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Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology and

Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

2 Simplified Bishop score including parity predicts successful

3 induction of labor
4 Q1 Joanna Ivars a, Charles Garabedian a,*, Patrick Devos b, Denis Therby c,
5 Sabine Carlier c, Philippe Deruelle a,d, Damien Subtil a,b
6 a
Jeanne de Flandre Hospital, Department of Obstetrics, 59045 Lille, France
7 b
EA 2694, UDSL, Univ Lille North of France, CHU Lille, 59045 Lille, France
8 c
Paul Gellé Hospital, Department of Obstetrics, 91 avenue Lagache, Centre Hospitalier, 59100 Roubaix, France
9 d
EA 4489, Univ Lille North of France, 59045 Lille, France

A R T I C L E I N F O A B S T R A C T

Article history: Objective: Our objectives were to confirm the predictiveness of parity for successful labor induction and
Received 4 March 2016 propose an improvement in the Bishop’s score to take parity into account and simultaneously simplify
Received in revised form 9 June 2016 the original Bishop score.
Accepted 11 June 2016
Study design: Retrospective study of 326 deliveries induced by oxytocin and amniotomy before
prostaglandins between January 1, 1987, and June 30, 1988. We conducted a univariate and then a
Keywords: multivariate analysis of the relation between successful labor induction – defined by vaginal delivery-
Labor induction
and the components of Bishop’s score and parity.
Bishop’s score
Parity
Results: Nulliparous accounted for 38% of the studied population. The mean Bishop at induction was
Simplified Bishop’s score 5.75  1.4. Fetal station, cervical effacement, and parity were the only factors associated with the success of
induction in this study. Removing the cervical position and consistency from the score as well as adding
parity significantly improved the prediction of success (ROC curves, AUC 0.88 vs 0.68, p < 0.001). By taking 5%
as the maximum risk of induction failure, a cutoff point of 4 for the new score makes it possible to induce
labor in 90% of the women that were considered in the study (vs 26% or 60%, according to whether the cutoff
point of the original Bishop’s score is set, respectively, at 7 or 6, p < 0.001).
Conclusion: Cervical position and consistency are not necessary for predicting successful labor induction
by oxytocin and amniotomy. We confirmed the usefulness of a simplified Bishop score that considers
parity.
ß 2016 Elsevier Ireland Ltd. All rights reserved.

10
11 Introduction Bishop’s score has the advantage of being universally known. 22
The cutoff point at which delivery can be induced without 23
12 Q2 In countries with high levels of perinatal health, labor is increasing the risk of cesarean delivery is generally 7 or 6, but this 24
13 induced for approximately 20% of women [1,2]. As widely known, varies from one country to another depending on different local 25
14 the induction of labor by oxytocin and amniotomy increases the guidelines [6–8]. However, that point is rarely reached in reality. 26
15 risk of cesarean delivery when the cervix is not sufficiently ripened What’s more, Bishop’s score does not include parity, even though 27
16 [3]. Numerous scores have been developed to predict the this variable is known for being closely associated with the 28
17 likelihood of a successful delivery after induction [4]; the most induction success [4,9–13]. Last, several authors have shown that 29
18 commonly used is the one described in 1964 by Bishop et al. [5]. some components of Bishop’s score have a low prognostic value for 30
19 This score assesses cervical ripeness using five components: the success or the failure of the induction [14]; this has led some 31
20 cervical length, consistency, position, and dilatation as well as individuals to propose simplified scores [15]. 32
21 station (of the presenting fetal part). These points all suggest that it might be useful to study a 33
version of Bishop’s score without some of the components and 34
which takes parity into account. Such a study would require a 35
series of patients induced with oxytocin and for whom each 36
* Corresponding author at: Hôpital Jeanne de Flandre, Université Lille Nord de component of Bishop’s score was measured before induction. 37
France, 1 rue Eugène Avinée, 59037 Lille Cedex, France. Tel.: +33 3 20 44 66 26; Unfortunately, it has been difficult to conduct this type of study for 38
fax: +33 3 20 44 61 11.
E-mail address: charles.garabedian@chru-lille.fr (C. Garabedian).
more than 20 years from now, mainly because an induction by 39

http://dx.doi.org/10.1016/j.ejogrb.2016.06.007
0301-2115/ß 2016 Elsevier Ireland Ltd. All rights reserved.

Please cite this article in press as: Ivars J, et al. Simplified Bishop score including parity predicts successful induction of labor. Eur J
Obstet Gynecol (2016), http://dx.doi.org/10.1016/j.ejogrb.2016.06.007
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Fig. 1. Components of the Bishop score and scores studied in this analysis.

40 oxytocin and amniotomy is so often preceded by a cervical parity, gestational age, epidural analgesia, the duration of labor, 85
41 ripening by prostaglandins when the cervix is unfavorable. This the mode of delivery, and the baby’s weight and condition at birth. 86
42 modifies the assessment of the cervical status and of the results Nulliparous was defined as none previous birth. 87
43 interpretation. The aim of the analysis was to study the role of parity and the 88
44 By reviewing some local records, we found a series of patients different components of Bishop’s score in the success of induction, 89
45 whose cervical status was assessed before a labor induction by and to establish – if possible – a more accurate predictive score 90
46 oxytocin and amniotomy and before prostaglandins were widely than the standard Bishop’s score [5]. This analysis was performed 91
47 used. We conducted a retrospective study to confirm the role of in five stages. First, we examined the relation between the 92
48 parity in the success of inductions by oxytocin and amniotomy. We components of Bishop’s score—to which we added parity—and the 93
49 were aiming at proposing an improvement of Bishop’s score that success of the induction. At that stage, the percentages were 94
50 would take into account simultaneously the parity and the compared with the Chi-2 or Fisher’s exact test, whenever 95
51 simplifications that were previously proposed in the literature. applicable. In the second stage, the variables that were significant- 96
ly associated with the success of the induction in the univariate 97
52 Materials and methods analysis (p < 0.20) were introduced by a forward stepwise 98
procedure into a logistic regression model. Given that the selection 99
53 This retrospective study analyzes the women who gave birth of the variables depended on the sample, we used a bootstrap 100
54 after a labor induction by oxytocin and amniotomy (in the event of resampling procedure in the third stage to obtain a stable selection 101
55 intact membranes) between January 1, 1987, and June 30, 1988 of variables. This procedure was artificially performed amongst 102
56 (date of the beginning of prostaglandin usage), in a university 500 samples of the same size—326 patients—drawn from the initial 103
57 hospital maternity ward. population. The indicators that were selected in over 70% of the 104
58 The case files were included in this study if they involved samples were retained in the construction of the new model [16]. 105
59 singleton pregnancies in cephalic presentation, with no uterine In the fourth stage, we compared the new model to the different 106
60 scar and no prenatal detection of a fetal malformation. Labor existing scores. We established the ROC (receiving operating 107
61 induction was considered for these pregnant women after 37 characteristics) curves, calculated their areas under the curve 108
62 weeks of gestation, either in the event of a maternal or fetal (AUC), and compared them [17]. In the fifth and final stage, we 109
63 disease, or because the patient had requested it. The induction arbitrarily agreed to use as the best cutoff point for each score the 110
64 must have been performed exclusively by the combination of one that provided the highest proportion of women for whom it 111
65 oxytocin in the absence of active labor (and not used for speeding was possible to induce labor with a maximum risk of failure of 112
66 up labor and amniotomy in case of intact membranes. The level of induction arbitrarily set at 5% (positive predictive value 113
67 oxytocin was progressively increased every 20 min if necessary (PPV)  95%). Each of these percentages was compared by a Chi- 114
68 and the amniotomy was done as soon as possible. 2 test for matched series. 115
69 The cervical assessment was noted according to the five usual The statistical analyses (comparisons of percentages, logistic 116
70 criteria used to describe Bishop’s score (Fig. 1). The indications for regression) were performed with SAS software V9.2 (SAS Institute 117
71 an induction were noted in the obstetric records and were Inc., Cary, NC). The ROC curves were performed with SPSS software 118
72 classified in four categories: prolonged pregnancy, premature (SPSS 13.0 for Windows, Inc., Chicago, IL). The different AUCs were 119
73 rupture of the membranes, maternal-fetal disease (mainly compared with MedCalc software v11.6.1, using the DeLong test 120
74 pregnancy-related hypertension, preeclampsia, and uncontrolled [18] (MedCalcSoftware, Broekstraat 52, 9030 Mariakerke, 121
75 diabetes, may they be pregnancy-related or predating the Belgium). Significance was set at 0.05. 122
76 pregnancy, or meconium on amnioscopy) or an induction Ethical approval was granted by the French Ethics Committee of 123
77 requested by the mother. research in Obstetrics and Gynecology (CEROG OBS 2015-11-08). 124
78 The success of the induction was arbitrarily defined as a vaginal
79 delivery, regardless of the duration of labor and of whether the Results 125
80 vaginal delivery was spontaneous or operative (instrumental). A
81 cesarean delivery during labor was considered as a failure of Between January 1, 1987, and June 30, 1988, the hospital had 126
82 induction, regardless of its indication. A cesarean for dystocia was 3861 deliveries, of which 368 (9.5%) happened after inducing labor 127
83 defined as a 3-h cervical stagnation. The other maternal and (Fig. 2). We excluded 42 deliveries from the analysis: 24 because 128
84 neonatal indicators considered in this study were the woman’s age, the data was incomplete (6.5%), 16 because they were induced 129

Please cite this article in press as: Ivars J, et al. Simplified Bishop score including parity predicts successful induction of labor. Eur J
Obstet Gynecol (2016), http://dx.doi.org/10.1016/j.ejogrb.2016.06.007
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Table 1
Description of the study population.

N = 326

Gestational age at induction (weeks, range) 39.9  1.4 [37–42+6]

No previous deliveries 125 (38.3)
Maternal age 27.4  1.4 [15.9–44.2]
Indication for induction
Prolonged pregnancy 74 (22.7)
Premature rupture of the membranes 68 (20.9)
Other maternal or fetal problem 106 (32.5)
Maternal request 78 (23.9)
Initial Bishop score 5.75  1.4 [1–9]
Epidural analgesia 288 (88.3)
Cesarean = failure of induction 31 (9.5)
For cervical dystocia 24
For fetal distress or other reason 7
Vaginal delivery = success of induction 295 (90.5)
Including instrumental vaginal delivery 63 (19.3)
Birth weight (g) 3370  520 [1800–4840]
Fig. 2. Flow chart of the population of the study. 5-min Apgar score < 7 6 (1.8)

The percentages are indicated between parentheses. We report the means with
their standard deviations and the percentages in square brackets.
130 before a gestational age of 37 weeks (4.3%), and 2 because of fetal
131 malformations (0.5%). As a result, we were able to study 326
132 women’s records. chances for success, with parity as the most often associated to 155
133 Nulliparas accounted for 38% of our study population. Three success factor (in 92% of samples) (Fig. 3). 156
134 quarters of the inductions were for medical reasons, mainly due to Given the stability of the association between a successful 157
135 a prolonged pregnancy or the rupture of membranes at term. The induction on one hand, and fetal station, cervical effacement, and 158
136 rate of epidural analgesia reached 88%, and the cesarean rate was at parity. On the other hand, we arbitrarily created a new score that 159
137 9.5%. In 19.3% of the cases, a forceps or vacuum extraction was we called a simplified Bishop’s score including parity, which 160
138 needed at the time of the delivery. Six children (1.8%) had 5-min includes the three mentioned indicators (plus cervical dilatation, 161
139 Apgar scores < 7, but all of them were healthy at discharge. for reasons explained in the discussion) (Fig. 1). We compared it 162
140 Overall, 295 deliveries (90.5%) met our definition of a successful with three other scores: the original Bishop’s score [5], the 163
141 induction (Table 1). simplified Bishop’s score described by Laughon et al. [15], and the 164
142 In the univariate analysis, the components of Bishop’s score original Bishop’s score to which we added parity (Fig. 1). Parity was 165
143 associated with a successful induction were fetal station (p = 0.03) taken into account in the score by adding two points for all patients 166
144 and cervical effacement (p = 0.02) (Table 2). Parity appeared to be who already had at least one vaginal delivery after 22 weeks. 167
145 closely associated to a successful induction, since primiparous and Fig. 3 and Table 4 present the study of the predictive value of 168
146 multiparous women had a significantly higher chance of success these four scores. Each of the two scores including parity had an 169
147 than nulliparas (97.0 vs 80.0%, p < 0.001). AUC close to 0.85 (Fig. 4), significantly higher than the other two, 170
148 After introducing dilatation, effacement, station, and parity into for which the AUC was close to 0.69 (p < 0.001). Equally, by 171
149 a forward stepwise logistic regression models (p < 0.2), three of choosing a cutoff point corresponding to a maximum failure 172
150 these were significantly associated with a successful induction (cesarean) rate of 5% (PPV  95%), the scores including parity had 173
151 (Table 3): fetal station, cervical effacement, and parity. Cervical the highest sums of sensitivity + specificity (Table 4). For the 174
152 dilatation was not associated with a successful induction in our simplified Bishop’s score that included parity, the highest 175
153 multivariate analysis (p > 0.05). Bootstrap resampling confirmed percentage of patients that could receive an induction with a 176
154 the stability of the correlation between these factors and the maximum risk of failure arbitrarily set at 5% (PPV  95%) was 90%. 177

Table 2
Success of induction according to Bishop score components and parity.

Number Success (%) p

Cervical consistency Firm 45/51 88.2 0.46

Intermediate 131/147 89.1
Soft 119/128 92.9
Cervical position Posterior 89/102 87.3 0.39
Median 192/209 91.9
Anterior 14/15 93.3
Cervical dilatation 0 cm 1/2 50.0 0.17
1–2 cm 283/313 90.4
3–4 cm 11/11 100
>5 cm 0 –
Fetal station (head) (relative to ischial spines) 3 cm 29/36 80.6 0.03
2 cm 190/211 90.5
1, 0 cm 76/79 96.2
2, 3 cm 0 –
Cervical effacement 0–30% 13/18 72.2 0.02
40–50% 109/123 88.6
60–70% 138/149 92.6
80% 35/36 97.2
Parity Nulliparas 100/125 80.0 <0.001
Primi- or multiparous 195/201 97.0

Please cite this article in press as: Ivars J, et al. Simplified Bishop score including parity predicts successful induction of labor. Eur J
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Table 3
Forward stepwise logistic regression of the probability of successful induction
according to the components of the Bishop score and parity.

OR 95% CI% p

Fetal station (relative to ischial spines) <0.001

3 cm 1 (ref)
2 cm 6.5 [1.7–24.4]
1, 0 cm 24.5 [4.2–143.3]
Cervical effacement <0.001
0–30% 1 (ref)
40–50% 3.3 [0.8–14.7]
60–70% 11.8 [2.4–57.2]
>80% 65.2 [4.2–143.3]
Parity <0.001
Nulliparous 1 (ref)
Primi- or multiparous 35.6 [9.9–128.1]

Only the components associated with successful induction in the univariate Fig. 3. Bootstrapping methods: percentage of samples in which the factor studied
analysis were tested (p < 0.20): effacement, fetal station, and parity. The factors was significantly associated with successful induction after resampling (only the
appear in the order of the forward logistic regression. factors for which a percentage of samples is greater than or equal to 70.0% are
retained).

178 Discussion of its frame [17], although in reality these two different methods 207
produced identical results within our data (data not shown). 208
179 In this study, we showed that parity is significantly associated We showed that parity was the most important factor in 209
180 with the success of labor induction and that cervical consistency predicting successful induction. It is unlikely that this result is 210
181 and position are not on the other hand. We then showed that by biased by the sample selection, since the logistic regression 211
182 simplifying Bishop’s score and by adding parity to it, we could confirmed the association in 92.2% of the bootstrap resampling. 212
183 improve the score’s performance by increasing the number of Our results are coherent with many other studies that indicate that 213
184 patients whose labor could be successfully induced by oxytocin previous delivery—at least primiparity—is associated with a 214
185 and amniotomy without increasing the risk of cesarean delivery. successful induction [4,9,10]. However, parity is not part of either 215
186 The cesarean rate was at 9.3% in our study, quite low compared the original Bishop’s score or of most of the scores published since 216
187 to the current average rate of 21% in France [19]. On the one hand, then [15,23]. Moreover, Bishop’s score was initially developed 217
188 the cesarean rate in France was also much lower at the moment of from a patients’ population that excluded nulliparous women [5]. 218
189 the study; on the other hand, this percentage of 9.3% was the The only authors that have taken parity into account in their scores 219
190 cesarean rate observed in cases of induction, a rate that is generally are Hughey et al. [24], and then Dhall et al. [25], who proposed 220
191 lower than the overall cesarean rate. It ranges in other series from adding four points to Bishop’s score for primiparous or multiparous 221
192 10 to 15%. In 1999, Yeast et al. [20] reported a 12% cesarean rate for women and applying only three cervical criteria (effacement, 222
193 labor induction in the state of Missouri, and in 2004, Goffinet et al. consistency, and dilatation). This change increased sensitivity from 223
194 [21] recorded a 13.2% rate in France, when the national rate was 86 to 88% but most importantly improved specificity from 47 to 224
195 clearly higher in each country during the same period. 90%. However, neither scores has been widely used in practice, 225
196 For each of the scores we compared, we chose a cutoff point that probably because each of them ended up being more complex than 226
197 theoretically enabled induction of the largest possible number of the original Bishop’s score. 227
198 women with a positive predictive value of 95% or more, which is a With regards to the predictive role of the factors that are 228
199 maximum risk of cesarean delivery set at 5%. The definition that generally included in Bishop’s score, the various studies that have 229
200 was found most frequently in the literature for the failure of labor been conducted until now are quite heterogeneous in terms of the 230
201 induction is a cesarean delivery [9,15]. In addition, the arbitrary population they consider—nulliparas [26], non-nulliparas[27], or 231
202 maximum risk set at 5% that we selected appears acceptable in mixed [9]—and by their definition of a successful induction: entry 232
203 relation to the risk of cesarean during spontaneous labor, which in active labor [28], or vaginal delivery within a time period that 233
204 Seyb et al. [22] assessed at 7.8%. We preferred to choose this may have been defined in advance [11]. The results of these studies 234
205 clinical cutoff point rather than the theoretical threshold that are divergent, but dilatation is often the factor most closely 235
206 minimized the distance of the ROC curve from the upper left angle associated with success [11,15,23,29,30]. The failure of cervical 236

Table 4
Q3 Predictive value of the five scores studied with a maximum risk of failure of 5% (PPV  95%).

Range AUCa Cut off for Se Sp PPV  95%b NPV Se + Sp % of patients for whom labor can be induced at
PPV  95%b the cut off point indicated in the third column

Bishop 0–13 0.697 7 0.28 0.93 0.97 0.12 1.21 26%d,§

6e 0.63 0.67 0.94e 0.16 1.30 60%d,§
6 nulli, 5 multi 0.78 0.68 0.96 0.25 1.46 73%d,§
Simplified Bishopc 0–9 0.684 5 0.26 0.97 0.99 0.12 1.23 24%d,§
-T
Bishop + parity 0–15 0.844 6 0.87 0.58 0.95 0.32 1.45 83%d,
Simplified Bishopc + parity 0–11 0.880 4 0.95 0.52 0.95 0.50 1.47 90%d
a
See Fig. 2.
b
PPV equal to or greater than 95% indicates a risk of cesarean less than 5%.
c
simplified Bishop = dilatation, station, effacement.
d
the percentage of patients for whom labor can be induced was compared between the simplified Bishop score including parity and the other scores, at the cutoff points
indicated in column 3. The comparison used a Chi-2 test for matched series. All the differences were statistically significant (§p < 0.001; – T p < 0.01).
e
The use of the Bishop score with a cutoff point  6 is associated with a risk of failure > 5%. It is nonetheless presented here for comparison with the other scores, as it is
31,32
widely used.

Please cite this article in press as: Ivars J, et al. Simplified Bishop score including parity predicts successful induction of labor. Eur J
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Fig. 4. ROC curves. Respective course of the sensitivity and specificity of each score studied for predicting the success of induction (n = 326).

237 dilatation to predict success in our study may be explained by the The main limitations of this study are linked to information loss 276
238 fact that this criterion could not be discriminant in our sample and recruitment bias inherent to retrospective studies. Our study is 277
239 because 96% of the women had a dilatation of 1–2 cm. As a result, it based on data from before prostaglandins were available, more 278
240 remains possible that dilatation may be a factor closely associated than 20 years ago, therefore from a time when practices were 279
241 with the success of induction in a population of patients more different from today. It still has the advantage of analyzing a 280
242 heterogeneous than ours [15]. We also want to highlight the fact population of women whose components of Bishop’s score were 281
243 that no other study that attempted to simplify Bishop’s score assessed before labor, without preliminary cervical ripening; it has 282
244 removed dilatation from their consideration [11,15,23]. On the since then become almost impossible to find such a population. 283
245 other hand, the fact that the cervical position and consistency did Today, the recourse to cervical ripening has almost become 284
246 not predict the success of the induction is consistent with most of standard routine for women with low Bishop’s scores; it may lead 285
247 the studies preceding ours [11,15,23]. In general, one relevant as a result to biasing the study of the correlation between the 286
248 problem of Bishop’s score is the fact that its subjectivity limits the score’s components and the induction success. Last, cesarean 287
249 ability to report results in a semi-quantitative scoring system. sections for fetal distress or other reasons were included amongst 288
250 Recent efforts to quantify some parameters of the score seem to failed labor induction and could be considered as a limitation, even 289
251 have slightly improved the diagnosis accuracy [31]. In particular, though the relatively low incidence of cesarean section probably 290
252 transvaginal ultrasounds allowed the measurement of cervical minimizes the influence of that bias. 291
253 length and tried to evaluate the cervical position by measuring the
254 cervical angle [32]. It is possible that digital palpation can Conclusion 292
255 adequately assess the cervical length, but not the cervical position.
256 Otherwise, it is also possible that these parameters actually do not Cervical position and consistency are not necessary in predict- 293
257 really improve the score. In regards to cervical consistency, there ing the success of a labor induction by oxytocin and amniotomy. 294
258 are recent elastographic findings that suggest that cervical stiffness We confirmed the usefulness of a simplified Bishop’s score that 295
259 can play a predominant role in the prediction of labor induction considers parity. 296
260 success [33]. Considering cervical dilatation, probably one factor
261 influencing the results is that the great majority of patients had a Conflict of interest 297
262 cervical dilatation of 1–2 cm.
263 The singularity of our study is to have combined the None. 298
264 simplification of Bishop’s score with the introduction of parity,
265 and to have showed that the most useful score was a simplified
Acknowledgments 299
266 Bishop’s score [15] combined with parity. This score is simple and
267 is the same for nulli-, primi-, and multiparas; 90% of the women in
We thank the entire maternity ward staff at the Roubaix 300
268 our study had a score equal to or greater than 4, with an induction
Hospital Center, which helped us perform this study. We want to 301
269 failure rate of 5%. Like Laughon et al. [15], we think that simplifying
particularly thank Monsieur Marc FRANCKZUK and Professor Denis 302
270 Bishop’s score is therefore both possible and generalizable. Its
QUERLEU for the advice they gave us at the beginning of this work. 303
271 simple dissemination amongst our team suggests that it is easy to
272 use, but its acceptability requires further assessments. Most of all,
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Please cite this article in press as: Ivars J, et al. Simplified Bishop score including parity predicts successful induction of labor. Eur J
Obstet Gynecol (2016), http://dx.doi.org/10.1016/j.ejogrb.2016.06.007