Obstetrics & Gynecology:
Ultrasonographic Evaluation of Myometrial Thickness and Prediction of a Successful External Cephalic Version
Buhimschi, Catalin S. MD; Buhimschi, Irina A. MD; Wehrum, Mark J. DO; Molaskey-Jones, Sherry RN; Sfakianaki, Anna K. MD; Pettker, Christian M. MD; Thung, Stephen MD; Campbell, Katherine H. MD; Dulay, Antonette T. MD; Funai, Edmund F. MD; Bahtiyar, Mert O. MD
From the Department of Obstetrics, Gynecology & Reproductive Sciences, Yale University, New Haven, Connecticut.
Supported by departmental funds.
The authors thank the nurses, fellows, residents, and faculty at Yale-New Haven Hospital, the Department of Obstetrics and Gynecology and Reproductive Sciences, and all the patients who participated in the study.
Corresponding author: Catalin S. Buhimschi, MD, Yale University, Department of Obstetrics, Gynecology & Reproductive Sciences, 333 Cedar Street, LLCI 804, New Haven, CT 06520; e-mail: email@example.com.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To test the hypothesis that myometrial thickness predicts the success of external cephalic version.
METHODS: Abdominal ultrasonographic scans were performed in 114 consecutive pregnant women with breech singletons before an external cephalic version maneuver. Myometrial thickness was measured by a standardized protocol at three sites: the lower segment, midanterior wall, and the fundal uterine wall. Independent variables analyzed in conjunction with myometrial thickness were: maternal age, parity, body mass index, abdominal wall thickness, estimated fetal weight, amniotic fluid index, placental thickness and location, fetal spine position, breech type, and delivery outcomes such as final mode of delivery and birth weight.
RESULTS: Successful version was associated with a thicker ultrasonographic fundal myometrium (unsuccessful: 6.7 [5.5–8.4] compared with successful: 7.4 [6.6–9.7] mm, P=.037). Multivariate regression analysis showed that increased fundal myometrial thickness, high amniotic fluid index, and nonfrank breech presentation were the strongest independent predictors of external cephalic version success (P<.001). A fundal myometrial thickness greater than 6.75 mm and an amniotic fluid index greater than 12 cm were each associated with successful external cephalic versions (fundal myometrial thickness: odds ratio [OR] 2.4, 95% confidence interval [CI] 1.1–5.2, P=.029; amniotic fluid index: OR 2.8, 95% CI 1.3–6.0, P=.008). Combining the two variables resulted in an absolute risk reduction for a failed version of 27.6% (95% CI 7.1–48.1) and a number needed to treat of four (95% CI 2.1–14.2).
CONCLUSION: Fundal myometrial thickness and amniotic fluid index contribute to success of external cephalic version and their evaluation can be easily incorporated in algorithms before the procedure.
LEVEL OF EVIDENCE: III
In 2009, the cesarean delivery rate in the United States rose to a record high of 32.9%, marking a 12th straight year of sustained increase.1 This represents more than a 50% increase since 1996 and qualifies cesarean delivery as the most common surgical procedure in the United States.1 This trend has generated considerable debate regarding the driving factors responsible for the high rate of cesarean delivery. Although no conclusive evidence exists as to which is the primary contributor to the increase, factors such as advanced maternal age at the time of first pregnancy, increased incidence of obesity, higher frequency of multiple pregnancies, level of medical training, and defensive medical practice may be held accountable for this trend.2
Cesarean delivery is not a benign surgery. Adverse short- and long-term maternal and fetal complications may be encountered.3–6 Therefore, decreasing the rate of both primary and repeat cesarean delivery has become a national and international goal.7–9 There is agreement that lowering the rate of cesarean delivery can be partially reached through careful assessment of the best mode of delivery for term breech singleton fetuses.9,10 The effect of a successful vaginal delivery for these fetuses is potentially major for the reason that approximately 85% of nonvertex presentations at term are breech.11
For the last decade, vaginal breech deliveries were approached cautiously and have virtually disappeared, because the associated neonatal morbidity has been judged excessive.12 However, the earlier American College of Obstetricians and Gynecologists position that a planned vaginal delivery of a term singleton breech was not appropriate has been revised10 based on maternal and fetal long-term follow-up data failing to demonstrate a benefit of scheduled cesarean delivery compared with deliberate vaginal birth.13,14 Conceivably, because the number of physicians skilled in performing vaginal breech deliveries has decreased substantially, breech presentation continues to be one of the most common indications for cesarean delivery.
External cephalic version has been advocated as a safe measure in an attempt to avoid a cesarean delivery.15 The ultimate goal is to attain vertex presentation by applying external pressure on the maternal abdomen. The success rate of an external cephalic version varies from 35% to 86%.15–17 Factors such as gestational age, parity, amniotic fluid volume, placental location, maternal weight, fetal spine, breech location and type, estimated fetal weight, anesthesia, different examiners, various patient populations, and the uterine tone may account for this broad range of success.15,18,19 Although the importance of each of these factors was difficult to quantify, a previous study indicated that uterine tone was one of the most significant markers of success.20 Because uterine tone was appreciated by the easiness with which fetal parts were palpated, this indicator had a large margin of subjectivity. Availability of ultrasonographic technology offers the potential of a more objective evaluation of uterine tone and better selection of candidates for external cephalic version.
The tension of a muscle at rest defines its physiological tonus. This is also applicable to the uterine wall.21 As previously reported by Deyer et al,22 uterine wall tonus is directly related to intrauterine pressure and radius of the uterine cavity but inversely proportional to thickness of the myometrium. Therefore, the thicker the uterine wall, the lower should be its tonus.21,23 We hypothesized that thickness of the myometrium is an important predictor of external cephalic version success. We tested our hypothesis by measuring myometrial thickness by ultrasonographic scanning immediately before an attempted external cephalic version maneuver.
MATERIALS AND METHODS
Myometrial thickness was measured in 114 consecutive pregnant women with breech presentations who were referred to Yale-New Haven Hospital as candidates for external cephalic version (May 2004 to July 2007). Eligible patients were enrolled based on availability of one of the investigators (C.S.B.). The institutional review board (Human Research Protection Program) of Yale University approved our research protocol. All women solicited for enrollment agreed to participate and provided written informed consent.
For clinical purposes, each woman's suitability for external cephalic version was evaluated through a nonstress test and a screening ultrasonographic scan intended to confirm breech presentation, calculate the amniotic fluid index, establish the placental position, and estimate the fetal weight. In accordance with the American College of Obstetricians and Gynecologists,15 selection of the appropriate candidates for an external cephalic version procedure based on strict inclusion or exclusion criteria is difficult. Although several conditions are uniformly accepted, many criteria should be interpreted as “relative” rather than “absolute” indications or contraindications. For the purpose of this study, eligibility criteria required a singleton fetus in breech presentation of at least 35 weeks estimated gestational age, intact membranes, amniotic fluid index 8 cm or greater, estimated fetal weight 4,000 g or less, and category I fetal heart rate testing. Exclusion criteria included: fetal anomalies or growth restriction (sonographic fetal weight less than 10% percentile for estimated gestational age) or both, multifetal gestations, history of vaginal bleeding, placental abnormalities (previa or vasa previa), uterine structural abnormalities, cervical cerclage, maternal hypertension, category II or III nonstress fetal heart rate patterns, labor contractions, and previous uterine scar.
For clinical relevance and generalizability of the findings, technical performance of the external cephalic version was left at the discretion of the attending physicians who remained unaware of myometrial thickness measurements. All the attending physicians who performed the procedures were board-certified by the American Board of Obstetrics and Gynecology. Before the procedure, all patients received 0.25 mg terbutaline subcutaneous. Women were placed in the Trendelenburg position to facilitate the displacement of the breech from the maternal pelvis. First, the external cephalic version method adopted either the “forward” or the “backward” technique by a single operator. Assistance from a second physician was requested in 52% (59 of 114) of the cases, when the initial attempt using the single-operator technique was unsuccessful. No more than three attempts were allowed. Procedures were suspended for unreasonable maternal discomfort. During the external cephalic version, fetal body displacement and heart rate were monitored continuously by ultrasonography. After the procedure, the fetal heart rate was continuously monitored for at least 30 minutes, independent of the success or failure of the external cephalic version. Rh immunoglobulin was administered to all Rh-negative women.
Subsequent to the external cephalic version maneuver, all women were followed to the point of delivery. Women who had a successful external cephalic version procedure were transferred to the birth unit for labor induction if estimated gestational age was 39 weeks or greater and cervical status was appreciated as favorable (Bishop score 4 or greater). If estimated gestational age was less than 39 weeks, pregnancy was allowed to continue with a recommendation for a nonstress test weekly until spontaneous onset of labor. A cesarean delivery was recommended for spontaneous reversion to a breech presentation or for intrapartum obstetric indications such as category III fetal heart rate or dystocia. In the setting of a failed external cephalic version, a cesarean delivery was performed if estimated gestational age was 39 weeks or greater. Pregnancy was allowed to continue if estimated gestational age was less than 39 weeks. Surgical delivery was recommended for cases with persistence of breech presentation at the time of spontaneous onset of labor or when estimated gestational age reached 39 weeks.
All ultrasonographic examinations were performed 15–20 minutes before the procedure and administration of terbutaline. To exclude ultrasonographic interoperator variability, all ultrasonographic examinations were performed by a single examiner (C.S.B.). Similar to our previous study,21 an abdominal ultrasonographic survey was performed using a 5.0- or 7.5-MHz transabdominal probe. The amniotic fluid index was measured using the four-quadrant technique.24 Oligohydramnios was defined as an amniotic fluid index 5 cm or less. The myometrium was ultrasonographically identified as the echohomogeneous layer between the uterine serosa and decidua. A standardized method of myometrial thickness measurement was adopted by applying the horizontal lines of the “+” calipers in the middle of the echogenic line defining the serosa and decidua, respectively (Fig. 1;video available at http://links.lww.com/AOG/A260 or by scanning the QR code [below] on your smartphone). At least three individual measurements were acquired and averaged for each site. Three different uterine wall sites were evaluated: lower segment (1.5–2 cm above reflection of the urinary bladder), midanterior wall (ultrasonographic probe placed 1 cm below the maternal umbilicus), and uterine fundus.25 Thickness of the fundal wall was measured by placing the scan probe in the midline above the uterine fundus. Measurements were performed once the entire curvature of the uterus was visualized. To assure consistency regarding the evaluation site, maternal aortic pulsations were identified before fundal myometrial thickness measurements. The intraobserver coefficient of variation for assessment of myometrial thickness was less than 5%. In addition to myometrial thickness, estimated fetal weight, and amniotic fluid index, several other ultrasonographic parameters were evaluated: 1) fetal breech type (frank, complete, footling); 2) fetal spine position (left, right, anterior, posterior, intermediate); 3) position of the fetal head (right, left, midline); 4) placental position (anterior, posterior, fundal); 5) placental thickness (evaluated at the site of umbilical cord insertion); and 6) maternal abdominal wall thickness (evaluated at midline by placing the probe on the same site used to evaluate myometrial thickness of the midanterior wall). Data derived from all these examinations were included in the final analysis.
Data sets were subjected to normality testing using the Shapiro-Wilk method. The data are reported as median and interquartile range and compared using Mann-Whitney rank sum test. Proportions were compared with χ2 or Fisher's exact tests as appropriate. Ninety-five percent confidence intervals (CIs) for proportions were calculated using the modified Wald method and GraphPad software. Multivariable logistic regression analysis was applied to identify any concurrent associations between maternal, fetal, and ultrasonographic independent variables and successful external cephalic version (version of the fetus from breech to vertex presentation) as the dependent variable. Receiver operating characteristics curve analysis was performed to identify the myometrial thickness cutoff point more likely to predict women with a successful external cephalic version. P<.05 was considered to indicate statistically significant differences.
In Table 1 we present the demographic and ultrasonographic characteristics of our study population as assessed at enrollment. The overall success rate of the external cephalic version was 46% (95% CI 37–55; 52 of 114). Fetuses of women who had a successful external cephalic version had higher ultrasonographic estimated fetal weight and presented more frequently as complete breech. The amniotic fluid index was significantly higher in women who had a successful version (Fig. 2A). There was no maternal or fetal morbidity related to the procedure.
In Table 2 we present the outcome characteristics of women who had an attempted external cephalic version. Women who were verted successfully to a cephalic presentation had longer gestations. After successful external cephalic version, four fetuses reversed spontaneously to a breech presentation. Vaginal delivery was achieved in 71% (95% CI 58–82; 37 of 52) of cases with successful external cephalic version procedures. In this group, indications for cesarean delivery were: dystocia (n=8), breech (n=4), failed induction (n=1), macrosomia (n=1), cord prolapse (n=1), and abruption (n=1). The group of women with successful external cephalic version delivered neonates with significantly higher birth weights. Overall the neonatal status at delivery was favorable for both groups with no differences in Apgar scores.
Ultrasonographic measurement of myometrial thickness showed that a significantly thicker fundal myometrium was associated with a successful external cephalic version (unsuccessful: odds ratio [OR] 6.7, 95% CI 5.5–8.4 compared with successful: OR 7.4, 95% CI 6.6–9.7 mm, P=.037; Fig. 2B). Thickness of the lower segment and midanterior uterine wall was not significantly different between groups (lower segment, unsuccessful: OR 4.3, 95% CI 3.3–5.1 compared with successful: OR 4.3, 95% CI 3.4–6.6 mm, P=.173; midanterior, unsuccessful: OR 6.1, 95% CI 5.1–6.9 compared with successful: OR 6.5, 95% CI 4.8–8.7 mm, P=.260).
In multivariable analysis, increased fundal myometrial thickness and high amniotic fluid index were the strongest independent predictors of external cephalic version success (amniotic fluid index: P=.002 and fundal myometrial thickness: P=.028) with variables such as maternal age, parity, body mass index, abdominal wall thickness, estimated fetal weight, placental thickness and location, and fetal spine and head positions excluded from the model based on P>.1 (Table 3). Frank breech presentation was associated with increased risk of external cephalic version failure (P=.036).
The receiver operating characteristics curve analysis determined that fundal myometrial thickness and amniotic fluid index were each able to significantly predict a successful compared with failed external version (area under the curve: myometrial thickness: OR 0.615, 95% CI 0.518–0.706, P=.032; amniotic fluid index: OR 0.678, 95% CI 0.583–0.763, P<.001). The optimal cutoffs to predict a successful version were 6.75 mm for myometrial thickness (positive predictive value: OR 57%, 95% CI 44–70, negative predictive value: OR 69%, 95% CI 54–82) and 12 cm for amniotic fluid index (positive predictive value: OR 59%, 95% CI 44–72, negative predictive value: OR 65%, 95% CI 51–76). A fundal myometrial thickness of greater than 6.75 or an amniotic fluid index of greater than 12 cm were each more likely associated with a successful external cephalic version (fundal myometrial thickness: OR 2.4, 95% CI 1.1–5.2, P=.029; amniotic fluid index: OR 2.8, 95% CI 1.3–6.0, P=.008). When analyzing the two variables in a combined algorithm, we noted that women who fulfilled both criteria (myometrial thickness greater than 6.75 mm and amniotic fluid index greater than 12 cm) were three times more likely to have a successful external cephalic version compared with those who did not meet any of the two criteria (χ2 P=.002; Fig. 3). Combining the two variables resulted in an absolute risk reduction for a failed version of 27.6% (95% CI 7.1–48.1) and a number needed to treat of four (95% CI 2.1–14.2).
In the present investigation we showed that thickness at the uterine fundus correlates with the success rate of an external cephalic version. These results were counterintuitive given that one might expect that only a thinner myometrium may ease with version of the fetus, yet our ultrasonographic data support Aisenbrey's et al20 previous assertion that uterine tone may be an important predictor of success for an external cephalic version maneuver.
Uterine tonus is a function of myometrial contractility and thickness.23 A number of laws of physics dictate the relationship between uterine wall tension and intrauterine pressure. Specifically, in a closed system such as a pregnant uterus with intact membranes, the uterine wall tonus is determined by the Laplace law (uterine tonus=[IUP×R]/2, where IUP=intrauterine pressure and R=radius of the uterus).26 Because uterine radius increases progressively during human gestation to accommodate the developing fetus, tonus of the uterine wall must also change accordingly to maintain a low intrauterine pressure. Although for evident reasons uterine tonus cannot be measured invasively, ultrasonographic myometrial thickness can be used as a surrogate indicator of its strength. In prior publications we reported that a thick myometrium indicates a relative state of low intrauterine pressure and thus decreased uterine tonus.25 These results were substantiated by the observation that in women with preterm premature rupture of membranes, a thick myometrium was associated with longer latency intervals.21 Based on the available data, we posit that increased thickness of the myometrium reflects a state of lower uterine wall tonus, which in turn facilitates manipulation and reposition of the fetus in utero.
By study design, all women enrolled in our study received terbutaline. This pharmacologic agent has been previously used as a facilitator of external cephalic version with various degrees of success.27–29 Whether terbutaline further lowers the myometrial wall tone and affects myometrial thickness in an individualized fashion remains unknown and would require further investigation.
The results of the present study have several clinical implications. External cephalic version offers a realistic opportunity of reducing the rate of cesarean delivery associated with breech presentation of the fetus at term.15 In our cohort, the rate of a successful external cephalic version and a subsequent vaginal delivery was 46% and 71%, respectively. This was comparable to prior literature reports.20,30,31 In addition, there has been much recent attention focused on the cost-effectiveness of external cephalic version.32 Tan et al determined that attempting external cephalic version is cost-effective compared with a scheduled cesarean delivery, providing that the success rate of external cephalic version is at least 32%. Therefore, ours and others' outcome data support the notion that external cephalic version is safe and economically sound. However, optimization of clinical algorithms to identify candidates with an increased likelihood of success is required.
For many years, investigators have searched for factors that are either predictive of success or failure of an external cephalic version. In the current study, some variables (ie, high body mass index, low parity) were not associated with a failed external cephalic version, whereas others such as frank breech presentation were confirmed. This should not come as a surprise given that in some studies, obesity was found to be associated with a higher failure rate,33 whereas others determined that maternal weight is not a predictor of success.34 Similar findings are applicable for parity and breech types.31,32 The available literature reflects that differences in external cephalic version outcomes most probably arise from the large diversity of study designs, sample sizes, and statistical methodologies used in each study. A review of the proposed contribution of each ultrasonographic variable that may facilitate or impede turning of the fetus from a breech to a vertex presentation is beyond the purpose of our article. Given the large heterogeneity of the published data, the reader is referred to two recent excellent review articles by Burgos and Kok et al.32,35 These most recent efforts suggest that although the contribution of parity, placental location, fetal position, amniotic fluid index, and many other variables has been extensively studied, the role of myometrial thickness as a surrogate of uterine tone has not been studied before. The results of the present investigation indicate that increased fundal myometrial thickness along with high amniotic fluid index were the strongest independent predictors of external cephalic version success. In combination, these two ultrasonographic variables can identify a group of patients in which external cephalic version is likely to be successful as well as a group of patients in which external cephalic version is likely to fail. One could argue that given its very low associated risks, the external cephalic version should usually be attempted, unless the chance for success is estimated as very low. We agree. It is difficult to imagine that 1 mm in fundal thickness alone would influence outcome. At this point, we imply that, in concert, fundal myometrial thickness as a reflection of uterine tonus and amniotic fluid index may influence the result of an external cephalic procedure. The clinical value of such measurements should be tested in large populations.
It remains unknown why myometrial thickness of the uterine fundus, but not that of other investigated sites, affected the outcome of the external cephalic version. In previous studies we showed that in the absence of labor, myometrial thickness of women with fetuses in vertex presentation did not differ among sites.25 It is conceivable that the uterine wall of women with fetuses in breech presentation was different at various sites. This could partially explain the lack of spontaneous version to a vertex presentation at term. We acknowledge that our sample size may be too small to depict such subtle differences in thickness and propose that further studies are needed to test this premise.
In summary, this study demonstrated that myometrial thickness of the uterine fundal wall and amniotic fluid index are factors associated with the success rate of an external cephalic version attempt. Both variables could be easily incorporated into scoring algorithms aimed at optimizing the selection of candidates who may have a successful version.
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