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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 33  |  Issue : 4  |  Page : 1286-1292

Angle of progression in women undergoing trial of labor after cesarean section in predicting mode of delivery


1 Department of Obstetrics and Gynecology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Obstetrics, Berket El-Sabaa Hospital, Menoufia, Egypt

Date of Submission25-Jun-2020
Date of Decision21-Jul-2020
Date of Acceptance28-Jul-2020
Date of Web Publication24-Dec-2020

Correspondence Address:
Saly S Abd-Elbaset
MBCH, Berket El-Sabaa, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_203_20

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  Abstract 


Objective
To assess the ability of ultrasonic measurement of angle of progression (AOP) in predicting mode of delivery in women undergoing vaginal birth after cesarean section (CS).
Background
The intrapartum ultrasound measurement of AOP is reliable regardless of the fetal head station assessed manually or the clinician's level of ultrasound experience.
Patients and methods
A prospective observational study was conducted from March 2019 to January 2020 at Menoufia University Hospital, including 100 patients with a history of previous one CS in spontaneous labor. Patients were followed up, and AOP was measured in them using transperineal ultrasound. Patients were divided into two groups according to mode of delivery as follows: group 1, delivered by CS, and group 2, delivered by normal vaginal delivery (NVD).
Results
The mean AOP was decreased in CS group (98.20 ± 15.83) than NVD group (112.21 ± 12.66). Additionally, at cutoff point of AOP less than 95 (86°), area under curve was 0.511 (95% confidence interval: 0.264–0.758; P = 0.024), with sensitivity of 71.4%, specificity of 85.5%, and accuracy 81.5%. However, at cutoff point of AOP more than 95 (113°), area under curve was 0.545 (95% confidence interval: 0.412–0.679; P = 0.016), with sensitivity of 85.7%, specificity of 69.4%, and accuracy 93.25%.
Conclusions
The AOP was significantly decreased in CS group than NVD group. The results prove a vital role for using this angle as a simple and accurate landmark to evaluate station of fetal head and provide a useful predictor for mode of delivery, particularly in patients with planned vaginal birth after cesarean delivery (VBAC).

Keywords: angle of progression, mode of delivery, predicting, transperineal ultrasound


How to cite this article:
Hossny NM, Shabana AA, Abd-Elbaset SS, Fathey AA. Angle of progression in women undergoing trial of labor after cesarean section in predicting mode of delivery. Menoufia Med J 2020;33:1286-92

How to cite this URL:
Hossny NM, Shabana AA, Abd-Elbaset SS, Fathey AA. Angle of progression in women undergoing trial of labor after cesarean section in predicting mode of delivery. Menoufia Med J [serial online] 2020 [cited 2024 Mar 29];33:1286-92. Available from: http://www.mmj.eg.net/text.asp?2020/33/4/1286/304493




  Introduction Top


Cesarean section (CS) delivery is a major surgical operation aimed at saving lives[1]. Globally, the proportion of sections, one of the most common surgeries, continues to rise, particularly in high-income and middle-income countries[1]. CSs should be performed when vaginal delivery poses a risk to the mother or the baby as in case of prolonged labor, fetal distress, or fetal malpresentation. The WHO underscores the importance of focusing on the needs of the pregnant mothers and discourages performing CSs with no need. Cesarean delivery without a medical need places mothers and their babies at risk of short-term and long-term health consequences[2]. It is associated with increased risk of blood transfusion, hysterectomy, maternal and neonatal death, uterine rupture, placenta previa, and placenta accreta. It also costs more and requires longer hospitalization than vaginal delivery[2].

Recent studies have shown that ultrasound imaging might allow dynamic and objective quantification of the level of fetal head descent in the birth canal. Various sonographic modalities have been employed for intrapartum determination of fetal head engagement. One of these modalities is the 'angle of progression' (AOP) of the fetal head, described as the angle between a line through the midline of the pubic symphysis and a line from the inferior apex of the symphysis to the leading part of the fetal skull[3]. Evaluation of this angle showed a good intraobsever and interobserver variability for the measurement that was less than 3°. Some authors concluded that the intrapartum ultrasound measurement of the AOP is reliable regardless of the fetal head station or the clinician's level of ultrasound experience. Intrapartum ultrasound imaging might allow the dynamic assessment of the progress of labor with prognostic potential and provides a more scientific basis for assessing labor[4].

There is a significant relationship between the measures of this angle and the success of vaginal delivery, whether assisted or spontaneous. If the angle was more than or equal to 120°, there was a 90% chance of having vaginal delivery. It has been used to predict successful instrumental vaginal delivery in fetuses with occipitoanterior position[5]. The measurement of this angle depends on fixed parameters, so the variability of this new ultrasound method was very low, and it can provide more objective assessment of the fetal head station at which a ventouse or forceps can be safely applied[6].

This study focused on the assessment of the ability of ultrasonic measurement of the AOP in predicting mode of delivery in women undergoing vaginal birth after CS.


  Patients and methods Top


A prospective observational study was conducted from March 2019 to January 2020 at Menoufia University Hospital including 100 patients with a history of previous one CS in spontaneous labor. Patients were followed up, and AOP was measured in them using transperineal ultrasound. Cases were divided into two groups according to mode of delivery as follows: group 1, delivered by CS, and group 2, delivered by normal vaginal delivery (NVD).

Ethical consideration

The study was approved by the ethical committee of Menoufia Faculty of Medicine, and an informed consent was obtained from all patients before the study was commenced.

The sample size was calculated using PASS 11.0 and based on a study carried out by El-Garhy et al.[7] who mentioned that an AOP more than or equal to 95° has a sensitivity of 85% and a specificity of 89%. A total sample size of 100 achieves 82% power to detect a change in sensitivity from 0.5 to 0.85 using a two-sided binomial test and 100% power to detect a change in specificity from 0.5 to 0.89 using a two-sided binomial test. The target significance level is 0.05. The actual significance level achieved by the sensitivity test is 0.0352 and achieved by the specificity test is 0.0295.

Selection criteria for the patients

The patients included in this study were selected according to inclusion and exclusion criteria.

Inclusion criteria

Women with a single prior CS presenting in their next pregnancy with a single, live fetus in vertex presentation, who have reached 37 weeks of gestation or more (37–40 ± 6), who did not have a contraindication to a planned VBAC and who were in active phase of labor (>3 cm cervical dilatation) were enrolled in the study.

Exclusion criteria

A prior high vertical (classical) uterine incision; an unknown type of prior uterine incision; a prior uterine rupture; certain types of prior uterine surgeries, such as fibroid removal; and multiple pregnancy; any contraindication to vaginal birth (including placenta previa, transverse lie, and active genital herpes infection); cephalopelvic disproportion as judged by the clinician; fetal anomalies associated with mechanical difficulties at birth (such as fetal hydrops, fetal ascites, hydrocephalus, omphalocele, or cystic hygroma) were the exclusion criteria. The inclusion/exclusion criteria are based on guidelines recommended by the Society of Obstetricians and Gynecologists of Canada, American College of Obstetrics and Gynecology, the Institute for Clinical Systems Improvement, and the National Institute for Clinical Effectiveness, UK.

All cases were subjected to the following:

History taking: it included personal history, with emphasis on patient's name, age, parity, and gestational age (weeks); present history, of the current pregnancy to fulfill the inclusion and exclusion criteria; obstetric history, with emphasis on number of prior pregnancies, deliveries, abortions, history of previous preterm labor, mode of delivery, CS numbers, and its details; and past history, including medical and surgical history, and family history.

General examination: it included vital signs, head and neck examination, chest and heart examination, limb examination, and systematic examination. All women were assessed by the physician on duty, including cardiotocography and vaginal digital examination, and when they were found in active labor, the study was done.

Gestational age: it was determined according to the last menstrual period if this had been confirmed by first trimester ultrasound examination, or by ultrasound alone if the sonographic determination of gestational age differed from the menstrual dating by more than 1 week.

Imaging by using ultrasonographic examination: the ultrasound assessment was performed by an experienced operator. The examination was conducted with IBE (Providian Medical Equipment LLC, Highland Heights, Ohio, USA) Sonata plus ultrasound systems equipped with a 3–5 MHz transabdominal two-dimensional convex transducer. Transperineal ultrasound was performed to measure the angle between the long axis of the symphysis pubis and a line extending from its most inferior edge tangentially to the fetal skull.

Technique: the use of the correct technique is essential. All women we assessed by the physician on duty. When they were found in active labor, the study was explained to them, and a written informed consent was obtained. All ultrasound assessments were performed with women in modified lithotomy position in absence of maternal pushing and uterine contractions. The ultrasound assessment was done as follows: the convex probe was enclosed in a latex glove covered with ultrasound gel and then placed between the labia below the symphysis pubis. The sagittal view, in which the long axis of the symphysis pubis could be ascertained, was obtained by gently rocking the transducer upward. While in this same plane, the leading portion of the fetal head could easily be discerned. On the sagittal view, a line was drawn on the screen between calipers placed at the two points identifying the long axis of the symphysis pubis. A second caliper line then was created on the frozen image that extends from the most inferior portion of the symphysis pubis tangentially to the fetal skull contour. The angle between the constructed lines was measured manually.

Assessment: the labor process of women included in this study was managed by the labor and delivery team, which was blinded to the AOP measurements. If multiple ultrasound examinations were performed in a woman, we included only the last examination.

Statistical analysis

Results were tabulated and statistically analyzed by using a personal computer using Microsoft Excel 2016 and SPSS version 21 (SPSS Inc., Chicago, Illinois, USA). Statistical analysis was done using descriptive statistics, for example, percentage (%), mean, and SD, and analytical statistics, which included t test, Fisher exact test, Mann–Whitney test, and receiver operating characteristic curve. A value of P less than 0.05 was considered statistically significant.


  Results Top


In the current study, there was no statistically significant difference between CS and NVD groups regarding patient age (P = 0.821), BMI (P = 0.058), and gestational age (P = 0.25). However, there was a statically significant difference between the studied groups regarding parity (P = 0.035). Patients with a history of previous one CS and no NVD before were more frequent among CS group (60%), whereas patients with a history of previous one CS and NVD before were more frequent among NVD group (71.77%). There was no statistically significant difference between CS and NVD groups regarding head station (P = 0.67), head circumference (P = 0.37), and fetal weight (P = 0.29). Moreover, occipitoanterior position was the most common position among CS and NVD groups, represented by 53.34 and 90.59%, respectively [Table 1]. There was a statistically significant difference between CS and NVD groups regarding the rate of cervical dilatation and effacement (P = 0.012 and P < 0.001). The mean rate of cervical dilatation and effacement of CS group (0.78 ± 0.16 and 58.67 ± 15.52, respectively) was lower than NVD group (1.2 ± 0.5 and 88.24 ± 8.33, respectively). In addition, there was a statistically highly significant difference between CS and NVD groups regarding condition of amniotic membrane on admission (P < 0.001). Most of the CS group (86.67%) had ruptured amniotic membrane. Conversely, most of the NVD group (70.59%) had intact amniotic membrane. There was a statistically significant difference between CS and NVD groups regarding angle of progression (P = 0.005). The mean AOP was decreased in CS group (98.20 ± 15.83) than NVD group (112.21 ± 12.66) [Table 2]. Results in the current study show that at a cutoff point of progression angle less than 95 (86), area under curve (AUC) was 0.511 [95% confidence interval (CI): 0.264–0.758; P = 0.024], with sensitivity of 71.4% and specificity of 85.5%, with accuracy 81.5%. However, at a cutoff point of progression angle more than 95 (113), AUC was 0.545 (95% CI: 0.412–0.679; P = 0.016), with sensitivity of 85.7%, specificity of 69.4%, and accuracy 93.25%., with P value less than 0.05, which indicates a statistically significant difference between both groups [Table 3] and [Figure 1]. There was no statistically significant difference between CS and NVD groups regarding fetal and maternal complications and Apgar score at 1 min (P > 0.05) [Table 4]. [Figure 2] (a) shows women delivered by CS (angle 89), (b) women delivered NVD (angle 118), (c) women delivered NVD (angle 102), (d) women delivered by CS (angle 87), (e) women delivered NVD (angle 120), (f) women delivered by CS (angle 93) [Figure 2].
Table 1: Comparison between cesarean section and normal vaginal delivery groups regarding patient age, BMI, gestational age, parity, head station, head circumference, fetal weight, and head position

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Table 2: Comparison between cesarean section and normal vaginal delivery groups regarding rate of cervical dilatation, effacement, condition of amniotic membrane on admission, and angle of progression

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Table 3: Determination of cutoff value of progression angle with sensitivity, specificity, and accuracy

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Figure 1: ROC curve of the accuracy of the angle of progression in the prediction of spontaneous vaginal delivery. ROC, receiver operating characteristic.

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Table 4: Comparison between cesarean section and normal vaginal delivery groups regarding fetal and maternal complications and Apgar score at 1 mi

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Figure 2: (a) Women delivered by CS (angle 89), (b) women delivered NVD (angle118), (c) women delivered NVD (angle 102), (d) women delivered by CS (angle 87), (e) women delivered NVD (angle120), and (f) women delivered by CS (angle 93). CS, cesarean section; NVD, normal vaginal delivery.

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  Discussion Top


The current study shows that there was a statistically significant difference between CS and NVD groups regarding AOP (P = 0.005). The mean AOP was decreased in CS group (98.20 ± 15.83) than NVD group (112.21 ± 12.66). These results were confirmed by several studies. El-Garhy et al.[7] found that women who delivered vaginally showed a statistically significant higher mean of the AOP than those delivered through CS (104.88 ± 7.10° vs. 86.58 ± 11.212°, respectively), with a P value less than 0.0001, which indicates a very high statistical significance between the AOP measurement in cases with NVD versus those who delivered by Kalache et al.[8] reported that measuring the AOP could assist in the obstetrician's decision to attempt a vaginal delivery or CS. An AOP of 120° in an occiput anterior fetal position was associated with a 90% probability of successful vaginal delivery. Shabana et al.[9] found that women who delivered vaginally showed a statistically significant higher mean of AOP of 98.68 ± 6.27 versus 87.04 ± 6.62 for those who delivered by means of CS (P < 0.0001), which indicates a very high statistical significance between the AOP measurement in cases with NVD versus those who delivered by means of Farhan[10] assessed the value of AOP measurement by transperineal ultrasound in the prediction of the outcome of induction of labor at term, whether vaginal or CS. There were significant correlations between AOP and induction-to-delivery interval and the mode of delivery. AOP was significantly wider in those who delivered vaginally than women delivered by CS. Ciaciura-Jarno et al.[11] found that the arithmetic mean for the AOP is 142.5° (the median 139.5°) in the group where patients delivered naturally and 113.4° in the group where a CS was performed (the median 113°). A prospective study conducted by Pereira et al.[12] found that the median AOP in degree was 89.1 (77.6–98.0) in vaginal delivery and 88.1 (77.4–92.7) in CS, and the differences between them did not reach significant level (P = 0.387).

In the current study, at cutoff point of progression angle less than 95 (86), AUC was 0.511 (95% CI: 0.264–0.758; P = 0.024), with sensitivity of 71.4% and specificity of 85.5%, with accuracy 81.5%. However, at cutoff point of progression angle more than 95 (113), AUC was 0.545 (95% CI: 0.412–0.679; P = 0.016), with sensitivity of 85.7%, specificity of 69.4%, and accuracy 93.25%, with P value less than 0.05 which indicates a statistical significance between both groups. In other study by Hinkson et al.[13], assessment of the angle before onset of labor was done, and it found that 95° as a cutoff value can predict delivery mode because it has the best diagnostic performance. It has been shown that an AOP more than or equal to 95° was associated with 98.7% chance of delivering vaginally in primigravida women. Moreover, Torkildsen et al.[14] defined an AOP of 110° as a cutoff value to predict vaginal delivery, which occurred in 87% of patients. These figures are greater than the dynamic cutoff values of the current work (95). In addition, Shabana et al.[9] found that at a cutoff angle of 93.5°, AOP correctly identified cases planned to deliver vaginally with a sensitivity of about 83.6% and a specificity of 88.9%, which was in range to our results. El-Garhy et al.[7] found that the first group with angle measurement less than 92.5 was comparable to the second group with angle more than 93.5. The first group included 21 women with AOP measurement less than 92.5°, where two (9.5%) cases had NVD, whereas the rest 19 (90%) cases were delivered by CS. However, in the second group with angle more than 93.5°, 74 (93.7%) cases were delivered with vaginal delivery and only five (6.3%) cases were delivered by CS. AOP correctly identified cases planned to deliver vaginally, with a sensitivity of ~97.4% and a specificity of 79.2%, with P value of 0.0001, which indicates a very high statistical significance between both groups. These differences may be the cause of lower cutoff point of the AOP (93.7°) compared with the 95° of our study. However, Eggebo et al.[15] found that AOP more than120° is found to be the best cutoff for successful instrumental vaginal delivery in the second stage of labor. In their study, they found that angle less than 110° was a good predictor of prolonged first stage of labor. Similar to our result, Levy et al.[16] appraised AOP in term pregnant women before onset of labor and concluded that a narrow angle (<95°) in nonlaboring nulliparous women at term is associated with a high rate of cesarean delivery, and an angle more than or equal to 95° was associated with vaginal delivery in 98.7% of nulliparous women. In particular, AOP provides an accurate means for assessing descent of the fetal head during labor. AOP measurement is highly reproducible regardless of the fetal head station or ultrasound expertise, as reported by Molina et al.[17]. In addition, AOP width has a good correlation with labor outcome and may lead to better management in women with prolonged or obstructed labor, as reported by Eggebo et al. [15]. Most importantly, as AOP is a strong predictor of complicated or failed instrumental delivery, its assessment may lead to better decision making before vacuum or forceps delivery, as reported by Sainz et al.[18] and Bultez et al. [19]. Our study showed that there was a statistically highly significant difference between CS and NVD groups regarding condition of membrane on admission (P < 0.001). Most of the CS group (86.67%) had membrane ruptured. Conversely, most of the NVD group (70.59%) had membrane intact.

Our results showed that there was no statistically significant difference between CS and NVD groups regarding fetal and maternal complications and Apgar score at 1 min (P > 0.05). Recently, Ramphul et al.[20] randomized 514 nulliparous women who were at more than or equal to 37 weeks of gestation with a singleton cephalic pregnancy to receive clinical assessment or both an ultrasound scan and clinical assessment before instrumental delivery. The incidence of incorrect diagnosis was significantly lower in the ultrasound group than the standard care group (1.6 vs. 20.2%; P < 0.001). However, the incidence of maternal and neonatal complications, failed instrumental delivery, and cesarean delivery did not differ significantly between the two groups. These results are also in agreement with our findings when the analysis was restricted to instrumental vaginal deliveries.

Finally, our study showed that there is a very important relationship between AOP and mode of delivery. According to this angle, we can choose patients with history of previous one CS who can take the chance of being delivered vaginally after CS with limited risk of complications, especially rupture uterus.


  Conclusion Top


In conclusion, the AOP was significantly decreased in CS group than the NVD group. The results prove a vital role for using this angle as a simple and accurate landmark to evaluate station of fetal head and provide a good predictor of the mode of delivery, particularly in patients with planned VBAC. Moreover, we recommend training programs for obstetricians with little ultrasound experience to measure the AOP with accuracy that can help in decision making regarding the mode of delivery.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
World Health Organization. Statement on caesarean section rates. Available from: http://apps.who.int/iris/bitstream/10665/161442/1/WHO_RHR_15.02_eng.pdf). [Last accessed on 2020 Jan].  Back to cited text no. 1
    
2.
Al Rifai RH. Trend of caesarean deliveries in Egypt and its associated factors: evidence from national surveys, 2005–2014. BMC Pregnancy Childbirth 2017; 17:417.  Back to cited text no. 2
    
3.
Betrán AP, Torloni MR, Zhang JJ, Gülmezoglu AM, WHO Working Group on Caesarean Section, Aleem HA, et al. WHO statement on caesarean section rates. BJOG 2016; 123:667–670.  Back to cited text no. 3
    
4.
Wiafe YA. The reliability, practicality and acceptability of using ultrasonography to monitor the progress of labour and delivery [doctoral dissertation] 2018.  Back to cited text no. 4
    
5.
Chan WW, Chaemsaithong P, Lim WT, Ada WT, Kwan AH, Leung TY, et al. Pre-induction transperineal ultrasound assessment for the prediction of labor outcome. Fetal Diagn Ther 2019; 45:256–267.  Back to cited text no. 5
    
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Bibbo C, Rouse CE, Cantonwine DE, Little SE, McElrath TF Robinson JN. Angle of progression on ultrasound in the second stage of labor and spontaneous vaginal delivery. Am J Perinatol 2018; 35:413–420.  Back to cited text no. 6
    
7.
El-Garhy ET, Mohammed AH, Abd-El-Motaal AO, Esmail MN. Prediction of delivery mode in pregnant women using angle of progression before onset of labour. Nat Sci 2012; 16:1–4.  Back to cited text no. 7
    
8.
Kalache KD, Dückelmann AM, Michaelis SA, Lange J, Cichon G, Dudenhausen JW. Transperineal ultrasound imaging in prolonged second stage of labor with occipitoanterior presenting fetuses: how well does the 'angle of progression predict the mode of delivery?. Ultrasound Obstetr Gynecol 2009; 33:326–330.  Back to cited text no. 8
    
9.
Shabana AA, Saleh SA, Soliman AA, Hamza HA, Nassar SM. Angle of progression in pregnant women before onset of labor in predicting the mode of delivery. Menoufia Med J 2018; 31:63–67.  Back to cited text no. 9
    
10.
Farhan FS. Prediction of the mode of delivery in women subjected to induction of labour by measurement of angle of progression. Mustansiriya Med J 2016; 15:5–10.  Back to cited text no. 10
    
11.
Ciaciura-Jarno M, Cnota W, Wójtowicz D, Niesluchowska-Hoxha A, Ruci A, Kierach R, et al. Evaluation of selected ultrasonography parameters in the second stage of labor in prediction mode of delivery. Ginekol Pol 2016; 87:448–453.  Back to cited text no. 11
    
12.
Pereira S, Frick AP, Poon LC, Zamprakou A, Nicolaides KH. Successful induction of labour: prediction by preinduction cervical length, angle of progression and cervical elastography. Ultrasound Obstet Gynecol 2014; 44:468–475.  Back to cited text no. 12
    
13.
Hinkson L, Araujo Júnior E, Moron AF. Ultrasound during the second stage of labour: is it effective to reduce the caesarean section rates. Rev Brasil Ginecol Obstetr 2015; 37:249–251.  Back to cited text no. 13
    
14.
Torkildsen EA, Salvesen KA, Eggebo TM. Prediction of delivery mode with transperineal ultrasound in women with prolonged first stage of labour. Ultrasound Obstet Gynecol 2011; 37:702–708.  Back to cited text no. 14
    
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Eggebo TM, Hassan WA, Salvesen KA, Lindtjorn E, Lees CC. Sonographic prediction of vaginal delivery in prolonged Labour: a two-center study. Ultrasound Obstet Gynecol 2014; 43:195–201.  Back to cited text no. 15
    
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Levy R, Zaks S, Ben-Arie A, Perlman S, Hagay Z, Vaisbuch E. Can angle of progression in pregnant women before onset of labour predict mode of delivery?. Ultrasound Obstet Gynecol 2012; 40:332–337.  Back to cited text no. 16
    
17.
Molina FS, Terra R, Carrillo MP, Puertas A, Nicolaides KH. What is the most reliable ultrasound parameter for assessment of fetal head descent?. Ultrasound Obstet Gynecol 2010; 36:493–499.  Back to cited text no. 17
    
18.
Sainz JA, Borrero C, Aquise A, Serrano R, Gutierrez L, Fernandez-Palacin A. Utility of intrapartum transperineal ultrasound to predict cases of failure in vacuum extraction attempt and need of caesarean section to complete delivery. J Matern Fetal Neonatal Med 2016; 29:1348–1352.  Back to cited text no. 18
    
19.
Bultez T, Quibel T, Bouhanna P, Popowski T, Resche-Rigon M, Rozenberg P. Angle of fetal head progression measured using transperineal ultrasound as a predictive factor of vacuum extraction failure. Ultrasound Obstet Gynecol 2016; 48:86–91.  Back to cited text no. 19
    
20.
Ramphul M, Ooi PV, Burke G, Kennelly MM, Said SA, Montgomery AA, et al. Instrumental delivery and ultrasound: a multicenter randomized controlled trial of ultrasound assessment of the fetal head position versus standard care as an approach to prevent morbidity at instrumental delivery. BJOG 2014; 121:1029–1038.  Back to cited text no. 20
    


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