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PLOS Medicine logoLink to PLOS Medicine
. 2023 Apr 6;20(4):e1004192. doi: 10.1371/journal.pmed.1004192

Impact of point-of-care ultrasound and routine third trimester ultrasound on undiagnosed breech presentation and perinatal outcomes: An observational multicentre cohort study

Samantha Knights 1,#, Smriti Prasad 2,#, Erkan Kalafat 3,4, Anahita Dadali 2, Pam Sizer 1, Francoise Harlow 1, Asma Khalil 2,5,6,*
PMCID: PMC10079042  PMID: 37023211

Abstract

Background

Accurate knowledge of fetal presentation at term is vital for optimal antenatal and intrapartum care. The primary objective was to compare the impact of routine third trimester ultrasound or point-of-care ultrasound (POCUS) with standard antenatal care, on the incidence of overall and proportion of all term breech presentations that were undiagnosed at term, and on the related adverse perinatal outcomes.

Methods and findings

This was a retrospective multicentre cohort study where we included data from St. George’s (SGH) and Norfolk and Norwich University Hospitals (NNUH). Pregnancies were grouped according to whether they received routine third trimester scan (SGH) or POCUS (NNUH). Women with multiple pregnancy, preterm birth prior to 37 weeks, congenital abnormality, and those undergoing planned cesarean section for breech presentation were excluded. Undiagnosed breech presentation was defined as follows: (a) women presenting in labour or with ruptured membranes at term subsequently discovered to have a breech presentation; and (b) women attending for induction of labour at term found to have a breech presentation before induction. The primary outcome was the proportion of all term breech presentations that were undiagnosed. The secondary outcomes included mode of birth, gestational age at birth, birth weight, incidence of emergency cesarean section, and the following neonatal adverse outcomes: Apgar score <7 at 5 minutes, unexpected neonatal unit (NNU) admission, hypoxic ischemic encephalopathy (HIE), and perinatal mortality (including stillbirths and early neonatal deaths). We employed a Bayesian approach using informative priors from a previous similar study; updating their estimates (prior) with our own data (likelihood). The association of undiagnosed breech presentation at birth with adverse perinatal outcomes was analyzed with Bayesian log-binomial regression models. All analyses were conducted using R for Statistical Software (v.4.2.0).

Before and after the implementation of routine third trimester scan or POCUS, there were 16,777 and 7,351 births in SGH and 5,119 and 4,575 in NNUH, respectively. The rate of breech presentation in labour was consistent across all groups (3% to 4%). In the SGH cohort, the percentage of all term breech presentations that were undiagnosed was 14.2% (82/578) before (years 2016 to 2020) and 2.8% (7/251) after (year 2020 to 2021) the implementation of universal screening (p < 0.001). Similarly, in the NNUH cohort, the percentage of all term breech presentations that were undiagnosed was 16.2% (27/167) before (year 2015) and 3.5% (5/142) after (year 2020 to 2021) the implementation of universal POCUS screening (p < 0.001). Bayesian regression analysis with informative priors showed that the rate of undiagnosed breech was 71% lower after the implementation of universal ultrasound (RR, 0.29; 95% CrI 0.20, 0.38) with a posterior probability greater than 99.9%. Among the pregnancies with breech presentation, there was also a very high probability (>99.9%) of reduced rate of low Apgar score (<7) at 5 minutes by 77% (RR, 0.23; 95% CrI 0.14, 0.38). There was moderate to high probability (posterior probability: 89.5% and 85.1%, respectively) of a reduction of HIE (RR, 0.32; 95% CrI 0.0.05, 1.77) and extended perinatal mortality rates (RR, 0.21; 95% CrI 0.01, 3.00). Using informative priors, the proportion of all term breech presentations that were undiagnosed was 69% lower after the initiation of universal POCUS (RR, 0.31; 95% CrI 0.21, 0.45) with a posterior probability greater of 99.9%. There was also a very high probability (99.5%) of a reduced rate of low Apgar score (<7) at 5 minutes by 40% (RR, 0.60; 95% CrI 0.39, 0.88). We do not have reliable data on number of facility-based ultrasound scans via the standard antenatal referral pathway or external cephalic versions (ECVs) performed during the study period.

Conclusions

In our study, we observed that both a policy of routine facility-based third trimester ultrasound or POCUS are associated with a reduction in the proportion of term breech presentations that were undiagnosed, with an improvement in neonatal outcomes. The findings from our study support the policy of third trimester ultrasound scan for fetal presentation. Future studies should focus on exploring the cost-effectiveness of POCUS for fetal presentation.

Author summary

Why was this study done?

  • Accurate knowledge of fetal presentation is essential for optimal care during pregnancy and birth. Vaginal breech delivery is associated with adverse maternal and perinatal outcomes.

  • Abdominal palpation has poor sensitivity (50% to 70%) for determination of fetal presentation.

  • The role of a routine third ultrasound assessment of fetal presentation has been reported but the impact on neonatal outcomes is yet to be determined.

  • There are limited reports on antenatal use of handheld point-of-care ultrasound (POCUS) for the determination of fetal presentation, but the impact of their systematic use for this purpose is largely unknown.

What did the researchers do and find?

  • We analysed 2 cohorts of pregnant women from 2 large teaching hospitals in the United Kingdom where a policy of routine third trimester ultrasound or POCUS has been implemented.

  • We studied the impact of routine third trimester ultrasound or POCUS on the percentage of all term breech presentations that were undiagnosed and adverse neonatal outcomes, in pre- and post-screening epochs.

  • Due to the rarity of adverse outcomes, we employed Bayesian regression analysis with informative priors. This statistical tool permits updating previous findings with new data to generate new evidence.

  • We found that the incidence of all term breech presentations that were undiagnosed reduced drastically in the post-screening epoch following the implementation of either a third trimester ultrasound (decreased from 14.2% to 2.8%) or POCUS (decreased from 16.2% to 3.5%). There was an associated improvement in neonatal outcomes.

What do these findings mean?

  • Our findings imply that a policy of either a third trimester ultrasound by sonographers or POCUS by trained midwives was effective in reducing the proportion of all term breech presentations at the time of birth that were undiagnosed and associated neonatal complications.

  • Cost-effectiveness of POCUS needs to be explored further for feasibility of implementation on a wider scale for assessment of fetal presentation at term.

Introduction

The incidence of breech presentation at term is 3% to 4% [1]. Breech vaginal birth is associated with an increase in both perinatal mortality and morbidity as well as maternal morbidity [27]. Correct knowledge of fetal presentation at term is essential for providing optimum antepartum and intrapartum care. Women with breech presentation at term can be effectively counselled about their options—external cephalic version (ECV), planned vaginal birth, or elective cesarean birth—with their inherent risks and perceived benefits [1]. There is substantial evidence that clinical examination is not accurate enough for determination of fetal presentation, with unacceptably high rates of missed breech/noncephalic presentations at term [8,9].

There are 2 modalities to screen for fetal presentation at term, each with its advantages and disadvantages: routine third trimester ultrasound or point-of-care/portable ultrasound (POCUS). Currently, routine third trimester ultrasound is not recommended by the United Kingdom National Institute for Health and Care Excellence (NICE) in low-risk pregnancies due to insufficient clinical and cost-effectiveness evidence [10,11]. In the UK, the current practice is to perform an early pregnancy risk assessment followed by referral pathways for low-risk and high-risk women. These risks relate to maternal, fetal, and placental pathology but are unrelated to the risk of breech presentation at term. Women deemed to be at high risk are referred for an ultrasound scan at 28 weeks’ gestation for fetal biometry with or without additional follow-up ultrasound scans. Low-risk women are followed up with clinical assessment (serial measurement of symphysio-fundal height) and referred for third trimester ultrasound if fetal growth restriction is suspected or if it is difficult to perform clinical examination, as in women with high body mass index (BMI), multiple pregnancy, or multiple uterine fibroids, or there is clinical suspicion of noncephalic fetal presentation at term [1214]. Emerging data from observational studies and a systematic review indicate that it is feasible to accurately diagnose fetal presentation at term by third trimester ultrasound, thereby reducing the proportion of all term breech presentations that were undiagnosed at the time of labour and birth [1518]. The clinical end point of any study of the diagnosis of breech presentation at term would be an improvement in neonatal outcomes, associated with reduction in incidence of undiagnosed breech. Hitherto published literature, however, could not demonstrate a translation of increased antenatal diagnosis of breech presentation into a statistically significant improvement in neonatal outcomes, most likely owing to the rarity of adverse outcomes.

Most of the data on the use of POCUS in antenatal settings are from low-resource settings where there is inadequate access to ultrasound owing to both material and physical constraints; hence, the focus is on task-shifting of obstetric ultrasound from sonographers to primary care providers [19,20]. A recently published review reported improved diagnostic accuracy with POCUS compared to clinical examination only, for high-risk obstetric conditions including fetal malpresentation, albeit studies were heterogeneous and referred to varying standards [21]. The Society of Obstetricians and Gynaecologists of Canada identifies POCUS as a useful modality for timely determination of fetal presentation [22]. A retrospective criterion-based audit performed in one of our study hospitals demonstrated that the use of POCUS by midwives in the antenatal ward/labour ward was associated with identification of previously unrecognized breech presentation, thereby preventing inappropriate induction of labour [23]. A recent validation study of POCUS in obstetric care showed near perfect agreement for assessment of fetal presentation [95.6% agreement, Kappa −0.887, 95% CI (0.78 to 0.99)] when compared to routine ultrasound [24]. There is, however, scanty literature on the diagnostic accuracy of POCUS in antenatal care settings for assessment of fetal presentation, compared to standard antenatal care, i.e., routine abdominal palpation, with referral for ultrasound when there is clinical suspicion of breech presentation.

In our study, we aimed to compare the impact of routine third trimester ultrasound or POCUS with standard antenatal care, on the incidence of overall and proportion of all term breech presentations that were undiagnosed at term, and on the related adverse perinatal outcomes.

Methods

The study included data from St. George’s University Hospital NHS Foundation Trust (SGH) and Norfolk and Norwich University Hospital NHS Foundation Trust (NNUH). For both centres, pregnancies were grouped according to whether they received routine third trimester scan (SGH) or POCUS (NNUH).

Routine third trimester scan cohort

We included a cohort of pregnant women who gave birth between 4 April 2016 and 30 September 2021, at SGH, a large teaching hospital in South West London. The chosen starting point was the date when birth records were first systematically entered into the current electronic database. At SGH, a policy of routine third trimester (at 36 weeks) ultrasound scan by sonographers for all pregnant women has been implemented since January 2020; this includes assessment of fetal biometry, umbilical and middle cerebral artery Doppler, placental localization, amniotic fluid volume, and fetal presentation. Following a diagnosis of breech presentation during the ultrasound scan, women are counselled about their options: ECV, planned cesarean birth, or planned vaginal birth. If women declined ECV or if it was unsuccessful, they were offered elective cesarean delivery from 39 weeks of gestation. The population was divided into 2 study groups: Group 1 (women who were offered and accepted a routine third trimester scan) and Group 2 (women who received standard antenatal care in line with national guidance, without a routine third trimester scan).

POCUS cohort

The POCUS cohort included pregnant women from NNUH where a policy of routine POCUS at the 36-week antenatal visit was fully adopted from November 2020 following stage-wise implementation in 2016. The POCUS is performed by a midwife using Vscan Air (GE Healthcare). NNUH is a large teaching hospital with approximately 6,000 births per year, and approximately 250 midwives working across the hospital and community. We included 2 groups: a historical cohort of women who received routine care—abdominal palpation and referral for selective ultrasound on clinical suspicion of breech presentation (2015) and those who had POCUS at the 36- to 37-week visit (November 2020 to 2021). Through 2016 to November 2020, POCUS was variably used, either on the labour ward or via referral from community midwives, on clinical suspicion of noncephalic presentation, and these women were not included in this study.

Training of midwives for POCUS cohort

The midwives in NNUH underwent a structured 3-month training programme. The workshops consisted of daily handheld scanning sessions with an hour of dedicated lectures. The theoretical lectures were followed by practice on consenting women in the antenatal ward. All the trainee midwives maintained a competency logbook, detailing both successful and unsuccessful cases. Following the initial workshops, “midwife champions” were identified who were deemed competent or held other ultrasound qualifications and were suitable for cascade training. POCUS training was a part of preceptor ship training of newly qualified midwives, while midwives working in nonpermanent roles were supported and advised to work with one of the champions.

The primary outcome was the proportion of all term breech presentations that were undiagnosed. Undiagnosed breech presentation was defined as follows: (a) breech presentation after the onset of labour or rupture of membranes at term; and (b) breech presentation diagnosed immediately before commencing induction of labour. The secondary outcomes included mode of birth, gestational age at birth, birth weight, incidence of emergency cesarean section, and the following neonatal adverse outcomes: Apgar score <7 at 5 minutes, unexpected neonatal unit (NNU) admission, hypoxic ischemic encephalopathy (HIE) 1 to 3, and perinatal mortality (includes stillbirths and early neonatal deaths).

Women with multiple pregnancies, preterm birth <37 weeks, and congenital abnormalities were excluded. Pregnancies undergoing planned cesarean section for breech presentation were excluded from the analysis of the study outcomes, except for the neonatal outcomes. Maternal demographic characteristics, antenatal, intrapartum, and perinatal data were extracted from Euroking E3 maternity information system and Viewpoint database (ViewPoint 5.6.8.428, ViewPoint Bildverarbeitung GmbH, Weßling, Germany). Routinely collected clinical data were collated from electronic health records and were deemed not to require ethics approval or signed patient consent as per the Health Research Authority (HRA) decision tool.

Statistical analysis

Descriptive variables were compared with Wilcoxon-signed rank test, t test, or chi-squared test, where appropriate. An adequately powered analysis is not practically feasible due to rarity of adverse outcomes following breech delivery. Therefore, we employed a Bayesian approach using informative priors from a previous similar study; updating their estimates (prior) with our own data (likelihood) [18]. The association of undiagnosed breech presentation at birth with adverse perinatal outcomes was analyzed with Bayesian log-binomial regression models and reported as RR (risk ratios) with credible intervals (CrI). Informative priors (N~μ, σ) for population mean were derived from Salim and colleagues and a weakly informative prior (Student t, df = 3) for model intercept. Prior parameters were estimated by using the log-risk ratios and log-confidence intervals from Salim and colleagues, and in case an effect could not be estimated in the original study due to a no-event situation, we added a single event to the corresponding group and reestimated the risk ratios. Two Markov chains were run for 1,500 iterations after an initial 500 burn-in period. Posterior probabilities were calculated using the probability density function of normal distribution. A sensitivity analysis using flat priors (noninformative) was also undertaken to investigate the weight of informative prior on the posterior density. Number needed to treat for important outcomes was calculated using current population numbers without incorporating external data. Convergence was checked with trace plots. All analyses were conducted using R for Statistical Software (v.4.2.0) using “brms” and “its.analysis” packages [25,26]. This study is reported as per the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guideline (S1 STROBE Checklist).

Results

Study cohorts

In the SGH cohort, there were 24,128 singleton pregnancies during the eligibility period, of which 16,777 births were before the introduction of universal third trimester ultrasound scan and 7,351 after. Baseline characteristics of included pregnancies are presented in Table 1. Women who gave birth before universal ultrasound scan were significantly younger (33.2 versus 35.7 years, p < 0.001), had similar BMI (25.6 versus 25.7 kg/m2, p = 0.194) and multiparity rate (49.6% [8,316/16,777] versus 49.2% [3,617/7,351], p = 0.612) compared to those who gave birth after. There was a slight drop in the proportion of births that were in women from black, Asian, and minority ethnic (BAME) background (39.3% [6,588/16,777] versus 37.9% [2,785/7,351], p = 0.044). The index of multiple deprivation (IMD) quintiles were similar between the 2 epochs (p > 0.05 for all quintiles; Table 1), as was the total number of breech presentations at the time of birth (3.4% [578/16,777] versus 3.4% [251/7,351], p = 0.953), including all diagnosed and undiagnosed cases. A comparison of the baseline characteristics, as well as the gestational age at delivery in weeks and mode of birth of pregnancies with breech presentation at birth in the study epochs before and after the introduction of universal 36-week ultrasound scan is shown in Table 2. Pregnancies with breech presentation at term were significantly more likely to be delivered by elective cesarean section (76.9% [193/251] versus 60.7% [351/278], p < 0.001) after compared to before the implementation of the universal 36-week ultrasound scan. Emergency cesarean section was lower (17.1% [43/251] versus 30.8% [178/578], p < 0.001) after compared to before the implementation of the universal 36-week ultrasound scan. A similar trend was noted for vaginal breech delivery (Table 2). The gestational age at birth was 39.1 weeks in both groups with a mean difference of 1 day. Although the difference was statistically significant, it would be deemed clinically inconsequential.

Table 1. Baseline characteristics of pregnancies in the study epochs before and after the introduction of universal 36-week ultrasound scan.

Variables Before universal 36-week scan (n = 16,777) After universal 36-week scan (n = 7,351) P value
Maternal age in years 33.2 ± 5.18 35.7 ± 5.39 <0.001
BMI, kg/m2 25.6 ± 5.35 25.7 ± 5.36 0.194
Parous, n (%) 8,316 (49.6) 3,617 (49.2) 0.612
Ethnicity, n (%)
 Caucasian 8,014 (47.8) 3,463 (47.1) 0.353
 BAME 6,588 (39.3) 2,785 (37.9) 0.044
 Not stated 2,175 (12.9) 1,103 (15.0) <0.001
IMD quintile, n (%)
 First 1,056 (6.3) 423 (5.8) 0.114
 Second 4,323 (25.8) 1,874 (25.5) 0.665
 Third 4,989 (29.7) 2,278 (31.0) 0.052
 Fourth 3,740 (22.3) 1,664 (22.6) 0.566
 Fifth 2,626 (15.6) 1,087 (14.8) 0.090
 Missing 43 (0.3) 25 (0.3) 0.318
All breech presentations, n (%) 578 (3.4) 251 (3.4) 0.953
Gestational age at delivery in weeks 39.8 ± 1.13 39.9 ± 1.18 <0.001
Mode of birth, n (%)
 Elective cesarean 2,019 (12.0) 959 (13.0) 0.029
 Emergency cesarean 2,169 (12.9) 845 (11.5) 0.002
 Vaginal breech, any 49 (0.29) 15 (0.20) 0.276
 Vaginal vertex, spontaneous 9,606 (57.3) 4,383 (59.6) <0.001
 Vaginal vertex, operative 2,934 (17.5) 1,149 (15.6) <0.001

Comparison between the 2 groups was performed using Wilcoxon-signed rank test, t test (for continuous variables), or chi-squared test (for binary or categorical variables), where appropriate.

BAME, black, Asian, and minority ethnic; BMI, body mass index; IMD, index of multiple deprivation.

Table 2. Baseline characteristics of pregnancies with breech presentation at birth in the study epochs before and after the introduction of universal 36-week ultrasound scan.

Variable After universal 36-week scan (n = 251) Before universal 36-week scan (n = 578) P value
Maternal age in years, median (IQR) 35.0 (31.0–38.0) 37.0 (33.2–40.0) <0.001
BMI in kg/m2, median (IQR) 24.0 (22.0–28.0) 24.0 (22.0–28.0) 0.616
Parous, n (%) 93 (37.1) 209 (36.2) 0.867
Maternal ethnicity, n (%) 0.177
 Caucasian 127 (50.6) 316 (54.7)
 Black 15 (6.0) 37 (6.4)
 Asian 34 (13.5) 77 (13.3)
 Mixed 12 (4.8) 11 (1.9)
 Any other ethnic group 22 (8.8) 61 (10.6)
 Not stated 41 (16.3) 76 (13.1)
IMD 10 groups, n (%) 0.755
 (0,2] 16 (6.4) 29 (5.0)
 (2,4] 64 (25.6) 135 (23.4)
 (4,6] 78 (31.2) 178 (30.8)
 (6,8] 53 (21.2) 128 (22.2)
 (8,10] 39 (15.6) 107 (18.5)
Gestational age at delivery in weeks, median (IQR) 39.1 (38.7 to 39.5) 39.1 (38.7 to 39.9) 0.006
Mode of birth#, n (%) <0.001
 Breech extraction 2 (0.8) 13 (2.2)
 Breech, forceps to aftercoming head 2 (0.8) 4 (0.7)
 Elective cesarean section 193 (76.9) 351 (60.7)
 Emergency cesarean section 43 (17.1) 178 (30.8)
 Spontaneous breech 11 (4.4) 32 (5.5)

Comparison between the 2 groups was performed using Wilcoxon-signed rank test, t test, (for continuous variables), or chi-squared test (for binary or categorical variables), where appropriate.

#These categories are mutually exclusive.

BMI, body mass index; IMD, index of multiple deprivation.

The percentage of all term breech presentations that were undiagnosed was 14.2% (82/578) before and 2.8% (7/251) after the implementation of universal screening (p < 0.001) (Table 3). The rate of elective cesarean delivery was higher during the universal scan epoch (13.0% [959/7,351] versus 12.0% [2,019/16,777], p = 0.029), while the emergency cesarean rate was lower (12.9% [2,169/16,777] versus 11.5% [845/7,351], p = 0.029) compared to the previous epoch. The total number of vaginal breech births reduced from 29 per 10,000 births to 20 per 10,000 births, but this difference did not reach statistical significance (p = 0.276). A regression discontinuity (interrupted time series) analysis showed significant variation in the number of undiagnosed breech presentations between 2 epochs (before and after universal ultrasound, p < 0.001) (Fig 1).

Table 3. Perinatal outcomes of breech presentations in the study epochs before and after the introduction of universal 36-week ultrasound scan in St George’s Hospital.

Outcomes Before universal ultrasound scan (n = 578) After universal ultrasound scan (n = 251) RR (95% CrI), flat prior* Posterior probability of adverse event reduction RR (95% CrI), informative prior Posterior probability of adverse event reduction
Term breech presentations that were undiagnosed, n (%) 82 (14.2) 7 (2.8) 0.26 (0.10, 0.59) 99.8% 0.29 (0.20, 0.38) >99.9%
NNU admission, n (%) 11 (1.9) 3 (1.2) 0.55 (0.12, 1.98) 79.7% 0.84 (0.55, 1.28) 78.0%
HIE, n (%) 2 (0.3) 1 (0.4) 1.19 (0.10, 25.1) 44.8% 0.32 (0.05, 1.77) 89.5%
Apgar <7 at 5 minutes, n (%) 11 (1.9) 2 (0.8) 0.35 (0.06, 1.42) 89.8% 0.23 (0.14, 0.38) >99.9%
Extended perinatal mortality, n (%) 2 (0.3) 0 (0.0) NE 0.21 (0.01, 3.00) 85.1%

*Weakly informative priors (N~μ,σ) for population mean and (Student t, df = 3) model intercept.

†Informative priors (N~μ,σ) for population mean was derived from Salim and colleagues and a weakly informative prior (Student t, df = 3) for model intercept.

CrI, credible interval; HIE, hypoxic ischemic encephalopathy; NE, not estimable; NNU, neonatal unit; RR, relative risk.

Fig 1. The number of term breech presentations that were undiagnosed during the study period in St. George’s University Hospital.

Fig 1

Dotted line represents the fitted regression curve with splines.

In the NNUH cohort, there were 9,694 singleton births during the eligibility period, of which 5,119 births were before the initiation of POCUS screening and 4,575 births after the complete implementation of POCUS. Women who gave birth before POCUS were significantly older (34.6 versus 31.6 years, p < 0.001) and had a lower BMI (25.6 versus 26.5 kg/m2, p < 0.001) than those who gave birth after. The percentage of all term breech presentations that were undiagnosed was 16.2% (27/167) before and 3.5% (5/142) after the implementation of universal POCUS screening (p < 0.001) (Table 4).

Table 4. Perinatal outcomes of breech presentations in the study epochs before and after the introduction of universal POCUS at 36 weeks in in Norfolk Norwich University Hospital.

Outcomes Before universal POCUS (n = 167) After universal POCUS (n = 142) RR (95% CrI), flat prior* Posterior probability of adverse event reduction RR (95% CrI), informative prior Posterior probability of adverse event reduction
Term breech presentations that were undiagnosed, n (%) 27 (16.2) 5 (3.5) 0.20 (0.07, 0.51) 99.9% 0.31 (0.21, 0.45) >99.9%
NNU admission, n (%) 5 (3.0) 3 (2.1) 0.53 (0.11, 2.40) 78.4% 0.84 (0.54, 1.34) 77.0%
HIE, n (%) 0 (0.0) 0 (0.0) NE NE
Apgar <7 at 5 minutes, n (%) 3 (1.8) 2 (1.4) 0.72 (0.10, 4.30) 63.0% 0.60 (0.39, 0.88) 99.5%
Extended perinatal mortality, n (%) 0 (0.0) 0 (0.0) NE NE

*Weakly informative priors (N~μ, σ) for population mean and (Student t, df = 3) model intercept.

†Informative priors (N~μ, σ) for population mean was derived from Salim and colleagues and a weakly informative prior (Student t, df = 3) for model intercept.

CrI, credible interval; HIE, hypoxic ischemic encephalopathy; NE, not estimable; NNU, neonatal unit; POCUS, point-of-care ultrasound; RR, relative risk.

Perinatal outcomes

We analysed the SGH cohort using Bayesian regression analysis with both flat (noninformative) and informative priors (Using data from Salim and colleagues) [18]. Regression with informative priors showed the percentage of all term breech presentations that were undiagnosed was 71% lower after the implementation of universal ultrasound (RR, 0.29; 95% CrI 0.20, 0.38) with a posterior probability greater than 99.9% (Table 3). Among the pregnancies with breech presentation, there was also a very high probability (>99.9%) of reduced rate of low Apgar score (<7) at 5 minutes by 77% (RR, 0.23; 95% CrI 0.14, 0.38). There was moderate to high probability (posterior probability: 89.5% and 85.1%, respectively) of a reduction of HIE (RR, 0.32; 95% CrI 0.05, 1.77) and extended perinatal mortality rates (RR, 0.21; 95% CrI 0.01, 3.00). Analysis using flat priors (noninformative) also showed that the percentage of all term breech presentations that were undiagnosed was 74% lower (RR, 0.26; 95% CrI 0.10, 0.59) with very high posterior probability of 99.8%. The reduction in low Apgar scores was also observed in flat prior analysis that corresponded to a 65% reduction (RR, 0.35; 95% CrI 0.06, 1.42) with a moderate to high probability (89.8%). The number needed to scan to prevent one case of undiagnosed breech presentation was 255 (95% CI: 192 to 376).

We analysed the NNUH cohort using the same methods. Using informative priors, the proportion of all term breech presentations that were undiagnosed was 69% lower after the initiation of universal POCUS (RR, 0.31; 95% CrI 0.21, 0.45) with a posterior probability greater of 99.9% (Table 4). There was also a very high probability (99.5%) of a reduced rate of low Apgar score (<7) at 5 minutes by 40% (RR, 0.60; 95% CrI 0.39, 0.88). Flat prior analysis also showed that undiagnosed breech presentation was lower by 80% (RR, 0.20; 95% CrI: 0.07, 0.51) with very high posterior probability of 99.9%. No inference could be made for HIE or extended perinatal mortality as there were no events in either period.

Discussion

In our study, use of a policy of either routine third trimester scan or routine third trimester POCUS was associated with a significant reduction in the proportion of all breech presentations that were undiagnosed at term, when compared to standard antenatal care. Short-term adverse perinatal outcomes, including NNU admission and low Apgar scores, were significantly lower for the pregnancies with diagnosed breech presentation at term following a policy for screening by either routine third trimester scan or POCUS. Previous studies were unable to study perinatal outcomes due to their small numbers.

Our cohorts are derived from real-world data from 2 large teaching hospitals in the UK. Much of the previously reported literature on use of third trimester ultrasound for diagnosis of breech presentation is from research settings with a dedicated breech clinic and available expertise and skills for manoeuvres like ECV and vaginal breech births. Conclusions from research settings may not be generalizable to clinical settings and may be prone to bias. Furthermore, our study is the first to compare the impact of POCUS with routine antenatal care for diagnosis of fetal presentation. Routine ultrasound scan is effective at reducing the proportion of all term breech presentations that were undiagnosed, but the clinical impact of this change is hard to assess owing to the rarity of adverse outcomes [18]. We employed a Bayesian approach using both informative priors from similar studies and flat priors as a sensitivity analysis that allowed us to estimate the effect of universal ultrasound in probabilistic terms without depending on P values.

There are some limitations to our study. Firstly, we did not have reliable data on ECV for both our cohorts. The universal scan might have implications, not just for babies that were breech at birth (e.g., ECV could be performed, which could lead to not being breech and therefore not being included in the outcomes, or some other benefit, or indeed, theoretically, harm). Salim and colleagues included all babies diagnosed as breech. The method employed by Salim and colleagues also has drawbacks as it did not include those undiagnosed before the universal scan. Nevertheless, it is unlikely to have had a substantial impact on our results given the low acceptance and variable success rates. This is reflected in the almost identical incidence of overall (undiagnosed and diagnosed) breech presentation before and after screening. Salim and colleagues also reported no difference in the rates of overall breech presentations despite systematic use of ECV with acceptance rates of as high as 80% [18]. Secondly, the number of adverse neonatal outcomes such as extended perinatal mortality and HIE were not sufficient to estimate an effect in the NNUH cohort. Finally, the maternity records at NNUH were uploaded on electronic database only from April 2015. Therefore, reliable data on demographic parameters like BMI, ethnicity, and IMD were not available for the first quarter of 2015. These factors, however, are unlikely to influence the results.

Our findings of a reduction in the proportion of all term breech presentations that were undiagnosed at term after implementation of routine third trimester scan resonates with those of Salim and colleagues, who reported a reduction from 22.3% to 4.7% following the introduction of universal third trimester scan, compared to standard antenatal care [18]. Yet there are no published data from the UK on the impact of routine POCUS on the reduction of the percentage of all term breech presentations that were undiagnosed at term. Observational studies from Kenya [19], Uganda [27], and Guatemala [28] have reported that midwives who underwent focused basic obstetric ultrasound training for 3 to 8 weeks were able to identify fetal presentation with high sensitivity and specificity. The proportion of all term breech presentations that were undiagnosed at term, however, could not be eliminated in both cohorts, with 7 and 5 such cases in the routine third trimester scan and POCUS cohorts, respectively. Most of these cases were a consequence of spontaneous version to breech from cephalic presentation in multiparous women. Salim and colleagues also described spontaneous version to breech in multiparous women (76% of cases of undiagnosed breech) in their cohort. Wastlund and colleagues reported in their prospective cohort of 3,879 women that a policy of universal third trimester scan virtually eliminated undiagnosed breech presentations in labour [16]. It should, however, be noted that their cohort comprised of nulliparous women only in a strict research setting.

We also noted a significant improvement in short-term neonatal outcomes including low Apgar scores at 5 minutes and NNU admission. Salim and colleague demonstrated a nonsignificant improvement in short-term neonatal outcomes [18]. Although we were unable to demonstrate an effect on outcomes such as HIE and neonatal mortality, observational data from low-resource settings report a reduction in neonatal mortality when women were referred in a timely manner for fetal malpresentation [29].

Accurate knowledge of fetal presentation at term is crucial for optimal antenatal and intrapartum care. Both routine third trimester scan by a sonographer/clinician or use of POCUS by trained midwives can achieve this objective. Although evidence suggests that a planned breech vaginal birth may be offered after careful case selection and counselling, a large proportion of maternity units in the UK and worldwide lack skilled providers for vaginal breech births. Antenatal identification of breech presentation would allow healthcare providers to offer unbiased information such that pregnant women feel empowered to make an informed decision and have a positive birth experience. A meeting of the UK National Screening Committee (NSC) in March 2021 acknowledged that ultrasound for fetal presentation appears promising; however, the committee recommended that further work on screening for fetal presentation could not be commissioned at that time. The NSC agreed to add screening for fetal presentation to the recommendations list for reconsideration in 3 years’ time if significant evidence evolves in the interim [30]. Our findings add to that evidence base. A cost-effectiveness analysis study conducted in the UK showed that universal third trimester ultrasound would “virtually eliminate” the proportion of all term breech presentations that were undiagnosed and would be cost-effective if fetal presentation could be assessed at £19.80 pounds per woman or less [16]. A National Institute for Health Research (NIHR) Health Technology Assessment (HTA) review has suggested that handheld portable ultrasound can readily close this gap as a low-cost device that antenatal care providers like midwives could use for fetal presentation with minimal training [31]. The major obstacles to routine third trimester scan policy include the costs incurred, whereas a policy of using POCUS in community clinics and the labour ward by healthcare providers, after a short period of training, appears to be as effective as a policy of routine third trimester formal departmental ultrasound. Implementation of POCUS in the community for fetal presentation would also curtail indirect costs by reduction in referrals for facility-based ultrasound based on clinical suspicion, apart from also instilling a sense of empowerment among the care providers and satisfaction among pregnant women. The policy of POCUS was acceptable to pregnant women in our cohort who wanted to avoid nonessential hospital visits during the COVID-19 pandemic. A potential pitfall of the portable ultrasound cited when used in low-resource settings was dependence on internet coverage, which is unlikely to be a deterrent in the UK. Nonetheless, regular audits, ongoing training, and quality improvement measures should be in place to support community healthcare providers to ensure safe practice.

Our data suggest that a policy of either third trimester ultrasound or POCUS by healthcare providers could be effective in reducing the proportion of all term breech presentations that were undiagnosed at birth with an associated improvement in neonatal outcomes.

Supporting information

S1 STROBE Checklist. STROBE checklist.

(DOCX)

Abbreviations

BAME

black, Asian, and minority ethnic

BMI

body mass index

CrI

credible intervals

ECV

external cephalic version

HIE

hypoxic ischemic encephalopathy

HRA

Health Research Authority

HTA

Health Technology Assessment

IMD

index of multiple deprivation

NICE

National Institute for Health and Care Excellence

NIHR

National Institute for Health Research

NNU

neonatal unit

NNUH

Norfolk and Norwich University Hospital

NSC

National Screening Committee

POCUS

point-of-care ultrasound

RR

risk ratio

SGH

St. George’s Hospital

Data Availability

Data cannot be shared publicly because consent was not obtained from women; permission for sharing data was not sought as part of ethical approval. Data is only available following approval from Research Ethics Committee and Confidentiality Advisory Group. Enquiries and requests should be made to the the Research Governance and Delivery team at St George's University of London (sgulREC@sgul.ac.uk).

Funding Statement

The author(s) received no specific funding for this work.

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Decision Letter 0

Beryne Odeny

25 Aug 2022

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Decision Letter 1

Philippa Dodd

16 Nov 2022

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Comments from the reviewers:

Reviewer #1:

This study assesses the 'impact' of a universal third trimester ultrasound on breech presentation. It concludes, using 2 'before and after' cohorts from 2 different units introducing 2 different types of 3rd trimester scans, that undiagnosed breech presentation is significantly reduced, that the incidence of breech presentation stays the same, and that the incidence of low Apgar scores is significantly reduced.

The first two findings subsequent to a universal scan have been shown before in a single unit cohort previously published in Plos Medicine (salim et al) to which this papers refers, and from which the analysis takes 'informative priors'. The reduction in undiagnosed breech has been shown too, albeit in nulliparous women in research setting, also published in this journal (Wastlund et al) (also cited in this paper). The reduction in Apgar scores was not 'significant' in the Salim study, but with this, it is. That this is so when more data is used should not be considered a surprise: antenatal diagnosis allows more caesarean sections (I note overall numbers not changed but no analysis is specifically presented on cs rates for breech babies- see point below) for breech babies: caesarean sections for breech improve short term outcomes and, according to the term breech trial and huge cohorts from the Netherlands, death.

The methodology requires scrutiny by a statistical reviewer and I am not one. This means that I do not fully understand- and apologise for this- how, for instance, despite my point above, the paper concludes that 5 min Apgar scores <7 are reduced, when using a simple chi-squared test amalgamating numbers from Salim et al and from this paper I calculate a chi-square statistic of 2.2251; p= 0.14: i.e. still 'not significant' in lay terms.

Although I have outlined that antenatal diagnosis will have benefits, the abstract suggests to the uninitiated reader like me that the paper actually demonstrates a reduction in HIE: 'There was moderate to high probability (posterior probability: 89.5% and 85.1%, respectively) of a reduction of hypoxic ischemic encephalopathy (HIE) (RR: 0.23, 95% CI: 0.14-0.38)… '. Yet this is not the case, the numbers simply being inadequate for this: table 2 shows just 2 before and 1 after the scan was introduced. Without fully understanding the methodology this seems disingenuous.

Another issue with this paper is the loss of the 'real world' (what happens in a unit when…) benefits to an impact/ 'changes subsequent to' paper. This is because of there being 2 different units, the intervention was slightly different (proper scan and presentation scan) and ECV was not documented/ discussed. This means it potentially has less relevance for a 'unit' and is more of a 'poor man's' (person's) RCT.

I remain surprised at all the research into a universal 'presentation only' scan. I think we know the answer- most breeches become diagnosed. This affects only about 5% of the population. Given the (accepted) benefits of elective caesarean for breech babies have probably been exaggerated (RCOG Greentop Guideline 2017) the overall effect on pregnancy safety is going to be small. And of course performing caesarean sections on all breech babies leads to a loss of skills and therefore probably increased risk for the small (in this study and that of Salim et al) but persistent breeches that still slip through. I make this comment because this pertains to the relevance of this- and other studies such as Salim et al- for overall pregnancy safety; in contrast, a 'proper' scan that could affect the other 95% as well is the one that needs the research attention.

I would like to see data on how many third trimester scans were actually performed- before and after.

No table data on gestation at birth or mode of birth is presented for the babies who were actually breech.

The lack of ECV data is acknowledged as a limitation but inadequately so. The Salim study they quote was not a 'research setting' and its data and discussion of ECV was comprehensive. This lack also causes the problem below:

By looking at outcomes in breech babies only at birth (this is not 100% clear at least in the table) an assumption is being made that the universal scan could not alter outcomes for other babies. It could- not just for babies that were breech at birth (eg ECV could be performed which could lead to not being breech and therefore not being included in the outcomes, or some other benefit, or indeed, theoretically, harm). Salim et al 'get around' this by including all babies diagnosed as breech. The method employed by Salim et al has drawbacks too (it did not include those undiagnosed before the universal scan), but the method used here should at least be justified and discussed as a limitation.

The pretty Figs 1 and 2 add little useful information bar perhaps demonstrating causality better re undiagnosed breech presentation- but this should be obvious by now.

In spite of my largely minor reservations, if this stands up to statistical review, this paper cleverly demonstrates one of the benefits to spreading the use of ultrasound in pregnancy.

Reviewer #2: This was a clinically meaningful study, well-written and generally easy to follow. The conclusions are clear and compelling. The role of midwives in delivering POCUS is especially unique and helpful given the potential for this model to be introduced more widely in clinical settings globally. The use of probabilities in the results is confusing to follow, the risk reduction is much easier to understand clinically, however these results are presented in the context of the analysis conducted.

The only suggested changes relate to the interpretation of findings. In the Discussion, I think it is important to clearly mention a) the role of mode of birth in the risk of neonatal adverse outcomes (ie what proportion of women with breech babies proceeded to CS and thus what was the impact of MOB on outcomes, if any, assuming that CS eliminates most of the breech-related risks of vaginal breech birth) and b) the role of parity or the proportion of multiparous women in each group.

Reviewer #3: 1. Line 120-122. "For both centers, pregnancies were grouped according to whether they received routine third-trimester scan (SGH) or POCUS (MNUH)." For the analysis, did the author include all the pregnancies or just include those received routine third-trimester scan at SGH or PROCUS at MNUH?

2. What's the reason for only including SGH cohort was in Table 1/Figure 1 ? How about the NNUH cohort?

3. As the log-binomial regression is used to analyze the association between undiagnosed breach presentation at birth and adverse perinatal outcomes, should the outcome be OR (odds ratio) rather than RR (relative risk?)

Reviewer #4: Thanks for allowing me to review your very interesting manuscript. I agree that the data presented show an impressive reduction in the chance of an undiagnosed breech presentation at term after both routine ultrasound screening and POCUS, carried out in two different hospitals. It would, of course, be a more rigorous study design to compare routine antenatal care with both routine ultrasound and POCUS in the same setting, or to have randomised rather than use a before and after design, but based on your data both methods appear to reduce the percentage of breech presentations that are undiagnosed at the start of labour or membrane rupture. I have a few minor points to make which could lead to some minor revisions:

1. I found the phrase 'the rate of undiagnosed breech' a bit confusing as it suggested to me that, for example, 14.2% of babies were presenting in labour as undiagnosed breeches. It might be better to say the 'percentage of all term breech presentations that were undiagnosed was 14.2%.....'

2. The statement that there was no significant change in the rate of vaginal breech birth (and the figures are given of 10 per 10,000, which was reducing to 5 per 10,000 after the scanning interventions) is somewhat surprising given the very significant change (reduction) in the percentage of undiagnosed breech presentations. Are you able to explain that?

3. These data would suggest to me that prior to the intervention most breech babies were born by c/section, so it is then a little hard to understand how such an improvement in perinatal outcome has been achieved. I realise that the outcome data were secondary outcomes but the paper seems to argue that there is a high rate of morbidity/mortality associated with vaginal breech birth, yet the improvement in perinatal outcomes has occurred without much change in the rate. Indeed, given the numbers quoted the numbers of term vaginal births at SGH during the study period would have reduced from about 17 in the pre-ultrasound period to 4 after. To have seen a measurable reduction in the rate of low Apgar scores and rates of HIE would be remarkable, and would imply that outcomes for vaginal breeches were very poor in the pre-ultrasound period. Can you comment further on this?

3. A minor point is that data is a plural noun and is sometimes used as a singular one (e.g. page 172)

4. Finally, I was left uncertain as to whether or not you would advocate a policy of routine ultrasound or POCUS or a hybrid of the two depending on risk? Or do you have plans to compare the two approaches in the same setting?

Any attachments provided with reviews can be seen via the following link:

[LINK]

Decision Letter 2

Philippa Dodd

19 Jan 2023

Dear Dr. Khalil,

Thank you very much for re-submitting your manuscript "Impact of Point of Care Ultrasound and routine third trimester ultrasound on undiagnosed breech presentation and perinatal outcomes: a retrospective study" (PMEDICINE-D-22-02818R2) for review by PLOS Medicine.

I have discussed the paper with my colleagues and the academic editor and it was also seen again by 4 reviewers. I am pleased to say that provided the remaining editorial and production issues are dealt with we are planning to accept the paper for publication in the journal.

The remaining issues that need to be addressed are listed at the end of this email. Any accompanying reviewer attachments can be seen via the link below. Please take these into account before resubmitting your manuscript:

[LINK]

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If you have any questions in the meantime, please contact me or the journal staff on plosmedicine@plos.org.  

We look forward to receiving the revised manuscript by Jan 26 2023 11:59PM.   

Sincerely,

Philippa Dodd, MBBS MRCP PhD

PLOS Medicine

plosmedicine.org

------------------------------------------------------------

Requests from Editors:

GENERAL

Thank you for your detailed and considerate responses to previous editor and reviewer comments. Please see below for further comments that we require you respond to in full.

TITLE

Thank you for revising your title suggest “Impact of Point of Care Ultrasound and routine third trimester ultrasound on undiagnosed breech presentation and perinatal outcomes: an observational multi-centre cohort study” or something similar

ABSTRACT

Thank you for revising your abstract and for including p-values as well as 95% CIs. For each outcome measure reported we request that both p-values and 95% CIs are reported. If not please clearly state the reasons why not, for purposes of transparent data reporting (please remember that when reporting p-values to report as p<0.001 or where higher the exact p-value as p= 0.002, for example).

Suggest reporting as follows – for example, line 59 - (RR: 59 0.29, 95% CI [0.20–0.38], p<0.001) for optimal reader accessibility.

Please note the use of parentheses around the CIs and the absence of the semi-colon. You may wish to consider separating upper and lower limits with commas rather than hyphens (as these can be confused with negative values) but we leave it to your discretion.

Please check and revise throughout, including in the main manuscript text and tables where relevant – please see below also

AUTHOR SUMMARY

Thank you for including an author summary which reads very nicely.

Line 100: we appreciate the explanation of your chosen methodological approach, suggest revising to ensure that the statement is interpretable to the more general reader – some may be unfamiliar with the concept of informative priors, for example

Line 103: “incidence of percentage…” suggest removing of percentage perhaps?

Line 104: suggest quantifying “drastically (a percentage will be adequate here)

Line 113: It would be helpful to elaborate on the reasons why assessing cost-effectiveness is necessary – i.e. for feasibility of implementation on a wider scale

METHODS and RESULTS

Please revise statistical reporting as suggested above

please quantify all reported percentages with numerators and denominators, for example line 271, “(12.9 vs 11.5%, p=0.029)” - please check and amend throughout

Please also report CIs where p-values are reported, if not please clearly state why not, for purposes of transparent data reporting

TABLES

Currently journal requirements stipulate that where 95% CIs are presented, including in tables, that p-values are also reported. Please include p-values but if not in your rebuttal letter, please clearly state the reasons why not, for transparency of data reporting

Table 3.a – suggest removing the SGH cohort row – perhaps a remnant of the previous version

DISCUSSION

Please remove the sub-heading conclusion.

Line 404: given the observational nature of the study suggest tempering the language here slightly, “Our data suggest that a policy….could be effective in…” or something similar, for example

SOCIAL MEDIA

To help us extend the reach of your research, please provide any Twitter handle(s) that would be appropriate to tag, including your own, your co-authors’, your institution, funder, or lab. Please include these in the manuscript submission form when you re-submit your manuscript

Comments from Reviewers:

Reviewer #1: the authors have addressed all points satisfactorily

Reviewer #2: Thank you for your thorough attempts to rectify requested changes. The manuscript has been satisfactorily updated and improved.

Reviewer #3: I appreciate authors' effors in addressing the questions and revising the paper. I have no further comments.

Reviewer #4: Thanks for responding to my previous comments and to those of other reviewers. I have three relatively minor additional points to make about your revised manuscript;

1. Line 50 (Abstract). Can you confirm that the statement 'the rate of breech presentation in labour was consistent across all groups (3-4%)' is correct and does this refer to all births? It seems very high if the usual exclusions of preterm, multiples, congenital anomalies are applied.

2. Line 116 (Introduction). Similarly, is this figure of 3-4% used in the Introduction inclusive of all births, and does it exclude multiple pregnancies?

3. Line 175. I would think that 'Southwest London' is usually written as 'South West London' but as I am not a resident of London I am happy to be corrected.

Any attachments provided with reviews can be seen via the following link:

[LINK]

Decision Letter 3

Philippa Dodd

7 Feb 2023

Dear Dr Khalil, 

On behalf of my colleagues and the Academic Editor, Dr. Anthea C Lindquist, I am pleased to inform you that we have agreed to publish your manuscript "Impact of Point of Care Ultrasound and routine third trimester ultrasound on undiagnosed breech presentation and perinatal outcomes: an observational multi-centre cohort study" (PMEDICINE-D-22-02818R3) in PLOS Medicine.

Prior to publication, on advice of the Academic Editor, whose comments are also included below, we require that you make the following final revisions:

This is an important study with direct clinical impact and will be of great interest to maternity clinicians globally.

The suggested revisions have generally been very appropriately addressed or appropriately rebutted. There are a few remaining issues to address:

Line 103 - wording doesn't make sense, needs to be clarified

Line 222 - 'excluding' should be 'excluded'

Line 226 - 'was' should be 'were' in keeping with the plural nature of data

Line 270-271 - reads as though the GA was the same (39.1 weeks) between groups but still significantly different - needs to be clarified, how can this differ?

Table 2 - mode of birth - needs to include in legend if all 3 breech vaginal birth categories (breech extraction, breech with forceps and spontaneous breech) were mutually exclusive or not? The same babies could all feasibly be included in all groups.

Line 317-318 - 'term' is used twice, only one is necessary

Line 328 - should read 'the first'

Line 331 - should read 'the rarity'

Line 349 - 'was not' should read 'were not' owing to plural data

Line 359-360 - 'term' is used twice, only needed once

Line 371 - remove 'the' from 'the neonatal'

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. Please be aware that it may take several days for you to receive this email; during this time no action is required by you. Once you have received these formatting requests, please note that your manuscript will not be scheduled for publication until you have made the required changes.

In the meantime, please log into Editorial Manager at http://www.editorialmanager.com/pmedicine/, click the "Update My Information" link at the top of the page, and update your user information to ensure an efficient production process. 

PRESS

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To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option to publish peer-reviewed clinical study protocols. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

Thank you again for submitting to PLOS Medicine, it has been a pleasure handling your manuscript. We look forward to publishing your paper. 

Best wishes, 

Pippa

Philippa Dodd, MBBS MRCP PhD 

PLOS Medicine

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 STROBE Checklist. STROBE checklist.

    (DOCX)

    Attachment

    Submitted filename: PLOS medicine reviewers Asma 27.12.2022.docx

    Attachment

    Submitted filename: PLoS reviewers comments 21.01.2023 Asma.docx

    Data Availability Statement

    Data cannot be shared publicly because consent was not obtained from women; permission for sharing data was not sought as part of ethical approval. Data is only available following approval from Research Ethics Committee and Confidentiality Advisory Group. Enquiries and requests should be made to the the Research Governance and Delivery team at St George's University of London (sgulREC@sgul.ac.uk).


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