Taiwanese Journal of Obstetrics & Gynecology 57 (2018) 374e378

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Taiwanese Journal of Obstetrics & Gynecology

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Original Article

Amniotic fluid index, single deepest pocket and transvaginal cervical

length: Parameter of predictive delivery latency in preterm premature
rupture of membranes
Young-Joo Lee, Seung-Chul Kim*, Jong-Kil Joo, Dong-Hyung Lee, Ki-Hyung Kim,
Kyu-Sup Lee
Department of Obstetrics and Gynecology, Biomedical Research Institute, Pusan National University School of Medicine, Busan, South Korea

a r t i c l e i n f o a b s t r a c t

Article history: Objective: Prediction of delivery latency complicated with preterm premature rupture of membrane
Accepted 10 August 2017 (PPROM) is crucial for reducing maternal and neonatal complications. Therefore, we investigated the
correlations between latency period and cut-off values of ultrasonographic parameters, ultimately pre-
Keywords: dicting delivery latency.
Amniotic fluid index Materials and methods: The retrospective study was performed on 121 PPROM patients enrolled between
Cervical length
March 2010 and July 2015. Parameters including amniotic fluid index (AFI), single deepest pocket (SDP)
Latency
and transvaginal cervical length (TVCL) were measured in 99 singleton pregnancies with PPROM. Latency
Preterm premature rupture of membranes
Single deepest pocket
was defined as the period from sonographic measurements to delivery day. The parameters were
analyzed independently by Wilcoxon rank sum test and Fisher's exact test. Cut-off values were deter-
mined using a receiver operating characteristic (ROC) curve.
Results: In delivery latency within 3 days, AFI and SDP were decreased with significantly shorter TVCL.
AFI and SDP had the highest sensitivity (82.2%) and SDP combined with TVCL showed the highest
specificity (75.9%) in area under curve (AUC) value. The predicted median latency period was less than 2
days within the cutoff value of parameter (AFI
7.72, SDP
3.2 and TVCL
1.69).
Conclusion: AFI and SDP combined with TVCL could be useful predictive parameters of the latency in-
terval from PPROM to delivery.
© 2018 Taiwan Association of Obstetrics & Gynecology. Publishing services by Elsevier B.V. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction
Preterm premature rupture of membranes (PPROM) is defined
by spontaneous rupture of the fetal membranes before 37
completed weeks and prior to labor onset [1]. The incidence of
PPROM is approximately 3% of all pregnancies [2]. In a term preg-
nancy, membrane rupture can result from shearing force due to
uterine contractions and weakened state by physical stretching
[3,4]. However, PPROM can be caused by pathologic mechanisms
such as intra-amniotic infection and uterine overdistension, both of
which have been widely observed in preterm gestational age. And
another well-known risk factor is the history of PPROM in prior
* Corresponding author. Department of obstetrics and gynecology, Pusan
National University School of Medicine, 179 Gudeok-ro, Seo-gu, Busan 49241,
South Korea. Fax: þ82 51 248 2384.
E-mail address: ksch0127@naver.com (S.-C. Kim).
pregnancy. Additional risk factors are short cervical length, low
body mass index (BMI), nutritional deficiency, cigarette smoking,
and low socioeconomic status [5e7].
Most pregnancies complicated with PPROM require hospitali-
zation because spontaneous labor or birth occurs within 1 week
from the onset of PPROM in half of the cases [3]. Chorioamnionitis is
one of the major maternal complications that can affect the
morbidity and mortality of mother and neonate. Its incidence is
15e25% and closely related to the duration of membrane rupture
[8]. Neonates born to women complicated with chorioamnionitis
have a higher incidence of sepsis and other complications such as
respiratory distress syndrome (RDS) and neurological injury [9,10].
Advanced gestational age, oligohydramnios or cervical dilata-
tion >1 cm at admission, and twin gestation have been associated
with shorter duration of the latency period [11,12]. In preterm birth,
transvaginal cervical length (TVCL) has been reported as a good
predictor because relative risk of preterm delivery is increased as

https://doi.org/10.1016/j.tjog.2018.04.008
1028-4559/© 2018 Taiwan Association of Obstetrics & Gynecology. Publishing services by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
 Y.-J. Lee et al. / Taiwanese Journal of Obstetrics & Gynecology 57 (2018) 374e378
cervical length is decreased [13,14]. Accordingly, several studies
have addressed the relationship between TVCL and latency to de-
livery to explore the predictive value of delivery latency according
to TVCL. Rizzo et al. reported that abnormally short cervical length
was associated with short delivery interval [15]. Shorter TVCL and
amniotic fluid index (AFI) & 5 predicted delivery latency within 7
days in women who presented with PPROM [16]. Oligohydramnios,
defined as the decrease of the deepest vertical pocket of amniotic
fluid & 2 or AFI & 5, is related to shorter latency period [17e20].
The foregoing findings indicate the importance of specific and
appropriate prediction of delivery latency in order to reduce
maternal and fetal complications via proper management. How-
ever, no studies have addressed the correlations between AFI, sin-
gle deepest pocket (SDP), TVCL, and latency interval to delivery.
Therefore, we investigated the latency period from PPROM to de-
livery according to AFI, SDP and TVCL, and we assessed the pre-
dicted delivery latency according to the cut-off values of these
parameters.
Materials and methods
The retrospective study was performed on patients who visited
the obstetrics clinic from March 2010 to July 2015. We investigated
women diagnosed as PPROM by history taking and physical ex-
amination with singleton pregnancy, between the gestational ages
of 23þ0 weeks to 36þ6 weeks. Twenty two of the 121 patients were
excluded because of inconsistency with diagnostic criteria (n ¼ 2),
cervical cerclage (n ¼ 8), delivery before ultrasound measuring
(n ¼ 1), and twin pregnancies (n ¼ 11). For the data analyses, we
included 99 pregnant women in study and flowchart of the study
design is shown in Fig. 1.
PPROM was diagnosed by physical examination confirmed by
gross vaginal leakage and nitrazine test of vaginal fluid samples. If
the patient showed no gross leakage but had a positive nitrazine
test, a placental alpha microglobulin-1 protein test (Amnisure®;
QIAGEN Corp., Valencia, CA, USA) was performed. All women
diagnosed as PPROM were hospitalized, and then we measured AFI,
SDP and TVCL. AFI was estimated by a four quadrant technique,
which was sum of deepest, unobstructed, and vertical length of
pocket of fluid in each quadrant. SDP was defined as the pocket of
maximal depth of amniotic fluid free of umbilical cord and fetal
Fig. 1. Flow-chart of the study population.
375
parts [21,22] and we measured TVCL at admission using the CLEAR
(Cervical Length Education and Review) guidelines with ultraso-
nography (Accuvix XQ; Medison, Seoul, Korea) [23]. Blood samples
for determining of C-reactive protein (CRP) level were drawn at
admission and within 24 h prior to delivery and measured using a
TBA200FR apparatus (TOSHIBA Corp., Tokyo, Japan).
Generally, ampicillin is mainly used for group B streptococcus
prophylaxis, but Escherichia coli are also highly identified in
pregnant women with PPROM [24]. Thus, the patients in this
study were administered with the second-generation cephalo-
sporin for this coverage. We continued intravenous antibiotics
until delivery day and azithromycin 500 mg was given addition-
ally for 3 days to the patient who had Mycoplasma or Ureaplasma
in vaginal culture. Patients received dexamethasone 6 mg given
intramuscularly 4 times, 12 h apart for fetal maturation. All
retrieved placenta was sent to the pathology department and
categorized by the grade of chorioamnionitis using established
diagnostic criteria [25].
The time of delivery was determined by individual circum-
stances. When following conditions are observed, induction of la-
bor was initiated or cesarean delivery was performed: signs of overt
infection or chorioamnionitis, including fever or elevated CRP;
active labor progression; and/or non-reassuring of fetal well-being.
However, we followed up with expectant management if the
obvious signs of infection or fetal distress were absent.
The SAS® version 9.3 software (SAS Institute, Cary, NC, USA) was
used for the statistical analyses. All data were entered into a data-
base and verified by a second independent person. The statistical
analyses involved demographics, maternal parameters, neonatal
outcomes, and placental histology by delivery latency at three days
(the median latency of our patients was found to be three days
when 24 h had passed from the final administration of the steroid)
with significance &5% and each median level was determined by
IQR (interquartile range) using a two-tailed test. Parameters with
statistically significant differences between the two groups were
identified using the Wilcoxon rank sum test and Fisher's exact test.
Cut-off values were estimated using a receiver operating charac-
teristic (ROC) curve and the Youden index to investigate the cor-
relations of TVCL, AFI, and SDP with the latency period. Based on
these results, we predicted the median latency period depending
on the cut-off value of each parameter.
376 Y.-J. Lee et al. / Taiwanese Journal of Obstetrics & Gynecology 57 (2018) 374e378

Results

The relationships of demographic and maternal parameters &3

days and >3 days of latency are presented in Table 1. Both groups
were similar with respect to maternal age, gravidity, parity, history
of prior preterm birth, gestational age (GA) and CRP at rupture of
membranes and within 24 h before delivery. BMI, GA at delivery,
AFI, SDP, and TVCL were significantly different with delivery latency
at 3 days. Thus, we adjusted AFI, SDP and TVCL value by BMI and GA
using logistic regression model. AFI and SDP below the cut-off
values were associated with delivery within 3 days (both
p ¼ 0.002), and the median TVCL was significantly shorter in
women who delivered within 3 days (p < 0.001).
The ROC curve estimated cut-off values of each parameter with
sensitivity, specificity, and area under curve (AUC) at delivery la-
tency within 3 days are presented in Table 2 and Fig. 2. AFI, SDP, and
TVCL had a sensitivity value of 82.2%, 82.2%, and 71.1% and speci-
ficities of 57.4%, 59.3%, and 72.2%, respectively. Because of the
higher predictive power at larger AUC values, we combined the
parameters to identify the optimal model with the higher AUC
values. The highest sensitivity and specificity value was observed
when SDP was combined with TVCL (77.8% and 75.9%, respectively),
along with the highest AUC value (0.803). Fig. 2. Cut-off values of parameter by delivery latency at 3 days. AFI, amniotic fluid
Table 3 summarizes the predicted median latency according to index; ROC, receiver operating characteristic; SDP, single deepest pocket; TVCL,
the cut-off values. The predicted median latency intervals were 5.6, transvaginal cervical length.

5.7, and 6.8 days with AFI > 7.72, SDP > 3.2, and TVCL > 1.69,
respectively. When AFI, SDP, and TVCL were less than their cut-off
value, the expected latency periods were 1.8, 1.8, and 1.4 days,
respectively; furthermore, each latency period decreased by 4e5
days. The sum of each factors were used to predict a more accurate
latency period. If the sum of AFI and TVCL was &8.57, the latency
period decreased to 1.6 days, and if the sum of SDP and TVCL was
&4.89, the latency period decreased 1.4 days. Patient with
parameters within the cutoff values were more likely to deliver in
less than 2 days.
Short-term neonatal outcomes were investigated using the
composite neonatal adverse outcome indicator (NAOI) [26]. There
were no statistically significant differences in neonatal outcomes
and placental histology according to delivery latency at 3 days, but
RDS, requirement of surfactants and mechanical ventilation and

Table 1
Demographics and maternal parameters by latency at 3 days.

Parameters Latency p

3 days (n ¼ 45) (45.5%) >3 days (n ¼ 54) (54.6%)

Age (years) 33.64 ± 4.01 34.57 ± 3.62 0.229

BMI (kg/m2) 26.60 ± 3.08 24.99 ± 3.62 0.020
Gravidity 1.84 ± 1.26 2.00 ± 1.06 0.179
Parity 0.40 ± 0.69 0.50 ± 0.69 0.357
Prior PB (%) 8 (17.8%) 6 (11.1%) 0.343
GA at PPROM 32.9 (27.2e34.6) 30.6 (28.6e34.5) 0.975
GA at delivery 33.2 (27.3e34.8) 34.0 (30.5e35.2) 0.048
a
AFI 3.5 (2.2e6.1) 8.5 (4.0e10.0) 0.002
a
SDP 1.8 (1.0e3.1) 3.6 (2.0e4.8) 0.002
a
TVCL (cm) 1.1 (0.7e1.9) 2.2 (1.6e3.0) <0.001
CRP at PPROM (mg/dL) 0.6 (0.3e2.3) 0.3 (0.1e1.5) 0.057
CRP within 24 h before delivery (mg/dL) 1.1 (0.4e2.3) 1.2 (0.3e2.1) 0.610

Some data were presented as median interquartile range and mean ± SD for continuous variables (Wilcoxon rank sum test) and percentage for categorical variables (Fisher's
exact test).
AFI ¼ amniotic fluid index; BMI ¼ body mass index; CRP ¼ C-reactive protein; GA ¼ gestational age; IQR ¼ interquartile range; PB ¼ preterm birth; PPROM ¼ preterm
premature rupture of membranes; SD ¼ standard deviation; SDP ¼ single deepest pocket; TVCL ¼ transvaginal cervical length.
a
Adjusted for BMI and GA at delivery.

Table 2
Cut-off value of parameter by delivery latency at 3 days.
a
AUC 95% CI Cut-off value Sensitivity (%) Specificity (%)

AFI 0.722 0.622e0.807
7.72 82.2 57.4

SDP 0.727 0.628e0.812
3.2 82.2 59.3
TVCL 0.749 0.652e0.831
1.69 71.1 72.2
AFI þ TVCL 0.766 0.670e0.845
8.57 80.0 63.0
SDP þ TVCL 0.803 0.711e0.876
4.89 77.8 75.9

AFI ¼ amniotic fluid index; AUC ¼ area under curve; SDP ¼ single deepest pocket; TVCL ¼ transvaginal cervical length.
a
Youden Index.
 Y.-J. Lee et al. / Taiwanese Journal of Obstetrics & Gynecology 57 (2018) 374e378 377

Table 3 periods were reduced to 1.6 and 1.4 days respectively. In these
Predicting median latency by cut-off value of each parameter. circumstances, clinicians should prepare for delivery promptly.
Parameter Cut-off value latency day (IQR) The evidence of relation between AFV remaining and short la-
AFI
7.72 1.8 (0.5e8.1)
tency interval is lacking. However, we presumed that larger tearing
>7.72 5.6 (3.2e12.8) of amniotic membranes or increased uterine contractility could
SDP
3.2 1.8 (0.4e8.4) induce more loss of AFV. Thus, we investigated the association
>3.2 5.7 (3.5e12.2) between histologic chorioamnionitis with alterations in maternal
TVCL
1.69 1.4 (0.4e5.2)
serum CRP and latency interval. The inflammatory change of fetal
>1.69 6.8 (2.5e10.5)
AFI þ TVCL
8.57 1.6 (0.4e8.1) membranes has been known to be part of the etiology of PPROM
>8.57 5.8 (3.2e12.8) [30]. Moreover, CRP as an indicator of maternal inflammation also
SDP þ TVCL
4.89 1.4 (0.4e5.1) has been reported with latency intervals [31]. Despite the briefs
>4.89 6.6 (3.2e11.5)
that factors related to inflammatory change were associated with
AFI ¼ amniotic fluid index; IQR ¼ interquartile range; SDP ¼ single deepest pocket; short latency interval [32], our results did not show a significant
TVCL ¼ transvaginal cervical length. correlation.
Other considerable factors associated with latency interval of
occurrence of neonatal sepsis and periventricular leukomalacia pregnancy complicated PPROM are present, and one of these is a
were relatively higher when latency exceeded 3 days (Table 4). birth history. Previous studies that evaluated the association be-
tween latency and parity reported conflicting and inconsistent
Discussion results. Melamed et al. and Test et al. suggested that the latency
period was shortened in nulliparous women [11,33]. But Aziz et al.
Accurate prediction of delivery latency in pregnancy with reported that parity was not associated with latency duration
PPROM is crucial for reducing maternal and neonatal complications [34]. Moreover, a number of studies examined the relationship
by appropriately timed administration of antenatal steroids and between prior preterm birth and latency period. Some reported
magnesium sulfate. Previous studies investigated the association of that the latency period was reduced in women with a prior pre-
latency period and one parameter. TVCL has been shown to be term birth [27] but others did not [12]. In our research, gravidity,
important for evaluating the progress of preterm labor. AFI and SDP, parity and prior preterm birth were not statistical relevant to
useful parameters of measuring amniotic fluid volume (AFV), also reduced latency period.
have been reported to association with decrease of latency interval Another factor in latency duration is maternal BMI: In our study,
[27e29]. However, these studies' authors did not estimate the the latency period was shorter in patients with higher BMI. Higher
predictive value of these factors. Therefore, through a retrospective BMI is associated with elevated maternal inflammation [35], but
review of medical records, we evaluated whether the combination BMI alone could not exactly reflect maternal inflammation and
of these factors was actually associated with latency period, and we nutrition status. Additional studies are required to figure out the
sought to confirm whether the latency period could be predicted. effects of maternal BMI and nutrition status on latency period in
We showed that if when parameters were within their cut-off cases of PPROM.
values, the median latency was shorter than two days. In addi- The association of neonatal outcomes with latency after
tion, combined cut-off values of two parameters had higher spec- PPROM is controversial. A latency period that exceeds 72 h has been
ificity and larger AUCs than single parameter cut-off values. TVCL reported to decrease adverse neonatal outcomes, whereas other
has been known as one of the important parameters to evaluate the authors revealed that in cases of shortened latency due to cho-
progress of preterm delivery. In this study, the combined parameter rioamnionitis and placental abruption, neonatal outcomes were not
of TVCL showed even higher sensitivity, specificity, and larger AUC affected [12,36]. Recent studies reported that RDS is caused by
compared with the single parameter used alone. Therefore, using insufficient surfactant production and pulmonary hypoplasia,
combined parameters could predict delivery latency more accu- which occurs more following membrane rupture at an early
rately in other studies [16]. As previously mentioned, in cases of AFI gestational age [37,38]. Some authors have suggested that
or SDP combined with TVSL were below 8.57 and 4.89, the latency decreased AFV is involved in microbial invasion and causes fetal

Table 4
Neonatal outcomes and placental histology according to latency at 3 days.

Latency p

3 days (n ¼ 45) >3 days (n ¼ 54)

10 Apgar, Median (IQR) 6.0 (4.0e7.0) 6.0 (4.8e7.0) 0.835

50 Apgar, Median (IQR) 8.0 (6.0e8.0) 8.0 (7.0e8.0) 0.974
Birth weight (g), Median (IQR) 1910 (1032e2360) 1965 (1508e2403) 0.225
Chorioamnionitis (Grade 1e3) 24 (53.3%) 30 (55.6%) 0.825
RDS 18 (40.0%) 23 (42.6%) 0.794
Need for surfactant 17 (37.8%) 22 (40.7%) 0.764
Need for mechanical ventilation 21 (46.7%) 28 (51.9%) 0.607
Neonatal sepsis 12 (26.7%) 20 (37.0%) 0.272
NEC 5 (11.1%) 3 (5.6%) 0.463
IVH 2 (4.4%) 1 (5.6%) 0.589
PVL 2 (4.4%) 3 (5.6%) 1.000
ROP 5 (11.1%) 6 (11.1%) 1.000
Death
Within 7 days after birth 3 (6.7%) 4 (7.4%) 0.976
More than 7 days after birth 2 (4.4%) 1 (1.9%)

All data was presented as median interquartile range for continuous variables (Wilcoxon rank sum test) and percentage for categorical variables (Fisher's exact test).
IQR ¼ interquartile range; IVH ¼ Intraventricular hemorrhage; NEC ¼ neonatal enterocolitis; PVL ¼ periventricular leukomalacia; RDS ¼ respiratory distress syn-
drome; ROP ¼ Retinopathy of prematurity.
378 Y.-J. Lee et al. / Taiwanese Journal of Obstetrics & Gynecology 57 (2018) 374e378
inflammatory response syndrome [10,39]. In this investigation,
respiratory complications, sepsis, and mortality rate were more
observed in patients with longer latency intervals without statis-
tically significance.
Although the present results show statistically significant evi-
dence of measuring the combination of AFV and TVCL, there are
some limitations in interpreting the results. First, we measured the
simple cervical length without considering the length of funneling.
Second, fetal presentation, which could influence on latency in-
terval in PPROM women, was not investigated. And the association
between inflammatory markers of serum or amniotic fluid, histo-
logic chorioamnionitis, and latency interval was not investigated.
Thus, additional studies are warranted that consider these factors.
Despite these limitations, AFI and SDP combined with TVCL
could be useful parameter for predicting latency interval of preg-
nancy with PPROM. With our strategy, clinicians might require less
effort to consider whether and when patient needs to be trans-
ferred to a tertiary center for proper management of prematurity.
Conflicts of interest statement
The authors have no conflicts of interest relevant to this article.
Acknowledgements
This study was supported by a clinical research grant in 2015
from Pusan National University Hospital and assisted with statis-
tical analysis by the Pusan National University Hospital Clinical Trial
Center Biostatistics Office.
References
[1] Practice bulletins no. 139: premature rupture of membranes. Obstet Gynecol
2013;122:918e30.
[2] Waters TP, Mercer B. Preterm PROM: prediction, prevention, principles. Clin
Obstet Gynecol 2011;54:307e12.
[3] Mercer BM. Preterm premature rupture of the membranes. Obstet Gynecol
2003;101:178e93.
[4] Moore RM, Mansour JM, Redline RW, Mercer BM, Moore JJ. The physiology of
fetal membrane rupture: insight gained from the determination of physical
properties. Placenta 2006;27:1037e51.
[5] Asrat T, Lewis DF, Garite TJ, Major CA, Nageotte MP, Towers CV, et al. Rate of
recurrence of preterm premature rupture of membranes in consecutive
pregnancies. Am J Obstet Gynecol 1991;165:1111e5.
[6] Bloom SL, Yost NP, McIntire DD, Leveno KJ. Recurrence of preterm birth in
singleton and twin pregnancies. Obstet Gynecol 2001;98:379e85.
[7] Mercer BM, Goldenberg RL, Moawad AH, Meis PJ, Iams JD, Das AF, et al. The
preterm prediction study: effect of gestational age and cause of preterm birth on
subsequent obstetric outcome. National Institute of Child Health and Human
Development Maternal-Fetal Medicine Units Network. Am J Obstet Gynecol
1999;181:1216e21.
[8] Ho M, Ramsey P, Brumfield C, Carlo W. Changes in maternal and neonatal
infectious morbidity as latency increases after preterm premature rupture of
membranes. Obstet Gynecol 2003;101:S41.
[9] Kenyon S, Boulvain M, Neilson JP. Antibiotics for preterm rupture of mem-
branes. Cochrane Database Syst Rev 2013;12, Cd001058.
[10] Yoon BH, Kim YA, Romero R, Kim JC, Park KH, Kim MH, et al. Association of
oligohydramnios in women with preterm premature rupture of membranes
with an inflammatory response in fetal, amniotic, and maternal compart-
ments. Am J Obstet Gynecol 1999;181:784e8.
[11] Melamed N, Hadar E, Ben-Haroush A, Kaplan B, Yogev Y. Factors affecting the
duration of the latency period in preterm premature rupture of membranes.
J Matern Fetal Neonatal Med 2009;22:1051e6.
[12] Ekin A, Gezer C, Taner CE, Ozeren M, Uyar I, Gulhan I. Risk factors and peri-
natal outcomes associated with latency in preterm premature rupture of
membranes between 24 and 34 weeks of gestation. Arch Gynecol Obstet
2014;290:449e55.
[13] Conde-Agudelo A, Romero R, Hassan SS, Yeo L. Transvaginal sonographic
cervical length for the prediction of spontaneous preterm birth in twin
pregnancies: a systematic review and metaanalysis. Am J Obstet Gynecol
2010;203. 128.e1e12.
[14] Iams JD, Goldenberg RL, Meis PJ, Mercer BM, Moawad A, Das A, et al. The
length of the cervix and the risk of spontaneous premature delivery. N Engl J
Med 1996;334:567e72.
[15] Rizzo G, Capponi A, Angelini E, Vlachopoulou A, Grassi C, Romanini C. The
value of transvaginal ultrasonographic examination of the uterine cervix in
predicting preterm delivery in patients with preterm premature rupture of
membranes. Ultrasound Obstet Gynecol 1998;11:23e9.
[16] Mehra S, Amon E, Hopkins S, Gavard JA, Shyken J. Transvaginal cervical length
and amniotic fluid index: can it predict delivery latency following preterm
premature rupture of membranes? Am J Obstet Gynecol 2015;212. 400.e1e.e9.
[17] ACOG practice bulletin. Antepartum fetal surveillance. Number 9, October
1999 (replaces Technical Bulletin Number 188, January 1994). Clinical man-
agement guidelines for obstetrician-gynecologists. Int J Gynaecol Obstet
2000;68:175e85.
[18] Piazze J, Anceschi MM, Cerekja A, Brunelli R, Meloni P, Marzano S, et al.
Validity of amniotic fluid index in preterm rupture of membranes. J Perinat
Med 2007;35:394e8.
[19] Jeon SR, Kwon J, Kim YH, Park Y-W. 510: prognostic factors associated with
prediction of longer latency in PPROM. Am J Obstet Gynecol 2009;201:S190.
[20] Thurnau G. The NICHD-MFMU antibiotic treatment of pProm study: impact of
initial amniotic fluid volume on pregnancy outcome. Am J Obstet Gynecol
1997;176:S53.
[21] Rutherford SE, Phelan JP, Smith CV, Jacobs N. The four-quadrant assessment of
amniotic fluid volume: an adjunct to antepartum fetal heart rate testing.
Obstet Gynecol 1987;70:353e6.
[22] Magann EF, Sanderson M, Martin JN, Chauhan S. The amniotic fluid index,
single deepest pocket, and two-diameter pocket in normal human pregnancy.
Am J Obstet Gynecol 2000;182:1581e8.
[23] Foundation PQ. Clear guidelines for cervical length. 2013. https://clear.
perinatalquality.org. [Accessed 20 March 2013].
[24] Zeng LN, Zhang LL, Shi J, Gu LL, Grogan W, Gargano MM, et al. The primary
microbial pathogens associated with premature rupture of the membranes in
China: a systematic review. Taiwan J Obstet Gynecol 2014;53:443e51.
[25] Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C. Amniotic
infection syndrome: nosology and reproducibility of placental reaction pat-
terns. Pediatr Dev Pathol 2003;6:435e48.
[26] Lain SJ, Algert CS, Nassar N, Bowen JR, Roberts CL. Incidence of severe adverse
neonatal outcomes: use of a composite indicator in a population cohort.
Matern Child Health J 2012;16:600e8.
[27] Crane JM, Hutchens D. Use of transvaginal ultrasonography to predict preterm
birth in women with a history of preterm birth. Ultrasound Obstet Gynecol
2008;32:640e5.
[28] Jia X. Value of amniotic fluid IL-8 and Annexin A2 in prediction of preterm
delivery in preterm labor and preterm premature rupture of membranes.
J Reprod Med 2014;59:154e60.
[29] Odibo AO, Talucci M, Berghella V. Prediction of preterm premature rupture of
membranes by transvaginal ultrasound features and risk factors in a high-risk
population. Ultrasound Obstet Gynecol 2002;20:245e51.
[30] van de Laar R, van der Ham DP, Oei SG, Willekes C, Weiner CP, Mol BW. Ac-
curacy of C-reactive protein determination in predicting chorioamnionitis and
neonatal infection in pregnant women with premature rupture of mem-
branes: a systematic review. Eur J Obstet Gynecol Reprod Biol 2009;147:
124e9.
[31] Ryu HK, Moon JH, Heo HJ, Kim JW, Kim YH. Maternal c-reactive protein and
oxidative stress markers as predictors of delivery latency in patients experi-
encing preterm premature rupture of membranes. Int J Gynaecol Obstet
2017;136:145e50.
[32] von Dadelszen P, Kives S, Delisle MF, Wilson RD, Joy R, Ainsworth L, et al. The
association between early membrane rupture, latency, clinical chorioamnio-
nitis, neonatal infection, and adverse perinatal outcomes in twin pregnancies
complicated by preterm prelabour rupture of membranes. Twin Res 2003;6:
257e62.
[33] Test G, Levy A, Wiznitzer A, Mazor M, Holcberg G, Zlotnik A, et al. Factors
affecting the latency period in patients with preterm premature rupture of
membranes. Arch Gynecol Obstet 2011;283:707e10.
[34] Aziz N, Cheng YW, Caughey AB. Factors and outcomes associated with longer
latency in preterm premature rupture of membranes. J Matern Fetal Neonatal
Med 2008;21:821e5.
[35] Aye IL, Lager S, Ramirez VI, Gaccioli F, Dudley DJ, Jansson T, et al. Increasing
maternal body mass index is associated with systemic inflammation in the
mother and the activation of distinct placental inflammatory pathways. Biol
Reprod 2014;90:129.
[36] Nayot D, Penava D, Da Silva O, Richardson BS, de Vrijer B. Neonatal outcomes
are associated with latency after preterm premature rupture of membranes.
J Perinatol 2012;32:970e7.
[37] Liu S, Tong X. The clinical comparative study of preterm respiratory distress
syndrome and transient tachypnea of newborn. Zhonghua Er Ke Za Zhi
2015;53:104e8.
[38] van Teeffelen AS, van der Ham DP, Oei SG, Porath MM, Willekes C, Mol BW.
The accuracy of clinical parameters in the prediction of perinatal pulmonary
hypoplasia secondary to midtrimester prelabour rupture of fetal membranes:
a meta-analysis. Eur J Obstet Gynecol Reprod Biol 2010;148:3e12.
[39] Espinoza J, Chaiworapongsa T, Romero R, Edwin S, Rathnasabapathy C,
Gomez R, et al. Antimicrobial peptides in amniotic fluid: defensins, calpro-
tectin and bacterial/permeability-increasing protein in patients with micro-
bial invasion of the amniotic cavity, intra-amniotic inflammation, preterm
labor and premature rupture of membranes. J Matern Fetal Neonatal Med
2003;13:2e21.