Educational inequality in stillbirth: temporal trends in Quebec from 1981 to 2009.
Savard, Noemie ; Auger, Nathalie ; Park, Alison L. 等
Stillbirth, an important contributor to perinatal mortality, (1) is
unequally distributed across socio-economic groups. (2) Educational
inequality in stillbirth has been documented in many high-income
countries (2-4) and the province of Quebec, Canada. (5,6) What is less
understood, however, is how trends in stillbirth-related educational
inequality have evolved over time. A Scandinavian study found that
educational inequality in stillbirth persisted from 1981 to 2000, (4)
but temporal trends in the last decade, or in other countries, to our
knowledge have not been determined. Furthermore, unexplained
stillbirths, (5,7-9) and stillbirths secondary to placental abruption,
obstetrical complications, asphyxia, (5,9) slow fetal growth, maternal
diseases,5 and non-chromosomal congenital anomalies, (5,10) are more
strongly associated with maternal education, but the lack of data on
time trends makes it difficult to determine whether associations vary
over time. Temporal trends that vary by cause are plausible. For
example, changes in prenatal diagnosis may have influenced specific
causes of stillbirth such as congenital anomalies and could have
affected trends over time. Temporal trends are important for evaluating
policy, programs and interventions aimed at reducing perinatal
mortality. A better understanding of temporal trends for the specific
causes of stillbirth most associated with maternal education may be
particularly informative, since women with less education could be
targeted based on the causes contributing most to inequality in
stillbirth.
Our objective was to determine temporal trends in inequality
related to maternal education for all-cause and cause-specific still
births over the last three decades in Quebec, Canada, as part of a
larger effort to understand and ultimately reduce social inequalities.
Quebec to our knowledge is the only Canadian province that documents
maternal education on fetal death registration certificates, and time
trends in educational inequality in stillbirth have not been studied in
the province. (5,6)
METHODS
Data and variables
Live births (N=2,454,845) and stillbirths (N=11,233) were obtained
from the Quebec live birth and stillbirth registries for the years
1981-2009. In Quebec, births showing any sign of life at delivery are
defined as live births, and intrauterine deaths [greater than or equal
to] 500 g are defined as stillbirths. Multiple births (N=57,660) were
excluded due to unique causes in the pathway leading to stillbirth. (11)
We also excluded 464 intentional terminations of pregnancy
(International Classification of Disease (ICD) codes 779.6 (9th
revision, before 2000) or P96.4 (10th revision, 2000 onward)), leaving a
final sample of 2,397,971 live births and 9,983 stillbirths. Three
periods were analyzed (1981-1989, 1990-1999, 2000-2009), to assess time
trends while ensuring a sufficient sample size per period.
Cause of fetal death was determined using the principal cause of
death recorded on stillbirth certificates, based on ICD codes. Five
categories of mortality were evaluated, including 1) placental abruption
or haemorrhage (7021, P021; excluding placenta previa), 2) cord
compression (7024, 7025, P024, P025), 3) congenital anomalies (740-759,
Q00-Q99), 4) unspecified (7799, P95), and 5) all remaining causes too
infrequent to be evaluated separately. These causes were selected based
on frequency in our data, and were grouped into clinically relevant
categories.
Maternal education, which is recorded on live birth and stillbirth
certificates in number of completed years from 0 to 30, was expressed as
a continuous cumulative rank score (ranging from 0 to 1) for the main
analyses. This score was computed by 1) assigning to the most educated
(30 years) a score corresponding to half the proportion of births with
30 years of education, 2) assigning to the next most educated (29 years)
a score corresponding to the sum of the proportion of births with
[greater than or equal to]29 years of education plus half the proportion
with 29 years of education, 3) and so on for all subsequent educational
levels. (5) To illustrate, assume that 1%, 2%, and 4% of mothers had 30,
29, and 28 years of education, respectively. In this example, mothers
with 30 years of education would be assigned a score of (0.01/2) =
0.005; those with 29 years a score of 0.01 + (0.02/2) = 0.02; those with
28 years a score of 0.01 + 0.02 + (0.04/2) = 0.05; and so on for the
remaining education levels. To account for changes in the distribution
of maternal education over time, the cumulative rank score was computed
for each period separately. Thus, within each period, the value of the
assigned rank reflected the cumulative distribution of maternal
education specific to that period. In secondary analyses, maternal
education was categorized as <11, 11-13, 14-15, and [greater than or
equal to] 16 years. This categorization reflects the Quebec education
system, where 11 years are required for a high school diploma, 14 years
for a college level trade certificate, and 16 years for a university
level bachelor's degree.
[FIGURE 1 OMITTED]
Covariates included maternal age (<20, 20-24, 25-29, 30-34,
[greater than or equal to]35 years), parity (0, 1, [greater than or
equal to] 2 previous pregnancies), legal marital status (yes, no), and
mother tongue (French, English, other, unknown). Data were missing on
maternal education for 143,135 live births (6%) and 2,646 stillbirths
(26%), age for 196 live births (<0.01%) and 73 stillbirths (0.01%),
and marital status for 668 stillbirths (0.7%). There was little change
in the proportion of missing data on education over time. Data were
assumed to be missing at random, and were imputed 5 times for each
period, based on the distribution of all known covariates (as well as
stillbirth status, gestational age, and year of birth) using the SAS
multiple imputation (MI) procedure. (12)
Statistical analysis
To achieve our objective of measuring educational inequality, we
used the relative index of inequality (RII) and the slope index of
inequality (SII) summary measures. The RII represents the ratio in the
risk of stillbirth for the least- relative to the most-educated mothers,
and the SII expresses the absolute difference in risk between the least-
and most-educated mothers. Unlike risk ratios and risk differences for
categorical education, the RII and SII use the distribution of education
for the whole population, and are obtained by regressing stillbirth
against the continuous education rank score, such that their computation
is affected by stillbirth rates throughout the education range. Because
the rank score ranges from 0 to 1, the parameter estimates for the RII
and SII equal the ratio and difference, respectively, in risk between
the least and most educated. (13)
The RII, SII, and 95% confidence intervals (CI) for all-cause and
cause-specific stillbirth, by period and for all periods combined, were
obtained in regression models using the SAS GENMOD procedure for
binomial outcomes, specifying a logarithmic (RII) or identity (SII) link
and accounting for the added variance due to imputation. (12) Models
containing the cumulative education rank score (exposure) and stillbirth
(outcome) were initially unadjusted, and subsequently adjusted for
maternal age, parity, marital status, and mother tongue. Gestational age
was not included in regression models to avoid biasing associations.
(14) Time trends in the RII and SII were assessed through pair-wise
comparisons between all three periods, using a T-test that accounted for
the added variance due to imputation. (12)
To capture temporal trends in stillbirth rates by educational
group, we assessed models containing an education-by-period interaction
term, with education expressed categorically. For each education group,
we obtained risk ratios (RR) and absolute risk differences (RD) for the
association between period and stillbirth, adjusted for maternal age,
parity, marital status, and mother tongue. RRs and RDs were computed
using the SAS GENMOD procedure for binomial outcomes with logarithmic
and identity links, respectively.
In sensitivity analyses, models were run excluding births with
missing data on education, age, and marital status. Models were also run
excluding stillbirths [greater than or equal to]41 weeks of gestation,
in the event that greater use of labour induction over time may have
influenced temporal trends. Models for stillbirth caused by congenital
anomaly were run including terminations of pregnancy, in the event that
terminations were due to anomalies. Statistical analyses were performed
using SAS 9.3 (SAS Institute Inc., Cary, NC). Ethics approval was waived
by the research ethics board of the University of Montreal Hospital
Centre.
RESULTS
Mean number of years of maternal education was 12.3 (median 12.0)
in 1981-1989, 13.3 (13.0) in 1990-1999, and 13.9 (14.0) in 2000-2009.
Stillbirth rates were inversely related to education, ranging from 2.4
per 1000 births for mothers with [greater than or equal to] 16 years
education to 4.3 for mothers with <11 years (Table 1, unimputed
data). Both all-cause and cause-specific stillbirth rates were highest
for mothers with <11 years education in all study periods, and tended
to decline between the first and last study periods for most causes of
stillbirth (Figure 1). Rates of stillbirths with unspecified causes, on
the other hand, were stable (most-educated mothers) or tended to
increase over time (less-educated mothers).
The overall RII indicated that the risk of stillbirth for the
least-educated mothers was twice that of the most-educated mothers
(adjusted RII 2.0, 95% CI 1.8-2.2) (Table 2). There was a statistically
significant rise in the RII over the study periods, increasing from 1.8
in 1981-1989 to 2.3 in 2000-2009 (p=0.05). The overall SII indicated
that mothers with the least education had an excess of 2.5 stillbirths
per 1000 births (adjusted, 95% CI 2.1-2.8) compared with the
most-educated mothers (Table 3). An excess absolute risk was observed in
all periods, and there was no statistically significant change between
the first and last period. The SII was lower in the middle period
compared with the first and last periods, but the difference was not
statistically significant.
Low education was associated with higher risk of stillbirth from
all causes in every period, as shown in Table 2 (RII) and Table 3 (SII).
The RII was largest for placental abruption, followed by "other
causes", while the SII was greatest for "other causes",
followed by placental abruption and unspecified causes. Over time, there
was a statistically significant increase in relative educational
inequality for stillbirth from "other causes"; a decrease in
absolute educational inequality in stillbirth caused by placental
abruption; and an increase in both relative and absolute educational
inequalities for unspecified stillbirth. For stillbirth caused by cord
compression or congenital anomalies, there was a statistically
non-significant decrease in absolute inequality between the first and
the last periods. Unadjusted models led to slightly weaker associations
between education and all-cause and cause-specific stillbirth, but
yielded similar temporal trends (data not shown).
Figure 2 illustrates the temporal trend in adjusted RRs and RDs for
all-cause stillbirth by education group. Between the first and last
period, mothers with [greater than or equal to]16 years education
experienced the largest relative decrease in stillbirth rates (RR 0.63,
95% CI 0.550.82), and mothers with <11 years education experienced
the smallest relative decrease (RR 0.72, 95% CI 0.63-0.83). The opposite
was observed for RDs, as mothers with [greater than or equal to] 16
years education had the smallest absolute decrease in stillbirth rates
(1.1 per 1000 births, 95% CI 0.7-1.5), while those with <11 years
education had the largest decrease (1.5, 95% CI 0.7-2.2). A
statistically significant decrease in stillbirth was observed for each
education group between 1981-1989 and 1990-1999. Between 1990-1999 and
20002009, a statistically significant decrease occurred only for the
most-educated group.
In sensitivity analyses, models excluding missing data yielded
similar findings. There were 448 stillbirths (4.5%) at [greater than or
equal to] 41 weeks of gestation, but no statistically significant
difference between education groups, and exclusion of these births
yielded similar results. Although educational inequality for stillbirth
due to congenital anomalies decreased between the first and last
periods, relative and absolute inequality for congenital anomalies
combined with terminations of pregnancy rebounded in 2000-2009 to the
level observed in 1981-1989 (RII 2.0, 1.6, and 2.0; SII 0.5, 0.2, and
0.6 per 1000 births for the 1980s, 1990s and 2000s, respectively). This
trend occurred with an increase in pregnancy terminations (0.02 per 1000
births in the 1980s vs. 0.5 per 1000 in the 2000s), and in rates of
stillbirth caused by congenital anomalies/terminations for all education
groups over time.
DISCUSSION
This study found that absolute educational inequality in stillbirth
persisted in Quebec between 1981 and 2009, despite a reduction in the
stillbirth rate for all education groups. There was a concomitant
increase in relative educational inequality in stillbirth. Most of the
reduction in stillbirth rates occurred between 1981-1989 and 1990-1999,
with an additional reduction in 2000-2009 for the highest-educated
mothers. The contributions of specific causes of stillbirth changed over
time, including a decrease in absolute inequality for placental
abruption and an increase for unspecified causes. These novel findings
are important because they suggest that educational inequality in
stillbirth persists in Quebec, and that stillbirths of unspecified cause
are an increasingly salient contributor to educational inequality.
Maternal education is known to be associated with stillbirth,
(2-6,15) but studies assessing temporal trends in inequalities are few,
and existing studies in Quebec have not looked at trends over time.
(5,6) Between 1981 and 2000, absolute educational inequality in
stillbirth increased in Sweden, persisted in Denmark and Finland, and
decreased in Norway. (4) Though not directly reflecting education,
indices of area deprivation used to measure socio-economic status showed
that inequalities in stillbirth persisted between 1981 and 2007 in
England. (16,17) Thus, our findings are comparable to time trends
documented in Europe.
In addition, we demonstrate that trends in inequalities differ by
cause of stillbirth. Absolute inequality in stillbirth due to placental
abruption decreased over time in Quebec, aligning with abruption-related
rates that decreased in all education groups. A similar trend was
observed for stillbirths caused by cord compression and congenital
anomalies, although the decrease in absolute inequality between
1981-1989 and 2000-2009 did not reach statistical significance. This
finding contrasts with England, where area-based socio-economic
inequality in stillbirth due to placental haemorrhage (abruption and
previa) persisted between 2001 and 2007, whereas no association was
found for stillbirth from mechanical causes (cord compression and
malpresentation). (17) Differences between England and Quebec may
reflect varying stillbirth definitions, study periods, social contexts,
and health care systems. Decreases in absolute inequality caused by
placental abruption, cord compression, and congenital anomalies in
Quebec, however, were counterbalanced by an increase in inequality due
to stillbirths of unspecified cause. In comparison, educational
inequality in "unexplained" stillbirth decreased between 1967
and 1998 in Norway. (8) However, the ICD definition of unspecified
causes may not be equivalent to "unexplained" causes in
Norway, where clinical and autopsy data were reviewed to determine the
reason for mortality. (8)
[FIGURE 2 OMITTED]
All-cause stillbirth, placental abruption, and unexplained
stillbirth share a number of potentially modifiable risk factors,
including smoking, obesity, and other maternal comorbidities such as
pre-existing hypertension. (2,7,9,18,19) While prevalence of obesity and
hypertension increased in Quebec in the past decade, (20,21) smoking
prevalence decreased, although socio-economic inequalities persist. (22)
These risk factors are thought to lie in the causal pathway between
education and stillbirth, but it is unclear how their changing
prevalence may have influenced trends in educational inequality for
stillbirth, particularly as placental abruption-related stillbirth
inequalities decreased concomitantly with an increase in unspecified
stillbirth inequalities. The extent to which these risk factors mediate
trends in educational inequality for all-cause and cause-specific
stillbirth over time remains to be determined.
Congenital anomalies are associated with folic acid intake, (23)
maternal obesity, pre-existing diabetes, (24) and advanced age.25 We
found that rates and absolute educational inequality in stillbirth
caused by congenital anomaly tended to decrease in Quebec, despite an
increase in prevalence of obesity and diabetes and the proportion of
pregnancies at advanced ages. (26) Mandatory folic acid fortification of
cereal products was implemented in 1998 in Canada, (23) but this does
not explain the decrease in educational inequality for stillbirth caused
by congenital anomalies at the start of the 1990s. A more likely
explanation is increased availability of screening and early diagnosis
of congenital anomalies, leading to pregnancy terminations. Indeed, the
rising proportion of stillbirths with termination of pregnancy recorded
as cause of death, along with the fall in proportion of stillbirths
coded as congenital anomalies since the 1980s, (27) support this
possibility. Moreover, our own analyses showed that the rate of
stillbirths caused by congenital anomalies/terminations increased over
time, such that no decrease in absolute educational inequality was
observed for the 2000s compared to the 1980s. The rebound in inequality
observed in the last decade may be related to the rise in pregnancy
terminations. (28) Although terminations may be motivated by reasons
other than congenital anomalies, these findings nonetheless suggest that
there may have been no change in absolute educational inequality for
stillbirth caused by congenital anomaly over time in Quebec.
Medical care may be a route through which education leads to
inequality in stillbirth from placental abruption and cord compression.
Suboptimal care, including delayed recognition of medical problems or
inadequate management, is thought to contribute to an important
proportion of stillbirths. (29) Although Canada provides universal free
access to health services, utilization of prenatal services can
nonetheless differ across educational groups. (30) We found, however, a
decrease in absolute inequality for placental abruption and possibly
cord compression, which suggests that the contribution of suboptimal
care to educational inequality in stillbirth, if any, diminished over
time.
Our study had limitations related to use of retrospective
administrative data. The validity of ICD coding to determine cause of
death is undetermined, and may have led to misclassifications. However,
misclassifications are expected to be non-differential by education
level. There was a change in ICD coding from the 9th to 10th revision in
2000, and additional changes in coding practices may have occurred over
time of which we were unaware. For instance, changes in coding practices
may have led to more stillbirths classified as unspecified over time,
although such a trend would also be expected to be non-differential by
education. Secondary causes of death were not recorded, including
underlying reasons for pregnancy terminations. Some terminations may
result from prenatal screening for congenital anomaly, which may
potentially be more frequent in educated mothers. Although this pathway
cannot explain our results (since educated women had lower rates of
stillbirth from congenital anomaly/termination of pregnancy), it does
illustrate the limitation of lack of data on secondary causes of death.
No data were available on maternal risk factors such as smoking, body
mass index, comorbidities, or other measures of socio-economic status,
such as income and occupation. Due to limited sample size, we could not
disaggregate stillbirths of "other causes", or look at finer
causes of death categories such as neural tube defects. Quebec's
definition of stillbirth ([greater than or equal to] 500 g) differs from
other Canadian provinces ([greater than or equal to] 20 gestational
weeks), but we have no reason to suspect that trends in educational
inequality over time would have differed had Quebec's definition
been based on gestational age. Finally, the causal pathways linking
education with stillbirth are unclear, and adjustment for maternal age,
parity, mar ital status, and mother tongue may not have been necessary,
although trends over time were not affected when models were not
adjusted for these variables.
Our study found persisting absolute educational inequality in
all-cause stillbirth over the last three decades in Quebec. While
educational inequality tended to decrease for most causes of stillbirth,
particularly placental abruption, inequality increased for stillbirths
of unspecified causes. To our knowledge, this is the first study to
document these temporal trends in Quebec. Considering the growing
contribution of unspecified causes to overall educational inequality in
stillbirth, a better understanding of the underlying components of
unspecified causes is needed to further address the education gap in
stillbirth.
Acknowledgements: NA was supported by a Chercheur-boursier Junior 1
award from the Fonds de recherche du Quebec--Sante.
Conflict of Interest: None to declare.
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Received: October 15, 2012
Accepted: January 24, 2013
Noemie Savard, MD, [1] Nathalie Auger, MD, MSc, frcpc, [1-3] Alison
L. Park, MSc, [2,3] Ernest Lo, PhD, [2] Jerome Martinez, MSc [2]
Author Affiliations
[1.] Department of Social and Preventive Medicine, University of
Montreal, Montreal, QC
[2.] Institut national de sante publique du Quebec, Montreal, QC
[3.] Research Centre of the University of Montreal Hospital Centre,
Montreal, QC Correspondence: Dr. Nathalie Auger, Institut national de
sante publique du Quebec, 190, boulevard Cremazie Est, Montreal, QC H2P
1E2, Tel: 514-864-1600, ext. 3717, Fax: 514-864-1616, E-mail:
nathalie.auger@inspq.qc.ca
Table 1. Unadjusted Stillbirth Rate per 1000
Births According to Maternal Characteristics,
Quebec, 1981-2009
Total Births Rate (95%
(Stillbirths) Confidence
Interval)
Maternal
education,
years
<11 344,991 (1540) 4.5 (4.2-4.7)
11-13 921,760 (3203) 3.5 (3.4-3.6)
14-15 472,141 (1334) 2.8 (2.7-3.0)
[greater than 523,281 (1260) 2.4 (2.3-2.5)
or equal to]
16
Maternal age,
years
<20 99,650 (559) 5.6 (5.1-6.1)
20-24 508,911 (2204) 4.3 (4.2-4.5)
25-29 915,380 (3334) 3.6 (3.5-3.8)
30-34 636,408 (2425) 3.8 (3.7-4.0)
[greater than 247,336 (1388) 5.6 (5.3-5.9)
or equal to]
35
Legally married
Yes 1,333,240 (5042) 3.8 (3.7-3.9)
No 1,074,046 (4273) 4.0 (3.9-4.1)
Language
French 1,891,828 (7622) 4.0 (3.9-4.1)
English 197,068 (794) 4.0 (3.7-4.3)
Other 264,193 (1005) 3.8 (3.6-4.0)
Parity
0 1,097,214 (5611) 5.1 (5.0-5.2)
1 849,386 (2511) 3.0 (2.8-3.1)
[greater than 461,354 (1861) 4.0 (3.9-4.2)
or equal to]2
Period
1981-1989 782,106 (3991) 5.1 (4.9-5.3)
1990-1999 859,543 (3314) 3.9 (3.7-4.0)
2000-2009 766,305 (2678) 3.5 (3.4-3.6)
Total * 2,407,954 (9983) 4.1 (4.1-4.2)
* May not sum to total as missing data are not
presented.
Table 2. Relative Index of Inequality (RII) for Education and
Stillbirth by Period, Quebec, 1981-2009 *
RII (95% Confidence Interval)
All Periods 1981-1989 1990-1999
All causes 2.0 (1.8-2.2) 1.8 (1.8-2.2) 2.1 (1.8-2.4)
Placental abruption 2.6 (2.1-3.2) 2.5 (1.8-3.5) 3.0 (1.9-4.8)
Cord compression 2.0 (1.6-2.5) 1.9 (1.3-2.9) 1.7 (1.1-2.8)
Congenital anomalies 1.7 (1.3-2.3) 1.9 (1.3-2.9) 1.6 (1.1-2.5)
Other causes 2.2 (1.9-2.6) 1.8 (1.4-2.5) 2.3 (1.8-2.9)
Unspecified 1.7 (1.3-2.2) 1.3 (1.0-1.8) 1.7 (1.2-2.4)
p-value
([dagger])
RII (95% Con-
fidence In-
terval)
2000-2009
All causes 2.3 (2.0-2.8) 0.05
Placental abruption 2.3 (1.5-3.6) 0.7
Cord compression 2.6 (1.5-4.5) 0.4
Congenital anomalies 1.6 (1.0-2.5) 0.5
Other causes 2.8 (2.2-3.6) 0.03
Unspecified 2.2 (1.5-3.3) 0.04
* Associations for least vs. most educated, adjusted for maternal
age, parity, marital status and mother tongue; all-period models
additionally adjusted for period.
([dagger]) p-value for 1981-1989 vs. 2000-2009.
Table 3. Slope Index of Inequality (SII) for Education and Stillbirth
by Period, Quebec, 1981-2009 *
SII (95% Confidence Interval)
All Periods 1981-1989 1990-1999
All causes 2.5 (2.1-2.8) 2.8 (2.1-3.5) 2.3 (1.8-2.7)
Placental abruption 0.5 (0.4-0.6) 0.6 (0.4-0.8) 0.6 (0.4-0.7)
Cord compression 0.2 (0.2-0.3) 0.4 (0.2-0.6) 0.2 (0.0-0.3)
Congenital anomalies 0.2 (0.1-0.3) 0.5 (0.2-0.7) 0.1 (0.0-0.3)
Other causes 1.0 (0.9-1.2) 1.0 (0.5-1.5) 1.0 (0.7-1.3)
Unspecified 0.4 (0.2-0.6) 0.2 (-0.0-0.5) 0.4 (0.1-0.6)
p-value
([dagger])
SII (95% Con-
fidence In-
terval)
2000-2009
All causes 2.6 (2.0-3.1) 0.6
Placental abruption 0.3 (0.2-0.5) 0.04
Cord compression 0.3 (0.1-0.4) 0.2
Congenital anomalies 0.2 (0.0-0.4) 0.09
Other causes 1.1 (0.8-1.4) 0.8
Unspecified 0.7 (0.4-1.0) 0.02
* Difference between least and most educated, adjusted for maternal
age (<20, 20-34, [greater than or equal to]35 years) and parity (0,
[greater than or equal to]1) for convergence; all-period models
additionally adjusted for period.
([dagger]) p-value for 1981-1989 vs. 2000-2009.
