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BIRTH 42:1 March 2015
62
Higher Cesarean Delivery Rates are
Associated with Higher Infant Mortality Rates
in Industrialized Countries
Ri-hua Xie, BSc, MSc, PhD, Laura Gaudet, MD, MSc, Daniel Krewski, MHA, PhD, Ian D.
Graham, PhD, Mark C. Walker, MD, MSc, and Shi Wu Wen, MB, MSc, PhD
ABSTRACT: Background: Recent data indicate that more than half of high-income
industrialized countries have a cesarean delivery rate of > 25 percent, which is higher than
the appropriate level considered by most health professionals worldwide. Methods: Data for
31 high-income industrialized countries in 2010 (or the nearest year) obtained from the World
Health Organization, Organization for Economic Cooperation and Development, World Bank,
and individual countries were analyzed in this study. We examined the correlation between
cesarean delivery rate and infant mortality rate with Pearson correlation coefficient analysis,
and examined the independent effect of cesarean delivery on infant mortality with multiple
linear regression analyses. Results: The cesarean delivery and infant mortality rates varied
substantially among the included countries: from 15.6 to 50.0 percent and from 1.9 per to 6.8
per 1,000 live births, respectively. Cesarean delivery rates were positively correlated with
infant mortality rates (Pearson correlation coefficient: 0.41, p < 0.05). The association
remained after adjustment for maternal age, infant sex, per capita GDP, and the Gini index
(p < 0.03), but disappeared after further adjustment for preterm birth (p = 0.07). In a
sensitivity analysis, the results were not appreciably affected by excluding births at < 22 weeks
of gestation, by weighting the data by the number of births in each country, or by excluding
data from particular countries with possible measurement issues (USA, Greece). Conclusions:
A higher cesarean delivery rate is associated with higher infant mortality rate among these
high-income industrialized countries. One of the mechanisms by which cesarean delivery affects
infant mortality is through iatrogenic prematurity. (BIRTH 42:1 March 2015)
Key words: cesarean delivery, high-income countries, infant mortality
The rate of cesarean delivery has increased dramatically
in some industrialized countries (1). The World Health
Organization (WHO) suggested an upper limit of 15
percent on cesarean delivery at the country level (2),
which was considered appropriate in terms of maternal
and perinatal morbidity and mortality. In an analysis of
cesarean delivery rates in 119 countries for data
reported from 1991 to 2003, Althabe et al found that
Ri-Hua Xie is a Professor in the Department of Nursing at the Hunan
University of Medicine, Huaihua, China; Ri-Hua Xie is a Research
Associate at the McLaughlin Centre for Population Health Risk
Assessment, Institute of Population Health, University of Ottawa;
Laura Gaudet is an Assistant Professor at the OMNI Research
Group, Department of Obstetrics and Gynecology, Faculty of Medicine and Clinical Epidemiology Program, Ottawa Hospital Research
Institute, University of Ottawa; Daniel Krewski is a Professor and
Director at the McLaughlin Centre for Population Health Risk
Assessment, Institute of Population Health, University of Ottawa; Ian
D Graham is a Senior Scientist at the Clinical Epidemiology Program, Ottawa Hospital Research Institute; Mark C. Walker is a
Professor and Chair at the OMNI Research Group, Department of
Obstetrics and Gynecology, Faculty of Medicine and Clinical Epidemiology Program, Ottawa Hospital Research Institute, University of
Ottawa; Shi Wu Wen is a Professor at the OMNI Research Group,
Department of Obstetrics and Gynecology, Faculty of Medicine and
Clinical Epidemiology Program, Ottawa Hospital Research Institute,
University of Ottawa, Ottawa, ON, Canada.
The authors have no competing interests in relation to this manuscript.
Address correspondence to Shi Wu Wen, OMNI Research Group,
Department of Obstetrics and Gynecology, University of Ottawa, 501
Smyth Road, Box 241, Ottawa, ON, Canada K1H 8L6.
Accepted December 1, 2014
© 2015 Wiley Periodicals, Inc.
63
BIRTH 42:1 March 2015
most low-income countries had a cesarean delivery rate
of < 10 percent, while > 30 percent of the middle- and
high-income countries exceeded 20 percent (3). There
was a statistically significant negative linear correlation
between cesarean delivery rate and neonatal and infant
mortality in low-income countries, but no such association existed in middle- and high-income countries (3).
The most recently available data from the WHO indicate that more than half of high-income countries have
a cesarean delivery rate in excess of 25 percent (4). We
hypothesized that the cesarean delivery rate exceeding
a certain threshold may actually do more harm than
good overall (Fig. 1). Cesarean delivery performed for
unjustifiable medical reasons may adversely affect the
health and well-being of infants because it shortens
gestational duration (5), bypasses the normal birth canal
and normal labor processes which offer benefits to
newborns (6–8), and affects the initiation of breastfeeding and quality of breastmilk (9,10). In this study, we
thus analyze recently published data from the World
Bank, WHO, Organization for Economic Cooperation
and Development (OECD), and individual countries to
examine the association between cesarean delivery and
infant mortality in high-income industrialized countries.
Methods
Data Sources
High-income industrialized countries in this study were
defined according to the United Nations (11), and
OECD member countries. We set up strict inclusion
criteria to select countries that are both economically
and socially homogeneous to allow the attainment of
comparable data and to minimize the influence of confounding on the study results. Since the majority of
recently available data on cesarean delivery and other
important demographic and clinical information available from publicly accessible sources were for 2010,
we used 2010 data whenever possible. If 2010 data for
any of the included countries were not available, we
used data for 2011 or the nearest year. Besides data on
cesarean delivery and infant mortality, we collected
data on maternal age, infant sex, multiple pregnancy,
gross domestic product (GDP) per capita, Gini index,
and preterm birth, as previous studies suggested that
these are important determinants of perinatal health
service use and perinatal outcomes (3,12–16).
Cesarean delivery data for different countries were
abstracted primarily from WHO reports for 2008, 2009,
2010, and 2011 (4,17,18), and were supplemented by
OECD data for 2010 (19). Because of lack of cesarean
delivery data in the WHO and the OECD reports for
Greece, we used a separate published report on mode
of delivery available for that country (20). GDP per
capita was obtained from World Bank reports (21), and
Gini index was derived from a 2010 OECD report
(22). Data on maternal age, infant sex, and multiple
pregnancy were from the United Nations (23),
European Perinatal Health Report (24), the Centers for
Disease Control and Prevention (CDC) (25), Statistics
Canada (26), Australian Bureau of Statistics (27), and
Korean Statistical Information Service (28). Preterm
Cesarean delivery
For pregnancies
with complications
For pregnancies
without complications
BENEFICIAL
HARMFUL
Saving life
Shortening gestaon duraon
Reducing health sequelae from
vaginal birth
• Sequelae to the bodily organs
caused by hypoxia from
prolonged labor
• Sequelae to the bodily organs
caused by mechanical injuries
Increasing risk of infecons
Fig. 1. Effect of cesarean delivery on infant health.
Affecng lung health
Affecng breast-feeding
BIRTH 42:1 March 2015
64
birth rates for the year 2010 were abstracted from the
WHO reports (29). Infant mortality rates were from
WHO (30), supplemented by European Perinatal Health
Report (24), CDC (31), and Statistics Canada (32).
Statistical Analysis
All analyses were carried out using SAS PC statistical
software version 9 (SAS Inc., Cary, NC, USA). We
used country-specific medians, means, ratios, and rates
as summary measures for both risk factors and outcomes. We calculated Pearson correlation coefficients of
country-specific mean maternal age, infant sex ratio
(male:female), multiple pregnancy (per 1,000 pregnancy), GDP per capita, Gini index, and preterm birth
(%) rate with country-specific cesarean delivery rate (%)
and infant mortality rate (per 1,000 live births). We then
performed multiple linear regression analyses to examine the effect of cesarean delivery rate on infant mortality in the following models: 1) cesarean delivery as the
independent variable; 2) cesarean delivery, maternal
age, and infant sex as the independent variables; 3)
cesarean delivery, maternal age, infant sex, GDP per
capita, and Gini index as the independent variables; and
4) cesarean delivery, maternal age, infant sex, GDP per
capita, Gini index, and preterm birth as the independent
variables. Cesarean delivery was the main exposure in
this study and was enforced into all regression models.
Maternal age and infant sex are known risk factors of
infant mortality and are associated with cesarean delivery (12,13). GDP per capita is a measure of the average
wealth of the general population and the Gini index is a
measure of the distribution of wealth within the population: a Gini index of zero represents perfect and a Gini
index of 100 percent represents maximal inequality.
Both GDP per capita and the Gini index have been considered to be important determinants of perinatal health
service utilization and perinatal outcomes (3,15,16).
Maternal age, infant sex, GDP per capita, and Gini
index were associated with either cesarean delivery rate
or infant mortality rate in the univariate analysis, and
were therefore included in the regression models. Preterm birth is a major risk factor for infant mortality (5)
and it was associated with infant mortality rate in the
univariate analysis. We hypothesized that increased
cesarean delivery rates may be associated with increased
infant mortality rates through its influence on preterm
birth (Fig. 1). As a result, we included preterm birth
rate in the final multiple regression model. This stepwise approach was designed to help assess which potential variable(s) possibly explain the observed association
between cesarean delivery and infant mortality. Previous studies suggested a major difference in the reporting
of infant mortality in the United States versus other
countries (33). We have therefore performed supplementary analysis after excluding data from the United
States. Additional sensitivity analyses excluding births
< 22 weeks of gestation, data from Greece, and weighting data by the number of births in the included countries were also performed. Excluding births < 22 weeks
of gestation can help ensure data comparability in terms
of reporting infant mortality (33). Because cesarean
delivery rate for Greece was not reported in the WHO
or the OECD report like the other European countries,
data excluding Greece can help assess if bias was introduced by including data from another source. Some
ecological analyses have used the number of observations in each unit of analysis to weight while others did
not (34). Performing analysis with versus without
weighting can help assess which approach is better in
this particular analysis.
Results
The median cesarean delivery rate across included countries was 25.3 percent, ranging from 15.6 to 50.0 percent
(Table 1). The median infant mortality rate was 3.5 per
1,000 live births, ranging from 1.9 to 6.8 per 1,000 live
births (Table 1). The medians (ranges) for maternal age,
infant sex (M:F), multiple pregnancy, GDP per capita,
Gini index, and preterm birth were 30.1 (28.0–31.4),
1.06 (1.04–1.07), 16.8 per 1,000 women (13.4–27.4),
39,507 US dollars (12,302–102,009), 0.30 (0.24–0.38),
and 7.4 percent (5.5–12.0), respectively.
The country-specific cesarean delivery rate was positively correlated with infant mortality (Pearson correlation coefficient: 0.41, p < 0.05), infant sex, and the
Gini index, while infant mortality rate was positively
correlated with preterm birth rate but negatively correlated with maternal age and GDP per capita (Table 2).
The positive association between cesarean delivery
rate and infant mortality rate remained significant
(p = 0.03) after adjusting for maternal age, infant sex,
GDP per capita, and the Gini index through multiple
regression analysis. However, the association became
insignificant after preterm birth was added to the equation (p = 0.07). Adjusted R2 values indicated that about
14 percent of the variation in infant mortality rates
might be explained by cesarean delivery rates
(Table 3).
The positive association between cesarean delivery
rates and infant mortality rates was not attenuated when
data from the United States was excluded (Tables 2
and 3). Additional sensitivity analyses excluding births
< 22 weeks of gestation, excluding data from Greece,
and weighting data by number of births in the included
countries yielded similar results (data available on
request).
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Table 1. Cesarean Delivery Rate, Infant Mortality Rate, and Related Factors in 31 Industrialized Countries, 2010
Country
Australia
Austria
Belgium
Canada
Czech Rep.
Denmark
Estonia
Finland
France
Germany
Greece
Hungary
Iceland
Ireland
Israel
Italy
Japan
Korea, Rep.
Luxembourg
Netherlands
New Zealand
Norway
Poland
Portugal
Slovakia
Slovenia
Spain
Sweden
Switzerland
United Kingdom
United States
Cesarean
delivery (%)
Mean
maternal
age
Infant
sex ratio
(M:F)
Multiple pregnancy
(per 1,000 women)
GDP per
capita
(US $)
Gini
index
Preterm
birth (%)
Infant mortality
rate (per 1,000
live births)
31.5
28.3
19.9
27.8
24.1
21.0
20.3
16.1
21.0
32.1
50.0
32.8
16.6
26.3
19.9
38.5
23.3
35.2
25.7
15.6
23.6
17.1
33.7
35.8
28.7
18.2
25.3
16.9
32.8
23.8
32.8
30.70
29.80
29.80
29.60
29.60
30.60
29.20
30.20
30.00
30.40
30.30
29.30
30.00
31.40
30.10
31.30
31.20
31.26
30.80
30.80
28.80
30.10
28.80
29.80
28.60
30.10
31.20
30.70
31.20
29.50
28.00
1.06
1.05
1.05
1.05
1.06
1.06
1.06
1.04
1.05
1.06
1.07
1.06
1.05
1.07
1.05
1.06
1.06
1.07
1.05
1.06
1.06
1.06
1.06
1.06
1.05
1.05
1.06
1.06
1.05
1.05
1.05
15.60
17.20
20.00
16.80
21.00
20.90
14.70
15.30
17.40
18.50
N/A
N/A
14.30
16.80
N/A
15.00
N/A
27.40
18.30
17.70
17.00
16.40
13.40
15.10
14.50
18.50
20.20
14.00
18.40
15.50
16.50
51746
44723
42960
46212
18867
56486
14110
43846
39186
40145
25851
12750
39507
46492
30389
33761
43118
20540
102009
46468
32796
86156
12302
21382
16036
22898
29863
49360
70370
36703
48358
0.34
0.26
0.26
0.32
0.26
0.25
0.32
0.26
0.29
0.30
0.31
0.27
0.30
0.29
0.37
0.34
0.33
0.32
0.29
0.29
0.33
0.25
0.31
0.35
0.26
0.24
0.32
0.26
0.30
0.34
0.38
7.6
10.9
7.9
7.8
7.3
6.7
5.7
5.5
6.7
9.2
6.6
8.6
6.5
6.4
8.0
6.5
5.9
9.2
8.1
8.0
7.6
6.0
6.7
7.7
6.3
7.5
7.4
5.9
7.4
7.8
12.0
4.2
3.5
3.5
4.9
3.4
3.3
3.5
2.6
3.5
3.5
4.0
5.6
1.9
3.5
3.6
3.4
2.4
3.5
2.0
3.7
4.9
2.5
5.1
3.1
6.8
2.8
4.0
2.4
3.8
4.4
6.3
N/A = not available.
Discussion
Our analysis of data from 31 high-income countries
revealed that higher cesarean delivery rates were associated with higher infant mortality rates. To our knowledge, this is the first study that shows a positive
correlation between infant mortality and cesarean delivery at the country level.
In an earlier study using data from 1991 to 2003 in
119 countries, Althabe et al found that cesarean delivery was protective in low-income countries, with lower
neonatal and infant mortality in countries with cesarean
delivery rates > 10 percent as compared to countries
with cesarean delivery rates < 10 percent (3). However,
they did not find any association between cesarean
delivery rate and neonatal and infant mortality in highincome countries (3). In the time period covered by
Althabe’s study, about 30 percent of the high-income
countries had cesarean delivery rates > 20 percent and
only a few had a cesarean delivery rate > 30 percent
(3). In our study using data from 2010, more than half
of the high-income countries had a cesarean delivery
rate > 25 percent and three countries (Greece, Korea,
and Portugal) had rates > 35 percent. Our results suggest when the cesarean delivery rate in a country
becomes excessive, its benefits for infants decrease and
its risks increase. These results warrant consideration in
terms of optimizing perinatal health care. Recent studies
BIRTH 42:1 March 2015
66
Table 2. Pearson Correlation Coefficients of Study Variables with Cesarean Delivery Rate and Infant Mortality Rate in
Industrialized Countries, 2010
Cesarean
delivery rate
Cesarean delivery rate
1
Infant mortality rate
0.41*,†
0.39*,‡
Maternal age
0.01†
0.07‡
0.63**,†
0.55**,‡
Infant sex
0.43*,†
0.47*,‡
0.01†
0.07‡
Multiple
pregnancy
GDP per capita
0.10†
0.11‡
0.12†
0.11‡
0.25†
0.26‡
0.41*,†
0.49*,‡
Gini index
Preterm birth
0.39*,†
0.37*,‡
0.27†
0.12‡
0.29†
0.25‡
0.37*,†
0.17‡
*p < 0.05; **p < 0.01; †All 31 countries; ‡Excluding data from the United States.
Table 3. Results of Multiple Linear Regression Analysis of the Association between Cesarean Delivery Rates and Infant
Mortality Rate in Industrialized Countries, 2010
Regression coefficient (b)
for cesarean delivery
p for cesarean
delivery
Overall
adjusted R2
0.06
0.05
0.06
0.05
0.05
0.05
0.05
0.05
0.02
0.04
0.01
0.02
0.03
0.04
0.07
0.07
0.14
0.12
0.52
0.43
0.49
0.40
0.48
0.38
Model I: All countries
Excluding data from the United States
Model II: All countries
Excluding data from the United States
Model III: All countries
Excluding data from the United States
Model IV: All countries
Excluding data from the United States
Model I: independent variable included only cesarean delivery rate; Model II: independent variables included cesarean delivery rate, mean maternal age, and infant sex ratio (M:F); Model III: independent variables included cesarean delivery rate, mean maternal age, infant sex ratio (M:F),
GDP per capita, and Gini index; Model VI: independent variables included cesarean delivery rate, mean maternal age, infant sex ratio (M:F),
GDP per capita, Gini index, and preterm birth rate.
echo our arguments. Ye et al found that once the primary cesarean delivery rate reached 10 percent, a further increase in cesarean delivery rate had no influence
on maternal, neonatal, and infant mortality rates (35). In
another study, MacDorman et al found that for low-risk
women with no recorded indications for cesarean delivery, neonatal mortality risk was significantly higher for
cesarean than for vaginal births (36). Altogether, these
data suggest that there is room to reduce unnecessary
cesarean sections without hurting the infants.
Our study has several strengths. We have restricted
our study to the most recently available data among
high-income OECD countries with good data metrics,
thus minimizing the potential for misclassification of
risk factors and outcomes. The data are from publicly
available sources and collected according to a priori
criteria, and no country that had both cesarean delivery
and mortality data was excluded from analysis, thereby
reducing risk of selection bias. Also, since international
referral for obstetric care was rare, referral bias, frequently observed in inter-institutional and inter-regional
comparisons of health outcomes (37) are not applicable
here. Finally, sensitivity analyses excluding data from
the United States or Greece, births < 22 weeks of
gestation, and weighting data by number of births in
the included countries yielded similar results, indicating
the robustness of the observed association.
The limitations of our study should be acknowledged. First, although ecological analysis is an appropriate research design for multicountry studies of this
type (38), confounding can be a problem in ecological
comparisons (39). Some important determinants of both
the need for medically justified cesarean delivery and
perinatal health outcomes such as the use of assisted
reproductive technology were not available. However,
data from available countries suggest that differences in
these factors have a limited influence on the observed
variations (40). Second, differences in the definition
and classification of infant mortality could affect international comparisons (33). Third, because of the small
sample size, we were unable to include all important
independent variables in the multiple linear regression
analysis, precluding an in-depth analysis of potential
interactions among these variables.
Despite the limitations of an ecological study, it is
unlikely that potential differences in pregnancy complications and definition/classification of infant mortality
can explain the observed association between cesarean
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delivery rates and infant mortality rates, although differences in maternity care practices between countries
may have influenced the observed association. The
association between cesarean delivery rate and infant
outcomes appears to be a “U-shaped” distribution, with
increased mortality and morbidity risks when cesarean
delivery rates are either too high or too low. As illustrated in Fig. 1, the cesarean delivery rate is a summary
measure of cesareans performed to prevent or treat
pregnancy complications in specific, high-risk subpopulations (medically indicated) and cesareans performed
in a low-risk subpopulation (medically not indicated).
Cesarean delivery is an effective intervention to reduce
infant mortality and morbidity when it is medically
indicated. However, for healthy women without clear
medical or obstetrical indications for cesarean, the
potential risks of cesarean delivery may outweigh the
benefits (5–10,41–43). In addition, elective cesarean
delivery before the due date shortens gestational duration and might result in mild or moderate preterm or
early term births (5). Infants born mild or moderately
preterm (32 through 36 gestational weeks) are still at
increased risk of death (41), and for infants born at
term (> 37 weeks of gestation), the shorter the gestation period, the higher the infant mortality and morbidity rate (42,43). The influence of mild and moderate
preterm and early term births at the population level is
high because the numbers in these categories are much
larger than those with very preterm births. We found
when entering preterm birth as an independent variable
in one of the regression models, the association
between cesarean delivery rate and infant mortality rate
became insignificant. There are other mechanisms
through which cesarean delivery may adversely affect
infant health. Cesarean delivery bypasses the normal
birth canal and normal labor process that offers benefits
to the newborns. The makeup of the vaginal microbiome may play an important role in the newborn’s
health. The initial pioneer microbes entering the body
influence the pattern of microbial succession, which is
associated with the availability of colonization sites
(6,7). Since infants born by way of cesarean delivery
have less exposure to maternal and environmental
microorganisms (more likely benign and beneficial
ones) at birth, they may tend to have binding niches
for “latecomers” (more likely pathological ones). The
lung function of infants born by way of cesarean delivery may also be affected, and these infants may have
delayed postnatal removal of lung fluid (8). Furthermore, cesarean delivery may adversely affect a
women’s ability to breastfeed or the production and
quality of breastmilk (9,10), reducing the beneficial
effect of breastfeeding on infant’s health (44).
The general consensus among clinician-scientists and
professional organizations alike is that the current level
of cesarean delivery rate in many countries, especially
in the industrialized countries, is too high (45–49).
Despite the recent increase in maternal age and prevalence of co-existing medical conditions (such as obesity, hypertension, and diabetes) (50,51), the most
common indications for cesarean delivery in countries/
regions with high cesarean delivery rates continue to be
the somewhat subjective diagnoses of labor dystocia
and fetal distress (45–47).
In summary, we found that cesarean delivery rate is
associated with increased infant mortality in highincome industrialized countries. This finding suggests
the need to develop practical strategies to lower the
high cesarean delivery rates in many industrialized
countries in the interests of perinatal health.
Acknowledgments
Dr. Wen is a recipient of Mid-Career Award from
CIHR’s Institute for Gender-Ontario Women’s Health
Council. Dr. Krewski is the Natural Sciences and Engineering Research Council of Canada Chair in Risk Science at the University of Ottawa. Dr. Mark Walker is
supported by a University of Ottawa Tier 1 Chair in
Perinatal Epidemiology.
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