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The impact of a routine late third trimester growth scan on the incidence, diagnosis, and management of breech presentation in Oxfordshire, UK: A cohort study
Ibtisam salim, eleonora staines-urias, sam mathewlynn, lior drukker, manu vatish, lawrence impey.
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The authors have declared that no competing interests exist.
* E-mail: [email protected]
Received 2020 Jan 23; Accepted 2020 Dec 16; Collection date 2021 Jan.
This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Breech presentation at term contributes significantly to cesarean section (CS) rates worldwide. External cephalic version (ECV) is a safe procedure that reduces term breech presentation and associated CS. A principal barrier to ECV is failure to diagnose breech presentation. Failure to diagnose breech presentation also leads to emergency CS or unplanned vaginal breech birth. Recent evidence suggests that undiagnosed breech might be eliminated using a third trimester scan. Our aim was to evaluate the impact of introducing a routine 36-week scan on the incidence of breech presentation and of undiagnosed breech presentation.
Methods and findings
We carried out a population-based cohort study of pregnant women in a single unit covering Oxfordshire, United Kingdom. All women delivering between 37+0 and 42+6 weeks gestational age, with a singleton, nonanomalous fetus over a 4-year period (01 October 2014 to 30 September 2018) were included. The mean maternal age was 31 years, mean BMI 26, 44% were nulliparous, and 21% were of non-white ethnicity. Comparisons between the 2 years before and after introduction of routine 36-week scan were made for 2 primary outcomes of (1) the incidence of breech presentation and (2) undiagnosed breech presentation. Secondary outcomes related to ECV, mode of birth, and perinatal outcomes. Relative risks (RRs) with 95% confidence intervals (CIs) are reported. A total of 27,825 pregnancies were analysed (14,444 before and 13,381 after). A scan after 35+0 weeks was performed in 5,578 (38.6%) before, and 13,251 (99.0%) after ( p < 0.001). The incidence of breech presentation at birth did not change significantly (2.6% and 2.7%) (RR 1.02; 95% CI 0.89, 1.18; p = 0.76). The rate of undiagnosed breech before labour reduced, from 22.3% to 4.7% (RR 0.21; 95% CI 0.12, 0.36; p < 0.001). Vaginal breech birth rates fell from 10.3% to 5.3% (RR 0.51; 95% CI 0.30, 0.87; p = 0.01); nonsignificant increases in elective CS rates and decreases in emergency CS rates for breech babies were seen. Neonatal outcomes were not significantly altered. Study limitations include insufficient numbers to detect serious adverse outcomes, that we cannot exclude secular changes over time which may have influenced our results, and that these findings are most applicable where a comprehensive ECV service exists.
Conclusions
In this study, a universal 36-week scan policy was associated with a reduction in the incidence but not elimination of undiagnosed term breech presentation. There was no reduction in the incidence of breech presentation at birth, despite a comprehensive ECV service.
Ibtisam Salim and co-workers report on incidence of breech presentation in pregnant women receiving a 36-week scan.
Author summary
Why was this study done.
The risk of complications at birth are higher in babies that are presenting breech, which is therefore a common reason for planning a cesarean section. In about a third, however, breech presentation is not discovered until labour. This leads to unanticipated cesarean birth or vaginal breech birth.
Recent data suggest that ultrasound screening in nulliparous women could virtually eliminate undiagnosed breech presentation but did not assess the effect in multiparous women who comprise more than 50% of all births.
Given that known breech presentation can often be corrected before birth, improved antenatal detection through screening could also lead to a lower incidence of term breech presentation, but this has never been tested.
What did the researchers do and find?
This study assessed breech outcomes of 278,250 term births before and after the introduction of a third trimester screening ultrasound, which increased the proportion of pregnancies screened from 39% to 99%.
The incidence of undiagnosed breech presentation fell substantially but 1 in 20 breech babies at term were still not diagnosed until labour.
The incidence of breech presentation at term did not reduce, albeit from an already low incidence.
What do these findings mean?
Introducing a third trimester screening scan into a maternity service is unlikely to prevent the occasional need for skills at breech birth, which themselves require experience.
That the incidence of term breech presentation did not decline with screening limits the latter’s usefulness, but where services for correction of breech presentation require and receive improvement, an effect might be anticipated.
Improvements in neonatal outcomes should not be assumed because of reduced expertise in management of those that still present as undiagnosed breech and with women exercising maternal preference.
Introduction
Breech presentation has an incidence at term of 3% to 4% and is more common among preterm births [ 1 ]. Vaginal breech birth has been associated with higher neonatal morbidity and mortality than cesarean (CS) [ 2 ] or cephalic birth. In an attempt to reduce birth-related complications, most breech babies are delivered by CS and thus breech babies make a substantial contribution to CS rates in developed countries [ 3 ]. Undergoing CS leads to both short- and long-term maternal complications [ 4 ] and may even be associated with long-term health consequences like obesity and diabetes for the newborn [ 4 – 6 ]. CS is costly and has financial implications for healthcare providers, which can be influenced by whether the procedure is elective or as an emergency [ 7 ].
If diagnosed antenatally, term breech presentation can often be corrected using external cephalic version (ECV) where the fetus is manipulated through the abdominal wall to a cephalic presentation. This is successful in nearly 50% of attempts; reversion to breech is rare and leads to a reduction in breech presentation at term [ 8 ]. The procedure is considered safe [ 8 – 10 ]. Those in whom ECV is declined, fails, or is contraindicated can be appropriately counselled regarding birth.
While antenatal assessment of presentation is a cornerstone of antenatal care, approximately one-third of breech babies are not diagnosed antenatally [ 11 ]. The sensitivity of clinical examination alone is reported as 70% [ 12 ]. This failure to diagnose breech presentation antenatally reduces the opportunity to correct it via ECV. It also means that undiagnosed breech babies may present in advanced labour and that CS is often performed as an emergency procedure. Further, it reduces the opportunity to appropriately counsel and prepare for those women desiring a vaginal birth.
Breech presentation is easily diagnosed using ultrasound. Given that spontaneous version from breech to cephalic occurs after 36 weeks in <10% [ 13 ], and reversion after ECV in less than 3% [ 10 ], universal ultrasound at late gestation should improve the rate of antenatal diagnosis and, logically, lead to a reduction in the incidence of breech presentation at term. In the United Kingdom, United States of America, and many European countries, third trimester ultrasound is not performed as routine clinical practice, although this trend is changing, with the primary clinical driver being attempting to detect babies at increased risk of stillbirth [ 14 ]. However, a corollary of this is an assessment of presentation by ultrasound at the time of fetal risk assessment.
We noted the findings of a large recent UK study that offered nulliparous women a universal scan at 36 weeks gestation [ 15 ]: The authors suggested that use of universal scanning at this gestation could virtually eliminate undiagnosed term breech presentation. Unfortunately, the findings cannot be applied to multiparous women who make up half the pregnant population but have a higher incidence of spontaneous version [ 13 ]. Because of this, and the relatively poor usage and success rate (14%) of ECV in the study, a further question remains unanswered. This is whether universal ultrasound, by allowing more usage of ECV, leads to a reduction in the incidence of term breech presentation.
From September 2016, a universal 36-week scan was offered to all women giving birth in Oxford University Hospitals NHS Trust (OUH). The aim of our study was to determine the “real world” impact of this policy on breech presentation at term.
This is a population-based cohort study of 4 years of births in a large UK teaching hospital, assessing the impact of a major change in unit policy: a universally offered late third trimester scan. Outcomes were prespecified ( S1 Analysis plan ). Primary outcomes were (1) the overall incidence of breech presentation and (2) the incidence of undiagnosed breech presentation. Secondary outcomes related to ECV clinic outcomes, mode of birth for breech presentation, and perinatal outcomes.
Pregnancies with an expected date of delivery (EDD) between 01 October 2014 and 30 September 2016 were compared those with an EDD of 01 October 2016 to 30 September 2018. All women delivering in OUH with a singleton, nonanomalous fetus were included, and the term group, women giving birth from 37+0 weeks’ gestation, were included in analysis.
All data were collected prospectively, with output from respective data collection systems: electronic patient record (Cerner Millennium) for maternity data, Badgernet (Clevermed) for neonatal data, Viewpoint (GE Healthcare) for ultrasound data, and prospective breech clinic records were merged. These were analysed using Stata 15 software (StataCorp, College Station, Texas). The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines were followed ( S1 STROBE Checklist ). Demographic characteristics, pregnancy, birth, and neonatal outcomes were summarised in the 2 groups with mean and standard deviation for continuous variables and count and proportion for categorical variables and compared by means of t test or chi-squared test as appropriate. Where missing values occurred, which was only among demographics, calculations were performed using only pregnancies with data as the denominator. Differences between the 2 groups were compared using relative risk (RR) ratio, calculated as the percentage of pregnancies with the outcome of interest after the introduction of the 36-week scan, divided by the percentage of pregnancies with the outcome of interest prior to its introduction, with 95% confidence intervals (CIs).
OUH is a large tertiary referral unit in the UK. A specialist-dedicated “breech clinic” has been in place since 1998. The normal care pathway is that all women from 35 weeks with an ultrasonographically proven breech presentation, or where breech presentation is suspected clinically, are referred unless a preexisting indication for CS exists. Nulliparous women are seen from 36+0 weeks; multiparous women from 37+0 weeks. Ultrasound is performed in the clinic, and women are assessed for their suitability for ECV according to published criteria [ 10 ] and which, if appropriate and accepted, is performed in the same clinic as described elsewhere [ 10 ]. The procedure itself or the operators did not alter over the period under study. In persistent breech presentations, the mode of birth is discussed: Women are assessed as described elsewhere [ 16 ] for their suitability for vaginal breech birth, which is planned depending on maternal choice. Alternatively, elective CS birth is offered.
In October 2016, it became unit policy that all women with a singleton fetus were offered a routine ultrasound scan between 35+0 and 36+6 weeks’ gestation, as part of a service initiative (Oxford Growth Restriction Identification Programme, OxGRIP). Prior to this, ultrasound scans were arranged ad hoc according to perceived clinical risk. The 36-week scan was prebooked at the anomaly scan, or later if the anomaly scan had not taken place in OUH. At the 36-week scan, the presentation and placental site were determined, the deepest pool of amniotic fluid and fetal biometry were measured, and the umbilical artery and middle cerebral artery Doppler pulsatility index (PI) assessed to calculate the cerebroplacental ratio (CPR). Where breech presentation was noted, women were referred directly to the breech clinic for an appointment from 36 or 37 weeks’ gestation according to their parity.
For the purposes of the analysis, different subgroups were created. A flow diagram ( Fig 1 ) demonstrates the possible flows of breech babies in the third trimester to aid understanding of these cohorts.
Fig 1. Pathways of the breech fetus in the third trimester. ECV, external cephalic version.
“Breech presentation at birth” was defined as where the fetus delivered breech or, if delivery had been by CS, this was the presentation at the start of surgery.
“Undiagnosed breech” was defined as where the presentation at birth (≥37+0 weeks) was breech, but the presentation had not been recorded at any ultrasound examination performed from 34+0 weeks and there had been no referral to the breech clinic, or there had been no elective CS with breech given as a primary or secondary indication or, if an ECV had been successful, breech presentation had not been recorded at any ultrasound following this.
“Breech in the third trimester” was a surrogate definition created to allow neonatal outcome data to take account of the risks of ECV as well as being breech presentation at birth. It was defined as breech presentation at birth, or at any scan from 35+0 weeks or where a successful ECV had been performed.
Ethics statement
The ethics approval was granted by the Health Research Authority, IRAS project ID 222260 and REC reference: 17/SC/0374 on 27/07/2017. Informed consent was not required as the analysis was of routinely collected patient data. The study is reported as per the STROBE guideline ( S1 STROBE Checklist ).
The cohort comprised 29,559 births after 24 completed weeks. Of these, 27,825 (94.1%) were at 37+0 weeks or beyond, of which 14,444 were born prior to the universal scan policy and 13,381 after its introduction. There were 740 breech presentations at birth from 37+0 weeks, of whom 58 (7.8%) delivered vaginally. There were a further 217 preterm breeches, of whom 57 (26.3%) delivered vaginally. Demographic details are shown in Table 1 : There were small but significant increases in mean BMI and maternal age. The number of women delivering at term undergoing any growth scan between 35+0 weeks and birth increased from 5,578 (38.6%) to 13,251 (99.0%) ( p < 0.001).
Table 1. Demographic characteristics of the study population.
* p -Value from t test or Pearson chi-squared test, as appropriate.
Missing data were 2% for body mass index and 7.8% for maternal ethnicity; <2% otherwise.
Table 1 describes the demographic characteristics of the cohort and demonstrates the increased usage of ultrasound following the introduction of the universal scan.
The incidence of breech presentation at term birth did not reduce (2.6% versus 2.7%; RR 1.02, 95% CI 0.89, 1.18; p = 0.76) ( Table 2 ). The incidence of undiagnosed breech presentation ( Table 3 ) was reduced from significantly 25.5% to 8.3% (RR 0.33; 95% CI 0.22, 0.48; p < 0.001), and in the group who actually laboured, from 22.5% to 4.7% (RR 0.21; 95% CI 0.13, 0.35; p < 0.001).
Table 2. Incidence, diagnosis, and mode of birth of term breech babies.
* p -Value from t test.
**Defined as breech presentation at delivery and either (1) no scan ≥35+0 weeks showing breech; (2) successful external cephalic version; or (3) no elective CS with breech presentation as primary/secondary indication.
***Labour started with undiagnosed breech: elective CS excluded.
CI, confidence interval; CS, cesarean section; NA, not applicable; RR, relative risk.
Table 3. ECV in babies delivering at term.
CI, confidence interval; ECV, external cephalic version; RR, relative risk.
The unaltered incidence of breech presentation occurred despite an increase in the number of breech babies seen in the clinic ( Table 3 ) and a possible increase in the overall number of successful ECVs (RR 1.20; 95% CI 0.96, 1.51; p = 0.10). There were nonsignificant increases in eligible women declining ECV, from 12.1% to 13.7% (RR 1.14; 95% CI 0.78, 1.66), and decreases in the success rate (49.5% to 45.3%) (RR 0.92; 95% CI 0.78, 1.08; p = 0.29) of ECV attempts, although not in the number of women where ECV was considered contraindicated (RR 0.69 95% CI 0.37, 1.30; p = 0.25).
The proportion of vaginal breech births reduced from 10.3% to 5.3% (RR 0.51; 95% CI 0.30, 0.87; p = 0.01), largely due to the reduction in undiagnosed breech presentation in labour; this may also be responsible for the possible increase in planned breech birth. Although the proportion delivered by elective CS was significantly increased (57.4% to 66.9%, RR 1.17; 95% CI 1.04, 1.31; p = 0.01), the reduction in emergency CS, from 32.4% to 27.8% (RR 0.86; 95% CI 0.69, 1.07; p = 0.18), was smaller.
Of the 17 term babies ( Table 2 ) who started labour unknown to be breech after the 36-week scan policy started, one (5.9%) had not had a scan, 13 (76.5%) were multiparous, and only 2 (11.8%) had been transverse or oblique at the 36-week scan. None of these babies had had a successful ECV where reversion to breech occurred, but this did occur in 1 pregnancy where it was subsequently diagnosed before birth. Table 4 examines morbidity and mortality in a manner that encompasses any risks of ECV and therefore using not just term breech presentation, but a surrogate for babies that were probably breech in the third trimester. There was a nonsignificant reduction in all markers of neonatal morbidity and the numbers of extended perinatal deaths (still birth or neonatal death <28 days of life) reduced from two to zero. One death was an intrapartum death with an unsupervised, unplanned birth at home of an undiagnosed breech baby; the other had been diagnosed but was an antepartum stillbirth.
Table 4. Perinatal outcomes of pregnancies with a third trimester * breech presentation.
*Combines breech at delivery and pregnancies that underwent successful external cephalic version for breech presentation.
NCAO, neonatal composite adverse outcome, including Apgar at 5 minutes <7, cord arterial pH <7.1, admission to neonatal intensive care unit, perinatal death (stillbirth or death within 28 days of life), or hypoxic-ischaemic encephalopathy Grade 1–3; NA, not applicable; NNU, neonatal unit.
We observed that the introduction of a universal third trimester ultrasound scan across an entire, large maternity unit was followed by a large reduction in the incidence of undiagnosed breech presentation but not its elimination: About 5% of breech presentations were still only detected in labour. Vaginal birth among breech babies was reduced: Before the universal scan policy, more than half of all actual vaginal breech births occurred in women with an undiagnosed breech presentation. CS birth for breech increased, although the reduction in the proportion performed as an emergency was relatively small. There was no alteration in the incidence of breech presentation at term despite a greater opportunity to use ECV to prevent it. Adverse neonatal outcomes were rare, and a nonsignificant benefit was observed.
In 2019, Wastlund and colleagues [ 15 ] demonstrated the clinical efficacy and cost effectiveness of a universal scan in terms of detection of breech presentation in a cohort of 3,879 nulliparous women recruited to a research study, suggesting that undiagnosed term breech presentation could be “virtually eliminated” in these women, and leading to inferences that term breech presentation could be reduced. Our population-based cohort of over 27,000 women of all parities, assessing the “real world” impact of introducing such a policy, suggests that a universal scan policy may be less effective in clinical practice.
Why the universal scan is not followed by elimination of undiagnosed breeches is largely due to the presence of multiparous women who make up more than 50% of most pregnant populations. In nulliparous women, there were only 4 undiagnosed breeches. Although reversion after ECV is not more common among multiparous women [ 10 ], spontaneous version is [ 13 ], and the Wastlund study [ 15 ] only comprised nulliparous women. It is not as if these women are easily identifiable as, for instance, “unstable”: Most undiagnosed breech babies were cephalic at the 36-week scan. This suggests it will be difficult to eliminate the undiagnosed term breech within existing resources or current scanning protocols.
The reduction in undiagnosed breech nevertheless means that there were only 2 vaginal breech births among 17 undiagnosed breeches after the introduction of the scan policy, approximating to 1/5,000 births. Vaginal breech birth may, however, be unavoidable where it is undiagnosed, and very late CS may be inadvisable [ 16 ] and cause harm [ 17 ]. Or vaginal birth may be preferred by the mother, as is the case in some European countries. The rarity of vaginal breech birth could further compromise skills for these occasions and limit maternal choice. Further, undiagnosed breech presentation will occur more often than this analysis suggests because of preterm birth, where breech presentation is much more common and labour progress can be rapid. It therefore remains essential that skills in vaginal breech birth are taught and maintained.
Why emergency CS reduced little following the introduction of a universal scan is difficult to explain. A reduction occurred among undiagnosed breech babies but not overall, and elective CS was indeed more frequent. It might have been because spontaneous labour occurred in the interval between booking the CS and the date of CS. This was not however because the elective CS had been booked late: There were no differences in gestation at birth, and there is no evidence that ECV promotes labour [ 16 ].
The introduction of a policy of a routine scan at 36 weeks for all singleton women is also not followed by a reduction in the incidence of breech presentation at term. It would be anticipated from the data in Wastlund and colleagues [ 15 ] that increased antenatal diagnosis would allow more breech babies to undergo ECV, so reducing the proportion of term babies who were breech. However, these authors could not realistically assess this crucial potential benefit because ECV was only attempted in less than half of their breeches and was successful in only 14.3% of attempts. In our cohort, ECV was more systematically used (>80%) and was much more successful, at 47.2% overall, a figure that is in line with our previously published data [ 10 ]. Our failure to reduce the incidence of breech presentation therefore requires explanation.
The UK RCOG Green Top Guideline [ 16 ] states “the greatest impediment to the use of ECV is the non-identification of breech presentation”, yet our increased antenatal diagnosis did not translate into a reduced incidence at birth. Firstly, although ECV was contraindicated slightly less often, there were small but nonsignificant increases in both refusal and ECV failure rates. A reduction in success rate is plausible: Factors associated with a lower success rate of ECV, namely, a nonpalpable fetal head and a high BMI [ 18 ] are also likely to lower the sensitivity of clinical examination, and therefore reduce the impact of routine ultrasound scanning. Equally, where breech is proven by ultrasound before the ECV appointment, more time may be available to seek opinion and advice that might lead to a refusal to undergo the procedure. Nevertheless, the overall number of women who had undergone a successful ECV was slightly increased: As a percentage of the entire term cohorts, this is 1.0% and 1.2% of all pregnancies before and after the introduction of the scan, respectively (RR 1.20; 95% CI 0.96, 1.51). There are many possible explanations. Only 1 reversion occurred. It is unlikely that more babies were delivered by the feet or breech where an elective CS was being performed anyway. The proportion of nulliparous women, in whom breech is more common, did not increase. The most likely explanation is due to the small but important number of breech babies that spontaneously turn to cephalic after 36 to 37 weeks. While the gestation age at the time of the ECV was not earlier after the universal scan policy, it is likely that at least some of the babies undergoing successful ECV would have spontaneously verted anyway. This does not mean that ECV is not effective: Meta-analysis of randomised controlled trials has shown it to reduce the number of breech presentations at birth [ 8 ]. It is merely that a proportion of breech babies turn anyway [ 13 ].
The influence of ECV on our interpretation is important. While the increased opportunity for ECV did not translate into fewer term breech presentations, the incidence of breech presentation was already very low, at 2.6%. This is likely to be because of relatively high existing detection rates and the comprehensive and successful existing ECV service. Our findings therefore only apply to units with good ECV services. The introduction of a universal scan where breech detection rates are low or where the initiative also involves an ECV service could reasonably reduce the incidence of term breech presentation.
We acknowledge other limitations in this study. Even with more than 27,000 births, we lack numbers to detect a small but genuine effect on morbidity or mortality. We analyse a surrogate for babies that were breech in the third trimester, rather than those that were breech at birth in order to be able to assess any impact of ECV on safety: Where a third trimester scan was not done, this will be inaccurate. Equally, our findings regarding mode of actual birth are influenced by offering vaginal breech birth, a policy which varies according to countries and individual units. We do not have more detailed maternal outcomes which would have been useful given the change in timing of CS birth. Finally, we acknowledge small but significant changes over the 4 years of the study: fewer births overall, increasing maternal age, and BMI. As this was not a randomised controlled trial, we cannot rule out that these, or other factors that we have not analysed, affected our results. These changes are not unique to OUH and reflect a changing demography [ 19 ]. However, there are strengths to the study design: In assessing the real world impact of a clinical implementation across an entire maternity unit, we are able to take account of factors such as these and of human and organisational factors that may not be apparent among research recruits.
The introduction of a universal late third trimester ultrasound does not necessarily lead to a reduction in the incidence of term breech presentation. Although much less common, undiagnosed breeches at term remain. Clinical skill, both for the detection and the management of vaginal breech birth, continue to remain important.
Supporting information
Acknowledgments.
We would like to acknowledge Dr Angelo Cavallaro, Anita Hedditch, the Breech Team, and all sonographers who contributed to this project.
Abbreviations
confidence interval
cerebroplacental ratio
cesarean section
external cephalic version
expected date of delivery
Oxford University Hospitals
Oxford Growth Restriction Identification Programme
pulsatility index
relative risk
Strengthening the Reporting of Observational Studies in Epidemiology
Data Availability
All relevant data are within the manuscript and its Supporting Information files.
Funding Statement
The authors received no specific funding for this work.
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Decision Letter 0
Louise gaynor-brook.
24 Jan 2020
Dear Dr Salim,
Thank you for submitting your manuscript entitled "The impact of a routine late third trimester growth scan on the incidence, diagnosis and management of breech presentation" for consideration by PLOS Medicine.
Your manuscript has now been evaluated by the PLOS Medicine editorial staff and I am writing to let you know that we would like to send your submission out for external peer review.
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Kind regards,
Louise Gaynor-Brook, MBBS PhD
Associate Editor, PLOS Medicine
Decision Letter 1
21 Aug 2020
Dear Dr. Salim,
Thank you very much for submitting your manuscript "The impact of a routine late third trimester growth scan on the incidence, diagnosis and management of breech presentation" (PMEDICINE-D-20-00199R1) for consideration at PLOS Medicine. We do apologize for the long delay in sending you a decision.
Your paper was evaluated by an academic editor with relevant expertise, and sent to independent reviewers, including a statistical reviewer. The available reviews are appended at the bottom of this email - one further reviewer has seen your paper, and we will forward his or her report on to you via email if/when it becomes available - and any accompanying reviewer attachments can be seen via the link below:
In light of these reviews, we will not be able to accept the manuscript for publication in the journal in its current form, but we would like to invite you to submit a revised version that addresses the reviewers' and editors' comments fully. You will appreciate that we cannot make a decision about publication until we have seen the revised manuscript and your response, and we expect to seek re-review by one or more of the reviewers, to include a new reviewer if needed.
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Please let me know if you have any questions. Otherwise, we look forward to receiving your revised manuscript in due course.
Richard Turner PhD, for Louise Gaynor-Brook, MBBS PhD
-----------------------------------------------------------
Requests from the editors:
You mention that all relevant data are included - are you able include patient-level data in supplementary files, for example?
Please quote the setting in the title (e.g., "in Oxford, UK") and add a study descriptor (e.g., "a cohort study") following a colon.
Please restructure the abstract to generate a combined "Methods and findings" section according to journal style. The final sentence of the new combined subsection should quote 2-3 of the study's main limitations.
In your abstract, please quote aggregate demographic details for study participants.
After the abstract, please add a new and accessible "Author summary" section in non-identical prose. You may find it helpful to consult one or two recent research papers published in PLOS Medicine to get a sense of the preferred style.
Early in the methods section of your main text, please state whether or not the study had a protocol or prespecified analysis plan (and if so attach the relevant document(s) as supplementary file(s)). Please highlight analyses that were not prespecified.
We notice an ethics approval date in 2017 quoted in the methods section - please explain how this relates to the date the study started. Also, we suggest noting the situation regarding participant informed consent - perhaps not required in routine care.
In table 1, we suggest "White" rather than "Caucasian" ethnicity.
Please adapt the first paragraph of your "Discussion" section to provide a summary of the study findings - i.e., employing wording such as "we found that ... was" rather than the more general "shows this is not the case", for example, with the latter moved to a subsequent paragraph if you wish.
In the "Conclusion" section at the end of the main text, please adapt the text to "In this study, we found that ... did not lead ..." to avoid over-generalizing conclusions from a single-centre study.
Please quote p values alongside 95% CI throughout the paper, where available.
Throughout the text, please format reference call-outs as follows: "... preterm births [1].".
Please remove all iterations of "[Internet]" from the reference list.
Please add a completed checklist for the most appropriate reporting guideline, which we suspect will be STROBE, as a supplementary document (referred to in the methods section, e.g., "See S1_STROBE_Checklist"). In the checklist please refer to individual items by section (e.g., "Methods") and paragraph number rather than by line or page numbers, as the latter generally change in the event of publication.
Comments from the reviewers:
*** Reviewer #1:
This article is about the impact that a change in procedure to routinely have late trimester scans has on various outcomes including breech presentation.
As a statistical reviewer, there is very little statistical considerations being reported in the article for me to be able to comment on, and only basic summary statistics and unadjusted two-sample tests are used to compare between the populations before and after the change in procedure. Similarly, given the methods of data collection there is very little on study design or methods that is relevant to comment on. Perhaps the only comment I would have for the statistics, is that the method of calculation for the Risk Ratio confidence interval should be stated.
The above comments are not implying that the article is not of value or that further statistics/analysis would be needed to answer the key question of interest, just that there are only very basic numbers reported and so the value of the paper will almost entirely be based on clinical judgement and relevance for which I couldn't reasonably contribute towards.
*** Reviewer #2:
General and specific comments included below. This paper is highly topical to an obstetric/maternity care audience, as the role of routine third trimester ultrasound continues to be considered in many developed settings worldwide.
There are already a few major papers looking at the identification of breech babies via routine T3 US and the consequent impact on care/outcomes - this paper attempts to investigate whether routine T3 ultrasound results in changes in antenatal detection, mode of birth and incidence of breech presentation in a 'real world' setting (primips and multips).
I think the premise is good and an important question but I think the findings that form the focus of this paper are not those that are most clinically relevant or significant. The paper concludes that routine T3 US did not reduce the presentation of breech at term but for a clinical audience, it is much more interesting and salient that routine US did significantly reduce the incidence/risk of undiagnosed breech before birth and labour - this is where the majority of breech-related morbidity lies so it would seem to be of great significance but is not how this paper is framed. I would suggest reframing the discussion of this paper if it is intended to be published for a clinical audience.
In the conclusion, an erroneous 'of'
States CS is 'more costly' - than what? Vaginal birth? Because elective CS for breech is arguably much less costly than breech vaginal birth. This needs to be clarified.
The paper states that the greatest negative of breech presentation at term is the contribution to CS rate but the key end-point/question of the study is incidence of breech presentation at term. Breech at term doesn't really matter in the clinical setting unless it changes a clinical outcome, such as emergency CS rate for undiagnosed breech specifically or unplanned vaginal breech births.
Only one line given about determining RR - how was this done statistically? This would seem a good study in which to use causal inference methodology and attempt to replicate the assumptions of an RCT, especially given the clear exposure of universal US and known differences in the demographic characteristics of pre and post US cohorts.
Summary of key findings:
No change in term breech presentation (S)
More breech presentation at clinic (S)
More planned breech VD (NS)
Fewer actual breech VD (S)
More elective CS overall (S)
Fewer emergency CS overall (NS)
Significant reduction in undiagnosed breech before birth and before labour - these are narrow CI and surely clinically significant findings!
Hard to work out how (Table 1) gestational age at delivery could be significantly different between the pre and post-OxGRIP groups given numbers provided?
Table 1 reports breech at delivery as 2.6 vs 2.7 and the text states breech at term is the same - these are potentially different things, needs to be clarified if being used interchangeably.
Planned vaginal breech increased but actual vaginal breech reduced overall (not in those in whom breech was diagnosed) - Was this because X% of planned breech births reverted to cephalic before birth or because they were delivered by CS??
Table 3 indicates that undiagnosed breech before birth was significantly reduced from 25.5% to 8.3% and that amongst the undiagnosed breech babes at term, breech undiagnosed before labour was significantly reduced - this seems to be an important clinical end-point.
Error - 'the proportion of breech babies giving birth' does not make sense - 'being born vaginally' perhaps?
Also, 'a surrogate for babies that were breech in the third trimester babies' - an extra 'babies'?
It would be informative to know whether those two breech babies that died pre-OxGRIP were born via vaginal birth or were undiagnosed breech even?
The study is likely under-powered to detect any meaningful reductions in adverse perinatal outcomes but still demonstrates a trend towards reduction across all outcomes - seems important in the context of the study.
The authors seem to emphasise the findings of the study that are not of greatest clinical significance. The steady rate of term breech presentation pre and post routine T3 US is not that interesting, but the significant reduction in actual vaginal breech births and in undiagnosed breech presentation at birth or pre-labour is of great clinical significance and will get the attention of a clinical readership - would seem to justify the intervention. Further, although not powered to determine significance, the trend towards better neonatal outcomes, though rare, is also meaningful for clinicians. This is the main reason to care about breech presentation at term and therefore the role of routine T3 US, not so much the change in breech presentation or caesarean section rates.
Error: First paragraph says 'at last' instead of 'at least'
Error: 'Whilst the gestation at the time of the ECV gestation at ECV' - sentence does not make sense
Any attachments provided with reviews can be seen via the following link:
Submitted filename: PLOSMed_RoutineUSBreech.docx
Author response to Decision Letter 1
Collection date 2021 Jan.
22 Sep 2020
Submitted filename: Response to reviewer_R1.docx
Decision Letter 2
26 Oct 2020
Thank you very much for submitting your revised manuscript "The impact of a routine late third trimester growth scan on the incidence, diagnosis and management of breech presentation in Oxford, UK: A cohort study" (PMEDICINE-D-20-00199R2) for consideration at PLOS Medicine.
Your paper was discussed with our academic editor and re-seen by two reviewers, and by a new statistical reviewer. The reviews are appended at the bottom of this email and any accompanying reviewer attachments can be seen via the link below:
In light of these reviews, we will not be able to accept the manuscript for publication in the journal in its current form, but we would like to invite you to submit a further revised version that addresses the reviewers' and editors' comments fully. You will recognize that we cannot make a decision about publication until we have seen the revised manuscript and your response, and we plan to seek re-review by one or more of the reviewers.
We hope to receive your revised manuscript by Nov 16 2020 11:59PM. Please email us ( [email protected] ) if you have any questions or concerns.
Please let me know if you have any questions. Otherwise, we look forward to receiving your revised manuscript shortly.
Bearing in mind the observational design of your study, please adapt wording throughout your paper which ascribes causality to the policy change. For example, at line 44 we ask you to amend the wording to "In this study ... was associated with a reduction in the incidence of undiagnosed breech ...".
Similarly at line 270, we suggest amending the text to "It is difficult to explain why the policy was associated with a non-significant reduction in emergency CS. While there was an apparent fall in the number of undiagnosed breech babies but not overall ...", or similar.
In the title, would "before and after study" be a more appropriate study descriptor than "cohort study"?
Please harmonize Oxford/Oxfordshire in title and paper. In the abstract, we suggest adapting the text to note that the study was done at a single centre.
Please make that "principal" at line 20.
Please refer to the attached study plan early in the methods section of your main text, and highlight any non-prespecified analyses.
Please use the notation "p<0.001" throughout.
We suggest removing the attached RCOG abstract.
In the attached study plan, we suggest deleting the text about the "helper second author".
Are you able to include participant-level data in supplementary files, or deposit these at a publicly-accessible repository?
The authors have made considerable effort to incorporate the reviewers feedback and comments and the resulting manuscript is clearer and more compelling as a result. The paper present a very large cohort study with interesting findings and I feel it should be published. This iteration of the paper presents a much more clinically-relevant perspective and is much easier to comprehend - the first version was confusing in parts between what was and was not impacted by the US screening intervention. The discussion is now much more balanced and fair, and presents reasonable recommendations for other units based on the findings and limitations of this study.
*** Reviewer #3:
Having reviewed the authors' response and the submitted new version of The impact of a routine late third trimester growth scan on the incidence, diagnosis and management of breech presentation in Oxford, UK: A cohort study" (PMEDICINE-D-20-00199R2) by Dr Ibtisam Salim and colleagues for PLOS Medicine I think it is suitable for publication in Plos Med.
Authors responded well to the suggestions of my comments and the second reviewer. The manuscript is clear, only the 2 pre-specified cohorts (pre vs post scan) are used and outcome is well-defined. The new stated conclusion that a routine ultrasound considerably reduced the incidence of undiagnosed term breech presentation at birth is clear, even though this did not result in no undiagnosed breech presentation, a reduction in the incidence of breech presentation and better neonatal outcome. I agree fully with their comment that it is extremely important to show that the introduction of a third trimester scan does not reduce the incidence of breech presentation at delivery, particularly in a unit with widespread and successful use of ECV and therefore obstetricians with clinical skills for vaginal breech delivery should remain.
*** Reviewer #4:
I confine my remarks to statistical areas of this paper. I have a couple of issues to resolve before I recommend publication
First, there is no reason to do the tests on lines 137-138. For "table 1" analysis the key is effect size, not significance. Even very small differences were significant here, but not meaningful. Also, eliminate the p value column in table 1.
Second, and more importantly, while it isn't exactly *wrong* to do t tests as the authors did, it would be better to use logistic regression and account for covariates. This will increase the staistical power of the tests, and also allow some other conclusions to be drawn.
Author response to Decision Letter 2
Submitted filename: Response to reviewers_R2.docx
Decision Letter 3
25 Nov 2020
Thank you very much for re-submitting your manuscript "The impact of a routine late third trimester growth scan on the incidence, diagnosis and management of breech presentation in Oxford, UK: A cohort study" (PMEDICINE-D-20-00199R3) for consideration at PLOS Medicine.
I have discussed the paper with our academic editor and it was also seen again by one reviewer. I am pleased to tell you that, once the remaining editorial and production issues are dealt with, we expect to be able 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:
Our publications team ( [email protected] ) will be in touch shortly about the production requirements for your paper, and the link and deadline for resubmission. DO NOT RESUBMIT BEFORE YOU'VE RECEIVED THE PRODUCTION REQUIREMENTS.
In revising the manuscript for further consideration here, please ensure you address the specific points made by each reviewer and the editors. In your rebuttal letter you should indicate your response to the reviewers' and editors' comments and the changes you have made in the manuscript. Please submit a clean version of the paper as the main article file. A version with changes marked must also be uploaded as a marked up manuscript file.
Please also check the guidelines for revised papers at http://journals.plos.org/plosmedicine/s/revising-your-manuscript for any that apply to your paper. If you haven't already, we ask that you provide a short, non-technical Author Summary of your research to make findings accessible to a wide audience that includes both scientists and non-scientists. The Author Summary should immediately follow the Abstract in your revised manuscript. This text is subject to editorial change and should be distinct from the scientific abstract.
We hope to receive your revised manuscript within 1 week. Please email us ( [email protected] ) if you have any questions or concerns.
We ask every co-author listed on the manuscript to fill in a contributing author statement. If any of the co-authors have not filled in the statement, we will remind them to do so when the paper is revised. If all statements are not completed in a timely fashion this could hold up the re-review process. Should there be a problem getting one of your co-authors to fill in a statement we will be in contact. YOU MUST NOT ADD OR REMOVE AUTHORS UNLESS YOU HAVE ALERTED THE EDITOR HANDLING THE MANUSCRIPT TO THE CHANGE AND THEY SPECIFICALLY HAVE AGREED TO IT.
Please note, when your manuscript is accepted, an uncorrected proof of your manuscript will be published online ahead of the final version, unless you've already opted out via the online submission form. If, for any reason, you do not want an earlier version of your manuscript published online or are unsure if you have already indicated as such, please let the journal staff know immediately at [email protected] .
Please let me know if you have any questions. Otherwise, we look forward to receiving the revised manuscript shortly.
------------------------------------------------------------
Requests from Editors:
We suggest making that "Oxfordshire" in the title.
At line 26, please adapt the text to "We carried out a population-based ..." or similar.
Please restructure the end of the "Methods and findings" subsection of you abstract. The final sentence should begin "Study limitations include ..." or similar, and should list 2-3 limitations. We suggest that one limitation should be the possible influence of secular changes over time on your findings.
The final sentence of the "Conclusions" subsection of your abstract seems rather disjointed, and we suggest running on the previous sentence, e.g., "... service, indicating that clinical skills ...". Alternatively the sentence could be removed.
At line 63, we suggest quoting the actual number of births.
Please remove the quotation marks at lines 63 and 116/7.
At line 72, please amend the text to "... is unlikely to prevent the occasional need for skills ...".
At line 77, we suggest adapting the text to "... reduced expertise in management of those ...".
Please begin the sentence at line 239 with "We observed that ..." or similar.
At line 246 and any other instances in the ms, we ask you to amend the word "trend". Please substitute a phrase such as "apparent non-significant benefit".
At line 323, we suggest substituting "rule out" for "disprove".
At line 325, please adapt the text to "However, there are also strengths to the study design: ...".
Please remove the information on funding from the acknowledgements section at the end of the main text. This information will appear in the article metadata via entries in the submission form.
Throughout the text, the labels for tables seem incorrect; e.g., at line 192, "S1_Table" should be "Table 1".
Please ensure that the attachments (e.g., STROBE checklist) are labelled as they are referred to in the text.
Comments from Reviewers:
The authors have responded to my suggestions.
I suggested removing the p values from Table 1. They said they would like to keep them, or better understand why I asked to remove them. Here is that explanation:
It isn't wrong to put the p values; that is, it doesn't violate any rules or assumptions or whatnot. But it is misleading. It perpetuates myths about p values. Just as, say, you wouldn't include meaningless medical information (like, say, patient's hair color) so you shouldn't include p values. P values tell you whether to reject a null hypothesis. But, here, there is no null hypothesis. The key issue is whether the two groups are different in any meaningful way. That is answered by the effect sizes. The fact that, e.g. the change in mean maternal age is significant isn't really relevant. It went up by 0.3 years. Unless there is some reason that that difference is of medical significance, why put in the p values?
But I won't insist on the removal, I just think it is a good idea.
I also suggested using logistic regression instead of t-tests. The authors responded that they felt they did not need to do so because the differences on the covariates were small; they wrote
<<<
The covariates for which adjustment might be meaningful would be those that might reasonably have influenced the diagnosis or management of breech resentation, whilst not being on the causal pathway whereby the intervention (a universal scan) is likely to have led to the changes observed.
>>>
This isn't necessarily so. Even if a variable is equal in the two groups, it can still change the parameter estiamates for the main independent variable. It can also decrease the standard error.
Again, I won't insist on the change because, as I noted originally, it isn't exactly wrong to do t-tests. But, again, I think logistic reg. would be better.
So, I marked "proceed without recommendation" and leave it to the authors and editors how to proceed.
Author response to Decision Letter 3
15 Dec 2020
Submitted filename: Response to reviewers_R3.docx
Decision Letter 4
16 Dec 2020
I am writing concerning your manuscript submitted to PLOS Medicine, entitled “The impact of a routine late third trimester growth scan on the incidence, diagnosis and management of breech presentation in Oxfordshire, UK: A cohort study.”
We have now completed our final technical checks and have approved your submission for publication. You will shortly receive a letter of formal acceptance from the editor.
PLOS Medicine
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