion of primiparus women (46%) and its rapid fall between 2010 and 2015 (43.1) [3 figure C9.2] at least will affect the results. The prevalence of smoking during pregnancy has decreased [28] seems to be true concerning Europe according to [3 Table R8.1] but discrepancies between countries are huge.

(*) Blondel B, Cuttini M, Hindori-Mohangoo AD, et al. How do late terminations of pregnancy affect comparisons of stillbirth rates in Europe? Analyses of aggregated routine data from the Euro-Peristat Project. BJOG. 2018;125(2):226-34. doi: 10.1111/1471-0528.14767.

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27 Apr 2021

Reviewer #1: The topic is very interesting and it is quite orginal to focus on late stillbirth.

The manuscript is exclusively discribing late stillbirth so the title is ambiguous according to me, I would have chosen "Stillbirth in term or late gestation in Stockholm during a 20-year period..."

Discribing causes of stillbirth according to the gestational age gives relevant informations. But the comparison of maternal caracteristics between pregnancies before and after 41WG is obvioulsy related to the factors associated to late pregnancies such as primiparity. The authors discuss the fact that ultrasound performed at 41WG did not lead to reduce the rate of stillbirth due to SGA, though the performance of late ultrasound should here be discussed.

We thank the reviewer for this comment. We have compared the proportion of nullipara still pregnant at gw 41+0 and the proportion of nullipara with sb from 41+0 and there is no significant difference. We have changed that throughout the manuscript. We agree that ultrasound examinations have limitations. In the discussion we have included: “This is in line with results from a large randomized study showing that repeated ultrasound examinations during the third trimester resulted in a slightly increased proportion of known SGA fetuses at birth without any difference in neonatal outcome [1]. “

Comparison of very small group of patients in tables 2a and 3a can not be conclusive (n=22).

We have put table 1a and 2a in supplementary material. We agree that there are few cases in that group.

figure 2 why did the authors excluded late stillbirth while that is the subject of the mansucript, why not showing the rate /1000 birth of late stillbirth?

We have included rate of stillbirth gw 41+0/1000 births and rate of stillbirth gw 41+0/1000 women still pregnancies still pregnant in that gestational week.

Reviewer #2: This paper from Stockholm Stillbirth Database reports stillbirth from the Stockholm county between 1998 and 2018. Not many countries have access to this kind of data.

Although purely descriptive as mentioned by authors in the discussion, and honestly not including very new data, this paper is arriving at the right time.

Since the publication of Grobman et al. study (Grobman WA, Rice MM, Reddy UM, Tita ATN, Silver RM, Mallett G, Hill K, Thom EA, El-Sayed YY, Perez-Delboy A, Rouse DJ, Saade GR, Boggess KA, Chauhan SP, Iams JD, Chien EK, Casey BM, Gibbs RS, Srinivas SK, Swamy GK, Simhan HN, Macones GA; Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal–Fetal Medicine Units Network. Labor Induction versus Expectant Management in Low-Risk Nulliparous Women. N Engl J Med. 2018;379(6):513-523) some teams around the world are thinking of inducing women at 39 weeks.

I would recommend to authors to try to analyze their data in order to look at data before and after 39 weeks.

We thank the reviewer for this comment, it is indeed an interesting question. However, it was not the scoop of this paper and this question will have to wait till another occasion.

I also would retrieve the cases with fetal malformations, TTS and immunization as independent factors and not considered as low risk pregnancies.

We are not sure about what the reviewer wants. There are some cases with malformations known or un-known. There are no cases caused by immunization since they occur in earlier gestational weeks. Twin pregnancies are excluded.

Reviewer #3: I would like to thank the authors for this article, which studies the incidence of term and later stillbirths on a large period ( 1998-2018) in Stockholm County. The authors divided this period in three unequal laps of time ( 1998-200,/2005-2013, 2014-2018) due to changes in the management of late term pregnancies. More, the authors provided information on this etiology of each stillbirths.

However, it is difficult to have a correct overview of how the changes in the management of late term/ prolonged pregnancy have influenced the rate of stillbirths in this population?

We thank the reviewer for this comment. We agree that it is not only difficult but in fact impossible to know how the changes in management have influences the stillbirth rate. It may be other differences, perhaps more general and probably multifactorial that have influenced the stillbirth rate. Since this is an observational study without the possibility to control for all other differences between the different time periods, we cannot answer why the rates have decreased. That is a limitation, however stillbirth is a rare outcome with methodological difficulties associated to that. One thing we can conclude is that the number of stillbirths has decreased as well as the proportion of stillbirth, however over all the years the proportion of stillborn SGA fetuses are the same over all time periods. We have managed to decrease the numbers however it seems we have not lowered the risk for the SGA fetuses.

Although the different curves are enough to understand the decrease in the incidence of stillbirths, Comparison groups were inadequate to understand if the population with stillbirths was also associated with different characteristics.

That being said, even though the overall is well written, there are sections that would benefit from rewriting, as the authors tend to lose sight of their objectives.

Here are some remarks I would like to share with the authors:

For the abstract:

The authors should state more clearly the objective of the study. ( to evaluate the incidence…) The term of primipara should be avoided and nulliparous should be preferred. This modification should be done all along the manuscript.

We thank the reviewer for these comments and have changed primipara to nulliparous. We have also made the objective clearer and now write:

“A recent report has shown Stockholm to have a lower incidence of stillbirth at term than most of the country”

Introduction :

There is a mistake in the incidence reported of stillbirths?. (wrong reference?)Reference 3 not available.

We thank the reviewer for this comment and have changed reference 3, we thank the reviewer for the comment on incidence, it was too many zeros, we have changed that.

The third paragraph dealing with the etiologies of stillbirth is too long, and some sentences are inappropriate with the subject (etiologies of preterm births). The authors should focus on the etiologies of stillbirths in term and late-term pregnancies.

We have rewritten paragraph 3 and we now write “A recent study comparing induction of labor at GW 41+0 to expectance and induction latest at GW 42+0 showed a lower risk of stillbirth in the former group [2]. These results and varying management policies between countries regarding postterm pregnancies have actualized the discussion regarding optimal time of induction of labor due to prolonged pregnancy. Fetal abnormalities, placental insufficiency, fetal growth restriction and infections are all common causes of stillbirth as is placental abruptio and umbilical cord complications [3, 4]. Main causes of stillbirth vary with gestational age [3, 5]. Pregnancies passing gestational week 41+0 are, in general, women without risk factors and without known pregnancy complications, hence to a large extent healthy women with healthy fetuses.”

Material and methods :

The authors referred to two registers: one is the Stockholm Stillbirth database and the second one the Swedish Pregnancy Register. Did these two registers collected the same data? How the variables were recorded?

We thank the reviewer for this comment. All variables used were the same and recorded in the same way for all years and for the two registers. We have made it more clear how variables were recorded.

During this period of 20 years, was the cause of stillbirths always determined by two physicians ? (obstetrician and a perinatal pathologist)

During the period of 20 years the cause of stillbirth was always determined by one perinatal pathologist and one obstetrician from each delivery ward in the county, a group of 7-10 persons, based on the classification, to secure that it was done the same way all the time. The perinatal pathologist and some of the obstetricians have been the same individuals for the whole time.

The Stockholm Stillbirth Classification should be more detailed: how was it validated? Is there a good agreement between physicians in the determination of one etiology of the stillbirth. What is the proportion of stillbirths which remain unexplained? This information is important to validate the results presented afterwards. Since when this classification was used? This should be discussed. What was the audit? how often is it?

We thank the reviewer for this comment. The Stockholm classification is used since 2002., Before 2002 we used a modified classification described by the Stockholm stillbirth group in: (Petersson K, Bremme K, Bottinga R, Hofsjö A, Hulthén-Varli I, Kublickas M, et al. Diagnostic evaluation of intrauterine et al death in Stockholm 1998-99. Acta Obstet Gynecol Scand. 2002;/81:/284-92)

The causes of stillbirth are the same in the Stockholm classification and the earlier used classification, even though the definitions of causes are more strictly defined in the Stockholm classification why it is unlikely to have any significant impact on the primary causes included in this study. The causes in the classification is based on facts from the post partal investigations and with clear information about how to judge every found sign of pathology. The classification is validated and showed a high degree of agreement (described in ref 16). We have added additional information in the methods section. There are audit meetings approximately 5 times a year. There are clear definitions of every cause of death and what is claimed for the certainty of the cause. The work and the group have been almost the same since 2002. There are between 12-13% cases which remain unexplained.

I am doubtful with the description of the group 37+0 -40+6 weeks? To my point of view, the authors evaluate how modifications of late term/ prolonged pregnancies have influenced the incidence of stillbirths in this population. Therefore, description of this latest group ( ≥41 +0 ) is enough. If no, it should be interesting to provide information on the overall incidence of stillbirths.

We are not completely sure that we understand what the reviewer wants. We think that it is valuable to compare the late term stillbirths with another group of stillbirths and we find full term stillbirths before GW 41+0 a valuable comparison group. The overall incidence of stillbirth is provided (from GW 22+0).

The dating of the beginning of the pregnancy seemed to be based on routine ultrasound at 18-20 weeks. Was it the case during all the study? What about the first trimester scan? This should be discussed, as we could imagine that a better determination of the beginning of the pregnancy would have allowed to decrease the probability of a real prolonged pregnancy?

We thank the reviewer for this comment. The dating was based on the routine ultrasound until 2014. From 2015 the dating was based on the first trimester ultrasound in GW 11-13 if the first trimester ultrasound was done and the biparietal diameter was >21mm. If biparietal diameter was <21 mm or if the first trimester ultrasound was not performed the dating was based on the routine ultrasound in GW 18-20. Information added in the methods section.

Maternal age seemed to be unchanged when it is described with means. However, it would be appreciated if maternal age was handled also a categorial variable ( to see if the proportion of women aged more than≥35 or 40 years was modified.)

We thank the reviewer for this comment. We have added information on proportions of women aged >35 and >40 years.

If there is no information on the country of patients who were born out of Sweden , this variable should be removed.

We have added more detailed information about region of maternal birth.

Can the authors quote the reference which say that oligoamnios was related to as single deepest pool ≤20 mm? Same for AD≤110mm?

We have added references.

Results:

Were there 6 maternity units during all the period? If no, please remove this sentence.

We have excluded that sentence. During a short time 140303 – 160531 there were 7 maternity units in Stockholm county.

The results presented referred to the description of maternal characteristics in the overall population study (1998-2018) and those related to women of the last period (2014-2018). There is no description of maternal characteristics of the two previous groups?

We have added tables comparing all time periods in supplementary material.

How the infectious cause was retained? What were the elements which were requested to keep this etiology?

We thank the reviewer for this comment. The diagnosis was set according to the Stockholm Stillbirth classification and for a definite diagnosis signs of fetal pneumonia or positive fetal heart blood or amnion culture and signs of placental infection was claimed. For a probable diagnosis placental signs of chorioamnionitis plus vasculitis or funicitis or signs of choriomnionitis in placenta together with clinical signs of chorioamnionitis or positive cultures.

A comparison of maternal characteristics for each period of time would be more adequate, than comparison between stillbirths occurring before and after 41 weeks of gestation.

We have added tables with comparisons for each time period in supplementary.

The primary result (incidence of stillbirth) should be presented before the causes of stillbirth.

We thank the reviewer for this comment, we have changed and now present the incidences first.

Table 3 reports only 12 different causes of stillbirths, whereas the classification used described 17 causes (table 1). How many stillbirths were unexplained between the three periods?

The reported causes of death were the causes with at least one case. There were 13 % unexplained stillbirths between 1998-2004, 12.94% between 2005-2013 and 12.36% between 2014-2018.

Discussion :

The discussion is difficult to read, as the ideas follow without order or hamony.

Legend 2 : evolution of stillbirths in Sweden should be removed.

We cant find that sentence.

The discussion should be

It seems to be missing information here.

.

Reviewer #4: Your article titled Stillbirth in Stockholm during a 20-year period, incidence and causes with focus on term and late term gestations is submitted for publication in Plos One. My first remark should encourage you to explain to the reader why Stockholm is a good place to study the future of stillbirths.

-1- Do you consider Stockholm's rates to be among the lowest in the world? Is the question of continuing a long-term gestation beyond 41 GW or of interrupting labor at the 41th GW a priority question that arises or will arise in all countries? In other words, does the situation in Sweden, and in particular Stockholm, serve as an example for other countries?

Please see comment 3 reviewer 3. And in addition, when to induce labour is of course of relevance in Sweden as in other countries and the interest elevated in Sweden after the so called SWEPIS-study (ref 10).

The finding in the report from the National Board of Health and Welfare, that the incidence of term stillbirth was lower in Stockholm County than most of other counties in Sweden, make Stockholm an interesting place to study term and late term stillbirths.

We want to believe it, but the increase in the average age of women at the birth of their children, the heavy smoking during pregnancy, and the fight against social discrimination are also priorities for the countries even among the richest of the planet?

It seems to me that you should indeed give more arguments because other very recent publications relate exactly to the same subject (PLOS medicine 2020) and we would like your article to be able to both distinguish itself from it and also demonstrate that the subject is important for other countries, see reference (* from the Euro-Peristat Project) for example, but you mentioned an earlier reference [20].

We thank the reviewer for an interesting comment, can you please name the reference since we have not found it.

-2- You seem to think that your statistical measurements of both gestational age and the number of stillbirths have not been affected by errors, of course, but when we know the statistical difficulties in certain countries in distinguishing abortions for therapeutic causes from stillbirths, the international reader would like to have a sentence to be enlightened on this point.

We thank the reviewer for this important comment. We have added: “There are no cases of late abortions among the stillbirth cases. “

You could argue that to avoid the statistical problem of termination of pregnancy, you chose to primarily study long-term pregnancy of 40 GW to 42+ because the effect of termination of pregnancy is large only at short gestation times. However, this should affect the statistical measure of Sweden's stillbirth rate at the standard 36 GW threshold and you could mention this point.

All stillbirth cases have been scrutinized and there are no cases of late abortion among them.

-3- Your article, like other similar articles, does not frankly conclude on the benefit of inducing late pregnancy and your discussion is very interesting. But one wonders what would you need to be able to conclude and not just say that the woman must be informed of the risks incurred in each two cases of either termination or continuation of the pregnancy. And it seems from what you write that you need more statistical power, and you wonder why you do expand to the entire Sweden, or even why you do not prefer to do individual participant data meta-analyzes as of other colleagues. One of your main reference concerns a paper published in January 2019 in BMJ, but a paper published in December 2020 in Plos medicine should be mentioned.

We thank the reviewer for this comment and are not sure about what reference from Plos Dec 2020 should be mentioned, could you please add a title?

-4- It is difficult to get a figure related to the title of your article: 20 years period of stillbirth in Stockholm? Figure 2, should be the place but there is no definition of stillbirths (22GW, 37GW ?). Stagnation of Sweden a whole since 10 years is not discussed.

We thank the reviewer for this comment, until June 2008 the official statistic reported in Sweden was from gw 28+0. From 1 July 2008 the official statistic reported is from gw 22+0, this is now clarified in the text note under figure 2. The numbers for Stockholm county is from GW 22+0 for all three time periods.

-5- An important point that you do not discuss concerns the high proportion of women born outside Sweden (48% table 2) and how it is related to stillbirth rate.

We thank the reviewer for this comment, and have added a sentence of this in discussion third paragraph: “Foreign-born women, especially those born in sub-Saharan Africa and the Middle East, are overrepresented in the group of women affected by stillbirth, [6] Sweden has had an increasing group of foreign-born women since many years”

-6- How a relatively higher proportion of primiparus women (46%) and its rapid fall between 2010 and 2015 (43.1) [3 figure C9.2] at least will affect the results. The prevalence of smoking during pregnancy has decreased [28] seems to be true concerning Europe according to [3 Table R8.1] but discrepancies between countries are huge.

The proportion of primiparous women has been between 40-45% in Sweden since the 70th. It is true that the proportion of smoking has decreased as well as the proportion of pregnant women with a BMI >25.

1. Henrichs J, Verfaille V, Jellema P, Viester L, Pajkrt E, Wilschut J, et al. Effectiveness of routine third trimester ultrasonography to reduce adverse perinatal outcomes in low risk pregnancy (the IRIS study): nationwide, pragmatic, multicentre, stepped wedge cluster randomised trial. BMJ (Clinical research ed). 2019;367:l5517. Epub 2019/10/17. doi: 10.1136/bmj.l5517. PubMed PMID: 31615781; PubMed Central PMCID: PMCPMC6792062 www.icmje.org/coi_disclosure.pdf and declare: for the current study (the IRIS study), AdJ and JW received funding from the Netherlands Organisation for Health Research and Development; no financial relationships with any organisations that might have an interest in the submitted work in the previous three years; no other relationships or activities that could appear to have influenced the submitted work.

2. Wennerholm UB, Saltvedt S, Wessberg A, Alkmark M, Bergh C, Wendel SB, et al. Induction of labour at 41 weeks versus expectant management and induction of labour at 42 weeks (SWEdish Post-term Induction Study, SWEPIS): multicentre, open label, randomised, superiority trial. BMJ (Clinical research ed). 2019;367:l6131. Epub 2019/11/22. doi: 10.1136/bmj.l6131. PubMed PMID: 31748223.

3. Stormdal Bring H, Hulthen Varli IA, Kublickas M, Papadogiannakis N, Pettersson K. Causes of stillbirth at different gestational ages in singleton pregnancies. Acta obstetricia et gynecologica Scandinavica. 2014;93(1):86-92. Epub 2013/10/15. doi: 10.1111/aogs.12278. PubMed PMID: 24117104.

4. Bodnar LM, Parks WT, Perkins K, Pugh SJ, Platt RW, Feghali M, et al. Maternal prepregnancy obesity and cause-specific stillbirth. The American journal of clinical nutrition. 2015;102(4):858-64. Epub 2015/08/28. doi: 10.3945/ajcn.115.112250. PubMed PMID: 26310539; PubMed Central PMCID: PMCPMC4588742.

5. The Stillbirth Collaborative Research Network Writing Group. Causes of death among stillbirths. JAMA. 2011;306(22):2459-68. Epub 2011/12/15. doi: 306/22/2459 [pii]

10.1001/jama.2011.1823. PubMed PMID: 22166605.

6. Ekeus C, Cnattingius S, Essen B, Hjern A. Stillbirth among foreign-born women in Sweden. European journal of public health. 2011;21(6):788-92. Epub 2011/01/13. doi: 10.1093/eurpub/ckq200. PubMed PMID: 21224278.

7 May 2021

Stillbirth in term and late term gestations in Stockholm during a 20-year period, incidence and causes.

PONE-D-21-01718R1

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14 May 2021

PONE-D-21-01718R1

Stillbirth in term and late term gestations in Stockholm during a 20-year period, incidence and causes.

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