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Cesarean Delivery: Review

Cesarean Delivery and Cerebral Palsy


A Systematic Review and Meta-analysis
Michael OCallaghan,

PhD,

and Alastair MacLennan,

OBJECTIVE: To examine the association of cesarean


delivery and cerebral palsy using a systematic literature
review and meta-analysis.
DATA SOURCES: MEDLINE, Embase, and ClinicalTrials.
gov were systematically searched for articles relating to
cerebral palsy and cesarean delivery from inception until
December 2012. Only articles reporting confirmed cases of
cerebral palsy were included. Meta-analysis was used to
assess combined results and also the following subgroups:
emergency cesarean; elective cesarean; term delivery; preterm delivery; and delivery of breech-presenting newborns.
METHODS OF STUDY SELECTION: Literature searches
returned 1,874 articles with 58 considered in full. Studies
were selected if they reported an endpoint of cerebral
palsy, an intervention or risk of cesarean delivery, were in
English, and gave sufficient details to perform meta-analysis.
TABULATION, INTEGRATION, AND RESULTS: Nine
casecontrol and four cohort studies were included in
the overall analysis. Meta-analysis showed no overall
association of cesarean delivery with cerebral palsy (odds
ratio [OR] 1.29; 95% confidence interval [CI] 0.921.79;
3,810 case group participants and 1,692,580 control group
participants). Emergency cesarean delivery was associated
with increased risk of cerebral palsy (OR 2.17; 95% CI
1.582.98), whereas there was no significant association
between elective cesarean delivery and cerebral palsy
(OR 0.81; 95% CI 0.411.58). Any type of cesarean delivery
From the Discipline of Obstetrics and Gynaecology, School of Paediatrics and
Reproductive Health, Robinson Institute, University of Adelaide, Adelaide, South
Australia, Australia.
Supported by the Australian National Health and Medical Research Council
(grant no. 1019928) and CP Alliance Research Foundation.
The authors thank Michael Draper for designing the literature search strategy.
Correspondence to: Emeritus Professor Alastair MacLennan, Head of the
Australian Collaborative Cerebral Palsy Research Group, Robinson Institute,
Discipline of Obstetrics and Gynaecology, Womens & Childrens Hospital, University of Adelaide, South Australia, Australia; e-mail: alastair.maclennan@
adelaide.edu.au.
Financial Disclosure
The authors did not report any potential conflicts of interest.
2013 by The American College of Obstetricians and Gynecologists. Published
by Lippincott Williams & Wilkins.
ISSN: 0029-7844/13

VOL. 122, NO. 6, DECEMBER 2013

MB ChB, MD

(elective or emergency) for term newborns was associated


with cerebral palsy (OR 1.6; 95% CI 1.052.44), whereas
there was no association between any type of cesarean
delivery and cerebral palsy in preterm newborns (OR 0.81;
95% CI 0.471.40). Cesarean delivery did not significantly
modify cerebral palsy risk for breech-presenting newborns (OR 0.51; 95% CI 0.132.05).
CONCLUSION: A review of the literature does not
support the use of elective or emergency cesarean
delivery to prevent cerebral palsy.
(Obstet Gynecol 2013;122:116975)
DOI: 10.1097/AOG.0000000000000020

esarean delivery rates have increased over the


past 40 years from approximately 5% to more
than 30% in many industrialized countries without
any overall change in cerebral palsy rates, which
remain 22.5 per 1,000 deliveries.1,2 In particular,
cerebral palsy rates in those born at term have remained the same.3 Both elective cesarean delivery
before labor and emergency cesarean delivery during
labor have increased six-fold without affecting cerebral palsy rates.4 Fear of cerebral palsy litigation is
a major influence on the defensive decision-making
of the obstetrician to perform a cesarean delivery.5,6
This is despite modern research showing that the neuropathology of cerebral palsy is mostly established
antenatally and uncommonly in labor.710 There is
some evidence that cesarean delivery reduces the risk
of neonatal encephalopathy;11 however, most cases of
mild to moderate neonatal encephalopathy do not
result in cerebral palsy, and most cases of cerebral
palsy are not preceded by neonatal encephalopathy.12,13 Very few cases of cerebral palsy are likely
to have severe acute de novo intrapartum hypoxia
as the primary cause.8,10,14 Brain imaging of children
with cerebral palsy can show a wide variety of radiologically determined neuropathologies, which include
intraventricular hemorrhage in preterm newborns,
often leading to ventriculomegaly and secondary
white matter loss, developmental disorders, localized

OBSTETRICS & GYNECOLOGY

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Table 1. Summary of Studies Included

Year (Years
Assessed)

First Author

2010 (19672001)

Moster25

Norway

Not defined

Term

2010 (19902005)
2008 (19821990)

Kulak26
Nielsen27

Poland
Denmark

Not defined
Emergency

Term
Not defined

2005 (not stated)

Stelmach28

Estonia

Emergency

Not defined

2006 (19902000)
2004 (19841993)

Gurbuz29
Greenwood30

Turkey
United
Kingdom

Elective
Not defined
Elective

Not defined
Not defined
Term

Elective

Preterm, 32 wk of
gestation or less
Preterm, 3336 wk
of gestation
Preterm, less than
32 wk of gestation
Preterm, less than
32 wk of gestation
2428 wk of
gestation
Preterm, 2433 wk
of gestation

Country

Cesarean
Type

Elective
1995 (19841990)

Murphy31

United
Kingdom

Emergency
Elective

Gestational
Age

Presentation

Study Design

Not specified Population-based


follow-up
Not specified Casecontrol
Not specified Population-based
casecontrol
Not specified Matched
casecontrol
Not specified
Not specified Casecontrol
Not specified Casecontrol
Not specified
Not specified
Not specified Casecontrol
Not specified

1985 (19771982)

Kitchen32

Australia

Not defined

1998 (19781989)

OShea33

United States

Not defined

1999 (19791986)

Krebs34

Denmark

1985 (19711977)

Svenningsen35 Sweden

Not defined

Term

1974 (not stated)

Churchill36

Not defined

2011 (19902005)

OCallaghan20 Australia

Preterm, less than


36 wk of gestation
Not defined
Not specified Casecontrol
Not defined
Not specified
Less than 37 wk of
gestation

United States

Term

Emergency
Elective
Not defined

Not specified Cohort


Not specified Casecontrol
Not specified
Breech
Population-based
casecontrol
Breech
Long-term
follow-up
Not specified Cohort

CP, cerebral palsy; OR, odds ratio; CI, confidence interval; GA, gestational age.

unilateral cerebral infarction after cerebral artery


thrombosis, evidence of damage from antenatal infection, and periventricular leukomalacia. The latter can
be attributable to a variety of causes, including
chronic or acute hypoxia. Potential genetic causes also
may contribute to many of the cerebral palsy pathologies.15,16
The aim of this literature review was to examine
the association of cerebral palsy and cesarean delivery
conducted electively or after labor had commenced in
newborns born at term or prematurely and in those
presenting breech.

SOURCES
The search strategy considered only full articles published in English. Articles published until December

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OCallaghan and MacLennan

2012 were searched using Embase, ClinicalTrials.gov,


and PubMed (MEDLINE) databases (see Appendix 1,
available online at http://links.lww.com/AOG/A446
for details of search terms).

STUDY SELECTION
Relevant references cited within these articles were
also selected. For inclusion, articles needed to report
cerebral palsy as an endpoint with cesarean delivery
as a risk factor and provide sufficient details for
inclusion in a meta-analysis. The review did not
include cases in which a confirmed neurologic diagnosis of cerebral palsy was absent. Articles undergoing full-text review were considered for inclusion by
both authors and discrepancies were resolved by
discussion. Data were extracted from articles using

Cesarean Delivery and Cerebral Palsy

OBSTETRICS & GYNECOLOGY

Case Definition
CP diagnosis in
benefits record
CP diagnosed at
age 25 y
Spastic CP
CP diagnosis

CP diagnosis at
age 2 y
CP diagnosis at
age 5 y

On CP register,
age 35 y

No. of Children With


CP Delivered by
Cesarean/Total No.
of Children With CP
279/1,938
56/213
87/271
17/153

Control Definition
Singletons born
19672001
Non-CP
Non-CP
From birth register,
matched

No. of Children in the


Control Group Delivered
by Cesarean/Total No. of
Children in the Control Group

OR

120,793/1,680,503

2.17

50/280

1.6

1.042.47

51/217
8/268

1.7
4.3

1.092.65
1.7610.5
1.135.68
0.973.03

95% CI
1.92.5

17/153
26/101

Non-CP

13/268
46/308

2.54
1.7

10/126

Non-CP

12/290

2.6

1.16.3

12/73
11/36
12/59

Non-CP
Non-CP
Selected from population
birth register

114/286
15/70
19/234

0.3
2
2.7

0.20.7
0.85.3
1.26.1

98/234
26/144
57/80 (not GA-matched)
44/80 (GA-matched)
6,145/8,076

0.3
1.3
1.3
1.8
1.2

0.20.7
0.394.26
0.72.3
1.03.4
0.43.3

191/626

5.92

0.711.10

2/44

3.97

0.6929.7

189/848

2.43

1.893.13

124/780

1.39

1.01.94

27/60

1.52

0.832.81

CP at age 2 y
CP at age 1 y

10/59
4/18
59/160

CP on register

13/18

CP at 2-y
follow-up

1/13

CP at 1-y
follow-up

7/44

CP diagnosis
on register
CP diagnosis
on register

175/426

Non-CP, breechpresenting
newborns
Non-CP, breechpresenting
newborns
Matched by GA,
birth weight, place
of birth; non-CP
Non-CP

66/317

Non-CP

Non-CP
Non-CP

126/227

a standardized form and were checked by both


authors. Data extracted included title, authors, date
of publication, country, study design, type of cesarean
delivery (emergency defined as after labor had
commenced; elective defined as planned more than
24 hours before delivery), indication for cesarean
delivery, outcome measure, length of follow-up,
number of participants with cerebral palsy delivered
by cesarean, number of comparison participants
delivered by cesarean, cerebral palsy description,
gestational age included, presentation at time of
delivery, and multiplicity. Study quality was assessed
using a modified Newcastle Ottawa Scale17 for nonrandomized studies in meta-analyses.
Meta-analysis was conducted using Review Manager Software 5.1. Fixed-effects analysis was used
when there was no evidence for heterogeneity (P..05,

VOL. 122, NO. 6, DECEMBER 2013

x2 test; I2 also reported), and a random-effects analysis


was used when heterogeneity was significant
(I2.30%). Funnel plots were used to assess publication bias for each meta-analysis. Subgroup analysis
included cesarean delivery described as either elective
or emergency, gestational age subgroups, and
cephalic or breech presentation. Outcomes are reported as odds ratios (ORs) with 95% confidence intervals (CIs).

RESULTS
Searching PubMed, ClinicalTrials.gov, and Embase
returned a total of 1,874 articles after removal of
duplicates. Fifty-eight articles were considered in-full,
with 13 articles retained for inclusion in the analysis.
Figure 1 outlines the selection process that left 13 articles for inclusion in the analysis. Characteristics of

OCallaghan and MacLennan

Cesarean Delivery and Cerebral Palsy

1171

Articles retrieved from


PubMed and Embase
N=2,510
Duplicates removed: n=647
Remaining articles
n=1,874

Articles excluded: n=1,822


Reviews, editorials, case
reports, case series, letters,
and observational reports: 50
Not in English: 22
No cesarean intervention or
cerebral palsy endpoint: 1,750

Remaining articles
n=41
Articles added
(identified in references): n=17
Remaining articles
for review
n=58

Articles included
n=13

Articles excluded after fulltext assessement. No cerebral palsy


endpoint, individual outcome
numbers not reported, cesarean
intervention grouped with other
interventions: n=45

Fig. 1. Flow diagram of search.


OCallaghan. Cesarean Delivery and Cerebral Palsy. Obstet Gynecol 2013.

these studies are presented in Table 1. Meta-analysis


showed no overall association of cesarean delivery with
cerebral palsy (Fig. 2A; OR 1.29; 95% CI 0.921.79;
I2586%). Emergency cesarean delivery was associated
with increased risk of cerebral palsy (Fig. 2B; OR 2.17;
95% CI 1.582.98; I2542%). Elective cesarean delivery
was not associated with a significant reduction in cerebral palsy (Fig. 2C; OR 0.81; 95% CI 0.411.58;
I2586%). Neonates born at term were more likely to
have cerebral palsy when delivered by any type of
cesarean (Fig. 2D; OR 1.6; 95% CI 1.052.44), whereas
those born preterm were less likely to have cerebral
palsy when delivered by cesarean, although not significantly (Fig. 2E; OR 0.81; 95% CI 0.471.40; I2555%).
Breech-presenting newborns were not statistically less
likely to have cerebral palsy when delivered by cesarean (Fig. 2F; OR 0.51; 95% CI 0.132.05; I2541%).
Funnel plots of each analysis showed moderate
asymmetry, suggesting possible publication bias,
with the exception of elective cesarean delivery
(Appendix 2, available online at http://links.lww.
com/AOG/A447). Statistical tests for asymmetry
were not possible because of the low number of individual studies included.

CONCLUSION
Overall, cesarean delivery is not associated with
a reduced risk of cerebral palsy, whether the cesarean
be elective or emergency. This meta-analysis does not
support an overall increase or decrease in the risk of
cerebral palsy with cesarean delivery (OR 1.29; 95%

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OCallaghan and MacLennan

CI 0.921.79). The analysis included a total of 3,810


cerebral palsy case group participants and 1.7 million
control group participants taken from 13 separate
studies. Because cesarean delivery is performed for
a variety of reasons, subanalysis was performed to
consider more detailed classifications.
Emergency cesarean delivery was associated with
an increased risk of cerebral palsy (OR 2.17; 95% CI
1.582.98). Emergency cesarean delivery is usually
defined as being performed once labor has commenced and may be indicated for a variety of fetal
or maternal reasons. Because some of these indications may be risk factors for cerebral palsy,18,19 the
association seen may represent confounding by indication. None of the studies examined provided details
about the indication for cesarean delivery. This analysis did not provide evidence supporting elective
delivery to reduce the likelihood of cerebral palsy
(OR 0.81; 95% CI 0.411.58). This subanalysis
included 764 case group participants and 1,928 control group participants. Again, the reasons for cesarean delivery before labor are varied, were not
documented, and could confound the results. Newborns delivered by cesarean delivery at term were
more likely to have cerebral palsy (OR 1.6; 95% CI
1.052.44), a result possibly confounded by indication
for delivery type. Newborns delivered preterm had
a lower risk of cerebral palsy, although this was not
statistically significant (OR 0.81; 95% CI 0.471.40).
More individuals with cerebral palsy are born at
term,2 although early gestational age is a particular
risk factor for cerebral palsy.20 The six studies assessing cesarean delivery in preterm newborns used varying criteria to define preterm (less than 36, 2428, less
than 32, and 2433 weeks of gestation), and this complicates the interpretation of the findings. Analysis of
studies only reporting preterm birth as less than 33
weeks of gestation showed a significant reduction in
cerebral palsy (OR 0.52; 95% CI 0.380.70), but this
subanalysis was not prespecified and included only
small numbers. Larger studies focusing on individual
subgroups (eg, less than 32 weeks of gestation and less
than 36 weeks of gestation) will provide more robust
evidence for changes in clinical practice. It is plausible
that cesarean delivery may protect against cerebral
palsy, because in the very preterm neonate a common
pathway to the neuropathology that later causes cerebral palsy is early neonatal intraventricular hemorrhage.18 This occurs in the well-vascularized
neuronal glial precursor cells of the germinal matrix
and disruption to cerebral blood flow and intraventricular blood clotting can block cerebral spinal fluid
circulation, causing ventriculomegaly and subsequent

Cesarean Delivery and Cerebral Palsy

OBSTETRICS & GYNECOLOGY

Study or
Subgroup

Cases
Control
Odds Ratio
Odds Ratio
Events Total Events
Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
A. Cesarean delivery and cerebral palsy (overview)
44
2
44
3.0% 3.97 (0.7820.33)
7
Churchill, 1974
646
141
9.6% 0.59 (0.390.88)
33 235
Greenwood, 2004
308
46
8.7% 1.97 (1.143.41)
26 101
Gurbuz, 2006
144
26
18
4.6% 1.30 (0.394.26)
4
Kitchen, 1985
8,076
6,145
18
5.4% 0.82 (0.292.29)
13
Krebs, 1999
280
50
9.5% 1.64 (1.072.53)
56 213
Kulak, 2010
279 1,938 120,793 1,680,503 11.1% 2.17 (1.912.47)
Moster, 2010
234
117
59
8.4% 0.59 (0.331.07)
22
Murphy, 1995
217
51
9.7% 1.54 (1.032.31)
87 271
Nielsen, 2008
1,154
313
587
10.8%
1.87 (1.522.31)
241
OCallaghan, 2011
80
44
8.7% 0.48 (0.280.82)
59 160
OShea, 1998
268
21
153
8.4% 3.36 (1.876.04)
34
Stelmach, 2005
626
191
13
2.1% 0.19 (0.021.47)
1
Svenningsen, 1985
Subtotal (95% CI)
3,810
1,692,580 100.0% 1.29 (0.921.79)
Total events
862
127,940
Heterogeneity: Tau2= 0.25; Chi2
=87.82, df=12 (P< .001); I2=86%
Test for overall effect: Z=1.49 (P=.14)

B. Emergency cesarean and cerebral palsy


12
59
234 12.7%
Murpy, 1995
19
87 271
217 30.6%
Nielsen, 2008
51
1,154 45.7%
OCallaghan, 2011 175 587
189
17 153
268 10.9%
Stelmach, 2005
8
Subtotal (95% CI)
1,070
1,873 100.0%
Total events
291
267
Heterogeneity: Tau2= 0.04; Chi2=5.20, df=3 (P=.16); I2=42%
Test for overall effect: Z=4.80 (P< .001)
C. Elective cesarean and cerebral palsy
141
33 235
Greenwood, 2004
98
10
59
Murphy, 1995
124
66 587
OCallaghan, 2011
13
17 153
Stelmach, 2005

27.2%
646
22.4%
234
28.4%
1,154
22.0%
268
2,302 100.0%

2.89 (1.316.36)
1.54 (1.032.31)
2.17 (1.712.75)
4.06 (1.719.65)
2.17 (1.582.98)

0.59 (0.390.88)
0.28 (0.140.59)
1.05 (0.771.44)
2.45 (1.165.20)
0.81 (0.411.58)

Subtotal (95% CI)


1,034
Total events
126
376
Heterogeneity: Tau2= 0.39; Chi2=21.36, df=3 (P< .001); I2=86%
Test for overall effect: Z=0.63 (P=.53)
D. Term cesarean delivery and cerebral palsy
Greenwood, 2004
290 15.1%
12
10 126
Krebs, 1999
11.9%
8,076
6,145
18
13
Kulak, 2010
280 29.0%
50
56 213
Moster, 2010
279 1,938 120,793 1,680,503 40.1%
Svenningsen, 1985
3.9%
626
191
13
1
1,689,775 100.0%
Subtotal (95% CI)
2,308
Total events
359
127,191
Heterogeneity: Tau2= 0.11; Chi2=10.18, df=4 (P=.04); I2=61%
Test for overall effect: Z=2.18 (P=.03)

2.00 (0.844.75)
0.82 (0.292.29)
1.64 (1.072.53)
2.17 (1.912.47)
0.19 (0.021.47)
1.60 (1.052.44)

E. Preterm cesarean delivery and cerebral palsy


44
2
44
7.7% 3.97 (0.7820.33)
Churchill, 1974
7
235
129
646
21.3% 0.43 (0.270.70)
Greenwood, 2004
23
18
26
144
11.5% 1.30 (0.394.26)
Kitchen, 1985
4
59
117
234
19.6% 0.59 (0.331.07)
Murphy, 1995
22
227
27
60
19.8% 1.52 (0.862.70)
OCallaghan, 2011 126
160
44
80
20.2% 0.48 (0.280.82)
OShea, 1998
59
1,208 100.0% 0.81 (0.471.40)
Subtotal (95% CI)
743
Total events
241
345
Heterogeneity: Tau2= 0.31; Chi2=18.55, df=5 (P=.002); I2=73%
Test for overall effect: Z=0.75 (P=.45)

Fig. 2. Cesarean delivery metaanalysis.


OCallaghan. Cesarean Delivery and
Cerebral Palsy. Obstet Gynecol 2013.

F. Breech presentation cesarean delivery and cerebral palsy


Krebs, 1999
13
18
6,145
8,076 67.6% 0.82 (0.292.29)
Svenningsen, 1985
1
13
191
626 32.4% 0.19 (0.021.47)
Subtotal (95% CI)
31
8,702 100.0% 0.51 (0.132.05)
14
6,336
Total events
Heterogeneity: Tau2= 0.47; Chi2=1.69, df=1 (P=.19); I2=41%
Test for overall effect: Z=0.95 (P=.34)

Test for subgroup differences: Chi2=16.39, df=5 (P=.006); I2=69.5%

pressure on and thinning of white matter. The microvasculature of the germinal matrix is frail, and possibly
the potentially less traumatic, less hypoxic, and shorter
cesarean delivery may lead to less neonatal intraventricular hemorrhage and subsequently less cerebral palsy.
Most of the studies in this meta-analysis precede the

VOL. 122, NO. 6, DECEMBER 2013

0.01 0.1
Favors
interventions

10
100
Favors
control

recent introduction of maternal magnesium sulphate to


reduce cerebral palsy risk in the very preterm.21
There also are supporting data to suggest that
cesarean delivery reduces both the incidence of
intraventricular hemorrhage and its severity in very
preterm newborns.22,23 Thus, more studies are

OCallaghan and MacLennan

Cesarean Delivery and Cerebral Palsy

1173

merited to elucidate whether cesarean delivery should


be considered as an option when delivery of the very
preterm newborn is inevitable or required.
Strengths of this analysis are the systematic
identification of all relevant published studies and
their meta-analysis. The studies identified came from
diverse populations and the I2 value identified heterogeneity in all meta-analysis. This heterogeneity may
be the result of differing cerebral palsy diagnoses criteria between articles (eg, diagnosis at 1 or 5 years of
age), different selection strategies for control group
participants in the casecontrol studies, insufficient
reporting of cesarean delivery type, differing indications for cesarean delivery, or different criteria defining emergency cesarean delivery, elective cesarean
delivery, term, and preterm. The most common study
design of publications included in our analysis was
casecontrol. One population-based cohort study
was included, and further studies of this type would
be a valuable addition to the literature. Subanalyses
by gestational age were not appropriate for subgroups
of emergency or elective cesarean delivery because
the number of studies was low. Our results show
increased risk for cerebral palsy outcome in association with emergency cesarean delivery, with the likely
confounding that acute or chronic fetal compromise
will often precipitate this intervention. However, no
protective effect was shown for elective cesarean
delivery. The meta-analyses did not include one large
study (individual numbers allowing meta-analysis
were not provided)24 that reported similar findings
in term newborns. Elective cesarean delivery was
not associated with a decreased risk of cerebral palsy
(OR 1.01; 95% CI 0.751.37), whereas emergency
cesarean delivery was associated with an increased
risk (OR 1.80; 95% CI 1.621.99). Our analysis of
cesarean delivery for breech-presenting newborns
included only two studies and did not uncover any
significant associations (OR 0.51; 95% CI 0.221.19).
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Harold A. Kaminetzky Award


The American College of Obstetricians and Gynecologists (the College) and Obstetrics & Gynecology
have established the Harold A. Kaminetzky Award to recognize the best paper from a non-U.S.
researcher each year.
Dr. Harold A. Kaminetzky, former College Secretary and President, as well as Vice President,
Practice Activities, has had a long career as editor of major medical journals. His last editorship
was as Editor of the International Journal of Gynecology and Obstetrics. Dr. Kaminetzky has also had a
long interest in international activities.
The Harold A. Kaminetzky Award winner will be chosen by the editors and a special committee
of former Editorial Board members. The recipient of the award will receive $2,000.
Read the journal online at www.greenjournal.org

VOL. 122, NO. 6, DECEMBER 2013

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