DOI: 10.1111/1471-0528.

14938 Systematic review

www.bjog.org

What is the safest mode of birth for extremely

preterm breech singleton infants who are
actively resuscitated? A systematic review and
meta-analyses
M Grabovac,a JN Karim,a T Isayama,b,c S Korale Liyanage,a SD McDonalda,b,d
a
Department of Obstetrics & Gynecology, McMaster University, Hamilton, ON, Canada b Department of Health Research Methods, Evidence,
and Impact, McMaster University, Hamilton, ON, Canada c Neonatal Intensive Care Unit, Sunnybrook Health Sciences Centre, Toronto, ON,
Canada d Department of Radiology, McMaster University, Hamilton, ON, Canada
Correspondence: Dr M Grabovac, Department of Obstetrics and Gynecology, McMaster University, 1280 Main Street West, HSC 3N52G,
Hamilton, Ontario, Canada L8S 4K1. Email marinela.grabovac@medportal.ca

Accepted 27 August 2017. Published Online 2 November 2017.

Background The safest delivery mode of extremely preterm breech
singletons is unknown.
Objectives To determine safest delivery mode of actively
resuscitated extremely preterm breech singletons.
Search strategy We searched Cochrane CENTRAL, MEDLINE,
EMBASE, CINAHL and ClinicalTrials.gov from January 1994 to
May 2017.
Selection criteria We included studies comparing outcomes by
delivery mode in actively resuscitated breech infants between 23+0
and 27+6 weeks.
Data collection and analysis We synthesised data using random
effects, generated odds ratios, 95% confidence intervals and
number-needed-to-treat (NNT). Our primary outcomes were
death (neonatal, before discharge, or by 6 months) and severe
intraventricular haemorrhage (grades III/IV), stratified by
gestational age (23+0–24+6, 25+0–26+6, 27+0–27+6 weeks).
Main results We included 15 studies with 12 335 infants. We
found that caesarean section was associated with a 41% decrease
in odds of death between 23+0 and 27+6 weeks [odds ratio (OR)
0.59, 95% CI 0.36–0.95, NNT 8], with the greatest decrease at
23+0–24+6 weeks (OR 0.58, 95% CI 0.44–0.75, NNT 7). The OR at
25+0–26+6 and 27+0–27+6 weeks were 0.72 (95% CI 0.34–1.52) and
2.04 (95% CI 0.20–20.62), respectively. We found that caesarean
section was associated with 49% decrease in odds of severe
intraventricular haemorrhage between 23+0 and 27+6 weeks (OR
0.51, 95% CI 0.29–0.91, NNT 12), whereas the OR at 25+0–26+6
and 27+0–27+6 was 0.29 (95% CI 0.07–1.12) and 0.91 (95% CI
0.27–3.05), respectively.
Conclusions Caesarean section was associated with reductions in
the odds of death by 41% and of severe intraventricular
haemorrhage by 49% in actively resuscitated breech singletons
< 28 weeks of gestation. The data are mostly observational, which
may be inherently biased, and scarce on other morbidities,
necessitating thorough discussion between parents and clinicians.
Keywords Breech, caesarean section, extreme prematurity,
periviable, vaginal delivery.
Tweetable abstract Caesarean section associated with lower odds
of death and severe intraventricular haemorrhage in actively
resuscitated breech singletons <28 weeks.

Please cite this paper as: Grabovac M, Karim JN, Isayama T, Korale Liyanage S, McDonald SD. What is the safest mode of birth for extremely preterm
breech singleton infants who are actively resuscitated? A systematic review and meta-analyses. BJOG 2018;125:652–663.

common in early gestation, occurring in 30–35% of fetuses

Introduction
Preterm birth (PTB) is the leading cause of infant mortality
worldwide. Extreme PTB, defined as birth before 28 weeks
of gestation, represents 5% of PTB but contributes dispro-
portionately to the sequelae of PTB.1,2 Breech is more
between 22 and 28 weeks.3,4
The Term Breech Trial demonstrated that caesarean sec-
tion is the safest mode of delivery at term, with three times
lower risk of death or serious morbidity than vaginal
birth.5 In 1978, Ingemarsson et al.6 found that delivery by

652 ª 2017 Royal College of Obstetricians and Gynaecologists


caesarean section decreased the frequency of neonatal mor-
tality from 14.6 to 4.8% in infants who were born preterm
between 28 and 36+6 weeks of gestation. However, the
safest mode of delivery for preterm and extremely preterm
breech infants remains controversial.
None of the existing guidelines explicitly discuss mode
of delivery of extremely premature infants. The World
Health Organization and Royal College of Obstetricians
and Gynaecologists do not advise routine caesarean section
for preterm infants regardless of presentation.7,8 In con-
trast, the National Institute of Health and Care Excellence
guideline recommends consideration of caesarean section
for all women in preterm labour with a singleton breech
fetus.9 The 2016 American Congress of Obstetricians and
Gynecologists and Society for Maternal–Fetal Medicine’s
Obstetric Care Consensus on Periviable Birth do not rec-
ommend routine caesarean section for periviable delivery.10
The guidelines of the American Congress of Obstetricians
and Gynecologists11 and the Society of Obstetricians and
Gynecologists of Canada12 do not discuss mode of delivery
of preterm breech infants.
Given that active resuscitation is increasingly being con-
sidered at earlier gestations, the objective of this systematic
review was to determine the safest mode of delivery of
extremely preterm breech singleton infants born before
28 weeks of gestation, who are actively resuscitated.
Methods
We followed the Cochrane Handbook for Systematic
Reviews of Interventions (Version 5.1.0)13 and the PRISMA
statement.14 We registered the details of the protocol for
this systematic review on PROSPERO (CRD42016046682).
Information sources and search strategy
We searched five databases: Cochrane CENTRAL, MED-
LINE, EMBASE, CINAHL and ClinicalTrials.gov from Jan-
uary 1994 to May 2017, with the assistance of an
experienced research librarian (see Appendix S1). We con-
sulted Maternal–Fetal Medicine and Neonatology experts
for their knowledge of other studies published in this area.
We searched the references of included studies for addi-
tional articles. We imported all citations into bibliographic
software (ENDNOTE X7).15
Eligibility
We included all published randomised controlled trials
(RCT) and observational studies (cohort and case–control)
without language restrictions, which examined outcomes in
extremely preterm breech singleton infants, born by cae-
sarean section or vaginal delivery. We excluded other types
of publications (e.g. reviews, editorials, commentaries, case
studies, conference proceedings, studies published only as
ª 2017 Royal College of Obstetricians and Gynaecologists
Mode of delivery for extremely preterm breech singletons
abstracts), studies without sufficient data, duplicated stud-
ies or studies with systematic differences between the expo-
sure groups that would affect outcomes.
Our primary outcomes were either death before dis-
charge from the hospital, neonatal mortality or death by
6 months corrected age, depending on the death outcome
reported by the primary study. Our other primary outcome
was severe intraventricular haemorrhage (IVH grades III or
IV based on Papile’s grading) given the potential serious
long-term neurological developmental sequelae.16 We only
included actively resuscitated infants, as inclusion of infants
who did not receive active resuscitation could bias the
results in favour of caesarean section. We chose high-
income settings for our primary research question, as they
consistently offer resuscitation to infants ≥25 weeks of ges-
tation, and we explored low- or middle-income countries
as a secondary research question.17 We stratified primary
outcomes by preplanned gestational age categories: 22+0–
24+6, 25+0–26+6 and 27+0–27+6 weeks. However, as there
was only one infant in the 22+0–22+6-week category, we
amended the overall population to 23+0–27+6 weeks and
the individual category to 23+0–24+6 weeks.
We contacted authors for confirmation of active resusci-
tation, antenatal corticosteroids (ANCS) use and outcomes
stratified by gestational age (further detail in the Table S2).
Since the guidelines on the use of ANCS were published in
1994, for clinical relevance, we selected 1994 as the starting
point for literature searches.18
We selected outcomes based on the Grading of Recom-
mendations Assessment, Development, and Evaluation
(GRADE) system, depending on hierarchy of outcomes
and their importance in clinical decision-making, and
focusing on common major morbidities and long-term
outcomes.19
Our secondary infant outcomes were death before dis-
charge/neonatal mortality and severe IVH stratified by
birthweight categories (<500 g, 500–999 g, 1000–1500 g).
At the initial counselling and decision-making with future
parents, birthweight is often not available, nor is it always
reliable in very early gestation, hence, outcomes by birth-
weight were secondary outcomes.
Our main maternal outcome was mortality due to deliv-
ery complications. The full list of secondary infant out-
comes and maternal outcomes is detailed in the Table S3.
Data extraction
Two reviewers (MG and JK) independently screened the
titles and abstracts, and full texts. To assess inter-reviewer
agreement on study inclusion, we used the per cent agree-
ment due to limitations with the j statistics (low jdespite
high agreement). Using a piloted data collection form, we
extracted data on study characteristics, bias assessment and
outcomes. Discrepancies between reviewers were resolved
653
 Grabovac et al.
through discussion and consensus, and a third reviewer
(SDM) as necessary.
Risk of bias assessment
Each reviewer independently assessed the risk of bias by
using the Cochrane Collaboration’s tool for RCTs13 and a
modified Newcastle–Ottawa Scale (NOS)20 for observa-
tional studies. The NOS includes three categories, Selection,
Comparability and Outcomes, to assess bias. We modified
the Selection category, removing both 1. ‘Ascertainment of
exposure’, since our exposures of interest were all obtained
through medical records, and 2. ‘Demonstration that the
outcome of interest was not present at the start’, as out-
comes would not be present at the time of the caesarean
section/vaginal birth, but rather only afterwards. In addi-
tion to addressing the most important confounder by
requiring active resuscitation in our inclusion criteria, we
also addressed another key confounder by limiting the pop-
ulation to singletons only. Hence, for the Comparability
category, in consultation with a maternal–fetal medicine
expert (SDM) and neonatologist (TI), we considered the
presence of intrauterine growth restriction (IUGR), ANCS
and chorioamnionitis as the other important confounders.
Two points were awarded if any two of the three con-
founders were controlled for or excluded. For our primary
outcomes of death and severe IVH, we modified the Out-
comes category of the NOS by removing the item assessing
whether follow up was long enough. The modified scale
awarded a maximum of six points, which was considered
a high-quality study. We planned to assess publication bias
with a funnel plot for outcomes with ten or more
studies.21
Summary measures and data synthesis
As we included only one RCT with limited data, in consul-
tation with a biostatistician, we quantitatively summarised
data together with the observational studies.22 We used
random-effects models to perform the meta-analyses as
between-study heterogeneity was expected. We generated
summary effects estimates using odds ratios (OR) and 95%
confidence intervals. We planned to pool and separately
analyse the unadjusted and adjusted odds ratios reported
by the included studies. Analyses were peformed using
REVIEW MANAGER (RevMan) Version 5.3.23 We used the I2
statistic to assess heterogeneity with I2 values of 0–40%
considered to be low, 30–60% moderate, 50–90% substan-
tial and 75–100% considerable.13
We calculated the number-needed-to-treat (NNT), i.e.
the expected number of women required to deliver by cae-
sarean section, rather than vaginally, for one woman to
avoid infant death or severe IVH. We used the formula as
per the Cochrane handbook for calculating NNT.13
654
Risk of bias across studies
We used the GRADE system to assess the confidence that
an effect size of a certain outcome is close to the interven-
tion’s true effects, which determines the quality of a body
of evidence. GRADE rates the quality of evidence for each
outcome as high, moderate, low or very low. RCTs start as
high-quality evidence and observational studies as low-
quality evidence, and then we either downgraded (RCTs
and observational) or upgraded (observational) the studies.
GRADE downgrades the quality of evidence in the presence
of risk of bias, inconsistency, indirectness, imprecision and
publication bias.24–29 GRADE recommends upgrading the
quality of evidence if a large effect size was present, and if
all plausible confounding would minimise the demon-
strated effect; a dose–response relationship was not applica-
ble in our meta-analyses. We used GRADEpro GDT
software.19
Subgroups and sensitivity analyses
We planned subgroup analyses for IUGR, the use of ANCS
and clinical chorioamnionitis, as we considered them sig-
nificant potential sources of heterogeneity. We planned two
sensitivity analyses to remove studies that excluded intra-
partum intrauterine fetal demise and studies with a NOS
score below six.
Results
Literature search
Our electronic searches generated 3294 articles (Med-
line = 1068, EMBASE = 1890, CINAHL = 255, Cochrane
Central = 81, ClinicalTrials.gov = 0). After duplicate
removal (n = 1130), two reviewers independently assessed
2164 titles and abstracts. We selected 154 articles for full
text review and identified an additional 31 articles from
references. We had an initial agreement for full text inclu-
sion of 86% between the two reviewers. If it was not stated
in the primary study (n = 46), we contacted authors to
determine outcomes for actively resuscitated infants, by
gestational age or birthweight, and information on stan-
dard use of antenatal corticosteroids if before the 1994
guidelines (Figure 1). We included a total of 15 studies,
from the USA (3),30–32 France (2),33,34 England,22 Italy,35
Sweden,36 Germany,37 Turkey,38 Canada,39 Australia,40 Tri-
nidad and Tobago,41 Hungary42 and Romania,43 with a
total of 12 335 infants (see Table S1).
We found that caesarean section was associated with a
41% decrease in the odds of death before discharge/to
6 months corrected age in actively resuscitated infants born
between 23+0 and 27+6 weeks of gestation compared with
vaginal birth (OR 0.59, 95% CI 0.36–0.95, 30% in cae-
sarean section group versus 43% in vaginal group, eight
ª 2017 Royal College of Obstetricians and Gynaecologists
 Mode of delivery for extremely preterm breech singletons

Records identified through database searching (n = 3294)

MEDLINE (n = 1068)
EMBASE (n = 1890)
Cochrane CENTRAL (n = 81)
CINAHL (n = 255)
CllinicalTrials.gov (n = 0)

Excluded duplicates
(n = 1130)

Studies identified through Records screened after duplicates removed

reference screening (n = 2164)
(n = 31) Records excluded in titles
and abstracts screening
(n = 2010)
Full-text articles or protocols assessed for
eligibility (n = 185)
Full-text articles excluded after review
(n = 137)
Population of interest not available: 67
No relevant exposure /intervention group: 4
Preliminary inclusion of studies with intent to Relationship between relevant exposures
contact authors (n = 48) and outcomes not examined: 27
No relevant study design: 27
No relevant publication type: 2
Author contact not Duplicate publications: 3
required and studies Articles could not be retrieved (authors were
Authors contacted (n = 46) contacted for full-text): 7
included (n = 2)

Authors No response
responded (n = 25) (n = 21)

Excluded (n = 14) Included (n = 11) Included (n = 2) Excluded (n = 19)

Reasons for exclusion: Reason for exclusion:

Active resuscitation not
explicitly stated: 7 Active resuscitation not explicitly
ANCS use not confirmed: 1* stated: 18
Data not provided: 2 Data are not stratified: 1
†
Wrong data provided: 1
Major bias between CS and
VD groups: 1
‡ Studies included in the final analysis (n = 15)
No stratification of singleton Retrospective cohort studies:13
and twin: 2 Prospective cohort study:1
Randomized control trial:1

Primary research question analysis: 9

Analysis by birth weight: 4
||
Analysis by planned mode of delivery: 0 (+2)
Analysis in non-high income countries: 2

Figure 1. Flow diagram of study selection process for the systematic review and meta-analyses of safest mode of delivery of extremely preterm
breech singleton infants who were actively resuscitated. ANCS, antenatal corticosteroids; CS, Caesarean section; VD, vaginal delivery. *Data collected
prior to 1994. Author did not confirm whether ANCS used routinely. †The total number of participants in the Caesarean section group varied
between two outcomes. The authors this small study were contacted for clarification, but a response was not received. ‡The two comparison groups
(CS and VD) were not treated equally, as one group received surfactant, and the other did not. ||Two authors, studying the planned mode of delivery,
provided raw data for planned CS and actual VD, and emergency CS. Hence, we were able to include these studies in the primary research question
and also in the analysis by planned mode of delivery.

studies, I2 = 55%, NNT = 8, 122 fewer deaths/1000 with death before discharge/to 6 months corrected age between
caesarean sections, GRADE assessment in Table 1, Figure 2, 23+0 and 24+6 weeks of gestation, compared with vaginal
see Table S9). We determined that caesarean section was birth (OR 0.58, 95% CI 0.45–0.75, 38% versus 51%, three
associated with a 42% significant decrease in the odds of studies, I2 = 0%, NNT = 7, 134 fewer deaths/1000 with

ª 2017 Royal College of Obstetricians and Gynaecologists 655

 Grabovac et al.

caesarean sections, Table 1, Figure 2). The odds of death
before discharge/neonatal mortality were not significantly
different between infants born by caesarean section com-
pared with vaginally at 25+0–26+6 weeks of gestation (OR
0.72, 95% CI 0.34–1.52, 23% versus 30%, five studies,
I2 = 0%) and at 27+0–27+6 weeks of gestation (OR 2.04,
95% CI 0.20–20.62, 24% versus 16%, three studies,
I2 = 52%).
Regarding our other primary outcome, severe IVH, cae-
sarean section was associated with a 49% reduction of the
odds in actively resuscitated infants between 23+0 and
27+6 weeks (OR 0.51, 95% CI 0.29–0.91, 8% versus 18%,
six studies, I2 = 0%, NNT = 12, 80 fewer severe IVH/1000
with caesarean sections, Table 1, Figure 3). Although we
did not find separate data for the 23+0–24+6-week strata,
we found that odds of severe IVH were not significantly
different for infants delivered by caesarean section com-
pared with vaginally at 25+0–26+6 weeks (OR 0.29, 95% CI
0.07–1.12, 6% versus 25%, four studies, I2 = 0%) and at
27+0–27+6 weeks (OR 0.91, 95% CI 0.27–3.05,16% versus
16%, four studies, I2 = 50%).
Regarding secondary outcomes, we found that caesarean
section was associated with a significant reduction in the
odds of death before discharge/neonatal mortality com-
pared with vaginal delivery in infants weighing 500–999 g
(OR 0.22, 95% CI 0.14–0.36, 16% versus 44%, three stud-
ies, I2 = 35%; see Table S4 and Figure S1), but not in other
groups. We found that caesarean section was associated
with significantly decreased odds of severe IVH in infants
weighing ≤1500 g compared with vaginal delivery (OR
0.16, 95% CI 0.06–0.43, 3% versus 19%, one study; see
Table S4 and Figure S2).
We found scarce data on other secondary neonatal out-
comes, none of which were statistically significant (see
Tables S5, S6 and Figures S3, S4).
In non-high-income countries, we found that cae-
sarean section was associated with a trend towards a
decrease in death before discharge in Romanian infants
born between 25+0 and 27+6 weeks (OR 0.42, 95% CI
0.17–1.05, one study, 37% versus 58%; see Table S7),
and a significant decrease in Turkish infants ≤ 1500 g
(OR 0.26, 95% CI 0.13–0.54, one study, 38% versus
70%; see Table S7).
We noted that the mean proportion of head entrapment
was 1.1% with caesarean delivery, whereas it was 5.5% with
vaginal delivery across four studies.31,33,34,39 D€ uhrssen

Table 1. Summary of findings for the primary outcomes of death and severe intraventricular haemorrhage by mode of delivery in a systematic
review and meta-analyses of the safest mode of delivery of extremely preterm breech singleton infants who were actively resuscitated

Outcome* GA category Number CS (n/N) VD OR (95% I2 NNT*** Strength of Absolute

(weeks) of (n/N) CI) for (%) recommendation**** effects
studies CS**

Death before 23+0–27+6***** 8 451/1530 218/508 0.59 55 8 Strong for CS 122 fewer deaths/
discharge/ (0.36–0.95) 1000 with caesarean
Neonatal 23+0–24+6***** 3 209/984 128/336 0.58 0 7 Strong for CS 134 fewer deaths/
mortality/ (0.44–0.75) 1000 with caesarean
Death 25+0–26+6 5 31/132 14/46 0.72 0 N/A Weak for CS 65 fewer/1000
< 6 months (0.34–1.52) (from 95 more to
175 fewer)
27+0–27+6 3 12/51 6/37 2.04 52 N/A Weak against CS 121 more/1000 (from
(0.20–20.62) 125 fewer to 637 more)
Severe IVH 23+0–27+6 6 40/476 28/155 0.51 0 12 Strong for CS 80 fewer severe IVH/
(0.29–0.91) 1000 with caesarean
23+0–24+6 0 – – – – – – –
25+0–26+6 4 4/62 7/28 0.29 0 N/A Weak for CS 162 fewer/1000 (from
(0.07–1.12) 22 more to 227 fewer)
27+0–27+6 4 8/51 6/38 0.91 0 N/A Weak for CS 12 fewer/1000 (from
(0.27–3.05) 110 fewer to 206 more)

GA, gestational age; CS, caesarean section; VD, vaginal delivery; n, number of cases within exposure group; N, total number in exposure group;
N/A, not applicable.
*All outcomes are of critical importance.
**Results shown in bold type are significant.
***Calculated for significant results only.
****Based on the GRADE quality of evidence assessment.
*****For Tucker Edmonds study, data used in meta-analyses included death up to 6 months corrected age (or 10 months uncorrected age for an
infant born at 23 and 24 weeks of gestation).

656 ª 2017 Royal College of Obstetricians and Gynaecologists

 Mode of delivery for extremely preterm breech singletons

Figure 2. Summary of odds ratios [95% confidence interval (CI)] of death by mode of delivery in a systematic review and meta-analyses of safest
mode of delivery of extremely preterm breech singleton infants who were actively resuscitated. CS, caesarean section; VD, vaginal delivery; IV, inverse
variance. Studies are arranged in descending order of quality according to a modified Newcastle Ottawa Scale. The numbers of asterisks after the
study name indicate the total number of points allocated out of a total of six. If two studies received the same number of points, the studies were
ordered according to date of publication. †Symbol before the study name indicates that the primary outcome in the study was neonatal mortality.
§
Symbol before the study name indicates that the primary outcome was survival until 6 months corrected age.

incisions were performed in one study for three cases of
head entrapment.33
We found few data on maternal outcomes. In the two
studies reporting type of incision, we found that classical
caesarean sections were performed more often than low
transverse ones (67% versus 33%).31,39 One study reported
that two women in the caesarean section group had post-
partum haemorrhage requiring a blood transfusion and
two of 39 women who delivered by caesarean section
required admission to the intensive care unit (ICU), com-
pared with zero of 26 women delivered vaginally.31 One
woman with severe pre-eclampsia was admitted to the ICU

ª 2017 Royal College of Obstetricians and Gynaecologists 657

 Grabovac et al.

Figure 3. Summary of odds ratios [95% confidence interval (CI)] of severe intraventricular hemorrhage (grades III/IV) by mode of delivery in a
systematic review and meta-analyses of safest mode of delivery of extremely preterm breech singleton infants who were actively resuscitated. CS,
caesarean section; VD, vaginal delivery; IV, inverse variance. Studies are arranged in descending order of quality according to a modified Newcastle
Ottawa Scale. The numbers of asterisks after the study name indicate the total number of points allocated out of a total of six. If two studies
received the same number of points, the studies were ordered according to date of publication.

due to pulmonary oedema and respiratory distress, whereas
the other sustained a small bowel injury.31
We assessed the risk of bias using the modified NOS. As
the majority of included studies did not account for two of
three confounders of interest, only two studies received the
maximum points (see Table S8). We performed a sensitiv-
ity analysis, focusing on high-quality studies, which showed
that the odds of death before discharge were not signifi-
cantly different in infants delivered by caesarean section
compared with vaginally (OR 0.45, 95% CI 0.11–1.76, 12%
versus 27%, two studies, I2 = 85%; see Figure S5) at 23+0–
27+6 weeks of gestation. We also found that the odds of
severe IVH were not significantly different in infants deliv-
ered by caesarean section compared with vaginally (OR
0.62, 95% CI 0.31–1.22, 8% versus 13%, two studies,
I2 = 0%; see Figure S6) at 23+0–27+6 weeks of gestation.
We were unable to perform subgroup analyses on IUGR,
ANCS and chorioamnionitis as data in included studies
were not stratified by gestational age. As studies did not
explicitly state the timing of demise, we were unable to
perform a sensitivity analysis removing studies that
excluded intrapartum intrauterine fetal demise.
Discussion
Main findings
In this systematic review on the safest delivery mode in
actively resuscitated extremely preterm breech singletons,
we found that caesarean section was associated with a 41%
reduction in the odds of death and 49% reduction in the
odds of severe IVH, with the largest benefit in the youngest
infants.

658 ª 2017 Royal College of Obstetricians and Gynaecologists


Strengths and limitations
Our systematic review has strengths. First, given the
increasingly early gestational ages at which resuscitation is
offered, having a systematic review focused on delivery
mode, specifically in extremely preterm breech infants, was
important because it had not previously been done. Sec-
ond, we also stratified data by gestational age, as we
hypothesised that outcomes might vary across the extreme
preterm period and narrower foci would be important for
parents and clinicians. Third, in our inclusion criteria we
addressed the most important confounder, active resuscita-
tion, and another key one, singletons. Regarding other key
confounders, two of the highest quality studies excluded
IUGR (Herbst and Kallen36 and Kayem et al.33), whereas
the former also excluded chorioamnionitis. Finally, we used
the GRADE guidelines to assess the data quality for each
outcome. Although the overall quality of evidence was low
for death at 23+0–24+6 weeks of gestation, and very low for
other outcomes, GRADE identifies situations in which low
or very low quality evidence may still lead to strong recom-
mendations in favour of the intervention.44 One such situa-
tion occurs when an intervention may reduce mortality in
a life-threatening situation, which applies to caesarean sec-
tion to prevent death.
Our main limitation was the dearth of primary ran-
domised studies, resulting in almost entirely observational
data that have an inherent bias. However, given failed
recruitment into previous RCTs, it is likely that clinicians
and parents will need to base decisions on the careful
assessment of observational data.22,45,46 Second, we imple-
mented rigorous methodology to minimise inclusion bias,
such as publishing our protocol, reporting inter-reviewer
agreement which was high, and contacting authors to max-
imise the proportion of included studies, but we cannot
rule out the possibility of inclusion bias given that some
authors were unable to provide data pertaining to our
research question or did not respond. Third, although most
authors either confirmed ANCS as the standard of care or
provided data indicating that rates of use were similar
between infants delivered vaginally and by caesarean sec-
tion, one large study (Tucker Edmonds et al.30) did not
have data on ANCS use, although those data were collected
from 2000 to 2009, when ANCS use was the standard.
Although some confounders might make outcomes with
caesarean section seem more favourable than they are,
other confounders might make outcomes with caesarean
section seem less favourable, because in several included
studies the indications for caesarean section involved causes
that may have worsened outcomes, including emergent
ones like cord prolapse, abnormal fetal heart rate, IUGR,
pre-eclampsia, retroplacental haematoma and suspected
chorioamnionitis.31,34 Hence, the benefit of elective
ª 2017 Royal College of Obstetricians and Gynaecologists
Mode of delivery for extremely preterm breech singletons
caesarean section might be higher than what is reported in
this systematic review, which includes results from both
elective and emergency caesarean sections. Although the
mean gestational ages of infants in the caesarean section
and vaginal groups were comparable across studies, and we
further defined relatively narrow gestational age strata,
infants born by caesarean section may have had greater ges-
tational age than those born vaginally, which would bias
the results in favour of caesarean section. Fourth, data were
scarce for secondary outcomes, especially long-term ones.
Tucker Edmonds et al.30 noted that survival benefit was no
longer significant at 6 months corrected age whereas it had
been at earlier time-points, and that morbidities in elec-
tively sectioned infants were twice as high as after vaginal
birth at 6 months corrected age. Although the Term Breech
Trial found no significant differences in maternal mortality
or serious morbidity between caesarean section and vaginal
delivery, most incisions were low transverse.5 For extremely
preterm breech infants, classical incisions are common, and
may carry increased risks of infection, haemorrhage and
uterine scar separation,47–49 (composite outcome of haem-
orrhage, infection, ICU admission or death, which had an
adjusted RR of 1.37, 95% CI 0.95–1.97).50 Moreover, data
on magnesium sulphate administration for fetal neuropro-
tection were scarce and nonexistent for ANCS duration.51
Although we had hoped to include infants at 22+0–
22+6 weeks, there was only one such infant born (born
vaginally and died), identifying a need for future study.
Finally, the definition of death varied across studies, and
hence our primary outcome of ‘death’ included neonatal,
before discharge and before 6 months corrected age.
Interpretation (in light of other evidence)
Although a 2012 Cochrane review52 concluded there was
insufficient evidence to recommend preferred delivery
mode for preterm infants as all included RCTs were termi-
nated due to recruitment failure, a systematic review of
observational studies concluded that caesarean section from
25+0 to 36+6 weeks was associated with a 37% reduced risk
of neonatal mortality (RR 0.63, 95% CI 0.44–0.92), but
advised caution given the observational data.53 They did
not examine < 25 weeks, and pooled all results for 25+0 to
36+6 weeks, without subgrouping by various time-points in
gestation.
A number of studies that did not meet our inclusion cri-
teria suggested that caesarean section was safer for extre-
mely preterm breech singleton infants (see Table S10). A
multi-centred Canadian study from 1991 to 1996 found
that caesarean was associated with increased survival of
breech singletons at both 24 weeks (unadjusted OR 2.19,
95% CI 1.10–4.34, no adjusted data) and 25 weeks (unad-
justed OR 1.87, 95% CI 0.98–3.56), but could not confirm
659
 Grabovac et al.
active resuscitation.54 A multi-centred Swedish study also
found that caesarean section was associated with signifi-
cantly lower breech singleton mortality between 23 and
25 weeks (19.4% versus 46.6%, P = 0.008, no adjusted
data), as well as nonsignificantly lower proportion of death
at 26–27 weeks of gestation (24.1% versus 41.7%, P value
not significant).55 An American study of singleton and twin
breech infants from 22 to 31 weeks found the mortality
rate increased with vaginal delivery (92.4 per 1000 in cae-
sarean delivery and 444.0 per 1000 live births in vaginal
delivery, caesarean/vaginal mortality rate ratio 0.21,
P < 0.05).56 A Swedish study of extremely preterm infants
found that the risk of death within the first 24 hours of
birth was increased with vaginal breech delivery (adjusted
OR 2.3, 95% CI 1.01–5.1), as was risk of developmental
delay at 2.5 years (adjusted OR 2.0, 95% CI 1.2–7.4).57
Additionally, a Canadian study58 found a greater propor-
tion of IVH among singleton and twin infants ≤32 weeks
of gestation delivered vaginally compared with caesarean
section (17% versus 9%, adjusted OR 1.1, 95% CI 0.9–1.5),
although not all studies found lower rates of IVH with cae-
sarean section.59,60
Conclusion
In conclusion, in our systematic review we found that cae-
sarean section was associated with significantly decreased
odds of death and IVH in actively resuscitated singletons
born between 23+0 and 27+6 weeks, although the data are
mainly observational and hence have inherent bias. In
infants born between 23+0 and 24+6 weeks, caesarean sec-
tion was associated with a significant reduction in odds of
death before discharge/to 6 months corrected age, which
according to GRADE would have a strong recommenda-
tion. With the caution that advantages may decrease over
time and the limited data on other infant and maternal
morbidities necessitate, both, more study and a thorough
discussion, our findings can be used by clinicians and par-
ents who desire active resuscitation of extremely preterm
breech infants.
Acknowledgements
We would like to thank authors who confirmed active
resuscitation and/or routine antenatal corticosteroid use:
Dr Andreas Herbst (Department of Obstetrics and Gynae-
cology, Clinical Sciences, University of Lund, Sweden); Dr
Brownsyne Tucker Edmonds (Department of Obstetrics
and Gynecology, Indiana University School of Medicine,
Indianapolis, IN, USA); Dr Alice Benjamin (Department of
Obstetrics and Gynaecology, McGill University, Women’s
Pavilion, Royal Victoria Hospital, Montreal, Canada). We
would also like to express our gratitude to authors of pri-
mary studies who have provided data for our meta-analyses
660
on actively resuscitated infants receiving corticosteroids: Dr
Tullio Ghi (Department of Obstetrics and Gynaecology,
University of Bologna, Bologna, Italy); Dr Gilles Kayem
(Department of Obstetrics and Gynaecology, Trousseau
Hospital, Universite Pierre et Marie Curie, APHP, Paris,
France); Dr Noemie Bruey (Department of Obstetrics and
Gynaecology, and Reproductive Medicine, CHU de Caen,
Caen Cedex, France); Dr Bharat Bassaw (University of the
West Indies, St Augustine Campus, Mt Hope Maternity
Hospital, Champs Fleurs, Trinidad, West Indies); Drs Laura
Mihaela Suciu and Lucian Puscasiu (Departments of Paedi-
atrics and Obstetrics and Gynaecology, University of Medi-
cine and Pharmacy Tirgu Mures, Tirgu Mures, Romania).
We are grateful to Dr Joseph Beyene, Cochrane Co-Chair
of the Methods Group, for his statistical input, which was
valuable to this manuscript. We value the contribution of
Ms Neera Bhatnager, BSc, MLIS, Head of Systems, Coordi-
nator of Research and Graduate Education Support, Health
Sciences Library, McMaster University, for her assistance in
developing the search strategies.
Disclosure statement
None declared. Completed disclosure of interests form
available to view online as supporting information.
Contribution to authorship
MG contributed to the study conception, performed the
searches, reviewed titles and abstracts, reviewed full text
articles, extracted data, performed data analyses and drafted
the manuscript. JK contributed to the study conception,
performed the duplicate review of titles and abstracts,
review of full text articles, and data extraction, as well as
reviewed the manuscript for important intellectual content.
TI contributed to the study conception, providing clinical
expertise to neonatal aspects of the study and reviewed the
manuscript for important intellectual content. SKL con-
tributed to data analyses and reviewed the manuscript for
important intellectual content. SDM conceived the study
idea, supervised the project and reviewed the manuscript
for important intellectual content.
Details of ethics approval
Not required.
Funding
Not funded.
Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Figure S1. Summary of odds ratios [95% confidence
interval (CI)] of death by mode of delivery stratified by
ª 2017 Royal College of Obstetricians and Gynaecologists

birth weight in a systematic review and meta-analyses of
safest mode of delivery of extremely preterm breech single-
ton infants who were actively resuscitated.
Figure S2. Summary of odds ratios [95% confidence
interval (CI)] of severe intraventricular hemorrhage (grades
III/IV) by mode of delivery stratified by birthweight in a
systematic review and meta-analyses of safest mode of
delivery of extremely preterm breech singleton infants who
were actively resuscitated.
Figure S3. Summary of odds ratios [95% confidence
intervals (CI)] for death by planned mode of delivery in a
systematic review and meta-analyses of safest mode of
delivery of extremely preterm breech singleton infants who
were actively resuscitated.
Figure S4. Summary of odds ratios [95% confidence
interval (CI)] for severe intraventricular hemorrhage by
planned mode of delivery in a systematic review and meta-
analyses of safest mode of delivery of extremely preterm
breech singleton infants who were actively resuscitated.
Figure S5. Summary of odds ratios [95% confidence
interval (CI)] for the sensitivity analyses of high quality
studies for death by mode of delivery in a systematic review
and meta-analyses of safest mode of delivery of extremely
preterm breech singleton infants who were actively resusci-
tated.
Figure S6. Summary of odds ratios [95% confidence
interval (CI)] for the sensitivity analyses of high quality
studies for severe intraventricular hemorrhage by mode of
delivery in a systematic review and meta-analyses of safest
mode of delivery of extremely preterm breech singleton
infants who were actively resuscitated.
Table S1. Characteristics of included and excluded stud-
ies (authors who were contacted and either responded or
did not respond) in the systematic review and meta-ana-
lyses of the safest mode of delivery of extremely preterm
singleton breech infants who were actively resuscitated.
Table S2. Detailed outline of author contact in a system-
atic review and meta-analyses of safest mode of delivery of
extremely preterm breech infants who were actively resusci-
tated.
Table S3. Secondary outcomes in a systematic review
and meta-analyses of safest mode of delivery of extremely
preterm breech singleton infants who were actively resusci-
tated.
Table S4. Summary of findings stratified by birth weight
category for death and severe intraventricular hemorrhage
by mode of delivery in a systematic review and meta-ana-
lyses of safest mode of delivery of extremely preterm breech
singleton infants who were actively resuscitated.
Table S5. Summary of findings for secondary neonatal
outcomes by mode of delivery in a systematic review and
meta-analyses of safest mode of delivery of extremely
ª 2017 Royal College of Obstetricians and Gynaecologists
Mode of delivery for extremely preterm breech singletons
preterm breech singleton infants who were actively resusci-
tated.
Table S6. Summary of odds ratios [95% confidence
interval (CI)] for analysis of death and severe intraventricu-
lar hemorrhage by planned mode of delivery for extremely
preterm breech singleton infants who were actively resusci-
tated.
Table S7. Summary of odds ratios (95% confidence
intervals [CI]) for analysis of death before discharge by
actual mode of delivery in non-high income countries for
extremely preterm breech singleton infants who were
actively resuscitated.
Table S8. Individual study risk of bias assessment for the
primary outcomes, death and severe intraventricular hem-
orrhage (IVH), using a modified Newcastle-Ottawa Scale in
the systematic review of the safest mode of delivery of
extremely preterm breech singleton infants who were
actively resuscitated.
Table S9. GRADE assessment of primary outcomes in
the systematic review of mode of delivery for extremely
preterm breech singleton infants who were actively resusci-
tated.
Table S10. Studies with populations defined by gesta-
tional age, which were excluded from the systematic review
and meta-analyses of safest mode of delivery of extremely
preterm breech singleton infants after author contact, and
whose data suggests caesarean section is safer.
Appendix S1. Search strategies for a systematic review
on the safest mode of delivery of extremely preterm breech
singleton infants (<28 weeks) who were actively resusci-
tated. &
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