The Journal of Maternal-Fetal and Neonatal Medicine, 2012; 25(4): 424428

2012 Informa UK, Ltd.

ISSN 1476-7058 print/ISSN 1476-4954 online
DOI: 10.3109/14767058.2011.569800

Preterm premature rupture of membranes in the presence of cerclage: is

the risk for intra-uterine infection and adverse neonatal outcome
increased?
MATTHEW D. LASKIN, YOAV YINON, & WENDY L. WHITTLE
Department of Obstetrics and Gynaecology, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada
Abstract
Objective. To determine whether preterm premature rupture of membranes (PPROM) in the presence of a cerclage is associated
with an increased incidence of intrauterine infection and/or adverse neonatal outcome compared to PPROM in the absence of
cerclage.
Study design. Patients diagnosed with PPROM with a cerclage (cases) between 2434 weeks were matched (1:2.6) for gestational
age at PPROM, gestational number, and chorionicity with patients diagnosed with PPROM without a cerclage (controls).
Results. Pregnancy latency period was not different but the rates of chorioamnionitis [clinical (26.6% versus 13.5%) and
histological (92.6% versus 65.4%)] and the rates of adverse perinatal outcome were higher following PPROM in the presence of a
cerclage compared with no cerclage.
Conclusion. The presence of a cerclage in patients with PPROM appears to increase the risk of intra-uterine infection and affect
neonatal outcome; it may not be justified to leave a cerclage in place in patients with PPROM.
Keywords: Cerclage, PPROM, chorioamnionitis

Introduction
Spontaneous preterm delivery (PTD) occurs in 58% of all
pregnancies, one-third of which is attributed to preterm
premature rupture of membranes (PPROM) [1]. In patients
with a cervical cerclage, regardless of the indication for the
suture, the rate of PPROM is estimated to be as high as 30%.
Routine care of patients with PPROM in the absence of labor
and/or fetal distress, since the publication of the ORACLE
trial in 2002, includes fetal and maternal surveillance for signs
of chorioamnionitis and/or fetal distress with the initiation of a
7-day course of erythromycin therapy to reduce the composite
risk of neonatal morbidity [2]. However, the management of
PPROM in the presence of a cerclage has not been well
defined. Studies by Ludmir et al. [3], Kuhn and Pepperell [4],
and OConnor et al. [5] each found an increase in pregnancy
latency (time from diagnosis of PPROM to delivery) but a
concomitant increase in perinatal morbidity and mortality
when a cerclage remained in situ after PPROM. In contrast,
studies by Yeast and Garite [6] and Kominiarek and Kemp
[7] detected no difference in obstetrical outcome with cerclage
removal or retention following PPROM. Jenkins et al. [8] and
McElrath et al. [9,10] compared patients with and without a
cerclage following PPROM and found no difference in
obstetrical and neonatal outcomes. Taken as a whole, the
data suggest that PPROM is not an absolute indication for
removal of the cerclage and that expectant management

following PPROM with a cerclage in situ may be appropriate.

However, each of these studies predates the ORACLE trial
finds supporting the use of erythromycin after the diagnosis of
PPROM. Therefore, the current study was undertaken to test
the hypothesis that PPROM in the presence of a cervical
cerclage is not associated with an increased incidence of
intrauterine infection and/or adverse neonatal outcome in the
current era of clinical practice. Our study objectives were to
determine whether there was a difference in latency, rates of
clinical and histological chorioamnionitis, and rates of adverse
intrauterine and neonatal outcomes in patients following
PPROM in the presence and absence of a cervical cerclage.

Materials and methods

A retrospective observational cohort study with matched
controls was conducted at Mount Sinai Hospital (Toronto,
Ontario, Canada) between January 2002 and December 2008
with institutional ethics board approval (REB08-0128-C).
Cases were identified by chart review as patients diagnosed
with preterm premature ruptured fetal membranes (PPROM)
between 24 and 34 completed weeks gestation in the presence
of a cervical cerclage. At our institution it is conventional
obstetrical practice to leave the cerclage in place following the
diagnosis of PPROM; in all of the cases, the cerclage was only
removed once the decision for delivery was made by the
attending physician. The types of cervical cerclage were

(Received 27 October 2010; revised 3 March 2011; accepted 4 March 2011)

Correspondence: Wendy L. Whittle, Department of Obstetrics and Gynaecology, Room 3157, Mount Sinai Hospital, 700 University Avenue, Toronto,
Ontario, Canada M5G 1Z5. Tel: 1-416-586-4800, 2452. Fax: 1-416-586-8718. E-mail: wwhittle@mtsinai.on.ca
These findings were presented at the Society for Maternal Fetal Medicine Annual Clinical Meeting, Chicago, USA; January 2010 (abstract no. 0443).

Perinatal outcome after PPROM with cerclage

categorized based on history as: (1) elective placed
prophylactically based on obstetrical history or in the presence
of a transvaginal ultrasound cervical length less than or equal
to 2.5 cm; (2) rescue placed when the cervix was dilated and
the fetal membranes visible at or beyond the internal cervical
os; and/or (3) repeat a rescue cerclage (as previously
defined) done in the presence of a previous cerclage placed
anytime in the current pregnancy. Controls were defined as
patients diagnosed with PPROM between 24 and 34
completed weeks gestation in the absence of a cerclage. The
cases were randomly matched 1:2.6 to controls for gestational
age at diagnosis of PPROM +2 days and year of delivery (to
account for subtle year-to-year changes in practice). The
clinical management of the case and control patients was at
the discretion of the attending physician.
The outcomes measured were: (1) latency defined as the
time (in weeks) from diagnosis of PPROM to delivery; (2)
clinical chorioamnionitis any of the following clinical events
that triggered delivery based on the discretion of the attending
physician: elevated maternal temperature (437.88C), maternal leukocytosis (414 6 109/l), and/or fetal tachycardia
(4160 bpm); (3) histological chorioamnionitis any of the
following identified on placental pathology: acute chorioamnionitis (grade IIII), acute deciduitis and/or funisitis; and (4)
adverse fetal and neonatal events including intrauterine fetal
demise, neonatal death (NND), neonatal sepsis, respiratory
distress syndrome (RDS), neonatal anemia, necrotizing
enterocolitis, and grade III and IV intraventricular hemorrhage (IVH). Each neonatal diagnosis was taken from the
coding diagnoses on the neonatal discharge summary and was
at the discretion of the attending neonatologist.
A significance value of p 5 0.05 was used in all statistical
analyses. Continuous variables were analyzed using an
unpaired t-test and categorical variables with a Fishers exact
test.

Results
A total of 668 patients were diagnosed with preterm
premature ruptured fetal membranes (PPROM) between 24
and 34 completed weeks gestation during the observation
period. Of these 76 (11.4%) were diagnosed with PPROM in
the presence of a cervical cerclage (cases) and 592 patients
(88.6%) had PPROM in the absence of a cerclage (controls).
From this cohort, 170 controls were matched to the 64 cases
upon eliminating all multiple gestational pregnancies. Table I
summarizes the demographics of the two matched groups.
There was no significant difference in maternal age, gravidy,

425

parity, or Celestone use. All cases and controls were planned

to initiate erythromycin treatment (250 mg QID for 7 days) at
the time of diagnosis; however, almost an equal number of
patients in both groups delivered prior to the initiation of
antibiotic therapy. As expected, there was a significantly
higher rate of prior spontaneous preterm birth and prior
PPROM in the case group (35.9% and 9.4%, respectively)
compared to controls (17.2% and 1.8%, respectively). As
well, there was a higher rate of cesarean section in the cerclage
group compared to the control group (46.8% versus 26.2%).
To account for the potential effect of gestational age at
diagnosis of PPROM on latency and obstetrical outcome the
gestational age at PPROM was categorized as either (1)
extreme prematurity with PPROM prior to 28 weeks gestation
or (2) mildmoderate prematurity with PPROM between 28
and 34 completed weeks gestation. When classified by
gestational age at PPROM, there were no significant
differences with respect to the mean gestational age at
diagnosis of PPROM, mean gestational age at delivery, and
mean latency interval (Table II).
The incidence of both clinical and histological chorioamnionitis in the study cohort as a whole is illustrated in Figure
1. As expected, the rate of histological chorioamnionitis was
greater than that of clinical chorioamnionitis for both the cases
and controls. Overall, there was a significantly higher rate of
both clinical and histological chorioamnionitis in the cases
versus controls (26.6% versus 13.5%; p 0.03; and 92.6%
versus 65.4%; p 0.02). The rates of both clinical and
histological chorioamnionitis were greatest in patients with
cerclage who were diagnosed with PPROM prior to 28 weeks
gestation as illustrated in Figure 2. If delivery occurred prior
to 28 weeks gestation, 35.9% of patients with cerclage were
diagnosed with clinical chorioamnionitis and delivered as
compared with only 15.1% of patients without a cerclage
(p 0.03). The overall incidence of histological chorioamnionitis in patients who delivered prior to 28 weeks gestation was
greater than 90%; in the presence of a cerclage the rate was
modestly increased (97.1% versus 90.2%; p 0.39). The
incidence of clinical and histological chorioamnionitis was
lower if delivery occurred after 28 weeks gestation in the
presence or absence of a cerclage. If delivery occurred after 28
weeks gestation there was no difference in the rate of clinical
chorioamnionitis triggering delivery between the cases and
controls (12.0% versus 12.8%; p 1.00); however, the rate of
histological chorioamnionitis was greater in the presence of a
cerclage (85.0% versus 53.7%; p 0.01). A history of preterm
birth did not influence the rate of clinical or histological
chorioamnionitis in either group of patients.

Table I. Patient demographics of both the cases and control groups.

Cases (n 64)
Maternal age (yrs)
Mean gravidy
Mean parity
Mean abortus
History PTB
History PPROM
Erythromycin use
Celestone use
Previous cerclage
Mode of delivery Vaginal C. section
Italic values: p  0.05.

31.6 5.6
32
11
11
35.9%
17.2%
71.9%
78.1%
17.2%
53.1%

(18-43)
(0-13)
(0-6)
(0-6)
(23)
(11)
(46)
(50)
(11)
(34) 46.9% (30)

Control (n 170)
31.2 6.2
32
11
11
9.4%
1.8%
60.6%
77.7%
0.0%
71.8%

(16-43)
(1-8)
(0-6)
(0-5)
(16)
(3)
(103)
(132)
(0)
(122) 28.2% (48)

p-value
1.00
1.00
1.00
1.00
0.0001
0.0001
0.13
1.00
0.0001
0.008

426

M. D. Laskin et al.

Table II. Mean gestational age at PPROM, delivery and latency for
both cases and controls.
Extreme prematurity
(delivery 528 weeks)

Case
(n 39)

Control
(n 53)

p-values

Mean GA at PPROM (wks)

Mean GA at delivery (wks)
Mean latency (wks)

24.8 1.7
25.8 1.7
1.0 1.7

25.4 1.4
27.0 2.0
1.6 2.1

0.78
0.66
0.83

Prematurity
(delivery 428 weeks)
Mean GA at PPROM (wks)
Mean GA at delivery (wks)
Mean latency (wks)

Case
(n 25)
31.5 2.3
32.1 2.0
0.6 0.6

Control
(n 117)
31.7 2.1
32.2 1.9
0.5 0.7

p-values
0.96
0.98
0.95

Figure 1. Incidence of clinical and histological chorioamnionitis.

(*p 5 0.05).

Figure 2. Incidence of clinical and histological chorioamnionitis

divided into gestational age at PPROM. (* and ap 5 0.05).

To determine any effect of cerclage type on the incidence

of infectious pathology, the cases were evaluated based on
cerclage classification. With respect to the cases, 28.1%
received an elective cerclage, 71.9% had a rescue cerclage
and of those 12.5% had a repeat cerclage. Overall, there were
no significant differences in the incidence of clinical chorioamnionitis triggering delivery when cases were compared by
cerclage type; however, the incidence of clinical chorioamnionitis in the cases was always greater than that of the control
group regardless of cerclage type. As well, there was a
significantly higher rate of histological chorioamnionitis
compared with controls (Figure 3).

Perinatal outcome data are presented in Figure 4. There

was a significantly greater incidence of sepsis (p 0.05),
neonatal respiratory distress (p 0.003), and neonatal anemia
(p 0.002) in the neonates delivered after PPROM in the
presence of a cerclage compared to neonates delivered
following PPROM in the absence of a cerclage. As well, there
was a trend to higher rates of rates intrauterine demise
(p 0.3), NND (p 0.14), and IVH (p 0.25) for neonates
delivered after PPROM in the presence of a cerclage but these
were not statistically significant values.

Discussion
Preterm premature rupture of the fetal membranes (PPROM)
accounts for approximately one-third of all spontaneous
preterm births and often is complicated by the presence of a
cervical cerclage. Traditional acute management of PPROM
in the absence of indications for delivery including chorioamnionitis, preterm labor, maternal and/or fetal distress is
expectant with the recent introduction of erythromycin
treatment to reduce neonatal morbidity based on the findings
of the ORACLE study [2]. However, there is a paucity of
information to guide the acute management of PPROM in the
presence of a cerclage as all studies predate the use of
erythromycin. In our study, the cerclage was only removed at
the time the patient went into spontaneous labor or a decision
was made for delivery (based on clinical chorioamnionitis,
fetal distress) as is the standard obstetrical practice at our
institution. The objective of our study was to determine
whether pregnancy latency, the rates of chorioamnionitis, and
adverse intrauterine and neonatal outcomes in patients
following PPROM differed in the presence and absence of a
cervical cerclage in the current era of clinical practice. We
determined that when compared with patients without a
cerclage, the latency period is not affected by the presence of
the cerclage but the rates of chorioamnionitis (both clinical
and histological) and the rates of adverse perinatal outcome
are higher following PPROM in the presence of a cervical
cerclage. The higher rate of chorioamnionitis is especially
pronounced when the patient is diagnosed with PPROM prior
to 28 weeks of gestation.
Latency was no different for patients diagnosed with
PPROM before and after 28 weeks of gestation both in the
presence and absence of a cerclage. The average time to
delivery was 710 days regardless of the cerclage and/or
gestational age at diagnosis. These findings are contrary to
several previous reports [35]. Kuhn and Pepperall (1977)
reported that regardless of the gestational age at diagnosis of
PPROM, latency was increased when the cerclage was left in
situ. This study was not a randomized control trial to
determine the effect of cerclage retention on latency, the
indications for cerclage retention or removal were not
specified and the sample size was limited to 31 patients with
cerclage removal retrospectively compared with 38 patients
with cerclage retention [4]. Ludmir et al. (1994) also reported
an increase in pregnancy latency with cerclage retention when
27 patients diagnosed with PPROM in the presence of a
cerclage were compared with 33 patients diagnosed with
PPROM without a cerclage; the cerclage was removed in 20
patients following PPROM with no specific protocol or
indication regarding cerclage removal versus retention [3].
However, Ludmir did determine that a greater portion of
patients whose cerclage was immediately removed delivered
within the first 24 h compared with those who retained the

Perinatal outcome after PPROM with cerclage

Figure 3. Incidence of clinical and histological chorioamnionitis based on cerclage type. (*,

Figure 4. Incidence of adverse fetal and neonatal outcomes. (*p 5

0.05).

cerclage suggesting that cerclage retention at least prolongs the

pregnancy by 48 h. Jenkins et al. (2000) retrospectively in a nonrandomized fashion compared immediate cerclage removal with
delayed removal at the time of delivery and found that the
delayed removal group had on average a greater than 5 day
increase in latency [8]. In contrast, and in keeping with our own
study design and findings, McElrath et al. (2000) presented a
casecontrol study with matching based on year of presentation;
51 patients had the cerclage retained until delivery, 30 patients
who had their cerclage removed immediately and both of these
groups were compared with women diagnosed with PPROM in
the absence of a cerclage [9]. There was no significant difference
in latency between the retained, removed, or control groups [9].
Similar findings were reported by Yeast et al. (1988). Taken as a
whole, there is very limited data in support of cerclage removal
or retention at the time of PPROM diagnosis on the sole basis of
latency alone. However, we speculate that latency is not affected
by the presence of the cerclage because the main trigger for
delivery is no longer cervical competence but appears to be
infectious pathology [6].
As expected, chorioamnionitis was the main outcome
associated with PPROM regardless of gestational age or
presence of cerclage. With a cerclage in situ and the diagnosis
of PPROM prior to 28 weeks gestation, over one-third of
these patients were delivered due to clinical chorioamnionitis
and over 90% of patients had histological chorioamnionitis at

427

and bp 5 0.05).

the time of delivery. The rate of clinical chorioamnionitis was

three times greater in these patients compared with patients
diagnosed with PPROM at the same gestational age without a
cerclage. These findings support the hypothesis that chorioamnionitis is a key etiologic factor associated with extreme
prematurity. After 28 weeks gestation, the rate of clinical
chorioamnionitis was similar between the two groups but still
accounted for 12% of deliveries and subacute chorioamnionitis was present in over 2/3 of patients regardless of cerclage
likely reflecting the co-incidence and/or the effect of subclinical chorioamnionitis on spontaneous PTD after PPROM.
The type of cerclage did not affect that rates subacute or acute
infection significantly and therefore should not be considered
in the algorithm of clinical management after PPROM.
Our data suggest that the presence of cerclage is associated
with an increased rate of intrauterine infection especially with
PPROM diagnosed prior to 28 weeks gestation. Our suggestion is echoed by Kuhn and Pepperall [4] and Ludmir et al.
[3] who determined that the rate of chorioamnionitis was
lower in the patients whose cerclage was removed at the time
of PPROM diagnosis. But our results are in contrast to those
reported by several authors. In the largest casecontrol study,
McElrath et al. (2002) did not detect any difference in the rate
of clinical chorioamnionitis or maternal postpartum fever in
women with PPROM with and without a cerclage [9]. The
same author also detected no difference in the rate of
chorioamnionitis when comparing cerclage removal or retention after PPROM [10]; these findings were confirmed by
Jenkins et al. (2000). Given that our study was conducted in a
different era of clinical practice as these previous studies it is
difficult to make direct comparisons regarding rates of
infection in the presence or absence or early removal of a
cerclage after PPROM [8]. Although, the majority of the
previous studies did not detect differences in neonatal
mortality or morbidity, our study, despite not being sufficiently powered to examine neonatal outcome, did detect a
higher rate of intrauterine demise, neonatal respiratory
distress, and neonatal anemia. Again, given that our study
was conducted in an era of erythromycin use post-PPROM
which has been shown to improve neonatal outcome, it is valid
to compare with previous studies but should be evaluated in
the context of todays clinical practice. What has become
apparent is there is limited data in support of cerclage
retention at the time of PPROM diagnosis on the basis of

428

M. D. Laskin et al.

perinatal outcome; the potential for increased rates of acute

and subacute chorioamnionitis and adverse neonatal outcome
infection with no difference in latency would suggest that
cerclage removal at the diagnosis of PPROM may be a
prudent clinical decision.
Our study had three salient points of conclusion. When
compared patients diagnosed with PPROM, the patients with
PPROM in the presence of cerclage had: (1) no change in
pregnancy latency, (2) a greater rate of subacute and acute
chorioamnionitis, and (3) a higher rate of adverse neonatal
outcome, especially sepsis, RDS and anemia. We acknowledge that our study is limited by its retrospective design and
power analysis. The rate of prior PPROM and prior preterm
birth was higher in the patients with a cerclage but the rate of
chorioamnionitis in this pregnancy were not affected by
obstetrical history; however, the differences in the rates of
chorioamnionitis and adverse neonatal outcome could be
explained by obstetrical history and not related to the cerclage.
However, taken as an isolated cohort of patients, women with
a cerclage in place and the diagnosis of PPROM may be at
significant risk of developing clinical and histological chorioamnionitis regardless of their obstetrical history. However,
given the aforementioned limitation, the findings in this study
provide a rationale for removal of the cerclage at the time of
PPROM. More importantly, our study provides a rationale for
a randomized control trial to address the clinical question:
retention versus removal of a cerclage in the presence of the
diagnosis of PPROM.
Declaration of interest: The authors report no conflicts of
interest. The authors alone are responsible for the content and
writing of the paper.

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