J. Perinat. Med.

2019; 47(5): 500–509

Max Mönckeberg*, Rafael Valdés, Juan P. Kusanovic, Manuel Schepeler, Jyh K. Nien,
Emiliano Pertossi, Pablo Silva, Karla Silva, Pía Venegas, Ulises Guajardo, Roberto Romero
and Sebastián E. Illanes

Patients with acute cervical insufficiency without

intra-amniotic infection/inflammation treated
with cerclage have a good prognosis
https://doi.org/10.1515/jpm-2018-0388 Results: Seventy patients underwent an amniocentesis
Received November 20, 2018; accepted December 16, 2018; to rule out IAI/I. The prevalence of IAI/I was 19%. Forty-
­previously ­published online March 8, 2019 seven patients underwent a cerclage. Patients with a cer-
Abstract clage had a longer median admission-to-delivery interval
(33 vs. 2 days; P < 0.001) and delivered at a higher median
Background: The frequency of intra-amniotic infection/ gestational age (27.4 vs. 22.6 weeks; P = 0.001) than those
inflammation (IAI/I) in patients with midtrimester cer- without a cerclage. The neonatal survival rate in the cer-
vical insufficiency is up to 50%. Our purpose was to clage group was 62% vs. 23% in those without a cerclage
determine the perinatal outcomes of cervical cerclage in (P = 0.01). Patients without IAI/I who underwent a cerclage
patients with acute cervical insufficiency with bulging had a longer median admission-to-delivery interval (43 vs.
membranes, and to compare the admission-to-delivery 1 day; P < 0.001), delivered at a higher median gestational
interval and pregnancy outcomes according to the results age (28 vs. 22.1 weeks; P = 0.001) and had a higher neonatal
of amniotic fluid (AF) analysis and cerclage placement. survival rate (67% vs. 8%; P < 0.001) than those with IAI/I.
Methods: This was a retrospective cohort study including Conclusion: The pregnancy outcomes of patients with
singleton pregnancies with cervical insufficiency between midtrimester cervical insufficiency and bulging mem-
15 and 26.9 weeks in two tertiary health centers. IAI/I was branes are poor as they have a high prevalence of IAI/I.
defined when at least one of the following criteria was Therefore, a pre-operative amniocentesis is key to iden-
present in AF: (a) a white blood cell (WBC) count >50 cells/ tify the best candidates for the subsequent placement of
mm3; (b) glucose concentration <14 mg/dL; and/or (c) a a cerclage.
Gram stain positive for bacteria. Three different groups
were compared: (1) absence of IAI/I with placement of a Keywords: amniotic fluid analysis; bulging membranes;
cerclage; (2) amniocentesis not performed with placement cervical cerclage; cervical incompetence; cervical
of a cerclage; and (3) IAI/I with or without a cerclage. insufficiency; cervical stitch; intra-amniotic infection;

*Corresponding author: Max Mönckeberg, MD, Department of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
Obstetrics and Gynecology, Faculty of Medicine, Universidad de Pablo Silva: Center for Research and Innovation in Maternal-
los Andes, San Carlos de Apoquindo 2200, Las Condes, Santiago, Fetal Medicine (CIMAF), Hospital Sótero del Río, Santiago, Chile;
Chile; and Department of Public Health and Epidemiology, Faculty and Division of Obstetrics and Gynecology, School of Medicine,
of Medicine, Universidad de los Andes, Santiago, Chile, Pontificia Universidad Católica de Chile, Santiago, Chile
Tel.: +56 (2) 226181381, E-mail: [email protected] Pía Venegas and Ulises Guajardo: Department of Obstetrics
Rafael Valdés and Karla Silva: Center for Research and Innovation and Gynecology, Faculty of Medicine, Universidad de los Andes,
in Maternal-Fetal Medicine (CIMAF), Hospital Sótero del Río, Las Condes, Santiago, Chile
Santiago, Chile Roberto Romero: Perinatology Research Branch, NICHD/NIH/DHHS,
Juan P. Kusanovic: Center for Research and Innovation in Maternal- Bethesda, MD and Detroit, MI, USA; Department of Obstetrics and
Fetal Medicine (CIMAF), Hospital Sótero del Río, Santiago, Chile; Gynecology, University of Michigan, Ann Arbor, MI, USA; Department
Division of Obstetrics and Gynecology, School of Medicine, of Epidemiology and Biostatistics, Michigan State University, East
Pontificia Universidad Católica de Chile, Santiago, Chile; and Lansing, MI, USA; and Center for Molecular Medicine and Genetics,
Perinatology Research Branch, NICHD/NIH/DHHS, Bethesda, MD Wayne State University, Detroit, MI, USA
and Detroit, MI, USA Sebastián E. Illanes: Department of Obstetrics and Gynecology,
Manuel Schepeler and Jyh K. Nien: Department of Obstetrics and Faculty of Medicine, Universidad de los Andes, Las Condes,
Gynecology, Clínica Dávila, Santiago, Chile Santiago, Chile; and Department of Obstetrics and Gynecology,
Emiliano Pertossi: Division of Obstetrics and Gynecology, School of Clínica Dávila, Santiago, Chile

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 Mönckeberg et al.: Cervical insufficiency and intra-amniotic infection/inflammation 501

intra-amniotic inflammation; MIAC; microbial invasion of Materials and methods

the amniotic cavity.
Study design and population

Introduction This is a retrospective cohort study including all singleton pregnan-

cies between 15 and 26.9 weeks of gestation with the diagnosis of cer-
vical insufficiency and bulging membranes who were admitted at the
Cervical insufficiency is defined as the inability of the
Hospital Sótero del Río and Clínica Dávila in Santiago, Chile, between
uterine cervix to retain the fetus in the absence of uterine
January 2009 and May 2017. Exclusion criteria were: (1) patients with
contractions in the second trimester [1–4]. This condi- the diagnosis of cervical insufficiency due to an asymptomatic short
tion occurs in approximately 0.15%–1% of live births cervix (<25 mm); (2) cases with cervical insufficiency who presented
[5–7] during the second trimester of pregnancy, and it with cervical dilatation at digital examination, but without bulging
is associated with spontaneous abortion, extreme pre- membranes at speculum examination; (3) patients with the diag-
nosis of clinical chorioamnionitis at admission; (4) cases for whom
maturity and adverse obstetrical and neonatal outcomes
there were incomplete or absent records of the results of AF analysis
[7–9]. Cervical cerclage has been successfully used in (if an amniocentesis was performed) or pregnancy outcomes; (5) twin
the management of patients with a history of second tri- gestations; and (6) fetal congenital anomalies.
mester losses and progressive shortening of the cervix We retrospectively reviewed all the medical records with the
in the second trimester [10–32], although there is some diagnosis of “cervical insufficiency” or “cervical incompetence” at
evidence against its efficacy [33–39]. The most severe admission and/or discharge, all surgical procedures that included
the terms “cervical cerclage” or “cervical stitch” and all the labora-
form of cervical insufficiency is the passive and pain-
tory records of non-genetic amniocenteses performed during the
less dilatation of the uterine cervix leading to bulging study period. Demographic and clinical characteristics of patients
membranes [40–42], and a solid body of evidence sup- were recorded, as well as data from previous pregnancies, the results
ports the benefit of placing a cerclage in those patients of maternal blood laboratory tests, as well as those of AF analysis.
[43–53]. Information regarding the inpatient management, pregnancy and
neonatal outcomes was also collected. All data obtained from medi-
The presence of intra-amniotic infection/inflamma-
cal records were recorded on a pre-specified database. The use of
tion (IAI/I) is associated with adverse pregnancy out- demographic, clinical, laboratory and sonographic data collected
comes in women with spontaneous preterm labor with from chart review was approved by the Institutional Review Boards
intact membranes [54–60], preterm prelabor rupture of of Hospital Sótero del Río and Clínica Dávila.
membranes (pPROM) [61–65] and cervical insufficiency. The standard management of patients with cervical insufficiency
Indeed, between 13% and 51% of patients with cervical with bulging membranes in the second trimester consists of a pre-
operatory amniocentesis to exclude IAI/I before the placement of a cer-
insufficiency and bulging membranes have a positive
vical cerclage. Yet, the final decision of performing an amniocentesis
amniotic fluid (AF) culture and the presence of IAI/I and placing a cerclage was at the discretion of the physician. Women
has been consistently associated with a poor progno- with the diagnosis of IAI/I are usually not considered candidates for a
sis [66–71]. It has been shown that 76% of patients with cervical cerclage, and they have expectant management under broad
cervical insufficiency and microbial invasion of the spectrum antibiotic coverage including ceftriaxone and metronidazole,
or ceftriaxone and clindamycin, with or without the addition of a mac-
amniotic cavity (MIAC) delivered within the first 48 h of
rolide. In patients with IAI/I, induction of labor is not routinely per-
admission [67]. Moreover, Mays et al. [68] reported that formed, except in cases in which maternal health is considered at risk.
patients without intra-amniotic infection managed with Based on that, patients were classified into the following
cervical cerclage delivered at a significantly higher ges- groups: (1) group 1: absence of IAI/I and managed with cervical cer-
tational age and had better neonatal survival rates than clage; (2) group 2: amniocentesis not performed and managed with
those managed without amniocentesis, or than patients cervical cerclage; and (3) group 3: presence of IAI/I, with or without
cervical cerclage.
with intra-amniotic infection but managed expectantly.
Collectively, these results indicate that IAI/I strongly
affects the pregnancy outcomes of patients with cervical
insufficiency. Definitions
The objectives of this study were to determine the
perinatal outcomes of cervical cerclage in patients with Spontaneous preterm delivery was defined by the presence of regular
acute cervical insufficiency with bulging membranes uterine contractions occurring at a frequency of at least two every
10 min associated with cervical changes before 37 completed weeks,
in the second trimester, and to compare the admission-
leading to preterm delivery. pPROM was diagnosed by sterile specu-
to-delivery interval and pregnancy outcomes according lum examination confirming pooling of AF in the vagina in associa-
to the results of the AF analysis and cervical cerclage tion with ferning tests when necessary, before 37 weeks of gestation
placement. and in the absence of labor. Clinical chorioamnionitis was diagnosed

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502 Mönckeberg et al.: Cervical insufficiency and intra-amniotic infection/inflammation

according to the criteria proposed by Gibbs et al. [72] including a Mann-Whitney U-test or Kruskal-Wallis test. Comparisons between or
maternal temperature of ≥37.8°C and two or more of the following among proportions were performed with chi-square (χ2) or Fisher’s
criteria: uterine tenderness, malodorous vaginal discharge, maternal exact tests, as appropriate. The statistical package used was STATA
leukocytosis (≥15,000 cells/mm3), maternal tachycardia (>100 beats/ v.14.2 (StataCorp, 2015, Stata Statistical Software: Release 14, Stata-
min) and fetal tachycardia (>160 beats/min). IAI/I was defined when Corp LP, College Station, TX, USA). A two-tailed, P-value <0.05 was
at least one of the following three criteria was present in AF [73–75]: considered statistically significant.
(a) a white blood cell (WBC) count >50 cells/mm3; (b) glucose con-
centration <14 mg/dL; and/or (c) a Gram stain positive for bacteria.

Results
Sample collection
Demographic and clinical characteristics of
AF was obtained by transabdominal amniocentesis under ultrasono-
graphic guidance. Samples of AF were transported to the laboratory
the study population
in a sterile capped syringe. AF WBC count, glucose concentration and
Gram stain were also performed shortly after collection in all patients Figure 1 shows the disposition of patients who are part of
as previously described [73, 74]. The results of these tests were used the study. Initially, 105 cases of cervical insufficiency were
for clinical management. AF cultures for aerobic, anaerobic and gen- identified. We excluded: (a) 15 cases of cervical insuffi-
ital mycoplasmas were performed at the discretion of the physician. ciency in which there was cervical dilatation, but without
bulging membranes at speculum evaluation; (b) seven
cases of twin pregnancies; (c) two cases presenting
Statistical analyses
<15 weeks; (d) two cases presenting >266/7 weeks; (e) one
patient was lost to follow-up; and (f) one case for whom
Normality of distribution in numerical variables was tested using
the results of AF analyses were not available.
the Shapiro-Wilk test. In variables fitting a normal distribution, com-
parisons between or among groups were made by t-test or one-way A total of 77 patients were included in the study. The
analysis of variance (ANOVA), as appropriate. In numerical variables demographic and clinical data, according to the results of
not fitting a normal distribution, comparisons were made using the AF analyses, are reported in Table 1. The mean gestational

Acute cervical insufficiency

(n = 105)

Excluded
• 15 cases: non-exposed fetal membranes
• 7 cases: twin pregnancies
• 2 cases: gestational age <15 weeks
• 2 cases: gestational age ≥27 weeks
• 1 case: missing amniotic fluid results
• 1 case: missing pregnancy outcome

Singleton pregnancies
acute cervical insufficiency with bulging membranes
(n = 77)

No intra-amniotic Amniocentesis Intra-amniotic

infection/inflammation not performed infection/inflammation
(n = 57) (n = 7) (n = 13)

Cervical cerclage Cervical cerclage Cervical cerclage

72% 57% 15%
(41/57) (4/7) (2/13)

Figure 1: Disposition of patients who are part of the study.

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 Mönckeberg et al.: Cervical insufficiency and intra-amniotic infection/inflammation 503

Table 1: Demographic and clinical characteristics of study population at admission, according to the results of amniotic fluid analyses.

No IAI/I (n = 57) Amniocentesis not IAI/I (n = 13) P-value

performed (n = 7)

Maternal age, years 28.4 (±7.3) 25.0 (±7.7) 26.8 (±5.8) 0.429
Gestational age, weeks 21.8 (±2.7) 21.9 (±1.0) 21.8 (±2.4) 0.999
Body mass index, kg/m2 27.8 (±5.6) 25.1 (±5.3) 30.0 (±5.4) 0.176
Nulliparity 58 (33/57) 71 (5/7) 69 (9/13) 0.675
Prior second trimester loss 18 (10/57) 14 (1/7) 0 (0/13) 0.271
Prior preterm birth 19 (11/57) 0 (0/7) 15 (2/13) 0.602
Prior cervical cerclage 4 (2/57) 0 (0/7) 0 (0/13) 1.000
Uterine malformation 2 (1/57) 14 (1/7) 0 (0/13) 0.201
Active smoking 11 (6/57) 0 (0/7) 0 (0/13) 0.770
Progesterone use before admission 14 (8/57) 0 (0/7) 15 (2/13) 0.731
Cervical dilatation, cm 2.9 ± 1.9 3.7 ± 3.1 4.3 ± 2.1a 0.059
Maternal heart rate, bpm 93 ± 12 92 ± 10 101 ± 10b 0.081
Body temperature, °C 36.5 ± 0.3 36.3 ± 0.7 36.7 ± 0.5 0.018
White blood cell count, ×103/mm3 11.6 ± 2.5 15.4 ± 6.8 15.1 ± 3.5c 0.005
C-reactive protein, mg/L 4.4 ± 5.5 24.5 ± 38.0 19.7 ± 23.8d 0.085

Values are expressed as percentage (proportion) or mean (±standard deviation). Bivariate analysis: aComparison between groups “No IAI/I”
and “IAI/I”: P = 0.015. bComparison between groups “No IAI/I” and “IAI/I”: P = 0.033. cComparison between groups “No IAI/I” and “IAI/I”:
P = 0.002. dComparison between groups “No IAI/I” and “IAI/I”: P = 0.025.

age at admission was 21.8 ± 2.5 weeks. Forty-seven (61%) with an intrauterine device (one case) and (f) suspected
patients were nulliparous, 17% (13/77) had a history of clinical chorioamnionitis occurring within 48 h of admis-
previous spontaneous preterm birth and 14% of patients sion (one case).
(11/77) had a history of second trimester pregnancy loss. On the other hand, 66% (51/77) of patients were con-
Two cases (3%) had a history of cervical cerclage due sidered candidates for a cervical cerclage and underwent
to cervical insufficiency in previous pregnancies, and this procedure. In 8% (4/51) of cases, rupture of the mem-
13% (10/77) were under vaginal progesterone treatment branes occurred during the cerclage. In these cases, the
because of a short cervix. procedure was stopped, and the patients were managed
At admission, 91% (70/77) of patients underwent an with antibiotic treatment. The remaining 47 patients
amniocentesis to exclude IAI/I. According to the results of received a cervical cerclage.
the AF analyses, 19% (13/70) of them had IAI/I. Patients Patients managed with a cervical cerclage had a sig-
with IAI/I had a significantly greater cervical dilatation nificantly longer admission-to-delivery interval [median
(mean: 4.3 ± 2.2 vs. 2.9 ± 2.0 cm, P = 0.015), higher maternal admission-to-delivery interval: 33 days, interquartile
WBC count (mean: 15.1 ± 3.5 cells × 103/mm3 vs. 11.6 ± 2.5 range (IQR): 12–89 vs. 2 days, IQR: 1–20, P < 0.001] and
cells × 103/mm3, P = 0.002) and higher maternal serum delivered at a significantly higher gestational age (median
concentrations of C-reactive protein (mean: 19.7 ± 23.8 vs. gestational age at delivery: 27.4 weeks, IQR: 23.4–35.9 vs.
4.4 ± 5.5 mg/L, P = 0.025) than patients without IAI/I. No 22.6 weeks, IQR: 21.4–25.6, P = 0.001) than those who did
adverse events were observed due to the performance of not have a cerclage. The neonatal survival rate in the cer-
the amniocenteses. clage group was 62% (29/47), compared to 23% (7/30) in
During the initial evaluation, 34% (26/77) of patients those without a cerclage (P = 0.01).
were not considered candidates for a cervical cerclage
and underwent expectant management. The main con-
traindications for cervical cerclage were: (a) presence of Perinatal outcomes according to amniotic
IAI/I (11 cases), (b) onset of spontaneous preterm labor fluid analysis and cervical cerclage
within 48 h after admission (nine cases), (c) pPROM
within 48 h of admission (two cases), (d) gestational age Table 2 displays the perinatal outcomes according to the
higher than 256/7 weeks (two cases), (e) current pregnancy status of the AF and cerclage placement. Patients without

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Table 2: Pregnancy outcomes according to amniotic fluid analysis and cerclage.

Group 1 P-valuea Group 2 P-valueb Group 3 P-valuec

Cerclage + no IAI/I Cerclage + amniocentesis IAI/I (n = 13)
(n = 41) not performed (n = 4)

Admission-to-delivery interval, days 43 (15.0–89.0) 0.675 21.5 (16.0–64.5) 0.010 1 (1.0–10.0) <0.001
Gestational age at delivery, weeks 28 (23.7–36.3) 0.523 25.4 (24.1–30.4) 0.047 22.1 (20.7–23.4) 0.001
Birth weight, g 1,212 (660–2,890) 0.531 897 (690–1,792) 0.032 550 (435–625) 0.002
Delivery <48 h from admission 2 (1/41) 0.911 0 (0/4) 0.029 69 (9/13) <0.001
Delivery <7 days from admission 12 (5/41) 0.613 0 (0/4) 0.029 69 (9/13) <0.001
Delivery <24 weeks 27 (11/41) 0.714 25 (1/4) 0.053 85 (11/13) 0.001
Delivery <28 weeks 49 (20/41) 0.321 75 (3/4) 0.426 92 (12/13) 0.005
Delivery <32 weeks 61 (25/41) 0.511 75 (3/4) 0.235 100 (13/13) 0.005
Neonatal survivald 67 (26/39) 0.607 75 (3/4) 0.022 8 (1/13) <0.001

Values are expressed as percentage (proportion) or median (interquartile range). aP-values for comparison between groups 1 and 2.
b
P-values for comparison between groups 2 and 3. cP-values for comparison between groups 1 and 3. dTwo newborns in group 1 were
delivered in participating centers and were posteriorly transferred to other centers for neonatal management. No information regarding
neonatal survival was available for both cases.

IAI/I who underwent a cervical cerclage had good preg- and without a cervical cerclage. Their median admission-
nancy outcomes. The median admission-to-delivery to-delivery interval was 1 day (IQR: 1–10 days), and the
interval was 43 days (IQR: 15–89 days), and the median median gestational age at delivery was 22 weeks (IQR:
gestational age at delivery was 28 weeks (IQR: 23.7– 20.4–23.9 weeks). Only one neonate survived; this case
36.3 weeks). In this group, the neonatal survival rate was was admitted at 25.6 weeks of gestation and delivered at
67% (26/39). There were no significant differences regard- 28.6 weeks (23 days after admission).
ing pregnancy outcomes between groups 1 and 2.
In contrast, patients with IAI/I (group 3) had a poor
pregnancy outcome. Their median admission-to-deliv-
ery interval was 1 day (IQR: 1–10 days), and the median
Discussion
gestational age at delivery was 22.1 weeks (IQR: 20.7–
23.4 weeks). This was significantly shorter compared to Principal findings of the study
groups 1 and 2. Moreover, the proportion of patients deliv-
ering within the first 48 h and 7 days after admission was (1) Sixty percent of patients with cervical insufficiency
significantly higher in group 3 compared with groups 1 and bulging membranes in the second trimester were
and 2. Indeed, 69% of patients presenting with cervical nulliparous; (2) patients with a cerclage had a signifi-
insufficiency with bulging membranes and IAI/I delivered cantly longer admission-to-delivery interval, as well as
within the first 48 h of admission, and the neonatal sur- significantly higher gestational age at delivery and neo-
vival rate was only 8% (1/13). natal survival rate than those who did not have a cerclage;
There were two patients in group 3 for whom a cer- (3) patients with cervical insufficiency and bulging mem-
vical cerclage was inserted. In both cases, the amniocen- branes without IAI/I, who underwent a cervical cerclage,
tesis was performed at the discretion of their physicians had a median admission-to-delivery interval of 43 days, a
at the time of cerclage placement. Unfortunately, the AF median gestational age at delivery of 28 weeks and a neo-
analyses were consistent with IAI/I. In both patients, the natal survival rate of 67%; (4) in contrast, patients with
cervical cerclage was not removed and underwent expect- cervical insufficiency and bulging membranes with IAI/I
ant management with broad spectrum antibiotics. The had a median admission-to-delivery interval of 1 day,
first case delivered at 23.3 weeks of gestation (11 days after a median gestational age at delivery of 22 weeks and a
admission), and the second case delivered at 23.4 weeks neonatal survival rate of 8%; (5) no maternal and fetal
(1 day after admission). Both neonates died shortly adverse events were reported during the performance of
after delivery. The remaining 11 cases of this group were the transabdominal amniocenteses; and (6) 8% of patients
managed expectantly with broad spectrum antibiotics ruptured the membranes during cerclage.

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 Mönckeberg et al.: Cervical insufficiency and intra-amniotic infection/inflammation 505

The role of emergency cerclage in cervical bulging membranes is well established in the literature
insufficiency [67–71, 90, 91]. The incidence of subclinical intra-amniotic
infection demonstrated by AF cultures has been reported
Previous studies have evaluated the effect of cervical as high as 51% [67, 69]. In the present study, the prevalence
cerclage on pregnancy outcomes in women with cervi- of IAI/I (based on AF Gram stain, WBC count and glucose
cal insufficiency and bulging membranes [43–53, 76–80], concentration) was 19%. In a similar population, Mays
reporting the benefits of this intervention. Evidence from et al. [68], using AF lactate dehydrogenase and glucose
a small randomized clinical trial [46] demonstrated that, concentrations, reported 38% (7/18) of amniocentesis sug-
in women with cervical insufficiency and bulging mem- gesting IAI/A. Also, Diago-Almela et al. [92], using a combi-
branes, placement of a cervical cerclage was associated nation of AF concentrations of interleukin-6, glucose, WBC
with a significant longer admission-to-delivery interval, count and leucocyte esterase test, reported an incidence of
higher gestational age at delivery and lower incidence of IAI/I of 64% (20/31). The mean gestational age at delivery
preterm birth <34 weeks compared to patients assigned to in patients without IAI/I was 35.1 weeks, and the reported
expectant management. In addition, Ehsanipoor et al. [53] neonatal survival was 100%. The prevalence of IAI/I in our
reported a systematic review and meta-analysis includ- study was lower compared to what has been previously
ing 10 studies [43–52] assessing the effects of cerclage in reported, probably due to the lower diagnostic perfor-
cases of cervical insufficiency and bulging membranes in mance of the AF markers used for detecting cases of IAI/I.
the second trimester, showing that an emergency cervical In our study, patients with IAI/I had a median admission-
cerclage significantly reduced the risk of preterm delivery to-delivery interval of only 1 day (IQR: 1–10). Moreover,
<34 weeks, and significantly increased the interval from 69% of these cases had labor and delivered within 48 h
admission to delivery, gestational age at delivery and from admission. These results are consistent with previous
overall neonatal survival compared to expectant man- studies. Other reports [67, 70] suggest that in patients with
agement. In agreement with those reports, we observed cervical insufficiency, bulging membranes and an amnio-
herein that placement of a cervical cerclage was associ- centesis suggesting IAI/I, the rates of delivery within 48 h
ated with a 31-day increase in the median admission-to- from admission were between 50% and 76%. In addition,
delivery interval compared with expectant management, Mays et al. [68] reported that the mean admission-to-deliv-
and with a significant increase in the gestational age at ery interval in patients with IAI/I was 3.8 ± 4.6 days, which
delivery and neonatal survival rates. is similar to what was found in our study.
Similarly, cervical cerclage has demonstrated benefits On the other hand, performing a cervical cerclage
in prolongation of gestation when used in populations at in patients without IAI/I increases the possibilities of
high risk of preterm birth [81–83]. A systematic review and achieving a favorable pregnancy outcome. Mays et al.
meta-analysis of randomized trials reported by Berghella [68] reported a mean gestational age at delivery of
et al. [84], including five trials [85–89], evaluated the effects 35.2 ± 4.2 weeks in this subgroup of patients, with a mean
of cervical cerclage versus no cerclage in patients with admission-to-delivery interval of 93.4 ± 33.1 days. Simi-
a history of preterm birth and a sonographic short cervix larly, Diago-Almela et al. [92] reported a mean gestational
(<25 mm) <24 weeks of gestation. Placement of a cervical age at delivery of 35.4 weeks, with a mean admission-to-
cerclage was associated with a significant reduction in the delivery interval of 89 days. These latency periods are
risk of preterm birth and perinatal morbidity and mortality. higher than those observed in our study. This may be
explained by the differences in diagnostic criteria used for
establishing the diagnosis of IAI/I, and differences in the
Cervical insufficiency and intra-amniotic magnitude of cervical dilatation at admission (2.5 ± 0.8 cm
infection/inflammation in Mays et al. and 2.9 ± 1.9 cm in our study). In previous
reports, advanced cervical dilatation with protrusion of
In this study, 91% of patients with cervical insufficiency membranes through external os has been systematically
and bulging membranes in the second trimester under- associated with adverse pregnancy outcomes [91, 93–104].
went an amniocentesis to rule out IAI/I before placement In this study, advanced cervical dilatation with bulging
of a cervical cerclage, and 34% of patients were not con- membranes was not considered an exclusion criterion for
sidered candidates for a cervical cerclage mainly due to cervical cerclage placement.
the presence of signs of IAI/I or onset of labor shortly after Altogether, these findings suggest that a significant pro-
admission. The role of IAI/I and its effects over the outcome portion of patients with cervical insufficiency are affected
of pregnancies in women with cervical insufficiency with by IAI/I, and that delivery will occur soon after admission

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506 Mönckeberg et al.: Cervical insufficiency and intra-amniotic infection/inflammation

as the optimal management of patients with IAI/I has not Research funding: This research was supported, in part,
been determined. Performing a cervical cerclage in patients by the Perinatology Research Branch, Division of Intra-
with IAI/I may be harmful for the mother and fetus, and also mural Research, Eunice Kennedy Shriver National Institute
ineffective in increasing the admission-to-delivery interval. of Child Health and Human Development, National Insti-
tutes of Health, Department of Health and Human Services
(NICHD/NIH/DHHS); and, in part, with Federal funds
from NICHD, NIH under Contract No. HSN275201300006C.
Strength and limitations
Employment or leadership: None declared.
Honorarium: None declared.
To our knowledge, this is the largest study reporting
Competing interests: The funding organization(s) played
patients who underwent an amniocentesis before cerclage
no role in the study design; in the collection, analysis, and
placement. The fact that patients with cervical insuffi-
interpretation of data; in the writing of the report; or in the
ciency and bulging membranes without IAI/I, who under-
decision to submit the report for publication.
went a cervical cerclage, had a neonatal survival rate of
67% is a major finding. This study has some limitations.
First, its retrospective design makes it especially suscep-
tible to selection bias, as the final decision of performing
or not a preoperatory amniocentesis, and subsequently
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