Factors associated with adverse perinatal outcomes for term breech

Transcription

Factors associated with adverse perinatal outcomes for term breech
Research
www. AJOG.org
OBSTETRICS
Factors associated with adverse perinatal outcomes for term
breech fetuses with planned vaginal delivery
Elie Azria, MD, PhD; Jean-Patrick Le Meaux, MD; Babak Khoshnood, MD, PhD; Sophie Alexander, MD, PhD;
Damien Subtil, MD, PhD; François Goffinet, MD, PhD; for the PREMODA Study Group
OBJECTIVE: We sought to identify factors associated with adverse perinatal
outcomes (APO) among term breech neonates with planned vaginal deliveries.
STUDY DESIGN: We conducted univariable and multilevel multivariable
analysis of the data collected in the multicenter prospective observational study PREsentation et MODe d’Accouchement (PREMODA) in
women with planned vaginal delivery giving birth to singleton term
breech babies. The end point was a composite set of APO.
RESULTS: Of 2502 women with planned vaginal delivery recruited in
the 174 participating centers, 1772 (71%) delivered vaginally. Adverse
outcomes were observed in 165 cases (6.59%). After adjustment, the
factors associated with them were geographic origin, gestational age
⬍39 weeks at birth, birthweight ⬍10th percentile, and annual number
of maternity unit births ⬍1500.
CONCLUSION: When strict conditions governed the selection of delivery
route and management of labor was rigorous, APO were not associated
with any prenatal or peripartum obstetric factors.
Key words: adverse perinatal outcome, breech, labor management,
vaginal delivery
Cite this article as: Azria E, Le Meaux J-P, Khoshnood B, et al. Factors associated with adverse perinatal outcomes for term breech fetuses with planned vaginal
delivery. Am J Obstet Gynecol 2012;207:285.e1-9.
T
he publication of the Term Breech
Trial (TBT) in 20001 abruptly changed
clinical practices around the world, dramatically increasing the cesarean rate for
breech births in those countries that had
not already adopted routine cesareans for
breech presentations.2-4 The trial’s conclusions, that neonatal mortality and severe
morbidity were higher in the births with
trial of labor than in those with planned
cesarean deliveries, must nonetheless be
interpreted in the light of its limitations.5-8
Its protocol for selecting women for vaginal delivery and for managing labor re-
sulted in a lack of external validity in the
eyes of many. Furthermore, at 2 years of
age, the risk of death or neurodevelopmental delay did not differ between the children of the 2 groups,9 and several retrospective single-center series comparing
planned vaginal delivery with planned cesarean delivery have demonstrated the
safety of vaginal delivery in settings where
the staff is experienced and the selection criteria for planned vaginal delivery strict.10-13 In 2006, the PREsentation et
MODe d’Accouchement (PREMODA)
study, a descriptive prospective multi-
From Institut national de la santé et de la recherche médicale U953, Epidemiological Research
Unit on Perinatal Health and Women’s Health (Drs Azria, Le Meaux, Koshnood, and Goffinet); the
Department of Obstetrics and Gynaecology, Bichat Claude Bernard Hospital, University Paris VII
(Dr Azria); and the Department of Obstetrics and Gynaecology, Port Royal Maternity, Cochin-Saint
Vincent-de-Paul Hospital, University Paris V (Dr Goffinet), Paris, and the Department of Obstetrics
and Gynaecology, Hôpital Jeanne de Flandre, Lille (Dr Subtil), France, and the Perinatal
Epidemiology and Reproductive Health Unit, Ecole de Santé Publique, Université Libre de
Bruxelles, Brussels, Belgium (Dr Alexander).
Received Feb. 26, 2012; revised May 31, 2012; accepted Aug. 14, 2012.
This study was supported mainly by 2 grants from the French Ministry of Health: numbers
AOM01123 (PH-RC 2001) and AOM03040 (PH-RC 2003). The research was also partly funded
by the French College of Gynecologists and Obstetricians, the French Society of Perinatal
Medicine, and the Belgian National Funds for Scientific Research. The funding sources had no role
in the study design, data collection, data interpretation, or writing of the report.
The authors report no conflict of interest.
Reprints: Elie Azria, MD, PhD, Service de Gynécologie Obstétrique, Groupe Hospitalier Bichat
Claude Bernard, 46, rue Henri Huchard, 75877 Paris Cedex 18 France. [email protected].
0002-9378/$36.00 • © 2012 Mosby, Inc. All rights reserved. • http://dx.doi.org/10.1016/j.ajog.2012.08.027
center study conducted in 174 centers in
France and Belgium (Appendix) and including ⬎8000 breech deliveries, reported
that risks of perinatal mortality or serious
neonatal morbidity were not higher in
planned vaginal, compared with planned
cesarean, deliveries (1.6% vs 1.45%, odds
ratio [OR], 1.1; 95% confidence interval
[CI], 0.75–1.61).14 This combination of reports has led some to reconsider what
might have been hasty reactions. The
American Congress of Obstetricians and
Gynecologists, which stated in 2001 that
planned vaginal delivery might no longer
be appropriate,15 revised their guidelines
to state that such delivery might be reasonable under hospital-specific protocol
guidelines for both eligibility and management.16 The Society of Obstetricians and
Gynaecologists of Canada has reached
similar conclusions.17
Residual complications for term breech
fetuses undergoing trial of labor nonetheless remain possible. A better understanding of the factors associated with adverse
perinatal outcomes (APO) in planned vaginal deliveries could improve screening of
patients eligible for trial of labor, but few
studies have sought to identify these.
The purpose of this secondary analysis
of the PREMODA data was to estimate
the effect of individual, practice, and in-
OCTOBER 2012 American Journal of Obstetrics & Gynecology
285.e1
Research
Obstetrics
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TABLE 1
TABLE 2
Criteria for planned vaginal
delivery recommended by Collège
National des Gynécologues
Obstétriciens Français
Perinatal outcome (excluding congenital abnormalities)
Criteria recommended by CNGOF in
2001
Birth traumaa,b
Perinatal outcome
8 (0.32)
.....................................................................................................................................................................................................................................
Brachial plexus injury
5 (0.2)
Parietal skull fracture
1 (0.04)
Significant genital injury
2 (0.08)
.....................................................................................................................................................................................................................................
Normal pelvimetry (x-ray or computed
tomography)
.....................................................................................................................................................................................................................................
..................................................................................................
Anteroposterior diameter of inlet
ⱖ105 mma
..............................................................................................................................................................................................................................................
a,b
Transverse diameter of inlet ⱖ120
mma
Intraventricular hemorrhage
..................................................................................................
..................................................................................................
Transverse interspinous diameter of
midpelvis ⱖ100 mma
...........................................................................................................
No hyperextension of fetal head
(ultrasonography)
...........................................................................................................
Fetal weight estimated between 25003800 g
...........................................................................................................
Frank breech
...........................................................................................................
Continuous electronic fetal heart rate
monitoring during labor
...........................................................................................................
Patient’s informed consent
...........................................................................................................
CNGOF, Collège National des Gynécologues Obstétriciens Français (French national college of obstetricians and gynecologists).
a
Planned vaginal delivery
N ⴝ 2502
n (%)
Measurements commonly accepted as defining normal
pelvimetry.
Azria. Planned vaginal delivery of term breech
fetuses. Am J Obstet Gynecol 2012.
Subdural hematoma
M ATERIALS AND M ETHODS
Patients
The PREMODA study was designed to
compare perinatal outcomes according
to planned mode of delivery for term
breech births in France and Belgium; its
methods and results are reported elsewhere.14 The secondary analysis presented here focuses on the planned vaginal delivery group. Using specific data
collected for this purpose about the process for deciding mode of delivery and
the management of labor and delivery,
we sought to identify the individual,
practice, and institutional factors associated with an increased risk of APO.
The data were prospectively collected
in volunteer maternity units from June
1, 2001, through May 31, 2002, in 138
centers in France, for 232,999 births, and
285.e2
1 (0.04)
..............................................................................................................................................................................................................................................
b
5-min Apgar ⬍7
37 (1.48)
5-min Apgar ⬍4
4 (0.16)
..............................................................................................................................................................................................................................................
a
..............................................................................................................................................................................................................................................
b
Tracheal intubation
26 (1.04)
Tracheal intubation and ventilation ⬎24 h
10 (0.4)
NICU hospitalization ⬎24 h
42 (1.68)
NICU hospitalization ⬎4 d
23 (0.92)
Intermediate care unit hospitalization ⬎4 d
78 (3.12)
..............................................................................................................................................................................................................................................
a
..............................................................................................................................................................................................................................................
b
..............................................................................................................................................................................................................................................
a
..............................................................................................................................................................................................................................................
b
..............................................................................................................................................................................................................................................
a,b
Seizure
4 (0.16)
..............................................................................................................................................................................................................................................
b
Parenteral or tubal feeding ⬎4 d
15 (0.60)
..............................................................................................................................................................................................................................................
a,b
Fetal death
2 (0.08)
Neonatal death
0
..............................................................................................................................................................................................................................................
a,b
..............................................................................................................................................................................................................................................
Fetal and neonatal mortality or serious neonatal morbidity
40 (1.60)
..............................................................................................................................................................................................................................................
Adverse perinatal outcome
165 (6.59)
..............................................................................................................................................................................................................................................
Perinatal outcome in planned cesarean delivery group is presented elsewhere.14
NICU, neonatal intensive care unit.
a
stitutional factors on the risk of APO in
term breech births for which vaginal delivery was planned.
0
..............................................................................................................................................................................................................................................
a,b
Criteria included in combined outcome “Fetal and neonatal mortality or serious neonatal morbidity”; b Criteria included in
combined outcome “Adverse perinatal outcome.”
Azria. Planned vaginal delivery of term breech fetuses. Am J Obstet Gynecol 2012.
from Jan. 1, 2002, through Dec. 31, 2002,
in 36 centers in Belgium, for 31,106
births. The study was approved by the
French Data Protection Authority.
The study included all women giving
birth in a participating maternity unit to
a singleton fetus in breech presentation
⬎37 weeks’ gestation, alive or not. Detailed reports were obtained for all
deaths before discharge and transfers to
neonatal intensive or intermediate care
units. All existing autopsy reports were
sought and obtained. All congenital
anomalies and reasons for hospitalization were coded according to the International Statistical Classification of Diseases, 10th Revision. All deaths before
discharge–fetal, neonatal, and postneonatal–were reviewed by an independent
expert committee to determine the cause
of each death and whether a planned ce-
American Journal of Obstetrics & Gynecology OCTOBER 2012
sarean delivery at 39 weeks might have
prevented it.
In 2001, vaginal delivery of fetuses in
breech presentation remained an acceptable option in France and Belgium. During
the study period, the recommendations by
the Collège National des Gynécologues
Obstétriciens Français (French national
college of obstetricians and gynecologists)
served as the reference for determining
mode of delivery (Table 1).18
Outcomes
An APO was defined as ⱖ1 of the following: fetal mortality after the delivery route
decision, neonatal mortality before discharge, 5-minute Apgar score ⬍7, tracheal
intubation, seizures ⬍24 hours of age, tube
feeding for at least 4 days, admission to the
neonatal intensive care unit for ⬎24 hours,
admission to an intermediate care unit for
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⬎4 days, birth trauma including subdural
hematoma, intracerebral or intraventricular hemorrhage, spinal cord injury, basal
skull fracture, peripheral-nerve injury
present at discharge, or clinically significant genital injury.
Research
TABLE 3
Factors associated with adverse perinatal outcomes, univariate analysis
of all women in planned vaginal delivery group (n ⴝ 2502)
APO, n ⴝ 165
n (%)
Factors
OR (95% CI)
Maternal characteristics
Factors studied
We studied 3 types of factors: individual,
practice, and institutional.
Individual factors included maternal
characteristics such as age at delivery,
geographic origin (native country), educational level, parity, previous vaginal
delivery, and previous cesarean delivery.
It also included neonatal characteristics
such as gestational age at birth, birthweight, and sex. At birth, small for gestational age was defined as birthweight
ⱕ10th percentile according to the French
birthweight standards.19
Practice factors included prenatal
care, ie, factors related to management of
labor and delivery: type of breech (frank
or not), premature rupture of membranes (yes/no), induction of labor (yes/
no), labor augmentation with intravenous oxytocin (yes/no), lack of progress
of cervical dilatation for at least 1 hour
between 5-10 cm (yes/no), duration of
first stage of labor between 5-10 cm, duration of passive phase of the second
stage of labor, duration of active pushing
(ⱕ20 minutes, ⬎20 minutes), and status
of medical staff present at delivery (midwife alone, junior physician without senior, senior obstetrician). The presence
or absence of a formal prenatal decision
about mode of delivery, recorded in the
medical file, was also collected, as were
each of the criteria for breech vaginal delivery listed in the French national guidelines (listed in Table 1).
Institutional factors were those related
to the institution in which delivery occurred, specifically, the number of annual
births and level of care. In France, maternity units are ranked in 4 levels according
to the neonatal care they provide: 1 (maternity unit with a pediatrician but no neonatology unit), 2a (maternity unit with a
special neonatal care nursery), 2b (maternity unit with an intermediate neonatal
care unit able to provide mechanical ventilation), and level 3 (maternity unit with
neonatal intensive care unit).
.....................................................................................................................................................................................................................................
Maternal age ⬎35 y (n ⫽ 380)
34 (9)
1.49 (1.02–2.22)
.....................................................................................................................................................................................................................................
Geographic origin
............................................................................................................................................................................................................................
Europe (n ⫽ 2047)
123 (6)
1
............................................................................................................................................................................................................................
Sub-Saharan Africa (n ⫽ 59)
6 (10.2)
1.77 (0.75–4.20)
............................................................................................................................................................................................................................
North Africa (n ⫽ 182)
14 (7.7)
1.30 (0.73–2.32)
Other (n ⫽ 87)
13 (14.9)
2.75 (1.48–5.09)
43 (7.8)
1.52 (1.02–2.28)
............................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
Educational level ⱕsecondary school (n ⫽ 553)
.....................................................................................................................................................................................................................................
Nulliparous (n ⫽ 1181)
84 (7.1)
1.18 (0.86–1.61)
No previous vaginal delivery (n ⫽ 1201)
87 (7.2)
1.23 (0.90–1.69)
4 (8.7)
1.36 (0.48–3.84)
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
Uterine scar (n ⫽ 46)
..............................................................................................................................................................................................................................................
Pregnancy care
.....................................................................................................................................................................................................................................
Cephalic version trial (n ⫽ 790)
47 (29)
0.85 (0.60–1.21)
No x-ray pelvimetry (n ⫽ 426)
36 (22)
1.39 (0.94–2.04)
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Pelvic measurements
.....................................................................................................................................................................................................................................
Anteroposterior diameter of inlet ⬍105 mm
(n ⫽ 25)
2 (1.6)
1.30 (0.30–5.55)
.....................................................................................................................................................................................................................................
Transverse diameter of inlet ⬍120 mm (n ⫽ 228)
18 (14.6)
1.33 (0.79–2.24)
Transverse interspinous diameter ⬍100 mm
(n ⫽ 236)
13 (11.3)
0.87 (0.48–1.58)
No US assessment of fetal head flexion (n ⫽ 874)
66 (42)
1.30 (0.93–1.80)
No formal decision of delivery route before labor
(n ⫽ 354)
31 (19)
1.42 (0.94–2.14)
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Labor
.....................................................................................................................................................................................................................................
Complete breech (n ⫽ 744)
59 (36.9)
1.32 (0.95–1.85)
PROM (n ⫽ 491)
37 (24.3)
1.22 (0.83–1.80)
Induction of labor (n ⫽ 222)
13 (7.9)
0.87 (0.49–1.56)
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
No labor augmentation with oxytocin (n ⫽ 519)
39 (36.1)
1.43 (0.95–2.15)
Lack of progress in dilatation (n ⫽ 470)
33 (22.5)
1.12 (0.75–1.67)
.....................................................................................................................................................................................................................................
a
..............................................................................................................................................................................................................................................
Neonate characteristics
.....................................................................................................................................................................................................................................
Gestational age at delivery, wk
............................................................................................................................................................................................................................
37 (n ⫽ 282)
33 (20.1)
2.51 (1.62–2.87)
38 (n ⫽ 491)
40 (24.4)
1.68 (1.12–2.51)
39-40 (n ⫽ 1394)
70 (42.7)
1
ⱖ41 (n ⫽ 334)
21 (12.8)
1.27 (0.77–2.10)
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
Birthweight percentile
............................................................................................................................................................................................................................
⬍10th (n ⫽ 142)
37 (22.7)
6.15 (4.05–9.36)
............................................................................................................................................................................................................................
10-90th (n ⫽ 2142)
116 (71.2)
1
............................................................................................................................................................................................................................
⬎90th (n ⫽ 202)
10 (6.1)
0.91 (0.47–1.76)
82 (50)
1.25 (0.91–1.72)
.....................................................................................................................................................................................................................................
Male
..............................................................................................................................................................................................................................................
Azria. Planned vaginal delivery of term breech fetuses. Am J Obstet Gynecol 2012.
(continued )
OCTOBER 2012 American Journal of Obstetrics & Gynecology
285.e3
Research
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TABLE 3
Factors associated with adverse perinatal outcomes, univariate analysis
of all women in planned vaginal delivery group (n ⴝ 2502) (continued)
APO, n ⴝ 165
n (%)
Factors
OR (95% CI)
Institutional characteristics
.....................................................................................................................................................................................................................................
Maternity unit activity, birth/y
............................................................................................................................................................................................................................
ⱕ1500 (n ⫽ 663)
54 (32.8)
1.85 (1.18–2.91)
1500-2000 (n ⫽ 700)
32 (19.4)
1
2000-2500 (n ⫽ 566)
36 (21.8)
1.42 (0.87–2.31)
⬎2500 (n ⫽ 573)
43 (26.1)
1.69 (1.06–2.71)
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
Level of maternity unit
............................................................................................................................................................................................................................
1 (n ⫽ 422)
16 (11.4)
0.49 (0.28–0.88)
2a (n ⫽ 346)
16 (11.4)
0.61 (0.35–1.08)
2b (n ⫽ 667)
48 (34)
0.98 (0.66–1.46)
3 (n ⫽ 834)
61 (43.3)
1
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
APO, adverse perinatal outcome; CI, confidence interval; OR, odds ratio; PROM, premature rupture of membranes; US,
ultrasound.
a
Defined as failure to progress ⱖ1 h.
Azria. Planned vaginal delivery of term breech fetuses. Am J Obstet Gynecol 2012.
Analysis
All characteristics were studied in patients included in the planned vaginal
group except characteristics of the late
stages of labor, which were studied only
in patients who actually delivered
vaginally.
Categorical variables were compared
with a ␹2 test or Fisher exact test if re-
quired. Continuous variables were compared by Student t test. A P value ⬍ .05
was considered significant.
Crude OR and 95% CI were calculated
for all factors studied in the univariable
analysis.
The numerous candidate variables for
multivariable analysis were grouped in 5
categories (maternal, pregnancy, labor,
TABLE 4
Factors associated with adverse perinatal outcomes, univariate
analysis on women who delivered vaginally (n ⴝ 1772)
No APO
n ⴝ 1668
APO
n ⴝ 104
151 (96)
155 (99)
Duration of second stage, min (SD)
30 (36)
33 (35)
Duration of active phase of second stage, min
(SD)
12 (9)
14 (10)
Factors
5-10 cm labor duration, min (SD)
OR (95% CI)
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
⬎20 min (n ⫽ 193)
176 (10.8)
17 (17.5) 1.76 (1.02–3.03)
..............................................................................................................................................................................................................................................
Person present at delivery
.....................................................................................................................................................................................................................................
Senior obstetrician (n ⫽ 1617)
1521 (92.5) 109 (95.1) 1
.....................................................................................................................................................................................................................................
Resident without senior obstetrician (n ⫽ 41)
39 (2.4)
2 (2)
0.81 (0.19–3.42)
Midwife alone (n ⫽ 87)
84 (5.1)
3 (3)
0.57 (0.18–1.82)
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
All values are expressed as n (%) except as specified.
APO, adverse perinatal outcome; CI, confidence interval; OR, odds ratio.
Azria. Planned vaginal delivery of term breech fetuses. Am J Obstet Gynecol 2012.
285.e4
American Journal of Obstetrics & Gynecology OCTOBER 2012
neonatal, and institutional characteristics) and analyzed in 5 separate multivariable models. Factors included in
these models were those with P ⬍ .25 in
the univariable analysis. Because gestational age and birthweight are standard
confounders, they were forced in the
models. Factors considered significant
(P ⬍ .20) were selected for the final multivariable analysis model.
We used multilevel logistic regression
models21 to take into account the hierarchical nature of data, ie, patients (level 1)
nested within maternity units (level 2).
These models consider correlations that
may exist for outcomes at a given center.
By taking such “cluster” effects into account, these models can better estimate
the effects associated with predictor variables and their variance, particularly
those associated with level-2 (here maternity-level) characteristics.
The analysis of factors related to labor
was performed on the entire population,
while analyses of the factors related to
end of labor and delivery were limited to
women with vaginal deliveries. Only the
final model is presented in this report.
Statistical analysis was performed with
Stata software, Version 9 (StataCorp,
College Station, TX) and HLM (SSI, Lincolnwood, IL).
R ESULTS
During the 12-month study period,
PREMODA included 8105 women: 1133
in Belgium and 6972 in France. During
this period, 264,105 births occurred in
the 174 participating centers, for a rate of
singleton term fetuses in breech presentation of 3.1%. The planned vaginal delivery group comprised 2526 women; 24
were excluded because of lethal congenital abnormalities. Among the 2502
women finally analyzed, 1772 (71%) delivered vaginally.
Mean maternal age was 29.9 years (SD
5) and 15.4% were age ⬎35 years. The
principal outcome measure, APO, was
observed in 165 newborns (6.59%) (Table 2), including 2 fetal deaths. The first
death involved a woman with planned
vaginal delivery after a previous cesarean
section; she delivered a stillborn baby
during an emergency cesarean during la-
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bor for uterine rupture. The second
mother had had 5 previous vaginal deliveries and missed several prenatal visits. Fetal death was diagnosed at 39 weeks and 6
days of gestation, but remained unexplained. There were no neonatal deaths.
Research
TABLE 5
Factors associated with adverse perinatal
outcomes, multivariate analysis
Factors
aOR (95% CI)
Maternal characteristics
.....................................................................................................................................................................................................................................
Univariable analysis
Maternal age ⬎35 years, geographic origin, and educational level below secondary school were the only individual
maternal factors associated with an increased risk of APO (Table 3). No pregnancy or labor factors were associated
with increased risk. Among the neonatal
factors, gestational age at birth of 37 and
38 weeks, compared with 39-40 weeks,
and birthweight ⬍10th percentile were
associated with this risk (Table 3). Birthweight ⬎90th percentile was not associated with APO.
An annual number of births ⬍1500 was
an institutional characteristic associated with
an increased risk of APO, and birth at a
level-1 compared with a level-3 facility was
associated with reduced risk (Table 3).
In the univariable analysis limited to
the subgroup of women who delivered
vaginally, the only factor related to the
end of labor and delivery associated with
an increased risk of APO was pushing efforts ⬎20 minutes (Table 4).
Maternal age
............................................................................................................................................................................................................................
⬎35 y
1.55 (0.98–2.44)
.....................................................................................................................................................................................................................................
Geographic origin
............................................................................................................................................................................................................................
Europe
1
Sub-Saharan Africa
1.69 (0.68–4.21)
North Africa
1.30 (0.71–2.39)
Other
2.48 (1.25–4.92)
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
No previous vaginal delivery
1.30 (0.90–1.85)
..............................................................................................................................................................................................................................................
a
Late labor and delivery
.....................................................................................................................................................................................................................................
Duration of active phase of second stage
............................................................................................................................................................................................................................
⬎20 min
1.63 (0.87–3.02)
..............................................................................................................................................................................................................................................
Neonate
.....................................................................................................................................................................................................................................
Gestational age at delivery, wk
............................................................................................................................................................................................................................
37
2.22 (1.38–3.59)
38
1.72 (1.12–2.65)
39-40
1
ⱖ41
1.57 (0.93–2.66)
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
Birthweight, g (SD)
............................................................................................................................................................................................................................
⬍10th centile
5.75 (3.62–9.12)
10-90th centile
1
⬎90th centile
1.03 (0.52–2.04)
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
Multivariable analysis
In the multivariable analysis of all
women for whom vaginal delivery had
been planned, the only maternal characteristic that remained significantly associated with APO was maternal geographic origin (Table 5). No factors
related to pregnancy, labor, or delivery
were associated with the risk of APO.
Specifically, in the subgroup of women
who delivered vaginally, pushing efforts
⬎20 minutes were not independently associated with APO.
Among the neonatal factors, gestational age at birth of 37 weeks (adjusted
OR [aOR], 2.22; 95% CI, 1.38 –3.59) or
38 weeks (aOR, 1.72; 95% CI, 1.12–
2.65), compared with 39-40 weeks, and
birthweight ⬍10th percentile (aOR,
5.75; 95% CI, 3.62–9.12) remained associated with an increased risk of APO.
An annual number of births ⬍1500
(aOR, 1.99; 95% CI, 1.17–3.40) re-
Institutional characteristics
.....................................................................................................................................................................................................................................
Maternity unit activity, birth/y
............................................................................................................................................................................................................................
ⱕ1500
1.99 (1.17–3.40)
1500-2000
1
2000-2500
1.28 (0.75–2.18)
⬎2500
1.36 (0.76–2.45)
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
Level of maternity unit
............................................................................................................................................................................................................................
1
0.39 (0.18–0.83)
2a
0.67 (0.34–1.31)
2b
0.98 (0.58–1.69)
3
1
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
............................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
aOR, adjusted odds ratio; CI, confidence interval.
a
Analysis performed only among women who delivered vaginally (N ⫽ 1772).
Azria. Planned vaginal delivery of term breech fetuses. Am J Obstet Gynecol 2012.
mained associated with increased risk after adjustment, and delivery in a level-1
compared with level-3 facility, with a
reduced risk (aOR, 0.39; 95% CI,
0.18 –0.83).
C OMMENT
This study shows that when vaginal delivery is planned for term breech fetuses
under standard practice conditions, a
geographic origin other than European,
OCTOBER 2012 American Journal of Obstetrics & Gynecology
285.e5
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Obstetrics
sub-Saharan, or North African; a birthweight ⬍10th percentile; and delivery
⬍39 weeks were the only individual factors independently associated with APO.
Practice factors were not independently
associated with an increased risk. Delivery at a level-1 (compared with level-3)
maternity unit was associated with reduced risk, whereas an annual number of
births ⬍1500 was associated with increased risk.
A strength of this analysis is the use of
a mixed model with random effects to
prevent the bias inherent in standard logistic models involving mutual dependence among subjects in the study population.20 This analysis strategy can take
into account the differences between
hospitals in both treatment policies and
expertise.
As the principal outcome variable in
the primary PREMODA analysis–fetal
and neonatal mortality and severe neonatal morbidity–was present in only 40
of the 2502 cases, a multivariable analysis
of that outcome lacked the power to assess all factors of interest. We thus defined an outcome criterion including
moderate morbidity. We did, nonetheless, perform the analysis with the initial
outcome and identified no relevant factors other than those identified with the
new outcome. The most relevant criterion is nonetheless the risk of death or
neurodevelopmental delay at the age of 2
years, used by Whyte et al9 in the TBT.
Unfortunately, the PREMODA study
did not have the substantial logistic resources required to assess this outcome.
Choosing APO, as defined above, as our
main outcome had the advantage of providing a global view of the risk for ⱖ1
adverse outcomes.
The association found between geographic origin and neonatal risk is difficult to interpret. Genetic, economic, and
social factors are likely linked simultaneously with geographic origin and perinatal risk and are thus confounding factors.
The category “other geographic origin”
is very heterogeneous (including the
Americas, Australia, and Asia) and perhaps includes the minority communities
that are less well integrated in France. As
only 87 women (3.5%) fell into this category, this result must be interpreted
285.e6
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with caution. The finding of elevated
perinatal risk among ethnic minorities is
consistent with previous studies.21 A
large part of this risk, however, has been
linked to preterm deliveries22 excluded
from our study. The high prevalence of
low socioeconomic status among the
non-Western women might be an explanation, at least partial, of their elevated
risks,23 but as we lack additional socioeconomic data about them, we cannot
adjust for it or further investigate this
point. Communication issues, such as
mother caregiver collaboration during
the second stage, may also be at stake
here.
Birthweight ⬍10th percentile was the
main risk factor for APO in this study. As
PREMODA did not include preterm
pregnancies, these low birthweights were
due principally to growth restriction.
This finding is consistent with a secondary analysis of the TBT data reporting
that birthweight ⬍2800 g was associated
with an increased risk of APO (OR, 2.13;
95% CI, 1.20 –3.80).24 Others have also
observed this association between low
birthweight and adverse outcome.25,26
Applying our logistic model to the planned
cesarean group (data not shown) showed
that birthweight ⬍10th percentile was
again the factor most closely associated
with APO (OR, 12.01; 95% CI, 8.35–
12.28). This finding suggests that the perinatal risk of low birthweight is related not
to the delivery route but to the growth restriction itself. Other support for this hypothesis comes from a report that the most
important risk factor for breech births is
low birthweight, and that cesarean delivery
does not improve perinatal outcome.26
A similar comment can be made about
delivery ⬍39 weeks. This factor was also
associated with an increased risk of APO
in the planned cesarean group, a finding
that suggests that the perinatal risk of
birth ⬍39 weeks is not related to mode of
delivery.
APO was not associated with failure to
comply with guidelines for vaginal delivery of term breech fetuses. These failures
include the absence of pelvic measurements, planning vaginal delivery despite
abnormal measurements, and failure to
explore fetal head flexion. The absence of
association might be due to lack of power
American Journal of Obstetrics & Gynecology OCTOBER 2012
related to the high guideline compliance
rate (82.8% had x-ray pelvimetry, 63.7%
had fetal head flexion assessed, and a formal decision about delivery route was
made before labor for 85.5%). It might
also reflect the minor nature of the noncompliance, as in planning vaginal delivery when transverse diameter of the inlet
measured 118 mm instead of 120 mm or
not taking pelvic measurements in
women with previous vaginal deliveries.
Evidence supporting this interpretation
can be found in the percentages of
women with a transverse diameter ⬍115
mm: only 2.9% in the planned vaginal
group, vs 18.3% in the planned cesarean
group. The failure to comply with these
criteria might therefore be interpreted as
decisions related to individual contexts
and thus less likely to generate adverse
outcomes. We must nonetheless remember that no scientific evidence justifies
the usefulness of these examinations or
the relevance of the thresholds chosen.
No practice-related factors (pregnancy or management of labor) were independently associated with APO. Perinatal outcome was not influenced by
type of breech, premature rupture of
membranes, labor induction, or poor
progress of labor. This finding is explained by the results of another analysis
of the PREMODA data, which showed
that these factors were associated with
cesarean delivery during labor27 and
suggests that such delivery is indeed protective in those conditions. This point is
important in guiding our practices, as it
shows that the current management of
labor in the participating centers is generally appropriate and further validate
our guidelines.
Looking at the institutional factors, we
note that the decreased risk in maternity
units with limited neonatal facilities
might well be due to a selection bias
linked to the higher prevalence of lowrisk pregnancies in these units compared
with level-3 maternity units. Another
relevant factor is that the variables listed
in our composite criteria included care
more easily–and more likely to have
been–provided for mild neonatal disorders in level-3 units than elsewhere. This
phenomenon, which leads to misclassification bias, was previously described in
Obstetrics
www.AJOG.org
a low-risk population with cephalic
presentation.28
Senior obstetricians were nearly always present at these deliveries (between
93.6-96.8%), and the proportion did not
differ according to type of maternity
unit. The increased risk associated with
the smallest maternity units (⬍1500 annual deliveries), compared with others,
suggests that their lack of practice with
vaginal breech deliveries might account
for some portion of the APO. The Canadian guidelines address this important
issue of training for infrequently used
skills,29 which calls attention to the need
to develop new methods to train
physicians.17
This study showed that planned vaginal delivery for term breech fetuses was
associated with rare APO. Moreover,
most of the factors associated with the
risk of an adverse outcome were not related to the medical care provided nor to
the planned route of delivery. These
findings provide additional evidence in
favor of the guidelines used in our population to decide on mode of delivery
and further suggest that planned vaginal
delivery under strict conditions for selection of patients and their clinical management remains a safe option for term
breech fetuses. The role of the annual
volume of delivery calls attention to the
need to develop new methods to train
physicians in rarely used skills.
f
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2. Hogle KL, Kilburn L, Hewson S, Gafni A, Wall
R, Hannah ME. Impact of the international term
breech trial on clinical practice and concerns: a
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3. Alexandersson O, Bixo M, Hogberg U. Evidence-based changes in term breech delivery
practice in Sweden. Acta Obstet Gynecol
Scand 2005;84:584-7.
4. Molkenboer JF, Bouckaert PX, Roumen FJ.
Recent trends in breech delivery in the Netherlands. BJOG 2003;110:948-51.
5. Goffinet F, Blondel B, Breart G. Breech presentation: questions raised by the controlled
trial by Hannah et al on systematic use of cesarean section for breech presentations [in
French]. J Gynecol Obstet Biol Reprod (Paris)
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6. van Roosmalen J, Rosendaal F. There is still
room for disagreement about vaginal delivery of
breech infants at term. BJOG 2002;109:967-9.
7. Kotaska A. Inappropriate use of randomized
trials to evaluate complex phenomena: case
study of vaginal breech delivery. BMJ 2004;
329:1039-42.
8. Glezerman M. Five years to the term breech
trial: the rise and fall of a randomized controlled
trial. Am J Obstet Gynecol 2006;194:20-5.
9. Whyte H, Hannah ME, Saigal S, et al. Outcomes of children at 2 years after planned cesarean birth versus planned vaginal birth for
breech presentation at term: the international
randomized term breech trial. Am J Obstet Gynecol 2004;191:864-71.
10. Giuliani A, Scholl WM, Basver A, Tamussino
KF. Mode of delivery and outcome of 699 term
singleton breech deliveries at a single center.
Am J Obstet Gynecol 2002;187:1694-8.
11. Kayem G, Goffinet F, Clement D, Hessabi
M, Cabrol D. Breech presentation at term: morbidity and mortality according to the type of delivery at Port Royal Maternity Hospital from 1993
through 1999. Eur J Obstet Gynecol Reprod
Biol 2002;102:137-42.
12. Alarab M, Regan C, O’Connell MP, Keane
DP, O’Herlihy C, Foley ME. Singleton vaginal
breech delivery at term: still a safe option. Obstet Gynecol 2004;103:407-12.
13. Albrechtsen S, Rasmussen S, Reigstad H,
Markestad T, Irgens LM, Dalaker K. Evaluation
of a protocol for selecting fetuses in breech presentation for vaginal delivery or cesarean section. Am J Obstet Gynecol 1997;177:586-92.
14. Goffinet F, Carayol M, Foidart JM, et al. Is
planned vaginal delivery for breech presentation
at term still an option? Results of an observational prospective survey in France and
Belgium. Am J Obstet Gynecol 2006;194:
1002-11.
15. American College of Obstetricians and Gynecologists. Committee on Obstetric Practice.
ACOG committee opinion no. 265, December
2001; mode of term single breech delivery. Obstet Gynecol 2001;98:1189-90.
16. American College of Obstetricians and Gynecologists Committee on Obstetric Practice.
ACOG committee opinion no. 340: mode of
term singleton breech delivery. Obstet Gynecol
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17. Kotaska A, Menticoglou S, Gagnon R, et al.
Vaginal delivery of breech presentation. J Obstet Gynaecol Can 2009;31:557-78.
18. Carbonne B, Goffinet F, Breart G, Frydman
R, Maria B, Uzan S. The debate on breech presentation: delivery of breech presentations; the
position of the National College of French Gynecologists [in French]. J Gynecol Obstet Biol
Reprod (Paris) 2001;30:191-2.
19. Leroy B, Lefort F. The weight and size of
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21. Gagnon AJ, Zimbeck M, Zeitlin J, et al. Migration to western industrialized countries and
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22. Blondel B, Supernant K, Du Mazaubrun C,
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Perinat Epidemiol 2000;14:194-210.
24. Su M, McLeod L, Ross S, et al. Factors
associated with adverse perinatal outcome in
the term breech trial. Am J Obstet Gynecol
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25. Gimovsky ML, Petrie RH, Todd WD. Neonatal performance of the selected term vaginal
breech delivery. Obstet Gynecol 1980;56:
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Breech delivery: an obstetrical analysis. Acta
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27. Roman H, Carayol M, Watier L, Le Ray C,
Breart G, Goffinet F. Planned vaginal delivery of
fetuses in breech presentation at term: prenatal
determinants predictive of elevated risk of cesarean delivery during labor. Eur J Obstet Gynecol Reprod Biol 2008;138:14-22.
28. Le Ray C, Zeitlin J, Jarreau PH, Breart G,
Goffinet F. The influence of level of care on admission to neonatal care for babies of low-risk
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29. Queenan JT. Teaching infrequently used
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2004;103:405-6.
A PPENDIX
PREMODA Study Group
Scientific Committee: F. Goffinet, S. Alexander, J. M. Foidart, S. Uzan, D. Subtil,
G. Bréart.
Data Monitoring and Analysis Committee: M. Carayol, F. Goffinet, D. Subtil, S. Alexander, J. M. Foidart, G. Bréart.
Institut national de la santé et de la recherche médicale U953, Epidemiological Research Unit on Perinatal Health
and Women’s Health (Goffinet, Bréart,
Carayol); Department of Obstetrics and
Gynaecology, Port Royal Maternity, Cochin-Saint Vincent-de-Paul Hospital,
University Paris V (Goffinet); and Department of Obstetrics and Gynaecology, Tenon Hospital, University Paris VI
(Uzan, Bréart), Paris, and Department of
Obstetrics and Gynaecology, Hôpital
OCTOBER 2012 American Journal of Obstetrics & Gynecology
285.e7
Research
Obstetrics
Jeanne de Flandre, Lille (Subtil), France,
and Ecole de Santé Publique, Université
Libre de Bruxelles, Brussels (Dr Alexander) and Department of Obstetrics and
Gynaecology, La Citadelle Hospital,
Liège (Foidart), Belgium.
Independent Expert Committee: Pediatricians: Professor (Pr) U. Simeoni
(Timone Hospital, Marseille, France); Pr
J. C. Rozé (Mother and Children’s Hospital, Nantes, France); Pr J. B. Gouyon (Dijon University Hospital, France); Pr P. Lequien (Hôpital Jeanne de Flandre, Lille,
France); P. H. Jarreau (Port-Royal Maternity, Cochin Hospital, Paris, France); Pr D.
Haumont (Saint-Pierre University Hospital, Brussels, Belgium). Obstetricians: Pr F.
Puech (Hôpital Jeanne de Flandre, Lille,
France); Pr P. Gaucherand (Croix-Rousse
Hospital, Lyon, France).
List of collaborators and participating
centers:
France
Région Alsace: Coordonnateur: Pr Langer:
Centre hospitalo-universitaire (CHU) de
Strasbourg (Pr Langer), Centre médicochirurgical obstétrique de Schiltigheim
(Dr Vayssiere), Centre hospitalier régional
(CHR) de Haguenau (Dr Lehmann), Centre médico-chirurgical de Colmar (Dr
Kutnahorsky), CHR de Mulhouse (Dr
Wiedemann), Clinique Sainte Anne, Strasbourg (Dr Jeanmougin), Clinique Diaconat, Mulhouse (Dr Blum)–Basse-Normandie: Coordonnateur: Pr Dreyfus:
CHU de Caen (Pr Dreyfus/Dr DenoualZiad), Centre hospitalier (CH) de Cherbourg (Dr Ulmann), CH de Lisieux (Dr
Zerger), CH de Saint Lo (Dr Refahi), CH
de Flers (Dr André), CH de la Ferté Macé
(Dr Nelle)–Région Bretagne: Coordonnateur: Pr Grall: CHU de Brest (Pr Collet),
CHU Hôtel Dieu, Rennes (Pr Poulain),
CHU Hôpital Sud, Rennes (Mme Pérrigot), CH de Lorient (Dr Getin), Clinique
mutualiste de la Sagesse, Rennes (Dr Aussel), CH de Saint Brieuc (Dr Giono-Renaud), CH de Saint Malo (Dr Weyl), CH
de Vannes (Mme Pierson), CH de Cornouaille (Dr Germain)–Région Centre:
Coordonnateur: Pr Perrotin: CHU Bretonneau, Tours (Dr Alonso), CHU Beffroi,
Tours (Dr Rapp), CH de Blois (Dr Montmasson), CHR d’Orléans (Dr Ceccaldi),
285.e8
www.AJOG.org
CHG de Chartres (Dr Guilbaud)–Région
Franche-Comté: Coordonnateur: Pr
Schaal: CHU de Besançon (Dr Riethmuller), CHG de Montbéliard (Dr Zurlinden), CHG de Belfort (Dr Terzibachian)–Région
Haute-Normandie:
Coordonnateur: Pr Verspyck: CHU de
Rouen (Pr Verspyck), CH de Mont Saint
Aignan (Dr Fournet), CH du Havre (Dr
Degré), CH d’Elbeuf (Dr Paquet), CH de
Dieppe (Dr Gandour), Clinique Saint-Romain, Rouen (Dr Thobois)–Région Ile de
France: Réseau Sud Ouest Francilien: Coordonnateur: Dr Audibert: CHU de
Clamat (Dr Audibert), Clinique des
Vallées,
Châtenay-Malabry
(Dr
Proust), Clinique de Meudon la Forêt (Dr
Chene), CH de Dourdan (Dr Lambert),
CH Sud Francilien site d’Evry (Mme
Lose), CH de Fontainebleau (Dr Fillippini), CH d’Orsay (Dr Devianne); Réseau
Ile de France Port-Royal: Coordonnateur:
Dr Harvey: CHU Cochin, Paris (Dr
Kayem), CHU Saint Vincent de Paul, Paris
(Pr Lepercq), CHU Saint Antoine, Paris
(Pr Carbonne), CH Notre Dame de Bonsecours, Paris (Dr Grovangrandi), CHU
Beaujon, Paris (Mme Grapin), CHU de
Colombes (Dr Crenn-Hebert), CH de
Neuilly sur Seine (Dr Galimard), CH
de Saint Cloud (Mme Pecourt), Hôpital
Militaire Begin, Saint Mandé (Dr Ponties),
Clinique Armand Brillard, Nogent sur
Marne (Dr Helvin), CH Les Diaconesses,
Paris (Dr Harvey); Réseau de Poissy: Coordonnateur: Dr Rozenberg: Centre hospitalier intercommunal (CHI) de PoissySaint Germain (Mme Bertaud); Réseau
inter-maternités de Saint-Denis: Coordonnateur: Pr Uzan: CH de Bondy (Dr Seince),
CHI de Montreuil (Dr Chitrit),
CHI de Villepinte (Dr Debièvre), Clinique
Vauban, Livry-Gardan (Dr Kamoun), Clinique du bois d’amour, Drancy (Dr Masson), CH de Montfermeil (Dr Ropert),
CHG de Saint-Denis (Dr Ekoukou), Clinique de l’Estrée, Stains (Dr Franche); Réseau Tenon: Coordonnateurs: Pr Uzan et
Dr Berkane: CHU Tenon, Paris (Dr Berkane), CHU Bichat, Paris (Pr Mandelbrot); CHI de Créteil (Pr Haddad et Dr
Touboul); CH de Saint Maurice (Dr Bardou)–Région Limousin: Coordonnateur:
Pr Philippe: CH de Brive (Mme Peron),
CH de Tulle (Mme Barbé), CHU de Limoges (Dr Eyraud), CH d’Ussel (Mme Leclerc)
American Journal of Obstetrics & Gynecology OCTOBER 2012
–Région Lorraine: Coordonnateurs: Pr
Boutroy, Dr Thiebaugeorges: CHU de
Nancy (Dr Thiebaugeorges), CH d’Epinal
(Dr Scotton), CHR Bonsecours, Metz (Dr
Lemarié), CH de Thionville (Dr Szwarcberg), CH Sainte Croix, Metz (Dr Ragage), Polyclinique Majorelle, Nancy (Dr
Cledat), Clinique Arc en Ciel, Epinal (Dr
Gaillet-Schiochet), Clinique Claude Bernard, Metz (Dr Adami)–Nord Pas de Calais: Coordonnateur: Pr Subtil: CH d’Arras
(Mme Finet), CH de Béthune (Dr Hay),
CH de Boulogne (Dr Churlet), Clinique
Côte d’Opale, Saint Martin les Boulognes
(Dr Renault), CH de Douai (Dr Dognin),
Clinique Saint Amé, Lambre-lez-Douai (Dr
Doutrelant), Clinique Villette, Dunkerque
(Mme Gosselin, Mme Deroose), CH de
Maubeuge (Dr Hubert), CH de Roubaix (Dr
Le Goueff), CH de Seclin (Dr Biausque), CH
de Valenciennes (Dr Massoni), CHU de Lille
(Pr Subtil), Clinique Cotteel, Villeneuve
d’Ascq (Mme Dumon)–Région Pays de
Loire: Coordonnateur: Dr Winer: Centre
hospitalierdépartementaleLaRochesurYon
(Dr Barreteau), CH de Saint Nazaire (Dr Gerard), Clinique du jardin des plantes, Saint
Nazaire (Dr Rousseau), CH de Cholet (Dr
Aireau), CHU de Nantes (Dr Winer), Maison de naissance, St Sébastien/Loire (Dr Berlivet), CHU d’Angers (Dr Gilard)–Picardie:
Coordonnateur:PrGondry:CHUd’Amiens
(Pr Gondry), Clinique Sainte Claire, Amiens
(Dr Degroote), CHG de Beauvais (Dr
Manela), CHG de Creil (Dr Cesbron), CHG
de Laon (Dr Boury), CHG de Saint Quentin
(Dr Closset), CHG de Soissons (Dr
Abboud)–Région Poitou-Charentes: Coordonnateur: Pr Pierre: CHU de Poitiers (Pr
Pierre), Clinique du Fief de Grimoire, Poitiers (Dr Bascou), CHG de Niort (Dr
Breheret), CHG d’Angoulême (Dr Tariel),
CHG de la Rochelle (Dr Quentin), Clinique
Sainte Anne, Châtellerault (Dr Boisselier),
CHGdeChâtellerault(DrGodard),CHGde
Bressuire(DrVillemonteix),CHGdeSaintes
(Dr Trousselle)–Région Provence Alpes
Côtes d’Azur: Coordonnateur: Pr D’Ercole:
CHU la Conception, Marseille (Dr Agostini), CHR de Draguignan (Dr Diquelou),
CHR de Hyères (Dr Eymery), CHR de la
Ciotat (Dr Pechikof), CHU Hôpital Nord,
Marseille (Pr D’Ercole), CHR de Salon de
Provence (Dr Maldiney), CHR de la Seyne
sur Mer (Dr Joly)–Région Rhône-Alpes
Lyon: Coordonnateur: Dr Vaudoyer: CHU
Obstetrics
www.AJOG.org
l’Hôtel Dieu, Lyon (Dr Vaudoyer), CHU la
Croix Rousse, Lyon (Pr Gaucherand), CHU
Lyon Sud, Lyon (Dr Coste)–Région RhôneAlpesGrenoble:Coordonnateur:DrVendittelli: CHU Nord et Sud, Grenoble (Dr Venditelli), Clinique Belledone, Saint Martin
d’Hères (Dr Benbassa), Clinique des Cédres,
Grenoble (Dr Boschetto), Clinique Mutualiste, Grenoble (Dr Leger), CHU de Saint Etienne (Dr Collet), CH de Bourg en Bresse (Dr
Frobert), CH d’Alberville (Dr Dardenne),
CH de Chambéry (Dr Houman), CH
d’Annecy (Dr Bernardi), CH de Valence (Dr
Broussard), CH de Roanne (Dr Gaja), CH
d’Evian les Bains et de Thonon les Bains
(Dr Thery), CH de Saint Julien en Genevois (Dr Tognelli), CH de Firminy (Dr
Albersammer).
Belgium
Belgique Coordonnateur: Pr Foidart:
CH Luxembourg (Dr Arendt), Hôpital
St Nikolaus Eupen (Dr Chantraine), Hôpital Ste Anne-St-Remi Bruxelles (Dr Befahy), CH Etterbeek-Ixelles (Dr Houben),
Hôpital Braine l’Alleud Waterloo Lillois
(Dr Busine), Hôpital St Elisabeth Bruxelles
(Dr Depierreux), CHR Warquignies
Boussu (Dr Mathieu), Intercommunale
Famenne Ardenne Condroz Ste Thérèse
Bastogne (Dr Colin), Réseau Hospitalier
de Médecine Sociale La Madeleine Ath (Dr
Coulon), CHU Saint-Pierre Bruxelles (Dr
Barlow), Réseau Hospitalier de Médecine
Sociale Tournai (Dr Delvoye), CH Françoise Rabelais Cesar de Paepe Bruxelles
(Dr Verougstraete), CH Peltzer La
Tourelle Verviers (Dr Deville), Centre de
Santé des Fagnes Chimay (Dr Dewille),
CHR Namur (Dr D’Huslt), Hôpital St Joseph Mons (Dr du Bois d’Enghien), CHU
Liège (Pr Foidart), CHU Tivoli La Louvière (Dr Francotte), CHR Haute Senne
Soignies (Dr Gielen), Intercommunale Fa-
Research
menne Ardenne Condroz Princesse Paola
Marche (Dr Gilles), CHR Val de Sambre
Auvelais (Dr Verheyen), Cliniques Universitaires St Luc Bruxelles (Pr Bernard, Pr
Hubinont), CH Mouscron (Dr Jacob),
Hôpital Reine Astrid Malmedy (Dr Lavalleye), CHU Brugmann Bruxelles (Pr Vokaer), Hôpital St Pierre Ottignies (Dr
Longueville), CH Jolimont (Dr Guilmot),
CHU Erasme Bruxelles (Dr Kirkpatrick),
CH Notre Dame Charleroi (Dr Sartenaer),
CH Hornu-Frameries (Dr Semoulin),
CHBA Seraing (Pr Van Cauwenberge),
Hôpital St Jean Bruxelles (Dr Venderick),
CH François Rabelais Français Reine Elisabeth Bruxelles (Dr Vermeulen), Hôpital
Notre Dame des Bruyères Chenée (Dr Vigis), Hôpital Notre Dame Tournai (Dr
Wauters), Hôpital Notre Dame Hermalle
(Dr Romedenne).
OCTOBER 2012 American Journal of Obstetrics & Gynecology
285.e9