3310jum1721-1878.online_Layout 1 9/22/14 11:22 AM Page 1733 ORIGINAL RESEARCH Association Between Second-Trimester Cervical Length and Cesarean Delivery in Multiparas Emily S. Miller, MD, MPH, Brett Einerson, MD, MPH, Sadia Sahabi, BA, William A. Grobman, MD, MBA Objectives—The purpose of this study was to determine whether there is an association between second-trimester cervical length and cesarean delivery in women with a prior vaginal delivery. Methods—We conducted a retrospective cohort study of multiparous women with singleton gestations who underwent routine cervical length screening between 18 and 24 weeks’ gestation and labored after 34 weeks. Cervical lengths were divided into quartiles, and the frequency of cesarean delivery was compared across the groups. Indications for cesarean delivery were also compared. A multivariable logistic regression was performed with cervical length as a categorical and a continuous variable to adjust for potential confounders. Results—Of the 2260 multiparas who met inclusion criteria, 63 (2.8%) underwent a cesarean delivery. We observed no association between the second-trimester cervical length quartile and the frequency of cesarean delivery (2.1%, 3.5%, 2.3%, and 3.1%, respectively; P = .434). Further analysis using cervical length as a continuous variable and controlling for potential confounding variables did not change this result (adjusted odds ratio, 1.08; 95% confidence interval, 0.80–1.46). Conclusions—The second-trimester cervical length quartile in multiparas is not associated with an increased frequency of cesarean delivery. This finding differs from studies of nulliparas. Key Words—cervical length; cesarean delivery; obstetrics; obstetric ultrasound; transvaginal sonograph Received December 6, 2013, from Northwestern University, Feinberg School of Medicine, Chicago, Illinois USA. Revision requested January 20, 2014. Revised manuscript accepted for publication January 31, 2014. Address correspondence to Emily S. Miller, MD, MPH, Northwestern University, Feinberg School of Medicine, 250 E Superior St, Suite 052185, Chicago, IL 60611 USA. E-mail: [email protected]. edu Abbreviations BMI, body mass index; CI, confidence interval; OR, odds ratio doi:10.7863/ultra.33.10.1733 T he cervix plays a pivotal role in regulating the timing and successful completion of labor. Histologically, remodeling and conditioning of the cervix begin long before the initiation of labor.1 Correspondingly, the cervix begins a process of progressive shortening, which is demonstrable by sonography in the second trimester.2 The consequences of a short cervical length are clear: women with a short cervix in the second trimester have an increased risk of preterm delivery.3–7 Since a short cervical length is associated with early labor, the converse might be true that a long cervical length is associated with ineffective preparation for labor. Indeed, a long cervical length near the end of pregnancy is associated with a higher likelihood of induction and cesarean delivery.8 Women with longer cervical lengths in the second trimester also may be at risk for cesarean delivery due to an increased chance of arrest disorders. One study of nulliparous women in the United Kingdom showed an association between a ©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:1733–1736 | 0278-4297 | www.aium.org 3310jum1721-1878.online_Layout 1 9/22/14 11:22 AM Page 1734 Miller et al—Second-Trimester Cervical Length and Cesarean Delivery in Multiparas longer cervical length in the second trimester and subsequent cesarean delivery.9 A subsequent investigation in the United States confirmed this relationship and found the increase in risk to be predominantly related to the increased risk of arrest of dilatation.10 However, multiparas are considerably less likely than nulliparas to require a cesarean delivery or to have an arrest disorder. Whether an association between second-trimester cervical changes and cesarean delivery also is present in multiparas is unknown. We hypothesized that, as in nulliparous women, multiparous women with a longer cervical length would have an increased frequency of cesarean delivery for labor arrest. Our objective, therefore, was to study, among women with a prior vaginal delivery and no prior cesarean delivery, whether cervical length measured during routine second-trimester screening is associated with the risk of cesarean delivery specifically in multiparas. Materials and Methods We conducted a cohort study of women who received routine cervical length screening between December 2010 and January 2012. The Institutional Review Board of Northwestern University approved this study. Women were included in this analysis if they were older than 18 years, had a singleton gestation, attempted a vaginal delivery, and delivered at or after 34 weeks’ gestation. Women who underwent a termination of pregnancy or had a fetal demise were excluded. During the study period at the institution where the study occurred, transvaginal cervical length assessment between 18 and 24 weeks’ gestation was considered a routine part of the anatomic survey. Cervical length was measured transvaginally by staff sonographers and verified by a sonologist, all of whom were previously trained according to the method of Iams et al.4 Records of all women who had a second-trimester cervical length measurement were identified by a query of the clinical sonographic reports. If multiple measurements were taken, the measurement taken closest to 20 weeks’ gestation was used. Once women with second-trimester transvaginal cervical length measurements were identified, their medical charts were reviewed to identify whether they met inclusion criteria. The charts of those eligible were then abstracted for demographic and obstetric characteristics, including maternal age, race/ethnicity, tobacco use, body mass index (BMI) at delivery, prior cervical excision procedures (eg, cold knife cone and loop electrosurgical excision procedures), method of conception, and pregnancy complications (eg, hypertensive disorders, diabetes or gestational 1734 diabetes, and oligohydramnios). The gestational age at delivery, type of labor (ie, induced or spontaneous), and birth weight in the index pregnancy also were abstracted. Cervical length was divided into quartiles to facilitate analysis. Baseline patient and obstetric characteristics of the study population were compared according to these quartiles. Comparisons were performed by the KruskalWallis test or χ2 analysis for continuous and categorical variables, respectively, and the nonparametric test for trend was used to assess trends of categorical variables. The primary outcome was cesarean delivery, which was compared according to the cervical length quartile. In addition, the indication for cesarean delivery, dichotomized as either an arrest disorder or “other” indication, was compared by cervical length quartile. Multivariable logistic regression was performed to determine whether cervical length (both as a categorical and a continuous variable) was independently associated with cesarean delivery. Variables were entered into a multivariable model if they showed an association with the cervical length quartile at a P < .1 level in the bivariable analysis. Odds ratios (ORs) and 95% confidence intervals (CIs) were estimated. All tests were 2 tailed, and P < .05 was used to define statistical significance. Analyses were performed with Stata version 11.1 software (StataCorp, College Station, TX). Results During the study period, 2260 multiparas met inclusion criteria. Of these, 63 (2.8%) underwent a cesarean delivery. The indications for cesarean delivery were a nonreassuring fetal status in 23 women (36.5%) and an arrest disorder in 40 (63.5%). Baseline demographic and clinical characteristics of the study population, stratified by cervical length quartile, are shown in Table 1. Compared to those in the lowest quartile, women with longer cervical lengths were more likely to be Hispanic and have a larger BMI. Women in the higher quartiles also were less likely to have undergone a prior cervical excision procedure. Finally, women with longer cervical lengths were more likely to deliver later and have higher neonatal birth weights. There was no significant relationship between cesarean delivery and the cervical length quartile (Table 2). When separated by indications for cesarean delivery, cervical length was not associated with the risk of cesarean delivery, even among the subset with cesarean delivery for arrest disorders. Results were similar when the nonparametric test for trend was used. Adjusting for potential confounders in J Ultrasound Med 2014; 33:1733–1736 3310jum1721-1878.online_Layout 1 9/22/14 11:22 AM Page 1735 Miller et al—Second-Trimester Cervical Length and Cesarean Delivery in Multiparas a multivariable logistic regression did not change this conclusion (Table 3). Similarly, when cervical length was entered into the regression as a continuous variable, there was no identified association between cervical length and the odds of cesarean delivery (adjusted OR, 1.08; 95% confidence interval, 0.80–1.46). To the best of our knowledge, this study is the first to investigate the relationship between cervical length and cesarean delivery in multiparous patients. The results are in contrast to previous studies of nulliparous patients. Smith et al9 first reported an association between the secondtrimester cervical length quartile and frequency of cesarean delivery in a large population of nulliparous women in the United Kingdom.9 A study from the United States confirmed these findings in a general population of nulliparous women undergoing routine cervical length screening.10 In both of these studies, the authors found a trend between an increasing second-trimester cervical length quartile and cesarean delivery. Both studies also found increased ORs for cesarean delivery among women in the fourth quartile Discussion In this study of multiparas with a prior vaginal delivery, we observed no association between second-trimester cervical length and cesarean delivery. The absence of an association existed for cesarean delivery in general as well as for cesarean delivery due to an arrest disorder. Table 1. Patient Characteristics Stratified by Cervical Length Quartile Characteristic 1st Quartile (n = 561) Cervical length, cm 3.6 (3.3–3.8) Gestational age at cervical length, wk 20.3 (19.9–20.7) Maternal age, y 33 (30–35) Race White 291 (58.1) Black 68 (13.6) Hispanic 112 (22.4) Other 30 (6.0) Smoked during pregnancy 13 (2.4) BMI at delivery 28.4 (25.9–32.3) Prior cervical excision procedure 63 (11.2) Method of conception In vitro fertilization 9 (1.8) Any ART 10 (1.9) Pregnancy complications Hypertensive disorder 28 (5.0) GDM or DM 35 (6.2) Oligohydramnios 12 (2.1) Gestational age at delivery, wk 39.1 (38.4–39.7) ≥39 357 (63.6) ≥41 16 (2.9) Induction of labor 228 (40.6) Birth weight, g 3380 (3075–3650) 2nd Quartile (n = 598) 3rd Quartile (n = 560) 4th Quartile (n = 540) 4.3 (4.1–4.4) 20.3 (19.9–20.7) 33 (29–36) 4.8 (4.7–4.9) 20.3 (19.9–20.7) 33 (29–36) 5.6 (5.3–6.1) 20.1 (19.9–20.7) 33 (29–36) 309 (56.6) 53 (9.7) 150 (27.5) 34 (6.2) 5 (0.9) 28.8 (26.1–32.4) 37 (6.1) 306 (59.0) 52 (10.0) 145 (27.9) 16 (3.1) 7 (1.3) 29.5 (26.6–33.0) 41 (7.3) 250 (51.1) 46 (9.4) 165 (33.7) 28 (5.7) 6 (1.2) 29.5 (26.9–33.7) 19 (3.5) .159 <.001 <.001 11 (2.0) 12 (2.2) 14 (2.7) 18 (3.5) 15 (3.0) 17 (3.4) .488 .272 25 (4.2) 39 (6.5) 18 (3.0) 39.3 (38.7–39.9) 411 (68.7) 31 (5.2) 238 (39.8) 3425 (3130–3715) 31 (5.5) 38 (6.8) 11 (2.0) 39.3 (38.9–40.0) 409 (73.0) 28 (5.0) 225 (40.2) 3450 (3175–3760) 18 (3.3) 36 (6.7) 7 (1.3) 39.3 (38.6–40.0) 371 (68.7) 31 (5.7) 188 (34.8) 3465 (3158–3775) .314 .985 .250 <.001 .009 .111 .165 .002 P <.001 .095 .764 .002 Data are presented as mean (range) and number (percent). ART indicates assisted reproductive technology; DM, diabetes mellitus; and GDM, gestational diabetes mellitus. Table 2. Frequency of and Indications for Cesarean Delivery Stratified by Cervical Length Quartile Parameter Cesarean delivery Indication Arrest disorder Other 1st Quartile 2nd Quartile 3rd Quartile 4th Quartile P 12 (2.1) 21 (3.5) 13 (2.3) 17 (3.1) .434 7 (1.2) 5 (0.9) 12 (2.0) 9 (1.5) 8 (1.4) 5 (0.9) 13 (2.4) 4 (0.7) .439 .573 Data are presented as number (percent). J Ultrasound Med 2014; 33:1733–1736 1735 3310jum1721-1878.online_Layout 1 9/22/14 11:22 AM Page 1736 Miller et al—Second-Trimester Cervical Length and Cesarean Delivery in Multiparas compared to women in the first quartile, adjusted for possible confounding factors (adjusted ORs, 1.68 and 1.77, respectively). The same trend was not identified in this population of multiparas. As anticipated, the rate of cesarean delivery in this group of multiparous women was low; more than 97% of all women in this study achieved a vaginal delivery. Thus, it is possible that the absence of an association between second-trimester cervical length and cesarean delivery was the consequence of inadequate statistical power. Despite a large sample of multiparas, the total number of cesarean deliveries was only 63 (2.8% of all deliveries). However, with our sample size and the baseline cesarean rate in this study population, we were powered to detect a 2.5-fold increase in the cesarean frequency between the highest and lowest quartiles. Also, there was no evidence of a trend by quartile in this study. If a true association between cervical length and cesarean delivery existed in multiparas, we would expect to see a “dose-response” trend, even if pairwise comparisons were not statistically significant. This study offers further insight into the importance of second-trimester cervical length in predicting the risk of parturition abnormalities. Mounting evidence suggests that a longer cervical length in nulliparas is predictive of labor arrest and cesarean delivery.9,10 Changes in the cervix well before the onset of labor, it seems, must play an important role in preparation for successful parturition. This study suggests that the same association between cervical length and cesarean delivery does not exist in multiparas, implying perhaps that cervical changes required for successful labor occur at a different time, or in a different unmeasured manner, in the pregnancies of multiparas. References 1. Garfield RE, Saade G, Buhimschi C, et al. Control and assessment of the uterus and cervix during pregnancy and labour. Hum Reprod Update1998; 4:673–695. 2. Salomon LJ, Diaz-Garcia C, Bernard JP, Ville Y. Reference range for cervical length throughout pregnancy: non-parametric LMS-based model applied to a large sample. Ultrasound Obstet Gynecol 2009; 33:459–464. 3. Okitsu O, Mimura T, Nakayama T, Aono T. Early prediction of preterm delivery by transvaginal ultrasonography. Ultrasound Obstet Gynecol 1992; 2:402–409. 4. Iams JD, Goldenberg RL, Meis PJ, et al. 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; 334:567–573. 5. Hasegawa I, Tanaka K, Takahashi K, et al. Transvaginal ultrasonographic cervical assessment for the prediction of preterm delivery. J Matern Fetal Med 1996; 5:305–309. 6. Hassan SS, Romero R, Berry SM, et al. Patients with an ultrasonographic cervical length < or =15 mm have nearly a 50% risk of early spontaneous preterm delivery. Am J Obstet Gynecol 2000; 182:1458–1467. 7. To MS, Skentou C, Liao AW, Cacho A, Nicolaides KH. Cervical length and funneling at 23 weeks of gestation in the prediction of spontaneous early preterm delivery. Ultrasound Obstet Gynecol 2001; 18:200–203. 8. Rao A, Celik E, Poggi S, Poon L, Nicolaides KH; Fetal Medicine Foundation Prolonged Pregnancy Group. Cervical length and maternal factors in expectantly managed prolonged pregnancy: prediction of onset of labor and mode of delivery. Ultrasound Obstet Gynecol 2008; 32:646– 651. 9. Smith GC, Celik E, To M, Khouri O, Nicolaides KH. Cervical length at mid-pregnancy and the risk of primary cesarean delivery. N Engl J Med 2008; 358:1346–1353. 10. Miller ES, Sakowicz A, Grobman WA. Association between secondtrimester cervical length and primary cesarean delivery. Obstet Gynecol 2013; 122:863–867. Table 3. Multivariable Analyses of Factors Associated With Cesarean Delivery Parameter Cervical length quartile 1st (referent) 2nd 3rd 4th Race White (referent) Black Hispanic Other Prior cervical excision procedure BMI Gestational age at delivery 1736 Adjusted OR 95% CI 1.00 1.48 0.98 1.32 0.69–3.17 0.42–2.25 0.60–2.90 1.00 1.62 1.52 1.70 0.57 1.02 1.20 0.69–3.80 0.82–2.85 0.58–5.01 0.14–2.40 0.97–1.07 0.95–1.52 J Ultrasound Med 2014; 33:1733–1736
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