org
OBSTETRICS
Mode of delivery of twin gestation with very
low birthweight: is vaginal delivery safe?
Eran Barzilay, MD, PhD; Shali Mazaki-Tovi, MD; Uri Amikam, BSc; Hila de Castro, MD;
Jigal Haas, MD; Ram Mazkereth, MD; Eyal Sivan, MD; Eyal Schiff, MD; Yoav Yinon, MD
OBJECTIVE: The purpose of this study was to determine whether vaginal delivery groups was evident in both twin A (17.6% vs 7.0%;
planned vaginal delivery is associated with increased risk of perinatal P .029) and twin B (15.7% vs 4.9%; P .014); however, these
death and morbidity in twin pregnancies that are complicated by a very differences were not significant after adjustment for possible con-
low birthweight of the second twin. founders (twin A: adjusted OR, 1.79; 95% CI, 0.58e5.55; twin B:
adjusted OR, 2.13; 95% CI, 0.63e7.25). In addition, subgroup
STUDY DESIGN: We conducted a retrospective cohort study of twin
analysis revealed that both cephalic-cephalic and cephalic-
pregnancies in which the second twins birthweight was 1500 g.
noncephalic twins who were delivered vaginally had increased risk
One hundred ninety-three twin gestations met the study criteria; pa-
for intraventricular hemorrhage. There were no significant differences
tients were classified into 2 groups according to the planned mode of
between the cesarean and vaginal delivery groups in the rates of Apgar
delivery: (1) cesarean delivery (n 142) and (2) vaginal delivery (n
score <7 at 5 minutes, arterial cord pH <7.1, composite adverse
51). In the vaginal delivery group, 21 pairs were in cephalic-cephalic
neonatal outcome, and neonatal mortality rate. However, the rate of
presentation at the time of delivery; 28 pairs were cephalic-
respiratory distress syndrome was significantly lower in the vaginal
noncephalic, and 2 pairs were noncephalic-noncephalic. Composite
delivery group (66.7% vs 69%; P .042; OR, 0.34; 95% CI,
adverse neonatal outcome was defined as the presence of neonatal
0.12e0.96).
death, respiratory distress syndrome, sepsis, necrotizing enterocolitis,
or intraventricular hemorrhage grade 3-4. CONCLUSION: Vaginal delivery of very low birthweight twins is asso-
ciated with an increased risk of intraventricular hemorrhage, regard-
RESULTS: Trial of vaginal delivery was successful for both twins in
less of presentation. Because of the small sample size and the
90.5% of cephalic-cephalic twins and 96.4% in cephalic-noncephalic
retrospective cohort design, large prospective randomized studies are
twins. The rate of intraventricular hemorrhage was significantly higher
needed.
in the vaginal delivery group (29.4% vs 8.5%, respectively; P .013;
adjusted odds ratio [OR], 3.65; 95% confidence interval [CI], Key words: intraventricular hemorrhage, mode of delivery, twin de-
1.32e10.1). The increased risk of intraventricular hemorrhage in the livery, very low birthweight
Cite this article as: Barzilay E, Mazaki-Tovi S, Amikam U, et al. Mode of delivery of twin gestation with very low birthweight: is vaginal delivery safe? Am J Obstet Gynecol
2015;212:.
some authors have advocated for cesarean were cephalic-cephalic; 28 pairs were Package for the Social Sciences (IBM
deliveries in cases of a second twin in a cephalic-noncephalic, and 2 pairs were SPSS version 19; IBM Corporation Inc,
nonvertex presentation and with an esti- noncephalic-noncephalic. The charts of Armonk, NY).
mated weight of <1500-2000 g.24,25 This all women and their infants were The study was approved by the local
view largely relies on extrapolation of reviewed for the variables of interest. institutional review board.
data from breech deliveries of singleton Maternal characteristics and their preg-
gestation.26,27 nancy outcomes were abstracted from R ESULTS
Other investigators have shown the obstetric electronic charts. The A total of 193 twin deliveries that were
adverse outcome in VLBW twins who following neonatal outcomes were complicated with VLBW of the second
undergo vaginal deliveries and proposed examined: Apgar scores at 5 minutes, twin were identied during the study
that cesarean delivery is the optimal cord blood PH, death, birth trauma period. Of them, 142 delivered by cesarean
route of delivery for all twins who are (spinal cord injury, skull fracture, frac- section without trial of vaginal delivery,
expected to have a birthweight <1500 g, ture of a long bone, peripheral nerve and 51 underwent trial of delivery. The
regardless of presentation.28 injury, and subdural or intracerebral vaginal delivery group included 2 cases of
Decisions regarding mode of delivery hemorrhage), respiratory distress syn- noncephalic-noncephalic twin pregnan-
in VLBW twins are based on very limited drome (RDS), sepsis, necrotizing en- cies that attempted vaginal delivery de-
data. This is especially true for preg- terocolitis (NEC), and intraventricular spite our consultation to have a cesarean
nancies with a VLBW second twin in a hemorrhages (IVH). Composite adverse delivery. The main indications for cesar-
nonvertex presentation. Therefore, we neonatal outcome was dened as the ean delivery were a noncephalic rst twin
aimed to evaluate the association be- presence of neonatal death, RDS, sepsis, (35.3%), intrauterine growth restriction
tween the mode of delivery and perinatal NEC, or IVH grade 3-4. (17.6%), maternal request (12.5%), sus-
morbidity and death in twin pregnancies Because decisions regarding the pected fetal distress (11%), and previous
that are complicated by VLBW of the planned mode of delivery are made per cesarean delivery (5.9%). Demographic
second twin. pregnancy for both twins, we chose to and clinical characteristics of the patients
analyze our data as outcomes per preg- are presented in Table 1. The groups did
M ETHODS nancy. Outcome measures were dened as not differ with regards to maternal age,
All twin deliveries in a single tertiary care outcomes for twin A, twin B, or any twin. parity, body mass index, rate of gestational
medical center from August 2004 to Comparison of continuous variables diabetes mellitus, male/female ratio, and
April 2011 were reviewed. Inclusion between the 2 groups was conducted rate of exposure to antenatal steroids.
criteria included (1) twin gestation and using Mann-Whitney U test or the Stu- However, the median gestational age at
(2) second twin birthweight of 1500 g. dent t test, as appropriate. Chi-square delivery was 31.4 weeks in the cesarean
Exclusion criteria included (1) gesta- test was used for comparison of cate- delivery group compared with 30.4 weeks
tional age at delivery of <24 weeks, (2) goric variables. Logistic regression anal- of gestation in the vaginal delivery group
fetal death of 1 or both twins before la- ysis was used to examine the relationship (P .025). Despite the signicant differ-
bor, and (3) major malformation diag- between mode of delivery and neonatal ence in gestational age at delivery, median
nosed in 1 or both twins. outcome measures. Adjustment was birthweights of both twins were not
The standard of care in our medical conducted for gestational age at delivery, signicantly different between the 2
center regarding twin delivery is to allow chorionicity, and antenatal steroid groups (twin A: cesarean delivery 1417.5 g
vaginal delivery of cephalic-cephalic and treatment because these factors have vs vaginal delivery: 1335 g; P .183; twin
cephalic-noncephalic twins, regardless been shown to be associated signicantly B: 1258 vs 1195 g; P .654). The rate of
of their estimated weight or the gesta- with perinatal death and neonatal monochorionic twins was signicantly
tional age, as long as the estimated morbidity and thus may have a con- higher in the cesarean delivery group
weight of twin B is not signicantly founding potential.29,30 The regression compared with the vaginal delivery group
higher (20%) than twin A. The de- model was limited to 4 variables to ac- (33.8% vs 11.8%; P .034). The mono-
livery is supervised by an experienced count for the small sample size.31 How- chorionic pregnancies in the cesarean
obstetrician under continuous fetal ever, we also used an alternate regression group included 4 cases of monoamniotic
monitoring, and the preferred method model that adjusted for maternal age, pregnancies. The higher rate of mono-
for delivering the noncephalic second parity, and birthweight in addition to chorionic pregnancies was adjusted for in
twin is total breech extraction with or gestational age at delivery, chorionicity, our regression model.
without internal podalic version. and antenatal steroid treatment. This In 8 cases in the vaginal delivery
A total of 193 twin gestations met the model was not used in subgroup analysis group, labor was induced because of
study criteria. Patients were classied according to presentation because the intrauterine growth restriction. Out-
into 2 groups according to the planned subgroups were signicantly smaller. come in induced twin pregnancies was
mode of delivery: cesarean delivery (n Signicance was accepted at a probabil- generally favorable (no cases of RDS,
142) and vaginal delivery (n 51). In ity value of < .05. Statistical analyses IVH, or death; 1 neonate with NEC),
the vaginal delivery group, 21 pairs were conducted with the IBM Statistical most likely because of the relatively
TABLE 3
Neonatal outcome
Cesarean delivery Vaginal delivery Adjusted Adjusted odds ratio (95% CI)
Variable (n [ 142), n (%) (n [ 51), n (%) P value P value Model 1 Model 2
Any twin
5-Min Apgar score <7 9 (6.3) 2 (3.9) .523 .09 0.2 (0.03e1.29) 0.26 (0.04e1.83)
Umbilical artery pH <7.1 a
2/74 (2.7) 0/31 (0) .362 .995 NA b
NAb
Composite outcome 107 (75.4) 37 (72.5) .693 .076 0.4 (0.14e6.91) 0.28 (0.09e0.88)
Death 8 (5.6) 4 (7.8) .575 .679 0.74 (0.18e3.08) 1.29 (0.25e6.55)
Respiratory distress syndrome 98 (69) 34 (66.7) .757 .042 0.34 (0.12e0.96) 0.25 (0.08e0.76)
Necrotizing enterocolitis 7 (4.9) 2 (3.9) .77 .809 0.82 (0.16e4.17) 1.37 (0.23e8.28)
Sepsis 18 (35.3) 48 (33.8) .847 .385 0.71 (0.33e1.53) 0.61 (0.26e1.47)
Intraventricular hemorrhage 12 (8.5) 15 (29.4) < .001 .013 3.65 (1.32e10.1) 4.86 (1.54e15.34)
Intraventricular hemorrhage 3 (2.1) 6 (11.8) .005 .281 2.56 (0.46e14.08) 4.88 (0.51e47.1)
grade 3-4
Neonatal intensive care 129 (90.8) 46 (90.2) .891 .751 0.78 (0.17e3.55) 0.69 (0.14e3.46)
unit admission
Twin A
5-Min Apgar score <7 4 (2.8) 0 .226 .997 NAb NAb
Umbilical artery pH <7.1 a
2/91 (2.2) 0/32 (0) .398 .997 NA b
NAb
Composite outcome 87 (61.3) 31 (60.8) .952 .116 0.49 (0.2e1.19) 0.34 (0.13e0.9)
Death 3 (2.1) 3 (5.9) .183 .716 0.66 (0.07e5.99) 0.86 (0.08e9.75)
Respiratory distress syndrome 83 (58.5) 29 (56.9) .844 .08 0.46 (0.19e1.1) 0.34 (0.13e0.88)
Necrotizing enterocolitis 2 (1.4) 1 (2.0) .784 .819 1.33 (0.11e15.87) 4.14 (0.17e102.4)
Sepsis 21 (14.8) 11 (21.6) .264 .871 0.92 (0.35e2.43) 0.68 (0.23e2)
Intraventricular hemorrhage 10 (7.0) 9 (17.6) .029 .311 1.79 (0.58e5.55) 2.16 (0.6e7.82)
Intraventricular grade 3-4 2 (1.4) 4 (7.8) .023 .321 2.66 (0.38e18.52) 3.47 (0.34e35.7)
Neonatal intensive care 111 (78.2) 42 (82.4) .527 .882 0.9 (0.22e3.56) 0.59 (0.13e2.74)
unit admission
Twin B
5-Min Apgar score <7 6 (4.3) 2 (3.9) .919 .152 1.06 (0.46e2.44) 0.22 (0.02e2.43)
Umbilical artery pH <7.1 a
1/88 (1.1) 0/37 (0) .515 .996 NA b
NAb
Composite outcome 94 (73.4) 34 (66.7) .951 .115 0.45 (0.17e1.21) 0.38 (0.13e1.1)
Death 6 (4.2) 4 (7.8) .317 .972 1.03 (0.23e4.57) 5.24 (0.26e105.3)
Respiratory distress syndrome 79 (55.6) 32 (62.7) .378 .499 0.73 (0.29e1.84) 0.41 (0.14e1.19)
Necrotizing enterocolitis 7 (4.9) 1 (2.0) .362 .389 0.39 (0.05e3.32) 0.67 (0.07e6.5)
Sepsis 37 (26.1) 12 (23.5) .722 .241 0.61 (0.27e1.39) 0.76 (0.3e1.93)
Intraventricular hemorrhage 7 (4.9) 8 (15.7) .014 .224 2.13 (0.63e7.25) 4.47 (0.99e20.1)
Intraventricular hemorrhage 2 (1.4) 3 (5.9) .084 .948 0.92 (0.08e10.53) 1.06 (0.04e27.1)
grade 3-4
Neonatal intensive care 124 (87.3) 45 (88.2) .866 .809 0.85 (0.23e3.07) 0.82 (0.22e3.1)
unit admission
Logistic regression was performed to correct for possible confounders that included gestational age, antenatal steroids, and chorionicity (model 1) or gestational age, antenatal steroids, chorionicity,
maternal age, birthweight, and parity (model 2).
NA, not available.
a
Umbilical artery pH was not available for all cases; the effective denominator is noted for each group; b Odds ratios were not calculated for cases with extremely high probability values (>.99).
Barzilay. Mode of delivery in VLBW twins. Am J Obstet Gynecol 2015.
TABLE 4
Neonatal outcome: subanalysis according to presentation
Vaginal delivery Adjusted odds ratio
Cesarean delivery cephalic-cephalic Adjusted (95% confidence
Variable (n [ 142), n (%) only (n [ 21), n (%) P value P value interval)
Composite outcome 107 (75.4) 16 (76.2) .934 .343 0.46 (0.09e2.3)
Death 8 (5.6) 1 (4.8) .87 .625 0.58 (0.06e5.18)
Respiratory 98 (69) 15 (71.4) .823 .251 0.4 (0.09e1.9)
distress syndrome
Intraventricular hemorrhage 12 (8.5) 7 (33.3) .001 .022 4.35 (1.24e15.38)
Intraventricular 3 (2.1) 1 (4.8) .464 .79 1.5 (0.07e30.3)
hemorrhage grade 3-4
Vaginal delivery
cephalic-noncephalic
only (n 28)
Composite outcome 107 (75.4) 19 (67.9) .408 .072 0.32 (0.09e1.11)
Death 8 (5.6) 2 (7.1) .756 .744 0.74 (0.12e4.63)
Respiratory 98 (69) 17 (60.7) .391 .041 0.27 (0.08e0.95)
distress syndrome
Intraventricular hemorrhage 12 (8.5) 8 (28.6) .003 .025 4.88 (1.22e19.23)
Intraventricular 3 (2.1) 5 (17.9) < .001 .055 6.58 (0.96e45.45)
hemorrhage grade 3-4
Logistic regression was performed to correct for possible confounders that included gestational age, antenatal steroids, and chorionicity.
Barzilay. Mode of delivery in VLBW twins. Am J Obstet Gynecol 2015.
decreased risk for RDS in the vaginal de- 144 twin pregnancies that delivered both the regression model was altered to
livery group was signicant after adjust- twins by cesarean delivery and 48 twin include more confounders, the only
ment only in the cephalic-noncephalic pairs that delivered both twins vaginally. difference that was noted in our results
subgroup (60.7% vs 69%; P .041; OR, The median gestational age was lower in was that the risk for composite outcome
0.27; 95% CI, 0.08e0.95). There were no the vaginal delivery group compared was signicantly lower in the vaginal
signicant differences compared with the with the cesarean delivery group (30.4 vs delivery group.
cesarean delivery group in all other 31.3 weeks); albeit, this difference was
outcome measures (NEC, sepsis, neonatal not statistically signicant (P .073). C OMMENTS
intensive care unit admission, low 5- Similar to analysis by intended mode of In this study, we examined the safety of
minute Apgar score, and low arterial pH) delivery, vaginal delivery was associated vaginal delivery of twins that was
for either cephalic-cephalic twins or with a signicant increase in risk for IVH complicated by VLBW of the second
cephalic-noncephalic twins (data not compared with cesarean delivery, a trend twin. There were no signicant differ-
shown). for increased risk for IVH grade 3-4 and ences in the rates of low Apgar score, low
Both cases of noncephalic-noncephalic a signicant reduction in risk for RDS arterial cord pH, composite adverse
pregnancies that attempted vaginal de- (Table 5). neonatal outcomes, or death between the
livery achieved vaginal delivery without Finally, we examined whether ex- vaginal delivery group and the cesarean
birth trauma or entrapment of the after- cluding the cases with a presenting delivery group. However, we have
coming head. One pair was born at 24 noncephalic presentation will change demonstrated that vaginal delivery of
weeks of gestation (both twins died during our results. Similar to our primary VLBW twins is associated with an
the rst 2 days of life). The other patient analysis, vaginal delivery was associated increased risk of IVH. This increase in
delivered at 31 weeks of gestation (both with a statistically signicant increase in risk was similar in cephalic-cephalic and
infants had RDS; twin A had sepsis, but risk for IVH, a trend for increased risk cephalic-noncephalic twins. The differ-
neither twin had IVH). for IVH grade 3-4 and a signicant ence in rate of IVH grade 3-4 did not
Next, we sought to assess whether our reduction in risk for RDS (Table 6). The reach statistical signicance, possibly
results will change if we divided the data depicted in Tables 5 and 6 was also because of the small sample size. On the
groups by mode of delivery instead of analyzed with the use of the second other hand, the risk for RDS appeared to
intended mode of delivery. There were regression model. In both cases, when be decreased in the vaginal delivery
TABLE 5
Neonatal outcome: subanalysis according to actual mode of delivery
Adjusted odds ratio
Cesarean delivery Vaginal delivery (95% confidence interval)
Variable (n [ 144), n (%) (n [ 48), n (%) P value Adjusted P value Model 1 Model 2
Composite outcome 109 (75.7) 34 (70.8) .503 .07 0.39 (0.14e1.08) 0.28 (0.09e0.87)
Death 8 (5.6) 4 (8.3) .491 .809 0.84 (0.2e3.5) 1.45 (0.29e7.32)
Respiratory distress syndrome 100 (69.4) 31 (64.6) .531 .038 0.36 (0.12e0.94) 0.24 (0.08e0.74)
Intraventricular hemorrhage 13 (9) 14 (29.2) .001 .017 3.53 (1.26e9.9) 4.58 (1.47e14.26)
Intraventricular hemorrhage 3 (2.1) 6 (12.5) .003 .217 2.96 (0.53e16.39) 5.73 (0.61e53.5)
grade 3-4
Logistic regression was performed to correct for possible confounders that included gestational age, antenatal steroids, and chorionicity (model 1) or gestational age, antenatal steroids, chorionicity,
maternal age, birthweight, and parity (model 2).
Barzilay. Mode of delivery in VLBW twins. Am J Obstet Gynecol 2015.
group compared with the cesarean de- prospective randomized trial compared Morales et al34 examined neonatal
livery group. Thus, vaginal delivery delivery strategies for twins between 32 outcome of 156 VLBW twin pairs who
may have a protective effect against RDS, and 38 weeks of gestation and reported were born from 1981-1986 and did
as has been suggested in previous on similar neonatal outcomes between not nd an advantage for cesarean de-
studies.32-34 planned cesarean delivery and planned livery. In accordance with our ndings,
Because low-grade IVH is considered vaginal delivery. However, the inclusion the aforementioned study demonstrated
to have less clinical impact compared criteria for this trial included estimated an increase in IVH grade 3-4 after
with high-grade IVH, the clinical sig- fetal weight of 1500-4000 g; therefore, vaginal delivery when at least 1 twin
nicance of an increase in IVH rate this study was not designed to address was noncephalic. However, the increase
without a signicant increase in the rate the issue of mode of delivery of VLBW in risk was not statistically signicant
of high-grade IVH is yet to be deter- twins.23 Our inclusion criteria were after correction for confounders. A
mined. Nevertheless, studies have shown based on birthweight and not estimated population-based study that included all
that low-grade IVH can impact the fetal weight. Taking into account the twin births in the United States from
neonatal brain35 and that low-grade accuracy of fetal-weight estimations, 1995-1997 has shown increased mo-
IVH may be associated with neuro- some authors suggested to use a 2000-g rbidity and death risk in vaginal de-
developmental impairment of preterm cutoff when considering mode of de- liveries of twins compared with cesarean
infants.36 livery.25 However, the twin birth trial deliveries13 with a more pronounced
Data on mode of delivery in twin demonstrated the safety of breech de- death risk in VLBW infants. However,
pregnancies complicated by VLBW livery of the second twin when estimated the data in this study were derived from
twins is very limited. Recently, a large fetal weight was 1500 g.23 many centers with great variability in the
TABLE 6
Neonatal outcome: a subanalysis restricted to cases with a cephalic presentation of the first twin
Adjusted odds ratio
Cesarean delivery Vaginal delivery Adjusted (95% confidence interval)
Variable (n [ 142), n (%) (n [ 49), n (%) P value P value Model 1 Model 2
Composite outcome 107 (75.4) 35 (71.4) .588 .068 0.387 (0.14e1.07) 0.28 (0.09e0.87)
Death 8 (5.6) 3 (6.1) .899 .534 0.62 (0.13e2.85) 1.14 (0.2e6.47)
Respiratory distress syndrome 98 (69) 32 (65.3) .631 .036 0.33 (0.12e0.93) 0.24 (0.08e0.74)
Intraventricular hemorrhage 12 (8.5) 15 (30.6) < .001 .006 4.42 (1.55e12.63) 6.03 (1.81e20.03)
Intraventricular hemorrhage 3 (2.1) 6 (12.2) .004 .191 3.14 (0.57e17.4) 6.15 (0.57e65.8)
grade 3-4
Logistic regression was performed to correct for possible confounders that included gestational age, antenatal steroids, and chorionicity (model 1) or gestational age, antenatal steroids, chorionicity,
maternal age, birthweight, and parity (model 2).
Barzilay. Mode of delivery in VLBW twins. Am J Obstet Gynecol 2015.
and method of delivery. Am J Perinatol 2000;17: controlled study of vaginal and abdominal de- 36. Klebermass-Schrehof K, Czaba C,
303-7. livery of the low birth weight breech fetus. Obstet Olischar M, et al. Impact of low-grade intraven-
17. Adam C, Allen AC, Baskett TF. Twin de- Gynecol 1979;54:310-3. tricular hemorrhage on long-term neuro-
livery: inuence of the presentation and method 27. Goldenberg RL, Nelson KG. The premature developmental outcome in preterm infants.
of delivery on the second twin. Am J Obstet breech. Am J Obstet Gynecol 1977;127:240-4. Childs Nerv Syst 2012;28:2085-92.
Gynecol 1991;165:23-7. 28. Barrett JM, Staggs SM, Van Hooydonk JE, 37. Minguez-Milio JA, Alcazar JL, Auba M, Ruiz-
18. Gocke SE, Nageotte MP, Garite T, Growdon JH, Killam AP, Boehm FH. The effect Zambrana A, Minguez J. Perinatal outcome and
Towers CV, Dorcester W. Management of the of type of delivery upon neonatal outcome in long-term follow-up of extremely low birth
nonvertex second twin: primary cesarean sec- premature twins. Am J Obstet Gynecol weight infants depending on the mode of de-
tion, external version, or primary breech extrac- 1982;143:360-7. livery. J Matern Fetal Neonatal Med 2011;24:
tion. Am J Obstet Gynecol 1989;161:111-4. 29. Mwansa-Kambafwile J, Cousens S, 1235-8.
19. Breathnach FM, McAuliffe FM, Geary M, Hansen T, Lawn JE. Antenatal steroids in pre- 38. Ment LR, Oh W, Philip AG, et al. Risk factors
et al. Prediction of safe and successful vaginal term labour for the prevention of neonatal deaths for early intraventricular hemorrhage in low birth
twin birth. Am J Obstet Gynceol 2011;205:237. due to complications of preterm birth. Int J weight infants. J Pediatr 1992;121:776-83.
e1-7. Epidemiology 2010;39(suppl 1):i122-33. 39. Ment LR, Oh W, Ehrenkranz RA, Philip AG,
20. Crowther CA. Caesarean delivery for the 30. Vergani P, Russo FM, Follesa I, et al. Peri- Duncan CC, Makuch RW. Antenatal steroids,
second twin. Cochrane Database Syst Rev natal complications in twin pregnancies after 34 delivery mode, and intraventricular hemorrhage
2000:CD000047. weeks: effects of gestational age at delivery and in preterm infants. Am J Obstet Gynecol
21. Hogle KL, Hutton EK, McBrien KA, chorionicity. Am J Perinatol 2013;30:545-50. 1995;172:795-800.
Barrett JF, Hannah ME. Cesarean delivery for 31. Sainani K. The limitations of statistical 40. Philip AG, Allan WC. Does cesarean section
twins: a systematic review and meta-analysis. adjustment. PM R 2011;3:868-72. protect against intraventricular hemorrhage in
Am J Obstet Gynecol 2003;188:220-7. 32. Jain NJ, Kruse LK, Demissie K, preterm infants? J Perinatol 1991;11:3-9.
22. Rabinovici J, Barkai G, Reichman B, Khandelwal M. Impact of mode of delivery on 41. Riskin A, Riskin-Mashiah S, Bader D, et al.
Serr DM, Mashiach S. Randomized manage- neonatal complications: trends between 1997 Delivery mode and severe intraventricular hem-
ment of the second nonvertex twin: vaginal de- and 2005. J Matern Fetal Neonatal Med orrhage in single, very low birth weight, vertex
livery or cesarean section. Am J Obstet Gynecol 2009;22:491-500. infants. Obstet Gynecol 2008;112:21-8.
1987;156:52-6. 33. Levine EM, Ghai V, Barton JJ, Strom CM. 42. Paul DA, Sciscione A, Leef KH, Stefano JL.
23. Barrett JF, Hannah ME, Hutton EK, et al. Mode of delivery and risk of respiratory dis- Caesarean delivery and outcome in very low
A randomized trial of planned cesarean or eases in newborns. Obstet Gynecol 2001;97: birthweight infants. Aust N Z J Obstet Gynaecol
vaginal delivery for twin pregnancy. N Engl J Med 439-42. 2002;42:41-5.
2013;369:1295-305. 34. Morales WJ, OBrien WF, Knuppel RA, 43. Malloy MH, Onstad L, Wright E. The effect of
24. Udom-Rice I, Skupski DW, Chervenak FA. Gaylord S, Hayes P. The effect of mode of de- cesarean delivery on birth outcome in very low
Intrapartum management of multiple gestation. livery on the risk of intraventricular hemorrhage in birth weight infants: National Institute of Child
Semin Perinatol 1995;19:424-34. nondiscordant twin gestations under 1500 g. Health and Human Development Neonatal
25. Chervenak FA, Johnson RE, Youcha S, Obstet Gynecol 1989;73:107-10. Research Network. Obstet Gynecol 1991;77:
Hobbins JC, Berkowitz RL. Intrapartum man- 35. Morita T, Morimoto M, Yamada K, et al. 498-503.
agement of twin gestation. Obstet Gynecol Low-grade intraventricular hemorrhage disrupts 44. Low JA, Galbraith RS, Sauerbrei EE, et al.
1985;65:119-24. cerebellar white matter in preterm infants: evi- Maternal, fetal, and newborn complications
26. Duenhoelter JH, Wells CE, Reisch JS, dence from diffusion tensor imaging. Neurora- associated with newborn intracranial hemor-
Santos-Ramos R, Jimenez JM. A paired diology 2015 [Epub ahead of print]. rhage. Am J Obstet Gynecol 1986;154:345-51.