Ultrasound Obstet Gynecol 2009; 33: 209212 Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.

6301

Cervical length and risk of antepartum bleeding in women with complete placenta previa
T. GHI*, E. CONTRO*, T. MARTINA*, M. PIVA*, R. MORANDI*, L. F. ORSINI*, M. C. MERIGGIOLA*, G. PILU*, A. M. MORSELLI-LABATE, D. DE ALOYSIO*, N. RIZZO* and G. PELUSI*
Departments of *Obstetrics and Gynecology and Internal Medicine and Gastroenterology, University Hospital of Bologna, Bologna, Italy

K E Y W O R D S: antepartum bleeding; cervical length; placenta previa; preterm delivery; ultrasound

ABSTRACT
Objective To evaluate if cervical length predicts prepartum bleeding and emergency Cesarean section in cases of placenta previa. Methods Between September 2005 and September 2007, cervical length was measured by transvaginal ultrasound in women with complete placenta previa persisting into the third trimester of pregnancy. A complete follow-up of pregnancy was obtained in all cases. Results Overall, 59 women were included in the study group. The mean SD gestational age at ultrasound was 30.7 2.7 weeks and the cervical length was 36.9 8.8 mm. Cesarean delivery was performed in all cases, at a mean gestational age of 34.7 2.3 weeks. Twenty-nine (49.1%) of the women presented prepartum bleeding and 12 (20.3%) required an emergency Cesarean section prior to 34 completed weeks due to massive hemorrhage. Cervical length did not differ signicantly between cases with and those without prepartum bleeding (35.3 9.3 mm vs. 38.4 8.2 mm; P = 0.18), but was signicantly shorter among patients who underwent emergency Cesarean section < 34 weeks due to massive hemorrhage compared with patients who underwent elective Cesarean section (29.4 5.7 mm vs. 38.8 8.5 mm; P = 0.0006). Conclusions Transvaginal sonographic cervical length predicts the risk of emergency Cesarean section < 34 weeks in women with complete placenta previa. Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd.

rising rates of Cesarean section. It is estimated to occur in between 0.2 and 0.3% of third-trimester pregnancies1 . A conclusive diagnosis of complete placenta previa is ascertained sonographically in the third trimester, when upward migration from the internal cervical os becomes unlikely2 . Women with placenta previa are at increased risk of prepartum maternal bleeding and emergency preterm Cesarean section leading to perinatal complications. Furthermore, in these cases the higher chance of postpartum complications, including uterine atony and placenta accreta, is well established. However, the risk of maternal hemorrhage or prematurity is unpredictable. In theory, such complications could be expected more frequently in those patients whose risk of preterm labor is also increased. An inverse relationship between cervical length measured by transvaginal ultrasound and the risk of spontaneous preterm labor has been clearly demonstrated3,4 . The aim of our study, therefore, was to determine if transvaginal ultrasound assessment of cervical length predicts the risk of prepartum bleeding or preterm emergency Cesarean section due to massive hemorrhage in women with complete placenta previa diagnosed in the third trimester of pregnancy.

PATIENTS AND METHODS

Between September 2005 and September 2007 all asymptomatic women diagnosed consecutively with complete placenta previa at the ultrasound laboratory of our University Hospital were selected for the purpose of this study. Patients had been referred to our center due to sonographic suspicion of placenta previa. Diagnosis of complete placenta previa was made by transvaginal ultrasound in the third trimester of pregnancy when the lower placental edge appeared to overlay completely the

INTRODUCTION
Placenta previa has been diagnosed increasingly in recent decades, due to the widespread use of ultrasound and the

Correspondence to: Dr T. Ghi, I Clinica Ostetrica-Ginecologica, Policlinico S. Orsola-Malpighi, Via Massarenti 13, 40100 Bologna, Italy (e-mail: tullio.ghi@aosp.bo.it) Accepted: 22 September 2008

Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd.

ORIGINAL PAPER

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Ghi et al. statistically signicant. Receiveroperating characteristics (ROC) curves were constructed to determine the accuracy of cervical length for the identication of women at high risk for prepartum vaginal bleeding and emergency Cesarean section < 34 weeks due to massive hemorrhage. The areas under the ROC curves together with their standard error were evaluated. The best cut-off was evaluated according to maximum likelihood ratio. The SPSS Version 13.0 (SPSS Inc., Chicago, IL, USA) statistical package was used to analyze data.

internal os of the uterine cervix. We excluded patients with any of the following conditions: gestational age < 27.0 and 36.0 completed weeks; multiple pregnancy; threatened preterm labor or premature rupture of membranes; history of bleeding in the current pregnancy; polyhydramnios; history of cervical cone biopsy; presence of cerclage; maternal use of vaginal progesterone; sonographic suspicion of fetal anomaly or fetal growth restriction; history of maternal disease or hypertensive disorder complicating the pregnancy. In all women included in the study group, cervical length was measured transvaginally at the time of diagnosis. Ultrasound examination was performed using a machine equipped with a multifrequency transvaginal probe (Tecnos and MyLab 50 Xview, Esaote, Genoa, Italy). Cervical evaluation was performed according to a standardized technique: women were asked to void their bladder before the examination. A true sagittal plane was obtained in order to visualize the full length of the cervical canal and cervical length was measured three times by placing the callipers on the internal and external os. The shortest measurement was then recorded. Following sonographic diagnosis of complete placenta previa, induction of lung maturity was carried out and elective Cesarean section was scheduled between 36 and 37 completed weeks of gestation. In all cases, low placental insertion was conrmed sonographically just prior to Cesarean delivery. If vaginal bleeding occurred prior to the scheduled Cesarean section, patients were admitted to the hospital and timing of delivery was decided according to the clinical condition of the patient. If the patient was clinically stable, delivery was carried out electively beyond 34 weeks of gestation, following documentation of fetal lung maturity by amniocentesis. In cases of massive maternal hemorrhage, emergency Cesarean section was performed before 34 weeks of gestation. Surgeons and obstetricians who assisted at the delivery were blinded to cervical length. Cases in which the indication for emergency Cesarean section was something other than massive hemorrhage or in which placenta accreta was diagnosed intraoperatively were excluded from the study. A complete follow-up of pregnancy was obtained in all cases, with the following variables being recorded: gestational age at delivery, neonatal weight, occurrence of prepartum bleeding, type of Cesarean delivery (elective vs. emergency Cesarean section due to massive hemorrhage). Mean cervical lengths in the groups with and without prepartum bleeding were compared retrospectively. Furthermore, we compared cervical length between patients who underwent elective Cesarean section and those who underwent emergency Cesarean section due to massive hemorrhage.

RESULTS
A total of 60 asymptomatic women with complete placenta previa were enrolled prospectively and included in the study group. A further ve more cases were considered ineligible due to previous bleeding in the current pregnancy. A case of placenta accreta was excluded retrospectively, leading to a nal population of 59 women. A summary of patient data and pregnancy outcome is provided in Table 1. Twenty-nine women (49.1%) were nulliparous, parity was 1 in 21 women and it was more than one in nine women. The mean SD gestational age at transvaginal ultrasound was 30.7 2.7 weeks and the cervical length was 36.9 8.8 mm. Cervical length did not vary signicantly between nulliparous and parous women (37.9 8.8 mm vs. 35.9 8.9 mm; P = 0.375). Cesarean section was performed in all cases, at a mean gestational age of 34.7 2.3 weeks. The mean birth weight was 2440.5 497.6 g. Twenty-nine (49.1%) of the women presented antepartum vaginal bleeding, 12 (20.3%) of whom required an emergency Cesarean section prior to 34 completed weeks due to massive hemorrhage (Table 2). There were no cases of emergency Cesarean section due to massive hemorrhage after 34 completed weeks of gestation. All women without prepartum bleeding reached the scheduled date for
Table 1 Patient characteristics and pregnancy outcome in 59 women with complete placenta previa in the third trimester of pregnancy Characteristic/outcome Maternal age (years) Parity 0 1 2 >2 Previous Cesarean section 0 1 >1 Gestational age at diagnosis (weeks) Cervical length (mm) All women Nulliparous women Parous women Gestational age at delivery (weeks) Birth weight (g)
n (%) or mean SD 34.9 4.5

29 (49.1) 21 (35.5) 6 (10.1) 3 (5.1) 11 (18.6) 12 (20.3) 7 (11.8) 30.7 2.7

36.9 8.8 37.9 8.8 35.9 8.9 34.7 2.3 2440.5 497.6

Statistical analysis
Data are reported as means and SDs. Continuous variables (cervical lengths) were compared using Students t-test. A two-tailed value of P < 0.05 was considered

Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd.

Ultrasound Obstet Gynecol 2009; 33: 209212.

Cervical length and bleeding in placenta previa

Table 2 Outcome of pregnancy according to cervical length in 59 women with complete placenta previa in the third trimester of pregnancy Cervical length (mean SD)
1.0

211

0.8
P

Outcome Vaginal bleeding With Without Cesarean section Emergency < 34 weeks Elective 34 weeks

n (%)

0.18
Sensitivity

29 (49.1) 30 (50.8) 12 (20.3) 47 (79.6)

35.3 9.3 38.4 8.2

0.6

0.0006
29.4 5.7 38.8 8.5

0.4

elective Cesarean section beyond 36 weeks of gestation, while in those with minor bleeding prior to the scheduled delivery, Cesarean section was performed electively after 34 weeks following documentation of fetal lung maturity. In no case was the indication for emergency Cesarean section something other than massive hemorrhage. The mean gestational age at delivery (32.5 1.4 weeks vs. 35.3 2.1 weeks; P = 0.00005) and mean birth weight (2136.6 356.6 g vs. 2518.1 501.5 g; P = 0.016) were signicantly lower in women who underwent emergency Cesarean section compared with those who underwent elective Cesarean section. The occurrence of prepartum bleeding and emergency section were comparable among nulliparous and parous women (OR, 1.46 (95% CI, 0.425.01) vs. 1.41 (95% CI, 0.513.87)). Cervical length did not differ signicantly between cases with and those without prepartum bleeding (35.3 9.3 mm vs. 38.4 8.2 mm; P = 0.18), but was signicantly shorter in patients who underwent emergency Cesarean section < 34 weeks due to massive hemorrhage compared with those who underwent elective Cesarean section 34 weeks (29.4 5.7 mm vs. 38.8 8.5 mm; P = 0.0006) (Table 2). ROC curves for cervical length in the prediction of vaginal bleeding and for cervical length in the prediction of emergency Cesarean section < 34 weeks are given in Figures 1 and 2, respectively. The best cut-off point for the identication of women at high risk for emergency Cesarean section < 34 weeks as determined from the ROC curve (Figure 2) was cervical length 31 mm (with 83.3% sensitivity, 76.6% specicity, 47.6% positive predictive value (PPV) and 94.7% negative predictive value (NPV) (P < 0.001). In particular, women whose cervical length was 31 mm at sonographic diagnosis of placenta previa had a 16 times higher risk of preterm Cesarean delivery due to massive hemorrhage (OR, 16.36 (95% CI, 3.3975.92)).

0.2

0.2

0.4 0.6 1 Specificity

0.8

1.0

Figure 1 Receiveroperating characteristics curve for cervical length in the prediction of vaginal bleeding in women with complete placenta previa in the third trimester of pregnancy.
1.0

0.8

Sensitivity

0.6

0.4

0.2

0.2

0.4 0.6 1 Specificity

0.8

1.0

Figure 2 Receiveroperating characteristics curve for cervical length in the prediction of emergency Cesarean section < 34 weeks in women with complete placenta previa in the third trimester of pregnancy.

DISCUSSION
Our study has conrmed that women with placenta previa are at higher risk of complications, including prematurity and severe hemorrhage. In this series, the chance of prepartum bleeding among women diagnosed sonographically with placenta previa in the third trimester was approximately 50%, while the risk of emergency Cesarean section prior to 34 completed weeks due to

massive hemorrhage was almost one in ve. This latter risk seemed to be higher among women whose cervical length was shorter. This observation may be of clinical value if our data are conrmed in larger series. Placenta previa is among the most frequently diagnosed obstetric conditions, with an increasing prevalence due to the widespread use of ultrasound and the rising rates of Cesarean section. However, women who are more prone to developing severe bleeding requiring an emergency premature delivery are not likely to be recognised in the preclinical stage. Consequently, all asymptomatic

Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd.

Ultrasound Obstet Gynecol 2009; 33: 209212.

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Ghi et al. possible coexistence with vasa previa7 , whereas its role in predicting the risk of maternal bleeding has been mostly unexplored. An increased thickness of the lower placental edge has been reported by some to increase the risk of prepartum hemorrhage10 . Others have shown a higher chance of massive bleeding among cases with an echo-free space and lacunae within the lower placental edge11 . Our ndings regarding a possible association between cervical length and the risk of preterm hemorrhage in patients with complete placenta previa have not been reported previously and may improve our ability to predict clinical course and to rene obstetric management in these cases. If our data are conrmed on larger numbers, an earlier hospital admission, or at least closer clinical monitoring, in women with placenta previa and short cervix may become a option.

women with complete placenta previa detected in the third trimester are usually scheduled for elective Cesarean section around 36 weeks of gestation unless vaginal bleeding occurs earlier. However, obstetric management is not tailored specically to the patient because individual risk of hemorrhage is difcult to predict. Our study seems to suggest that the shorter the cervix at the time of sonographic diagnosis of complete placenta previa in the third trimester, the higher the risk of severe prematurity and emergency Cesarean section due to massive maternal hemorrhage. In our series, if cervical length was 31 mm, the risk of preterm Cesarean section was almost one in two, whereas, due to the excellent negative predictive value of the ultrasound examination, whenever the cervical length was above this threshold, the need for preterm Cesarean section was rare. We controlled for possible confounding factors which might have contributed signicantly and independently to the outcomes, particularly the risks of vaginal bleeding and preterm delivery. Parity did not seem to interfere with the outcome, occurrence of prepartum bleeding or emergency Cesarean section not varying signicantly between nulliparous and parous women. Furthermore, we excluded retrospectively from the study a case of placenta accreta, as hemorrhage due to detachment would have been less likely in this case. The main limitation of our study is the small number of women enrolled, but, if our observations are conrmed in larger series, transvaginal measurement of cervical length could become part of the routine third-trimester scan in women with complete placenta previa in order to predict the risk of severe complications. The increased risk of preterm hemorrhage in women with complete placenta previa and short cervix could be explained by the fact that with a short cervix the chance of spontaneous preterm labor is increased. Sonographic detection of a short cervix has been demonstrated consistently to predict earlier occurrence of labor5,6 . A shorter cervix among women with placenta previa may therefore also herald premature onset of labor and possible detachment of the placenta from its low insertion. Classically, hemorrhage from placenta previa during labor has been related to the fact that, due to its inelastic structure, the placenta may not adapt to progressive cervical effacement and undergoes detachment7 . Our study suggests that in women with placenta previa, although the risk of minor prepartum bleeding does not seem to vary according to cervical length, shortening of the cervix even to a minor extent may predict an earlier placental detachment with massive hemorrhage. In women with placenta previa, the use of transvaginal ultrasound has been aimed more frequently at predicting persistence8 or adhesion9 of placenta or at detecting

REFERENCES
1. Tuzovic L. Complete versus incomplete placenta praevia and obstetric outcome. Int J Gynaecol Obstet 2006; 93: 110117. 2. Oppenheimer L, Holmes P, Simpson N, Dabrowski A. Diagnosis of low-lying placenta: can migration in the third trimester predict outcome? Ultrasound Obstet Gynecol 2001; 18: 100102. 3. Colombo DF, Iams JD. Cervical length and preterm labor. Clin Obstet Gynecol 2000; 43: 735745. 4. Iams JD, Goldenberg RL, Meis PJ, Mercer BM, Moawad A, Das A, Thom E, McNellis D, Copper RL, Johnson F, Roberts JM. The length of the cervix and the risk of spontaneous premature delivery. National Institute of Child Health and Human Development Maternal Fetal Medicine Unit Network. N Engl J Med 1996; 334: 567572. 5. Rozenberg P, Gillet A, Ville Y. Transvaginal sonographic examination of the cervix in asymptomatic pregnant women: review of the literature. Ultrasound Obstet Gynecol 2002; 19: 302311. 6. Palacio M, Sanin-Blair J, Sanchez M, Crispi F, Gomez O, Carreras E, Coll O, Cararach V, Gratacos E. The use of a variable cut-off value of cervical length in women admitted for preterm labor before and after 32 weeks. Ultrasound Obstet Gynecol 2007; 29: 421426. 7. Oyelese Y, Smulian JC. Placenta praevia, placenta accreta, and vasa praevia. Obstet Gynecol 2006; 107: 927941. 8. Oppenheimer L. Society of Obstetricians and Gynaecologists of Canada. Diagnosis and management of placenta praevia. J Obstet Gynaecol Can 2007; 29: 261273. 9. Sumigama S, Itakura A, Ota T, Okada M, Kotani T, Hayakawa H, Yoshida K, Ishikawa K, Hayashi K, Kurauchi O, Yamada S, Nakamura H, Matsusawa K, Sakakibara K, Ito M, Kawai M, Kikkawa F. Placenta praevia increta/percreta in Japan: a retrospective study of ultrasound ndings, management and clinical course. J Obstet Gynaecol Res 2007; 33: 606611. 10. Ghourab S. Third-trimester transvaginal ultrasonography in placenta praevia: does the shape of the lower placental edge predict clinical outcome? Ultrasound Obstet Gynecol 2001; 18: 103108. 11. Saitoh M, Ishihara K, Sekiya T, Araki T. Anticipation of uterine bleeding in placenta praevia based on vaginal sonographic evaluation. Gynecol Obstet Invest 2002; 54: 3742.

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Ultrasound Obstet Gynecol 2009; 33: 209212.