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Keywords:

  • cervix uteri;
  • Doppler ultrasound;
  • prolonged pregnancy;
  • spontaneous delivery;
  • three-dimensional imaging

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Objectives

To determine whether three-dimensional (3D) ultrasound including power Doppler examination of the cervix is useful for predicting time to spontaneous onset of labor or time to delivery in prolonged pregnancy.

Methods

A prospective study was conducted in 60 women who went into spontaneous labor. All underwent transvaginal 3D power Doppler ultrasound examination of the cervix immediately before a prolonged-pregnancy check-up at ≥ 41 + 5 gestational weeks. Univariate and multivariate logistic regression analysis was used to determine which of the following variables predicted spontaneous onset of labor > 24 h and > 48 h and vaginal delivery > 48 h and > 60 h: length, anteroposterior (AP) diameter and width of the cervix and of any cervical funneling; cervical volume (cm3); vascularization index (VI); flow index (FI); vascularization flow index (VFI); parity; and Bishop score. Multivariate logistic regression analysis was carried out both with and without Bishop score as a predictive variable. Receiver–operating characteristics (ROC) curves were used to describe the diagnostic performance of the tests.

Results

The areas under the ROC curves for Bishop score, cervical length, and logistic regression models did not differ significantly (areas ranging from 0.72 to 0.82). If Bishop score was not included in the logistic regression model, cervical length, VI and FI independently predicted delivery > 48 h, the likelihood increasing with increasing cervical length, decreasing VI and increasing FI.

Conclusions

In prolonged pregnancy cervical vascularization as estimated by 3D power Doppler ultrasound is related to time to delivery > 48 h, but the likelihood of delivery > 48 h can be predicted equally well using Bishop score alone or sonographic cervical length alone Copyright © 2006 ISUOG. Published by John Wiley & Sons, Ltd.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The traditional method for investigating cervical readiness for labor is digital examination, where the results of the examination are summarized in a Bishop score1. Although the Bishop score is recognized as a useful method, there are problems with its accuracy, because half of the cervix is not palpable at vaginal examination if the cervical canal is closed2. Transvaginal ultrasonography allows visualization of the entire cervix irrespective of whether the internal cervical os is closed or open at palpation. Studies have shown that transvaginal ultrasound examination of the cervix is a predictor of preterm, term or post-term delivery, and outcome of labor induction3–6. However, one research team found no relationship between sonographically measured cervical length and time to spontaneous onset of labor7. A few studies have suggested that three-dimensional (3D) ultrasound examination of the cervix will allow a more complete assessment of the cervix than two-dimensional (2D) ultrasound examination8,9.

There is evidence that angiogenic factors may play a role in cervical ripening and the birth process10. Therefore, we speculated that there might be changes in cervical vascularization during cervical ripening potentially detectable by 3D power Doppler ultrasound examination, and that this technique might be useful for predicting time to spontaneous onset of labor.

The aim of this study was to determine whether 3D ultrasound examination of the cervix, including 3D power Doppler ultrasonography, can provide useful information for predicting the time to spontaneous onset of labor or to vaginal delivery in prolonged pregnancy.

Patients and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The Ethics Committee of the Medical faculty of Lund University, Sweden, approved the study protocol. Informed written consent was obtained from all the women involved in the study after the nature of the procedures had been fully explained to them.

Women with a prolonged pregnancy were recruited as described elsewhere11. 121 consecutive women were asked to undergo a transvaginal ultrasound examination of the cervix using 3D gray-scale and power Doppler ultrasonography. Six women declined. Thus, a transvaginal 3D ultrasound examination of the cervix was performed in 115 women. Sixty of these women fulfilled all our inclusion criteria11 and constituted our study population.

Transvaginal sonography was carried out by a single operator (L.R.) using the same technique as described in detail elsewhere12,13. The equipment used was a GE Voluson 730 Expert ultrasound system (GE Healthcare, Zipf, Austria) equipped with a 2.8–10-MHz transvaginal transducer. The women were examined in the lithotomy position with an empty bladder. After switching the ultrasound system into the power Doppler mode and then into the 3D mode, an ultrasound volume containing the cervix was acquired and stored on the hard disk of the system for later analysis off-line. The following measurements were taken using ‘anyplane’ slicing: length, anteroposterior (AP) diameter and width of the cervix and of any cervical funneling. Funneling was defined as any visible opening of the internal cervical os. Cervical volume (cm3) and power Doppler flow indices, i.e. vascularization index (VI), flow index (FI) and vascularization flow index (VFI), were calculated using the Virtual Organ Computer-aided AnaLysis software (VOCAL)12,13. All ultrasound results were unavailable to the clinical staff.

After the ultrasound examination a digital examination of the cervix (Bishop score) was performed by the obstetrician in charge in the labor ward. The results were noted on a dedicated study form11. Clinical data about the pregnancy and delivery were obtained from KIKA-Journalen, a comprehensive information system developed at the Department of Obstetrics and Gynecology in Malmö, serving both as a patient record-keeping system and as a tool for quality control and other statistical purposes. Onset of labor was defined as the time when uterine contractions were regular with at least two contractions per 10 minutes.

Statistical analysis

Statistical calculations were carried out using the Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL, USA, version 12.02). The following outcome variables were chosen a priori: onset of labor > 24 h and > 48 h, and delivery > 48 h and > 60 h after the ultrasound examination. The statistical significance of a possible relationship between the outcome and the background variables was determined using univariate logistic regression analysis with likelihood ratios, the background variables examined being parity (parous women vs. nulliparous women), gestational age (< 42 + 0 vs. ≥ 42 + 0 gestational weeks), Bishop score, cervical length, AP diameter and width, flow indices, funneling (yes vs. no), and funnel size. Multivariate logistic regression analysis with stepwise selection of variables was used to determine which variables were independently associated with the outcome. Multivariate logistic regression analyses were made including parity (nulliparous women coded as 0 vs. parous women coded as 1), gestational age (< 42 + 0 gestational weeks coded as 0 vs. ≥ 42 + 0 gestational weeks coded as 1), and results of 3D ultrasound examination with and without Bishop score as predicting variables (all measurements in mm, funneling expressed as the mean of length, AP diameter and width, with 0 indicating absence of funneling). The likelihood ratio test was used to determine which variables to include in the logistic regression model, P < 0.05 being the threshold for inclusion. The objective of the model building process was to obtain a good fit for the data with the least number of independent variables. The application of the regression equation to data from each woman gave the probability for that woman to go into spontaneous labor > 24 h or > 48 h, and to deliver > 48 h or > 60 h, the estimated probability ranging from 0 to 1. Receiver–operating characteristics (ROC) curves14 were drawn for each diagnostic test (i.e. Bishop score, cervical length and the logistic regression models) to evaluate its diagnostic ability. The area under the ROC curve and the 95% confidence interval (CI) of this area were calculated. If the lower limit of the CI for the area under the ROC curve was > 0.5, the diagnostic test was considered to have a discriminatory potential. The statistical significance of a difference in the area under the ROC curve between the different diagnostic tests was determined as described by Hanley and McNeil15,16 using a customized computer program written in MATLAB (Version 6.5.0.180913a Release 13) designed by one of the co-authors (F. de S.). The ROC curves were also used to determine the mathematically best cut-off value for each diagnostic test, the best cut-off value being defined as the one corresponding to the point on the ROC curve situated furthest away from the reference line14. The sensitivity, false-positive rate, and positive and negative likelihood ratios of the mathematically best cut-off values with regard to predicting onset of labor > 24 h and > 48 h, and delivery > 48 h and > 60 h were also calculated. Two-tailed P≤0.05 was considered statistically significant.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The mean age ± SD of the women in the study was 31 ± 4.9 years and their mean body mass index in the first trimester was 28.7 ± 3.09 kg/m2. Twenty-nine (48%) women were parous. Nineteen women were examined at 41 + 5 to 41 + 6 weeks' gestation, 37 women at 42 + 0 weeks, and four women at 42 + 1 to 42 + 4 weeks. Vaginal delivery occurred in 56 (93%) women, and Cesarean section was performed in four women, the indications being fetal distress (n = 2), placental abruption (n = 1), and mother's own request (n = 1). In 14 patients information about Bishop score was unavailable.

Univariate analysis showed Bishop score to be lower, the cervix as measured by ultrasonography to be longer and wider, and cervical volume to be larger in women who went into spontaneous labor > 24 h than in those who went into labor earlier, whereas parity, gestational age, cervical AP diameter, the presence of funneling, funnel size and flow indices did not differ (Table 1). The same was true of women who went into labor > 48 h vs. ≤ 48 h, except that cervical width did not differ between these two groups. Bishop score was lower and the cervix was longer in women who delivered vaginally > 48 h or > 60 h than in those who delivered earlier. The only other variable that differed between these two groups was VI, which was lower in women who delivered vaginally > 60 h than in those who delivered earlier. Results with regard to delivery ≤ 60 h vs. > 60 h are shown in Table 1.

Table 1. Gestational age, parity, ultrasound results, and Bishop score for women with spontaneous onset of labor≤24 h vs. > 24 h after ultrasound examination and for women who delivered vaginally≤60 h vs. > 60 h
 Onset of labor ≤ 24 h, n = 21Onset of labor > 24 h, n = 39PDelivery ≤ 60 h, n = 34Delivery > 60 h, n = 22P
  1. AP, anteroposterior; FI, flow index; GA, gestational age; VFI, vascularization flow index; VI, vascularization index.

Parous women; n (%)9 (43)20 (51)0.53319 (56)7 (32)0.075
GA < 42 + 0 weeks at examination, n (%)8 (38)11 (28)0.43512 (35)4 (18)0.158
Three-dimensional ultrasound findings
 Cervix
  Length, median (range), mm7 (2–37)15 (2–40)0.0029 (2–40)19 (2–39)0.015
  AP diameter, mean ± SD, mm38 ± 10.137 ± 8.50.87439 ± 8.436 ± 10.30.220
  Width, mean ± SD, mm41 ± 5.244 ± 5.80.04744 ± 6.042 ± 6.00.330
  Volume, mean ± SD, cm324.2 ± 10.0933.7 ± 13.520.00527.6 ± 12.6533.7 ± 13.150.083
 Flow indices
  VI, median (range), %7.5 (0.3–23.7)4.5 (0.9–17.0)0.2687.1 (0.3–23.7)3.5 (0.9–16.4)0.050
  FI, mean ± SD29.2 ± 3.4729.3 ± 3.980.89129.3 ± 3.3729.2 ± 4.520.877
  VFI, median (range)2.0 (0.1–8.3)1.3 (0.2–5.6)0.3241.9 (0.1–8.3)1.0 (0.2–5.6)0.076
 Funnel
  n (%)12 (57)24 (62)0.74120 (59)14 (64)0.718
  Length, median (range), mm6 (1–20)8 (2–16)0.9205 (1–20)8 (2–16)0.466
  AP diameter, median (range), mm9 (5–16)9 (5–19)0.9057 (5–18)9 (5–19)0.900
  Width, mean ± SD, mm14 ± 5.015 ± 4.70.60615 ± 4.714 ± 4.50.366
 n = 18n = 28 n = 24n = 18 
Bishop score, mean ± SD5.8 ± 1.984.3 ± 1.760.0065.6 ± 1.973.8 ± 1.740.004

The results of multivariate logistic regression analyses are shown in Table 2. Areas under ROC curves for Bishop score, cervical length, and logistic regression models, and optimal cut-off values with regard to predicting onset of labor > 24 h and > 48 h, and vaginal delivery > 48 h and > 60 h, and the sensitivity, false-positive rate (1 − specificity), and positive and negative likelihood ratios for the mathematically optimal cut-off of each predicting variable are shown in Table 3. Bishop score and vascular indices did not enter any logistic regression model to predict onset of labor, only cervical length and width and parity did, the likelihood of onset of labor > 24 h increasing with increasing cervical length and width and the likelihood of onset of labor > 48 h being lower in parous women and increasing with increasing cervical length. If Bishop score was included in the logistic regression model building process it was the only variable independently related to vaginal delivery > 48 h, the likelihood of delivery > 48 h increasing with decreasing Bishop score. If Bishop score was not included in the logistic regression model, then cervical length, VI and FI independently predicted delivery > 48 h, the likelihood of delivery > 48 h increasing with increasing cervical length, decreasing VI and increasing FI. Cervical length and Bishop score were independent predictors of delivery > 60 h. The areas under the ROC curves did not differ significantly between the diagnostic tests (P = 0.14–0.92).

Table 2. Logistic regression models to predict time to onset of labor and delivery
 Maximum likelihood estimatesOdds ratio estimates
Standard estimatePEffectPoint estimate95% CI
Onset of labor > 24 h
 Model building including Bishop score (n = 46)
  Intercept−1.4140.040 
  Cervical length0.1490.008Cervical length1.1601.040–1.295
 Model building not including Bishop score (n = 60)
  Intercept−7.4090.012 
  Cervical length0.1290.004Cervical length1.1381.042–1.243
  Cervical width0.1470.020Cervical width1.1581.024–1.310
Onset of labor > 48 h
 Model building including Bishop score (n = 46)
  Intercept0.3440.749 
  Cervical length0.1070.008Cervical length1.1131.028–1.204
  Parity−1.4470.047Parity0.2350.057–0.979
 Model building not including Bishop score (n = 60)
 Intercept−1.5290.004 
 Cervical length0.0760.009Cervical length1.0791.020–1.142
Delivery > 48 h
 Model building including Bishop score (n = 42)
  Intercept3.4240.006 
  Bishop score−0.7220.003Bishop score0.4860.303–0.780
 Model building not including Bishop score (n = 56)
  Intercept−6.0190.036 
  Cervical length0.0660.037Cervical length1.0681.004–1.136
  Vascularization index (VI)−0.1540.045VI0.8570.737–0.996
  Flow index (FI)0.2030.047FI1.2251.003–1.495
Delivery > 60 h
 Model building including Bishop score (n = 42)
  Intercept0.6210.608 
  Bishop score−0.4420.033Bishop score0.6430.428–0.966
  Cervical length0.0820.048Cervical length1.0861.001–1.178
 Model building not including Bishop score (n = 56)
  Intercept−1.6380.004 
  Cervical length0.0760.011Cervical length1.0791.017–1.144
Table 3. Areas under receiver–operating characteristics (ROC) curves for Bishop score, cervical length and logistic regression models, and mathematically optimal cut-off values with regard to predicting start of labor > 24 h and > 48 h and delivery > 48 h and > 60 h, and the sensitivity, false-positive rate (1 − specificity), and positive and negative likelihood ratios for the mathematically optimal cut-off values
 Area under ROC curveOptimal False-positive 
 Estimate95% CIcut-off valueSensitivityrateLR+LR−
  • *

    The areas under the ROC curves to predict the outcome in these women do not differ significantly.

  • Larger values of the test result indicate stronger evidence for the outcome.

  • Smaller values of the test result indicate stronger evidence for the outcome. FI, flow index; LR + , positive likelihood ratio; LR−, negative likelihood ratio; VI, vascularization index.

  • 1

    Probability of onset of labor > 24 h = [ez/(1 + ez)] where z = −7.409 + (0.129 × cervical length) + (0.147 × cervical width).

  • 2

    Probability of onset of labor > 48 h = [ez/(1 + ez)] where z = 0.344 + (0.107 × cervical length)−(1.447 × parity).

  • 3

    Probability of delivery > 48 h = [ez/(1 + ez)] where z = −6.019 + (0.066 × cervical length)−(0.154 × VI) + (0.203 × FI).

  • 4

    Probability of delivery > 60 h = [ez/(1 + ez)] where z = 0.621 −(0.442 × Bishop score) + (0.082 × cervical length).

Onset of labor > 24 h 
 For women with results for Bishop score (n = 46)* 
  1st regression model10.8390.721–0.9580.560.820.174.80.21
  Cervical length0.7890.656–0.9218.5 mm0.820.332.50.27
 12.5 mm0.640.115.80.40
  Bishop score0.7240.569–0.88050.570.222.60.55
 For all women (n = 60)* 
  1st regression model10.8360.724–0.9480.560.850.194.50.19
  Cervical length0.7580.628–0.8898.5 mm0.850.382.20.25
 12.5 mm0.640.144.50.42
Onset of labor > 48 h 
 For women with Bishop score (n = 46)* 
  2nd regression model20.7880.659–0.9170.440.710.243.00.38
  Cervical length0.7830.646–0.9208.5 mm0.910.402.30.16
 12.5 mm0.710.203.60.36
  Bishop score0.7170.568–0.86750.760.362.10.37
 For all women (n = 60)* 
  2nd regression model20.7530.631–0.8750.440.720.292.50.39
  Cervical length0.7450.619–0.8718.5 mm0.920.511.90.16
Delivery > 48 h 
 For women with Bishop score (n = 42)* 
  Bishop score0.8160.682–0.95050.850.273.10.21
  3rd regression model30.8050.659–0.9500.390.850.233.70.19
  Cervical length0.7490.590–0.9088.5 mm0.900.412.20.17
 12.5 mm0.700.183.80.37
 For all women (n = 56)* 
  3rd regression model30.7840.654–0.9140.560.700.145.10.34
  Cervical length0.7360.596–0.8768.5 mm0.930.481.90.14
 12.5 mm0.740.213.60.33
Delivery > 60 h 
 For women with Bishop score (n = 42)* 
  4th regression model40.8060.668–0.9430.380.830.253.30.22
  Cervical length0.7860.643–0.9298.5 mm0.940.422.30.10
  Bishop score0.7520.602–0.90350.830.332.50.25
 For all women (n = 56) 
  Cervical length0.7480.618–0.8788.5 mm0.960.531.80.09

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Our results showed that both Bishop score and ultrasonographically-measured cervical length predicted time to spontaneous onset of labor and time to vaginal delivery in prolonged pregnancy. However, irrespective of whether Bishop score and sonographic cervical length were used as single predicting variables or as one of several predicting variables in a logistic regression model, they changed the likelihood of the outcome very little or at most to only a moderate degree17. This is in agreement with the results of studies performed in term pregnancies4,5,7. Our results also showed that VI seemed to be related to the time to vaginal delivery in prolonged pregnancy, VI being higher in women giving birth ≤ 60 h than in those giving birth later (P = 0.05). Moreover, if Bishop score was not included as a predicting variable in multivariate logistic regression analysis, then cervical length, VI and FI were independent predictors of delivery ≤ 48 h, the likelihood of delivery ≤ 48 h increasing with decreasing cervical length, increasing VI and decreasing FI. A possible interpretation of these findings is that with the progression of cervical ripening the density of small vessels in the cervix increases (increased VI reflects increased vessel density; FI should be low in small vessels, because small vessels contain few blood corpuscles, and therefore the back scattered energy should be low), supporting the theory that the cervix becomes increasingly vascularized during the cervical ripening process. To the best of our knowledge other research teams have not examined cervical vascularization in pregnancy using 3D power Doppler ultrasonography. Even though our results suggest that vascularization of the cervix is in some way related to cervical ripening, 3D power Doppler ultrasound examination of the cervix to predict time to vaginal delivery in prolonged pregnancy is probably not a very useful clinical method. It is a complex method that results in no substantial improvement in prediction when compared with use of the Bishop score alone or sonographically-measured cervical length alone.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This study was supported by the Swedish Medical Research Council (grants nos. K2001-72X-11605-06A and K2002-72X-11605-07B), two governmental grants (Landstingsfinansierad regional forskning, Region Skåne, and ALF-medel), and Funds administered by Malmö University Hospital. We express our special thanks to Dr Johan Molin, who helped us to retrieve the clinical data from KIKA-Journalen.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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