The Epidemiology of Stillbirth

Sven Cnattingius and Olof Stephansson

Stillbirths account for an increasing proportion of feto-infant mortality. Yet, causes of stillbirth are
rarely reported, and the causes of most stillbirths remain unknown. Few studies focus specifically on
the epidemiology of stillbirth. Major risk factors include high maternal age, smoking, and overweight.
The prevalence of delayed childbearing and, especially overweight, are increasing in most developed
countries. The proportion o f stillbirth attributable to overweight is likely to increase.

Copyright 9 2002 by W.B. Saunders

tillbirth currently accounts for m o r e than

S one third of all feto-infant mortality and

m o r e than 50% o f all perinatal deaths in develo p e d countries. 1,2 A m o n g n o n m a l f o r m e d fetuses/infants, stillbirth at 28 c o m p l e t e d gestational weeks or later accounts for m o r e than
50% of all feto-infant m o r t a l i t y ) Moreover, the
causes of stillbirth differ f r o m those of early
neonatal mortality, z,4 Despite the clear importance of stillbirth as a public health problem, few
studies have focused specifically on the epidemiotogy and cause of stillbirth.

Causes
In contrast to infant mortality, causes of stillbirth
are generally not registered i n vital statistics or
population-based research registers. T h e r e are
also substantial difficulties in d e t e r m i n i n g the
cause of stillbirth. First, weight a n d gestational
length are, in the case of a stillbirth, estimated at
delivery and not at time of death. This leads not
only to an overestimation of gestational length,
but the fetus may also have lost weight after
death. Thus, the i m p o r t a n c e of low birth weight
in relation to gestational age may therefore be
overestimated in stillbirth. Second, even if diagnostic investigations are p e r f o r m e d , there may
be difficulties in achiex4ng valid results. Pathological investigations must consider possible
changes occurring between the often u n k n o w n
time of death and time of investigation. W h e n
looking for an infectious cause, it may be unknown what infections should be considered lethal, and infections may also occur during or
after delivery.
A n u m b e r of m e t h o d s of g r o u p i n g causes of
death in stillbirth a n d neonatal deaths have
b e e n used. 5,6 T h e cause of stillbirth differs in
m a n y cases f r o m the cause of neonatal deaths,

which necessitates a specific classification system

for stillbirth. More importantly, diagnostic routines generally differ substantially between hospitals, and a successful classification of causes of
stillbirth is highly d e p e n d e n t on a standardized
and systematic clinical procedure. As m o r e than
1 factor may contribute to fetal death, m a n y
classifications have recognized the n e e d for a
hierarchical classification system, in which potentially lethal anomalies take p r e c e d e n c e over
other conditions. 5,6 Two o t h e r i m p o r t a n t causes
of stillbirth are prenatal infections, and above
all, fetal growth retardation. O t h e r causes include isoimmunization, abruptio placenta, maternal chronic diseases, pregnancy-related disorders (such as preeclampsia and gestational
diabetes), and umbilical cord accidents. Yet, despite all these possible causes o f stillbirth, a
substantial p r o p o r t i o n of stillbirths r e m a i n
unexplained. However, within the g r o u p of "unexplained" stillbirths, there is probably a relatively large g r o u p of fetuses with undiagnosed
fetal malnutrition, c h r o m o s o m a l aberrations, or
infections.

Stillbirth and G e s t a t i o n a l A g e
W h e n stillbirth is defined as a fetal death occurring at 20 weeks or later, 82% of all stillbirths are
r e p o r t e d to occur in the p r e t e r m period. 7 Also,
when stillbirth is defined as fetal death at 24
weeks or later or even at 28 weeks or later, the
From the Department of Medical Epidemiology, Karolinska Instituter, Stockholm.
Address ~'eprint requests to Sven Cnattingius, MD, PhD, Department
of Medical Epidemiology, Karolinska Instituter, PO Box 281, SE171 77 StockhoZm; e-mail: Sven. Cnattingius@mep.ki.se.
Copyright 9 2002 by W.B. Saundev's
O146-0005/02/2601-0005535. 00/0
doi:l O.1053/sper.2002.29841

Seminars in Perinatology, Vol 26, No 1 (February), 2002: pp 25-30

25

Cnattingius and Stephansson

26

majority of stillbirth occur preterm. 8,9 Since the

majority of stillbirths occur preterm, it may seem
paradoxical that the risk of stillbirth increases
with gestational age. However, as p o i n t e d out by
Yudkin et al, 1~ fetuses at risk of stillbirth at a
specific gestational age must include all live fetuses at that gestational age. By using this approach, Yudkin et aP ~ showed a consistent increase in risk of stillbirth by gestational age (Fig
1), an observation that has b e e n c o n f i r m e d by
o t h e r investigators, n,12 Thus, the risk of stillbirth
may be highest in the postterm period, which to
a large extent can be explained by increased
rates of small-for-gestational-age fetuses b o r n
postterm. 1~

Risk F a c t o r s
Maternal Age
T h e r e is g o o d evidence that it is b e c o m i n g increasingly c o m m o n a m o n g w o m e n to choose to
delay childbearing. In the United States, the
p r o p o r t i o n of first-time mothers who were age
30 or older increased f r o m 4% in 1969 to 21% in
1994.14 -The t r e n d of delayed childbearing has
occurred primarily a m o n g w o m e n with at least
high school education and is attributed to
w o m e n voluntarily p o s t p o n i n g pregnancies for
personal or professional reasons. Several large
epidemiological studies have r e p o r t e d that high

2,0
1s
1,e
o
Q

1,4

1,2

~, 0,8
0,6

Table 1. Odds Ratio (OR) and 95% Confidence

Intervals (CI) for Stillbirth by Maternal Age

Age (years)

OR

(95 % CI)
(reference group)

<30

1.0

30-34

1.3

(0.9-1.7)

35-39
40+

1.9
2.4

(1.3-2.7)
(1.3-4.5)

Data from reference 16.

m a t e r n a l age increases the risk of stillbirth. 15,16

Fretts et aP 6 r e p o r t e d that, c o m p a r e d to w o m e n
below 30 years, the risk of fetal d e a t h a m o n g
w o m e n aged 35 to 39 years was almost increased
24bld, while c o r r e s p o n d i n g risk for those 40 or
older was m o r e than doubled (Table 1). T h e risk
of stillbirth is especially p r o n o u n c e d a m o n g delayed childbearers, but probably also increased
a m o n g older parous women. Although the risks
of pregnancy-related disorders or complications,
such as preeclampsia, gestational diabetes, a n d
abruptio placenta increase with age, the agerelated increase in stillbirth cannot be explained
by these diseases, a2,a6 T h e age-related stillbirth
risk increases with advancing gestational age,
and older w o m e n have above all an increased
risk of u n e x p l a i n e d s t i l l b i r t h / A l t h o u g h the absolute increase in risk for the individual w o m a n
may be considered modest, the i m p a c t of delayed childbearing becomes m o r e i m p o r t a n t as
the p h e n o m e n o n b e c o m e s m o r e prevalent.
T e e n a g e pregnancies are, in contrast to high
m a t e r n a l age, m o r e associated with neonatal
death than stillbirthJ 7 This is not surprising,
since the risk of p r e t e r m birth, and especially
very p r e t e r m birth, is increased a m o n g teenage
childbearers (and especially very y o u n g teenagers), while the association between restricted
fetal growth and teenage childbearing is m o r e
controversial.IS

Parity

0,4
0,2
0,0
29

31

33

35

37

39

41

Gestationel age (weeks)

Figure l. Rate of stillbirth by gestational age, per

1,000 live fetuses at that gestational age. (Reprinted
with permission. I~)

Studies have r e p o r t e d an increased rate of stillbirth a m o n g nulliparas and g r a n d multiparas. n,m However, in 1 study, the U-shaped pattern between parity and stillbirth risk was,
a m o n g older women, evident in the t960s a n d
early 1970s, but not in the late 1970s and
1980s/6 T h e authors suggest that the reduction
in the parity-related risk of stillbirth over time

Epidemiology of Stillbirth

may be due to i m p r o v e d access to medical care

and changes of obstetrical practice.

Smokmg
T h e association between smoking and stillbirth
risk is well known and there is probably a causal
association. First, the risk of stillbirth increases
with the a m o u n t smoked. 2,2~ Second, there is a
supportive biological hypothesis. Smoking during pregnancy increases fetal carboxihemoglobin concentration and increases the vascular resistance, because of the vasoconstrictive effect of
nicotine and the r e d u c e d prostacyclin synthesis. 2~-23These toxic effects of tobacco smoke may
partly explain the causal association between
smoking and r e d u c e d fetal growthY 4 These effects may also contribute to the placental
changes a m o n g smokers, such as decidual necrosis, which in turn may lead to abruptio placenta. 25"26 In a study of Meyer a n d Tonascia, 27
the elevated risk of fetal death in smokers was
largely because of higher rates of placental abruption and placenta previa. A n o t h e r study
f o u n d a 40% overall increased risk of stillbirth
a m o n g smokers, but smokers who did not suffer
f r o m placental complications or delivered
growth retarded infants had no increased risk of
stillbirth, t2 Thus, it appears that the association
between smoking and stillbirth is explained by
the smoking-related risks of fetal growth retardation and placental complications. Third, the
hypothesis of a causal association between smoking during pregnancy and stillbirth is further
s t r e n g t h e n e d by a recent Danish study, reporting that smoking cessation in the first trimester
reduces the risk of stillbirth c o r r e s p o n d i n g to
that of nonsmokers. 23 This result also indicates
that smoking exerts its influence on stillbirth
after the first trimester. Smoking has b e e n rep o r t e d to primarily influence risk of p r e t e r m
stillbirth, ~2 and these results are in turn supp o r t e d by a finding that intrauterine growth retardation is a stronger risk factor for p r e t e r m
than for term stillbirth, s
Although the prevalence of smoking during
p r e g n a n c y has declined in m a n y countries, still
between 10% to 30% of the p r e g n a n t population in the western world smoke. 23,29 Thus,
smoking continues to be one of the most important preventable risk factors for stillbirth.

27

Maternal Body-mass Index

An association between maternal body-mass index (BMI) and stillbirth risk, with the highest
risk a m o n g overweight and obese w o m e n was
r e p o r t e d in 1993. 2o A Swedish register-based
study confirmed this and f o u n d that the association between increasing BMI and stillbirth risk
was highest a m o n g nutliparous women. 3~ A recent Swedish study on a n t e p a r t u m stillbirths
f o u n d that the association between early pregnancy BMI and stillbirth risk was strongest for
term stillbirths, suggesting an increasing effect
of a high BMI by gestational length. 31 T h e mechanisms for the BMI-related increases in risk of
stillbirth remain a matter of speculation. Overweight and obese w o m e n are m o r e likely to have
a low socio-economic status a n d are m o r e often
cigarette smokers. Pregnancy complications,
such as gestational diabetes, preeclampsia, and
eclampsia, are m o r e c o m m o n a m o n g overweight
and obese women. After excluding cases and
controls with weight-related pregnancy complications, the risk of stillbirth r e m a i n e d increased
a m o n g overweight women, but was attenuated
a m o n g obese w o m e n (Table 2). 3~ T h e prevalence of overweight and obesity is rising rapidly
in developed countries (Fig 2), 32 and in the
United States a third of the p r e g n a n t population
are overweight (BMI > 25). as If causal, overweight may f r o m a public health perspective be
the most i m p o r t a n t risk factor for stillbirth.

Table 2. Odds Ratio (OR) and 95% Confidence

Intervals (CI) for Antepartum Stillbirth by Bodymass Index (BMI) Among Nulliparous Women

All Cases and

Controls
(n = 613/660)*
BMI

-<19.9++
20.0-24.9
25.0-29.9
-->30.0

Excluding Cases
and Controls With
Gestational
Diabetes and
Preeclampsia
(n = 461/546)*

OR~

(95 % CI)

OR~

(95 % CI)

1.0
1.2
1.9
2.1

(0.8-1.7)
(1.2-2.9)
(1.2-3.6)

1.0
1.2
2.5
1.5

(0.8-1.8)
(1.5-4.0)
(0.7-3.0)

* Number of cases/controls.
t Adjusted for age, height, occupation, and cigarette smoking.
++Reference group.
Data from reference 31.

Cnattingius and Stephansson

28

%
20
15

D MI 25.0-29,9
[] BMI 30.0-34.9

10

[] BMI 35.0+

5
0
1960-62

1971-74

1976-80

1988-94

Figure 2. Prevalence of overweight and obesity

among women aged 20-29 years, United States 19601994. (Data from reference 32.)

Maternal Weight Gain During Pregnancy

Few studies have investigated the association between weight gain during pregnancy and stillbirth risk. Weight gain is related to prepregnancy BMI, and w o m e n with a high BMI gain
less weight during p r e g n a n c y ? T M Therefore, it
is i m p o r t a n t when analyzing the association between weight gain a n d risk of stillbirth to consider p r e p r e g n a n c y BMI as a c o n f o u n d i n g factor. Taffel et a135 showed an association between
low m a t e r n a l weight gain and stillbirth risk,
whereas-this was not f o u n d by Rydhstr6m et al. ~6
However, n o n e of these studies simultaneously
investigated the possible influences by other covariates. A recent Swedish study was able to take
such confounders into account and f o u n d no
association between pregnancy weight gain a n d
a n t e p a r t u m stillbirth risk. 31

Socio-economic Factors
Although it is generally known that socio-economic status influences stillbirth risk, 2~ the reasons remain essentially unknown. This is not
entirely because most studies have included few
covariates, but results f r o m a recent study suggest that the reasons for the association may be
h a r d to disentangle. 9 T h e group of w o m e n f r o m
low social class was favored by a reduced prevalence of delayed childbearers, but, on the o t h e r
hand, they were m o r e often smokers and overweight. Thus, the risks of stillbirth related to low
socio-economic status, were after adjustment for
maternal age, smoking and body mass index,
essentially the same as the crude risks. Moreover,
further adjustments for time of admittance to
antenatal care, n u m b e r of visits to prenatal care,
and a n u m b e r of o t h e r covariates, did not essentially c h a n g e these risks, n o r were the risks
e x p l a i n e d by i n c r e a s e d rates o f small-for-

gestational-age pregnancies or pregnancy-related disorders a m o n g w o m e n f r o m low social

class9 Residual c o n f o u n d i n g of alcohol a n d illicit drug use is a possible but not p r o b a b l e
explanation. Since the risk related to low social
class was primarily increased for t e r m stillbirth,
one may hypothesize whether these differences
are due to subtle differences in care.

Recurrent Stillbirth
T h e tendency to repeat pregnancy o u t c o m e s in
successive births is well known and also includes
risk of stillbirth. W o m e n with a previous stillbirth may, c o m p a r e d to w o m e n with no previous
stillbirth, have a 6 to 10-fold increased risk of
stillbirth in next pregnancy. 37,3s Although recurrence of stillbirth is m o r e c o m m o n a m o n g
w o m e n with diabetes or pregnancy-induced hypertensive diseases, and may also be associated
with recurrence of fetal growth retardation, such
factors probably only partly explain the risk of
repeating stillbirth, s7-~9

Maternal Hemoglobin Concentration

During normal pregnancy, the h e m o g l o b i n concentration falls until the 20th week of gestation,
remains fairly constant up to 30 weeks and thereafter rises slightly. These changes in h e m o g l o b i n
concentration are mainly due to an increased
plasma volume. In developed countries, b o t h
high a n d low h e m o g l o b i n concentration during
p r e g n a n c y have b e e n associated with small-forgestational-age and p r e t e r m births. Two studies
have r e p o r t e d increased rates of perinatal death
with b o t h low and high h e m o g l o b i n concentration during pregnancy, 4~ and 1 study f o u n d a
similar u-shaped association for stillbirth rates. 42
In a recently published study the risk of stillbirth
was increased for b o t h low (--<115 g / L ) and high
(>--146 g / L ) early pregnancy h e m o g l o b i n concentration, 43 and a relatively large decrease in
h e m o g l o b i n concentration during p r e g n a n c y
t e n d e d to be protective. T h e risk related to high
h e m o g l o b i n values was confined to a n t e p a r t u m
stillbirths without malformations, and especially
p r o n o u n c e d if the fetus also was growth-retarded (Table 3). T h e biological m e c h a n i s m for
the increased risk of stillbirth for high h e m o g l o bin concentration may be that plasma expansion
enhances fetal growth. T h e r e d u c e d b l o o d viscosity may favor b l o o d flow in the m a t e r n a l in-

Epidemiology of Stillbirth

T a b l e 3. O d d s Ratio (OR) a n d 95% C o n f i d e n c e

Intervals (CI) for Stillbirth by H e m o g l o b i n
C o n c e n t r a t i o n in First T r i m e s t e r

Antepmr
Stillbirth Without
Malformations
All
(n = 519/610)*

SGA-stillbirths
(n = 137/390)*

First Hb g/L

ORt

(95% CI)

OR?

(95% CI)

--<115
116-125
126-135 (ref.)
136-145
-->146

1.7
0.9
1.0
1.0
2.0

(1.0-2.8)
(0.6-1.2)

1.5
0.4
1.0
1.1
4.2

(0.6-3.9)
(0.2-0.8)

(0.7-1.4)
(1.1-3.8)

(0.6-2.1)
(1.3-13.9)

* Number of cases and controls.

t Adjusted for age, height, BMI, occupation, smoking, early
pregnancy weekly change in Hb, and week of first Hb measurement.
Source: Stephanssou et al. JAMA 2000;284:2611-7.

tervillous space and prevent thrombosis in the

uteroplacental circulation.

Multiple Birth
Since twins are m o r e likely to be growth-retarded and to be delivered preterm, they have an
increased risk of stillbirth and (above all) neonatal death. A particular concern is monozygotic
twins, who have p o o r e r survival than dizygotic
twins. 44,45 If 1 twin dies in utero, the cotwin is n o t
only at increased risk of fetal death, but also runs
an increased risk of cerebral palsy and o t h e r
cerebral impairments. 44 The relative i m p o r t a n c e
of twin pregnancy as a risk factor for stillbirth is
likely to increase, as the rate of twin pregnancies
are increasing. 46

Conclusions
In contrast to infant mortality, the decline in
stillbirth rates have, in most countries, b e e n less
obvious. The majority of stillbirths dies unexpectedly preterm, when possibilities to detect
warning signs, such as fetal growth restriction,
are limited. Major maternal risk factors include
m a t e r n a l smoking, high maternal age, and overweight, but why high maternal a g e and overweight influence stillbirth risk remains to be
determined. In contrast to smoking, the prevalence of delayed childbearing and overweight
are increasing in most developed countries.

29

Thus, the relative i m p o r t a n c e of these factors is

likely to increase.

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