P Lea Morello

Julien Mancini

Xavier Carcopino

T a g g e d H 1 Predictors factors of the absence of high-grade intraepithelial lesion in excisional therapy specimenT a g g e d E n d T a g g e d

Objectives: To identify predictive factors of the absence of high-grade intraepithelial lesion (HGSIL) in cervical excisional therapy specimen. Methods: Data from 835 women who underwent excisional therapy for a cervical intra epithelial lesion at the department of Gynaecology from two university hospitals, between January 2015 and December 2020 were reviewed. Demographic data, referral cytology, colposcopic findings, results of cervical biopsy and endocervical curettage were retrieved. Primary outcome was the absence of HGSIL on cervical excisional specimen analysis defined by the identification of no intraepithelial lesion or of low-grade lesion only. Results: The absence of HGSIL on specimen was observed in 137 (16.4%) cases. Three factors were identified to have a significant and independent impact on the probability of the absence of HGSIL on specimen: age higher than 40 years (aOR: 1.8; 95%CI: 1.1-3.0; p=0.024), a small abnormal transformation zone (TZ) (aOR: 2.3; 95%CI: 1.4-3.7; p=0.001) and the result of the cervical biopsy at the time of colposcopic assessment not showing HGSIL (aOR: 8.6; 95%CI: 4.7-15.5; p < 0.001). No significant impact of the referral cytology nor of the colposcopic impression were observed. Conclusion: Although the result of cervical biopsy performed at the time of colposcopic assessment is the key risk factor for the absence of HGSIL on excisional specimen, age over 40 and a small abnormal TZ are the two other identified risk factors. Practitioners should consider these findings when deciding for excisional therapy.

T a g g e d E n d T a g g e d P Keywords:

High-grade intraepithelial lesion Excisional therapy Colposcopy Risk factor Surgery T a g g e d E n d T a g g e d H 1 IntroductionT a g g e d E n d T a g g e d P Cervical cancer is a strictly virus-induced cancer and must necessarily go through precancerous stages (HGSIL) before invasion [1].

T a g g e d E n d T a g g e d P Over the last decades, screening programmes have demonstrated to consistently reduce the incidence and mortality of cervical cancer [2 -5]. Ablative and/or excisional treatments of HGSIL are highly effective for preventing progression to cancer [6]. Large loop excision of the transformation zone (LLETZ) is the most widely used treatment in routine practice [6]. Although highly efficient, this excisional procedure is associated with increased risk of subsequent premature delivery [7,8]. Additionally, healing process might result in cervical stenosis and endocervical extent of the squamocolumnar junction, jeopardizing long-term post-treatment follow-up [9][10][11].T a g g e d E n d T a g g e d P With the tendency to delay the age of first pregnancy and the high number of patients diagnosed with HGSIL in childbearing age, limiting the consequences of excisional therapy is a genuine public health issue [12]. Although excisional therapy should be indicated in patients with proven HGSIL or at least with a maximal probability of HGSIL, colposcopic appreciation is sometimes difficult. Excisional therapy may be indicated despite a negative biopsy, or even in the lack of a biopsy if colposcopy did not show any abnormality with a type 3 transformation zone following high-grade referral cytology Despite proven HGSIL at preoperative cervical biopsy, specimen analysis does not always confirm this diagnosis, possibly ending in low-grade lesion (LGSIL) only and even sometimes in the lack of any lesion. The risk of having no HGSIL on the excision specimen despite HGSIL at cervical biopsy is estimated to be 25% [14,15]. Identified risk factors for such situation are a low-grade referral cytology, minor changes colposcopic impression, CIN2 at cervical biopsy, and non-16/ 18 high-risk HPV infection [14,[16][17][18][19]. Considering the absence of any lesions, previous studies report a risk between 16% and 19% with risk factors being the same as those mentioned above, as well as a prior negative HPV testing, or a low HPV viral load [20][21][22]. Overall, few studies have evaluated this risk, with most of them suffering from methodological flaws such as retrospective nature and small size of the studied population. Additionally, these studies focused on one or two main risk factors only and didn't consider all pre-operative factors as a whole [23,24]. In most of these studies, although overall colposcopic impression was reported, precise details were lacking such as the type of the TZ, the size of the abnormal TZ and the numbers of cervical biopsies performed [14,16]. More studies are therefore needed to precisely identify risk factors of the absence of HGSIL in cervical excisional therapy specimen, helping clinicians to select patients in whom an excisional therapy is useless without risking missing an invasive lesion.T a g g e d E n d T a g g e d P The aim of this study is to determine predictive factors of the absence of HGSIL when performing an excisional therapy and therefore to establish a profile of patients in whom it is preferable to opt for surveillance rather than surgical excisional therapy.T a g g e d E n d T a g g e d H 1 Materials and methodsT a g g e d E n d T a g g e d H 2 PatientsT a g g e d E n d T a g g e d P Medical charts from all women who underwent excisional therapy at the department of Gynaecology from two university hospitals between January 2015 and December 2020 were retrieved and analyzed. All women who had an excisional therapy performed following a referral colposcopic examination eventually completed with one or multiple cervical biopsies were included. Patients with invasive carcinoma on cervical biopsy and with ungradable intra epithelial lesion on the excisional specimen were excluded. Patients for whom clinical data were missing, especially precise initial colposcopic examination report data were also excluded from our analysis.T a g g e d E n d T a g g e d P Indications of colposcopy were abnormal screening cervical cytology, abnormal looking cervix and post-coital bleeding. Colposcopic examinations were performed by experienced colposcopists after systematic staining with 5% acetic acid followed by 3% iodine. Colposcopic findings were classified according to the 2011 IFCPC nomenclature [25]. Cervical biopsies were possibly performed according to colposcopists' decision, depending on colposcopic findings and impression. No see and treat management were performed. Some patients were also referred directly for large loop excision of transformation zone (LLETZ) after that a colposcopy had been performed elsewhere, with colposcopic and cervical biopsies' reports attached.T a g g e d E n d T a g g e d P The study protocol received institutional approval from the Ethics Committee of the French college of Obstetricians and Gynaecologists (CEROG-2022-GYN-0302).T a g g e d E n d T a g g e d H 2 Excisional therapiesT a g g e d E n d T a g g e d P All excisional therapies were performed in theatre under either local or general analgesia. Except for one patient who had a cold knife conisation, all had a LLETZ performed. Excisional therapies were carried out under direct colposcopic guidance. No excisional therapy was performed during pregnancy.T a g g e d E n d T a g g e d H 2 DataT a g g e d E n d T a g g e d P Medical data including patients' characteristics, indication of colposcopy, referral cytology, colposcopic impression, type of TZ, size of the abnormal TZ, results of possibly performed cervical biopsy and endocervical curettage were retrospectively retrieved from medical charts. Patients with a history of repeated abnormal screening cervical cytologies were defined by at least two subsequent abnormal results (either low grade, high grade or both). Abnormal TZ was considered as small if only one cervical quadrant of the cervix was affected. Collected data included demographic data such as age, height, weight, smoking status, history of immunosuppression, parity, menopausal status and possible pregnancy at the time of colposcopy. Final histological diagnosis was collected directly from the pathology report. The main outcome was the absence of HGSIL on cervical excisional specimen analysis defined by the identification of no intraepithelial lesion or of LGSIL only.T a g g e d E n d T a g g e d H 2 Statistical analysisT a g g e d E n d T a g g e d P Continuous variables were expressed as mean ( § standard deviation) and compared using t-tests. Categorical variables were expressed as counts (%) and compared using x 2 or Fisher's exact tests.

Binary logistic regressions were then used to identify factors associated with the he absence of high-grade intraepithelial lesion in cervical excisional therapy specimen. Backward stepwise procedure was performed to select statistically significant factors in the multivariate models, first selecting in the regression variables displaying univariate association with a significance threshold of p=0.20, then removing from the model non-significant variables (threshold of p=0.05). A forward stepwise procedure was also used to confirm the variable selection. The C-index (area under ROC curve) and the Akaike Information Criterion (AIC) were used to compare model fit. All statistical tests were two-sided using a threshold p-value of 0.05. Analyses were performed using SPSS Statistics 20.0 (IBM Inc., Armonk, NY, USA).T a g g e d E n d T a g g e d H 1 ResultsT a g g e d E n d T a g g e d H 2 PatientsT a g g e d E n d T a g g e d P During the study period, a total of 962 excisional therapies were performed in both participating centers. Forty patients were excluded because of an invasive carcinoma on the cervical biopsy and 12 because of an ungradable intraepithelial lesion on the surgical specimen. Data was missing for 75 procedures, and patients were therefore excluded. Finally, a total of 835 excisional procedures were included for analysis.T a g g e d E n d T a g g e d P Patient's characteristics are summarized in Table 1. The mean age was 40.4 ( §10.4) years with 153 (18.3%) menopausal women. Twenty-one (2,5%) women were diagnosed with an intra-epithelial lesion during pregnancy, with the decision of excisional therapy made after a new colposcopic examination following delivery. A type 3 transformation zone was observed in 185 (22.4%) cases. Normal colposcopic examination was observed in 13 (1.6%) cases, with minor and major changes observed in 202 (24.4%) and 521 (62.6%) cases, respectively. No biopsy had been performed during colposcopy in 59 (7.5%) patients: 16 had a endocervical curettage only showing HGSIL; 27 had a high-grade referral cervical cytology with colposcopy showing a type 3 TZ with no abnormality identified (of whom 12 had a history of treatment for HGSIL); 10 had a previous biopsy showing HGSIL several months earlier with a colposcopic control just before the excisional therapy showing persistent major changes; 3 had a persistent LGSIL; 3 had an endocervical lesion at colposcopy inaccessible to a biopsy. One and two or more biopsies were performed in 376 (47.9%) and 350 (44.6%) cases, respectively. Cervical biopsies T a g g e d E n d T a g g e d P showed the absence of HGSIL in 58 (7.4%) cases. All of these 58 patients were referred for a diagnosis cone biopsy despite a negative biopsy for various reasons: history of repeated abnormal cervical cytologies with a colposcopic examination finding a type 3 transformation zone twice, persistent low-grade lesion for more than two years, colposcopic signs suggesting invasion. Finally, of the 835 excisional therapies included, the absence of HGSIL was found in 137 (16.4%) specimen with 61 (44.5%) of them showing no intraepithelial lesion at all.T a g g e d E n d T a g g e d H 2 Identification of risk factors for the absence of HGSIL in excisional specimenT a g g e d E n d T a g g e d P Patients with no HGSIL on excisional specimen were significantly older than others: 47.0 ( § 11.5) years vs. 39.1 ( § 9.6) years, respectively (p<0.001) (Table 2). They were significantly less likely to T a g g e d E n d T a g g e d P smoke: 56 (41.8%) vs. 369 (53.6%), respectively (p=0.013). Repeated abnormal screening cervical cytologies prior to excisional therapy was more often observed in these patients: 13 (9.5%) vs. 16 (2.3%), respectively (p<0.001). Patients with no HGSIL were significantly more likely to have a type 3 transformation zone at referral colposcopic examination: 67 (49.3%) vs. 118 (17.1%), respectively (p<0.001). The overall colposcopic impression was less severe in these patients as major changes or changes suggestive of invasive cancer were significantly less often reported: 60 (43.8%) vs. 461 (66.3%) and 4 (2.9%) vs. 25 (3.6%), respectively (p < 0.001). Patients with no HGSIL on excisional specimen were more likely to have a small abnormal TZ than others: 64 (67.4%) vs. 286 (43.5%), respectively (p<0.001). When performed, these patients were also likely to have a significantly lower mean number of cervical biopsies performed: 1.24 ( §1.03) vs. 1.55 ( §0.84), respectively (p<0.001). Finally, those patients were significantly more likely to have had an ECC performed: 21 (15.3%) vs. 36 (5.2%), respectively (p < 0.001).T a g g e d E n d T a g g e d P An analysis of the impact of the time lapse between colposcopy and excisional therapy and between referral cytology and excisional therapy on the probability of the absence of HGSIL on specimen was also performed. No significant impact was found for those delays.T a g g e d E n d T a g g e d H 2 Multivariate analysisT a g g e d E n d T a g g e d P In multivariate analysis, three factors were found to have a significant and independent impact on the probability to achieve the absence of HGSIL on the excisional specimen (Table 3). Age was one of those, with a cut-off of 40 years significantly increasing this probability: aOR 1.8 (95%CI: 1.1-3.0; p=0.024). The second independent risk factor was the identification of a small abnormal TZ: aOR 2.3 (95%CI: 1.4-3.7; p=0.001). The risk factor with the strongest effect was a cervical biopsy showing no HGSIL: aOR 8.6 (95% CI: 4.7-15.5; p<0.001). Adding age and the identification of a small abnormal TZ to the model with cervical biopsy alone improved the C-index from 0.662 to 0.747 and the AIC from 476.0 to 463.9 (likelihood ratio test p <0.001). Neither the severity of cytological abnormalities, nor of colposcopic impression were found to significantly impact the risk of the absence of HGSIL on excisional specimen.T a g g e d E n d T a g g e d H 2 Risk of no HGSIL in patients with a cervical biopsy showing HGSIL or ADKIST a g g e d E n d T a g g e d P Among the 695 patients with initially proven HGSIL or ADKIS following initial colposcopy and biopsy, 58 (9.7%) were finally found to have no HGSIL on excisional specimen analysis. The same two risk factors for the absence of HGSIL were identified in this population: age, with a cut-off of >40 years (p=0.028), and a small abnormal TZ at colposcopic examination (p=0.003) (Table 4).T a g g e d E n d T a g g e d H 1 DiscussionT a g g e d E n d T a g g e d P Our study shows the results of the cervical biopsy at the time of colposcopic examination along with the size of the abnormal TZ and the age of the patients to be the three independent risk factors for the absence of HGSIL on the excisional specimen in routine practice. Surprisingly and contradictory to previous literature, the referral cytology results and the colposcopic impression were not identified as risk factors [14,16,22]. With the inclusion of all excisional therapies that were performed following a referral colposcopic examination, whatsoever the practice of previous cervical biopsy and its result, our study aimed to assess the risk of the absence of HGSIL in routine clinical situation and not in very selected population. However, with such outcome observed in only 137 (16.4%) patients and the absence of intra epithelial lesion in 61 (7.3%) patients, the rates reported are lower than those commonly reported in literature [14,15,[20][21][22]. This result somehow testifies for the strict selection of patients T a g g e d E n d T a g g e d E n d T a g g e d P undergoing excisional therapy in our institution; such selection possibly biasing our results. We therefore believe this situation to explain why referral cytology nor colposcopic impression were identified as risk factors for the absence of HGSIL. Thus, the previous selection of patients undergoing excisional therapy was likely to have been already guided by the results of the referral cytology along with colposcopic impression. Although it is possible our study could not be representative of all practices, we believe our study to be relevant for clinical practice in optimal settings.T a g g e d E n d T a g g e d P The fact that age was found to have a significant impact on the absence of HGSIL is unexpected and contradictory with results from previous studies [14,16,21,22]. Additionally, one could expect the risk of the absence of HGSIL on excisional specimen to decrease with T a g g e d E n d LGL: low-grade lesion; TZ: transformation zone.

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y Only one cervical quadrant affected. T a g g e d E n d T a g g e d P age, along with the increasing probability for cervical cancer [1]. Our finding could simply reflect a higher acceptance for excisional therapy in older women without any childbearing issue and therefore for the appliance of less selection criteria in older women. In our study, the size of the abnormal transformation zone was also significantly associated with the absence of HGSIL. Our study is the first to identify this risk factor [17,21]. However, the impact of the size of the TZ has been already demonstrated to influence the probability for underdiagnosis of HGSIL as more biopsies are commonly required with the increasing size of the abnormal TZ [26,27]. Additionally, the likeliness of HGSIL has been shown to increase with the size of the TZ [28]. One could consider our result to support the likeliness of a full removal of a possible HGSIL by the cervical biopsy performed at the time of initial colposcopic examination in case of a small abnormal TZ.T a g g e d E n d T a g g e d P The result of the biopsy was the risk factor with the most important impact on the probability of the absence of HGSIL. This result is consistent with previous published data [16,17,20]. Previous studies also demonstrated a significant association of prior negative HPV testing and low HPV viral load [21,22]. We could not investigate the impact of HPV testing as our patients had no such test performed. This is explained by the introduction of HPV testing for primary screening in women over 30 in our country only in 2019, shortly before the end of our inclusion period.T a g g e d E n d T a g g e d P Along with the age, our results emphasize the importance of colposcopic examination with biopsy prior to excisional therapy. Using these three risk factors as a scoring system, the absence of HGSIL varied from 3% in women with none of those three risk factors identified up to 68% in those over 40 having a small abnormal TZ and a cervical biopsy showing no HGSIL. Although imperfect and hardly exploitable in women with only one or two identified risk factors, such gradation in the final risk of the absence of HGSIL on excisional specimen could be applied in routine practice. Avoidance of excisional therapy in women combining all these three risk factors could be considered. In these selected women, clinicians could opt for surveillance rather than excisional therapy with closed surveillance by an experienced colposcopist. Prospective studies are needed to properly assess this hypothesis. Finally, although our study didn't find a significant association between the absence of HGSIL and the delay between colposcopic examination and excisional therapy, a slight trend can be noticed, with an increase of the delay in patients with absence of HGSIL, which should be explored in further studies.T a g g e d E n d T a g g e d P Despite the large number of patients included, our study suffers from limitations inherent to its retrospective nature that should be considered when interpreting our results. However, we believe this bias to be limited by the use of exhaustive hospital databases, surgical and histological reports, and the very low rate of excluded cases due to missing data. Additionally, a selection bias cannot be ruled out as all included cases were treated in the two centers only, in which practices are well codified and might differ from other centers. We believe the large inclusion criteria to be a major strength of our study. Indeed, the inclusion of all women who underwent an excisional therapy whether a cervical biopsy had been performed or not, and no matter the result, is highly representative of what is done in routine clinical practice and makes our results exportable to most of clinical settings. Finally, in considering multiple details from the referral colposcopic examination, we did not restrain our analysis to the sole colposcopic impression and made a precise analysis of colposcopic criteria such as the type or the size of the TZ.T a g g e d E n d T a g g e d H 1 ConclusionT a g g e d E n d T a g g e d P Although the result of cervical biopsy performed at the time of colposcopic assessment is the key risk factor for the absence of HGSIL on excisional specimen, age over 40 and a small abnormal TZ are the two other identified risk factors. Combining these three risk factors improved the prediction of the absence of HGSIL. Thus, excisional T a g g e d E n d T a g g e d P therapy could be avoided in women combining those three risk factors. Instead, these women could be offered close surveillance by an experienced colposcopist. Practitioners should consider these findings when deciding for excisional therapy.

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  a g g e d E n d T a g g e d E n d Abbreviations: HPV, Human Papilloma Virus; HGSIL, High-grade lesion; LGSIL, Lowgrade lesion; CIN, intra epithelial neoplasia; TZ, transformation zone; ECC, endocervical curettage; LLETZ, Large loop excision of the transformation zone; IFCPC, International Federation of Cervical Pathology and Colposcopy; AIC, Akaike information criterion; ADK, in-situ adenocarcinoma; AGC, Atypical Glandular Cells; ASCH, Atypical Squamous Cell cannot exclude High grade lesion; ASCUS, Atypical Squamous Cell of Undetermined Significance; HSIL, High grade Squamous Intraepithelial Lesion; LSIL, Low-grade squamous intraepithelial lesion T a g g e d E n d T a g g e d E n d Disclosure of source(s) of financial support: None. T a g g e d E n d IRB status: The study protocol received institutional approval from the Ethics Committee of the French college of Obstetricians and Gynaecologists (CEROG-2022-GYN-0302). T a g g e d E n d Pr ecis: Cervical biopsy showing no high-grade lesion (HGSIL), small abnormal transformation zone and age over 40 are risk factors for the absence of HGSIL. T a g g e d E n d * Corresponding author at: Department of Obstetrics and Gynaecology, Hôpital Nord, APHM, chemin des Bourrely 13015 Marseille, France. E-mail address: xavier.carcopino-tusoli@ap-hm.fr (X. Carcopino). https://doi.org/10.1016/j.jogoh.2023.102550 2468-7847/© 2023 Published by Elsevier Masson SAS. T a g g e d E n d J Gynecol Obstet Hum Reprod 52 (2023) 102550 T a g g e d F i g u r e T a g g e d E n d Contents lists available at ScienceDirect Journal of Gynecology Obstetrics and Human Reproduction journal homepage: www.elsevier.com T a g g e d F i g u r e T a g g e d E n d T a g g e d E n d T a g g e d P [13].

  T a g g e d E n d T a g g e d H 1 Declaration of Competing InterestT a g g e d E n d T a g g e d P All authors have no conflict of interest to declare.T a g g e d E n d T a g g e d H 1 ReferencesT a g g e d E n d T a g g e d P [1] Melnikow J, Nuovo J, Willan AR, Chan BK, Howell LP. Natural

Table 1

 1 Patients' characteristics (n= 835).

	Age Mean (years) ( §SD)	40.4 ( § 10.4)
	BMI Mean ( §SD)	23.6 ( § 5)
	Smoking	425 (51.6)
	Immunosuppression*	45 (5.4)
	Nulliparous	231 (28)
	Postmenopausal	153 (18.3)
	History of previous treatment for HGL	104 (12.5)
	Excisional therapy	96 (11.5)
	Laser ablation	8 (1)
	History of repeated abnormal screening cervical cytologies prior	29 (3.5)
	to excisional therapy**
	Referral screening cytology
	ASCUS	149 (17.8)
	HSIL	219 (26.2)
	LSIL	159 (19)
	AGC	17 (2)
	ASCH	181 (21.7)
	Other	102 (13.2)
	Colposcopy performed during pregnancy	21 (2.5)
	Type 3 TZ	185 (22.4)
	Colposcopic impression
	Normal examination	13 (1.6)
	Minor changes	202 (24.4)
	Major changes	521 (62.6)
	Suggestive of invasive cancer	29 (3.5)
	Aspecific findings	66 (7.9)
	Small abnormal TZ y	350 (46.5)
	Number of cervical biopsies performed
	0	59 (7.5)
	1	376 (47.9)
	≥ 2	350 (44.6)
	Cervical biopsy results
	Absence of any intraepithelial lesion	16 (2)
	LGL	42 (5.4)
	HGL	678 (86.8)
	ADKIS	17 (2.2)
	Ungradable intraepithelial lesion	28 (3.6)
	ECC	57 (6.8)
	ECC results
	Absence of lesion	16 (28.1)
	Low grade lesion	4 (7)
	HGL	28 (49.1)
	In situ adenocarcinoma	2 (3.5)
	Ungradable CIN	7 (12.3)
	Values are expressed as n (%), otherwise specified.
	HIV positive (n=15), auto-immune disorders under immunosuppressors therapies (n=18),
	immune deficiency (n=2) and transplanted patients under immunosuppressors (n=10).
	** low-grade cytologies (n=20) and high-grade cytologies (n=9).

ADK: in-situ adenocarcinoma; AGC: Atypical Glandular Cells; ASCH: Atypical Squamous Cell cannot exclude High grade lesion; ASCUS: Atypical Squamous Cell of Undetermined Significance; ECC: endocervical curettage; HGL: High-grade lesion; HSIL: High grade Squamous Intraepithelial Lesion; LGL: low-grade intraepithelial lesion; LSIL: low-grade squamous intraepithelial lesion; TZ: transformation zone. * y Only one cervical quadrant affected.

Table 2

 2 Comparison of patients' characteristics depending on the final histology of excisional specimen.

	Excisional specimen analysis	p
	No lesion or LGL	High grade lesion or more*

ADKIS: adenocarcinoma in-situ; AGC: Atypical Glandular Cells; ASCH: Atypical Squamous Cell cannot exclude High grade lesion; ASCUS: Atypical Squamous Cell of Undetermined Significance; ECC: endocervical curettage; HGL: High-grade lesion; HSIL: High grade Squamous Intraepithelial Lesion; LGL: low-grade intraepithelial lesion; LSIL: low-grade squamous intraepithelial lesion; TZ: transformation zone. * Patients with high-grade lesion, in situ adenocarcinoma or invasive lesion. ** Only one cervical quadrant affected.

Table 3

 3 Multivariate analysis of risk factors predicting absence of high-grade lesion or more in excisional specimen.

	Factor	aOR (95%CI)	p
	Age > 40 years	1.8 (1.1-3.0)	0.024
	Small abnormal TZ y	2.3 (1.4-3.7)	0.001
	Cervical biopsy showing no lesion or LGL	8.6 (4.7-15.5)	< 0.001

Table 4

 4 Impact of age and size of the abnormal TZ on the probability of the absence of HGL on excisional specimen among patients having had HGL on previous cervical biopsy (n=695).

	Excisional specimen	p
	Absence of HGL HGL or more

Values are expressed in n (%), otherwise specified. HGL: high-grade lesion. *Include patients with absence of intra epithelial lesion, low grade intra epithelial lesion or ungradable intra epithelial lesion on cervical biopsy.

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T a g g e d E n d L. Morello, J. Mancini and X. Carcopino Journal of Gynecology Obstetrics and Human Reproduction 52 (2023) 102550


Răzvan Anghel

Constanţa Court

Considerations regarding the inclusion in working time of periods during which the worker participates in team building activities*

I. Introduction

Although carried out and studied since the 1 1960s, team building activities gained popularity in Romania around 2000, when their organisation entered the offers of travel agencies, currently considering that the market for these services in our country is constantly growing 2 .

Inevitably, the increase in these activities has increased the likelihood of conflict situations occurring in the course of their conduct, some of which have led to the referral to the courts, which makes it useful to analyse the legal regime of those activities and their time, especially since such activities often take place during daily or weekly rest periods or public holidays 3 .

Team building activities have the appearance of pleasant, recreational activities, which would not have the characteristics of an activity falling within the duties of the employees, being able to take many forms such as activities in the free space, excursions, hiking, games, discussions, celebrations, etc., generally outside the workplace, whether or not associated with vocational training activities. The disputes identified in judicial practice have, however, called into question this appearance, being necessary in order to clarify the legal regime of this activity a multidisciplinary approach.

II. Terminology and conceptual clarifications

Team building is characterised in the literature as the most popular and frequently used method of organizational development intervention 4 . The purpose of this activity in which the members of a team participate is its development, increasing 5 its efficiency with positive financial consequences for the employer, improving social relations between team members, clarifying roles, solving tasks and interpersonal problems affecting the functioning of the team, achieving results, setting and achieving targets 6 . At the same time, it has been shown in the doctrine that team building aims to develop problem-solving capacity or to acquire new skills and perceptions that facilitate participation in the realisation of a proposed change 7 being an adaptive mechanism for organizational changes 8. Another goal of this activity is to increase the cohesion of the team so that it works more efficiently and easily 9 .

Team building activities are sometimes correlated, combined, or associated with team training activities; however, this type of activity differs significantly from team building in that the latter is in principle not oriented towards professional skills, is not systematic and usually takes place in places that do not simulate workspace 10 . However, given that communication and networking skills acquire professional relevance, it can be difficult to distinguish between the two activities.

Finally, team building should not be confused with purely recreational activities organised jointly by the members of a team themselves, at their own expense, even at the initiative of the formal leader of the team but outside the employer's organisational framework, and must be separated from the motivational activities offered by the employer, purely recreational activities offered to employees as a gift, rewards, by bearing costs and without pursuing any purpose, with the voluntary participation of team members, this type of reward having the exclusive role of stimulating performance [such as individual or group trips (incentive trips) whose costs are borne by the employer] 11 .

III. Jurisprudential Examination

It is interesting, however, that, from a legal point of view, the classification of these activities is presented differently by employers in conflicting situations, depending on the interest pursued, which requires a correlated analysis by the courts. In situations where the institution competent to carry out the tax audit considered that the expenses involved in organising the team building activities were expenses for the remuneration of staff, which entailed certain tax burdens, the employers argued that those expenses were incurred for the purpose of carrying out the activity and obtaining profit, statement accepted or not by the courts in the cases identified, in relation to the established facts.

For example, in a dispute, it was held 12 that 'the team building activities were carried out in the interests of the employer, namely to obtain profit from the team's work', and the fact that they took place on weekly rest days is not such as to dispel that conclusion. In another case, the complainant claimed 13 that certain expenses relating to team-building activities are deductible as this action aimed at "improving the team through discussions on how information flows within the company; identifying the factors that can lead to the optimisation of expenditure; better capitalisation of working time; identification and dimensioning of investment needs in the next period; discussions on marketing activity and identification of ways that may lead to the possibility of obtaining contracts on the external market'; in that case, however, the court rejected those arguments, holding, in essence, that the purpose and necessity of the expenditure for the company's revenue-generating activity had not been established.

Also, in another case, in which the same arguments were raised, the appeal court considered that costs for team building actions were not deductible because they were unrelated to the training of employees and therefore unrelated to the company's income 14 . Also, on the grounds that the activity of team building were not related to the training of employees, the administrative court considered the conclusions of the Court of Auditors to be correct regarding the employer's (public institution) obligation to recover the costs incurred for that purpose, since those activities were for relaxing 15 and, therefore, not allowed by the public budget rules.

On the contrary, however, in situations where the employer's liability for the organisation of this type of activity was sought, the defences were diametrically opposed, and in some cases they were accepted by the courts in the cases identified, and in other cases rejected.

For example, in a case in which an employee applied for additional salary entitlements on the grounds that the period allocated to team building activities must be regarded as working time and participation in those activities must even be considered additional work or work performed during the weekly rest days, the employer claimed that she did not owe those rights, essentially stating 16 that those activities, carried out on weekends, were optional and did not, in essence, involve the performance of work, being organised to improve the interpersonal relationships within that company. The specialized labor court held in that case that none of the activities indicated by the applicant were part of her duties, since they were activities which do not constitute a performance of work, with the result that it was not possible to claim payment of a salary, but possibly compensation, provided that the actual damage that had occurred to her was demonstrated.

On the contrary, in another case, an employee was accused by the employer that 'he had committed a serious misconduct, namely that the employee... left the group and the space where the team-building was organised, without notifying anyone' 17 .

The question of the employer's liability for the organisation of team building activities was also raised in criminal matters, in case of personal injury in the course of those activities.

For example, in one case, several employees took part in a trip organised by the director of the company, on which occasion they rented ATV-type vehicles and one of the employees caused an accident resulting in personal injury to another employee, the former being convicted of the offence of personal injury due to fault. The court seised dismissed the employer's liability as a civilly responsible person for finding, in essence, that the 18 act of the defendant employee was not committed in the performance of the duties entrusted to him because both the defendant and the victim were in their free time, choosing to carry out an activity which was not part of a predetermined programme, so that "the fact that the trip was organised by the employer is not such as to create even a necessary correlation between the performance of the office which the defendant performed and the commission of the wrongful act; moreover, the wrongdoing was not only not committed in the interests of the principal, but there is not even an appearance in this regard". defendant's statements and witness statements) resulted in the fact that the schedule of the trip was not established by someone, but he was made according to the choice of each of the participants'.

It
In another case, where, in the company where the victim was employed, a 'exit' was organised with colleagues in order to have fun at a karting runway, on which occasion she suffered an accident and serious bodily injury, neither was the question of the employer's liability but only a question of the legal person organising that activity for customers 20 .

IV. Legal regime of team building activities and their time

From a theoretical point of view, it is certain that the team building activity is, in the employers' conception, a useful practice for their work from the point of view of the efficiency of the employees, which they organise and finance and which they regard as an investment in human resources which, like any investment, is meant to generate profit.

It is true that, from the point of view of the fiscal regime, as a connection between this activity and obtaining income by the employer for the deduction expenses being necessary, it seems that the demands of probation are higher and the taxable subject does not always manage to prove this connection, especially in the context where, even in specialized literature has shown that, despite the common belief about effectiveness of team-building, there is no very clear evidence in this regard 21 . However, even in the light of those doubts, the effectiveness of those practices and their usefulness for the employer's activity cannot be ruled out simply because they do not concern the training of employees, since those two activities are, as I have pointed out, different in their object and nature, even though the general aim is also to improve the activity of employees. In addition, any initiative aimed at improving the work can be a failure and may prove ineffective for many reasons, which in itself does not mean that it did not have the stated purpose. The analysis should be made, in this case, in relation to the purpose and object of team building activities, in which, indeed, some purely recreational and entertainment activities, declared fictional as team building activities, could not be classified in this category.

But in the employment relationships, in the relationship between the employer and the employee, the team building activity is, theoretically, always an activity organised by the employer for its own use. The question which arises in order to determine whether participation in those activities forms part of the employee's professional activity is whether or not the subordination relationship subsists during the period concerned.

The difficulty of the disputes arising in this context lies not so much in the theoretical aspects as in the correct classification of an activity which does not constitute the main professional activity of the employee.

This difficulty arises, as is apparent from the case-law identified, from the overlapping and combination of team building activities with professional training activities, but also with purely recreational activities, offered to employees as gifts and rewards. From this point of view, tax matters can only constitute an element which, among others, leads to a correct determination of the nature of the activity.

I believe that the time allocated to team building activities, once their character is certain, should be included in working time, but not for the purpose of remuneration, but for the protection of health and safety at work.

In contrast to the provisions of Art.111 of the Romanian Labor Code, which, for the purpose of determining remuneration, provides for the actual performance of work for the inclusion of a period in the working time, and the provisions of Article 120 of the Romanian Labor Code, which defines additional work as a work actually performed, the time allocated to participating in team-building activities cannot be included in the working time envisaged when quantifying the remuneration and those activities cannot be considered as additional work.

A different situation, with an exceptional nature, can possibly be identified only in the person of an employee who is responsible for organising the team-building activities at their place, who is not only in the position of participant and actually performs the work, performing tasks established by the employer to organize the team building activities.

From the perspective of Directive 2003/88, for the sole purpose of protecting health and safety at work, the time spent on participating in team-building activities may be included in working time if the conditions laid down by the definition contained in Article 2(1) of the Directive, as interpreted by the CJEU, are met.

In this respect, since team-building activities are apparently unrelated to the work performed by employees, members of the team, it is rather useful to check whether the period affected by this activity may constitute resting time.

In a recent judgment, the 22 CJEU summarized the features of rest time on the basis of its previous case-law, holding, in essence, that a period during which no work is actually carried out in favour of the employer does not necessarily constitute rest time, but only those in which the constraints imposed on the worker do not reach such a degree of intensity preventing him from managing and dedicating himself to his own interests and the constraints must result from employer requirements or imposed by laws, regulations or collective agreements and not from natural elements or choices of the employee or from the lack of special recreational possibilities (parag.32, 38, 40-42).

In the same vein, the Court added new elements in its analysis of the constraints to which the worker is subject to the management of his own time, holding that the actual possibility for the worker to carry out another paid activity during the guard at home or the possibility of refusing to participate in part of the interventions requested from him constitutes an important indication that such constraints are limited in nature 23 . It has also been established that, in the analysis of the existence of these constraints, account should not be taken of those inherent in a short rest period (e.g. several tens of minutes of a break which does not allow long distance travel outside the workplace) and in general those which would exist independently of the requirements of the function 24 . Similarly, in this analysis, account must not be taken of the consequences of the worker's free choices with regard to the determination of his residence which determines the distance from work, the duration of the journey and the reaction time if he is required to intervene or those determined by natural elements 25 .

It can therefore be concluded from the case-law of the CJEU that rest time is a period during which, although the employment relationship and the obligations of the employee subsist, they involve some minor constraints which allow the worker, in fact, to rest and devote himself to leisure and leisure activities, to manage his time with a sufficient degree of freedom to be able to pursue his own interests reasonably and to remain within his social environment and with his family, in order to recover the ability to work lessened by the fatigue generated by the performance of the tasks incumbent on him under the individual employment contract, so as to prevent the risk arising from the accumulation of periods of work without rest in terms of occupational safety and health, understood as complete physical, mental and social well-being, in the perspective of continuing professional activity.

Finally, in the recent case-law to which reference has been made, there appears to be a tendency of the CJEU to refrain from laying down solutions to the specific situation at issue and to transfer to the national court the analysis of the classification of a given period in working time or rest time, indicating indicative elements which should be analysed in an 'overall assessment of all the circumstances of the case in order to determine whether the worker is subject to constraints which objectively and very significantly affect his or her ability to manage his time freely'. 26 To this end, it is necessary to examine some relevant elements in order to verify whether, during that period, the employee is free from any obligation towards the employer and can dispose of his time according to his own will: §1. Initiative, responsibility for organisation and purpose of the work

From the point of view of human resources theory, team building activities are by nature some organised by the employer in his own interest, on his initiative, essentially to increase the efficiency of employee teams. Their organisation can be systematic, planned and with an allocated or sporadic budget, depending on the needs and funding possibilities. As a result, it is necessary to check whether the place, date and manner of organisation are required by the employer.

A relevant element may be the source of the financing of those activities and the accounting regime applied by the employer himself, which is relevant to the administrativefiscal case-law. However, this must be analysed in the broader context of the other relevant factors, since sometimes expenses for apparently team building activities form part of a system of rewards consisting of trips and excursions, in order to evade the tax on income of a salary nature, as is apparent from the court ruling in a case in which the employee responsible was penalised disciplinaryly for that practice 27 . §2.

Mandatory nature of participation

This character should be checked in the least restrictive manner possible. Thus, there is no need for a formal provision of the employer for the participation of employees in that activity, and there may also be a mere invitation or notice. It must be verified, however, whether the non-participation in these activities has consequences for the employment relationship, such as the situation in which it is relevant in the context of a professional evaluation, promotion process, or leads to the conclusion that the employee concerned does not have the skills and competences the improvement of which has been sought through team-building actions, with effects of the same type. The binding nature may also result from factual aspects leading to the conclusion that non-participation in such activities leads to pressure on the employee or mobbing actions. A fortiori is binding when the non-participation, leaving the activity or acts committed during that activity entail disciplinary liability.

Such an analysis may be facilitated by the existence of internal regulations of the employer. For example, it follows from the content of a judgment of the French Court of Cassation that a corporate culture suggestively called "fun & pro" was formally implemented at the level of a company, implying the obligation of employees to attend seminars and celebrating employer's achievements; the refusal to participate in these events, together with the imputation of communication deficiencies in the employment relations, was the reason for the dismissal of the employee concerned; the French court annulled the dismissal decision on the ground that the obligation to participate in those activities organised by the employer infringed the employee's freedom of expression but correlated with the finding that the employer encouraged promiscuity, excesses, including alcohol consumption and intimidation of employees during those festivities28 . Therefore, the possibility that participation in such activities would be binding was not ruled out in the present case, since the decision to annul the dismissal decision was based rather on the justified nature of the refusal to participate; however, even in such a case, when the employee accepts the way the team-building activities are carried out, if participation is mandatory and the refusal attracts disciplinary responsibility, the time affected should be considered as working time.

V. Conclusions

Therefore, when and if team-building activities are imposed on employees by the employer, in terms of time, place and organization, pursuing employer's own aim of improving employment relationships, workers being at the employer's disposal, without being able to freely dispose of the time declared as rest time and to devote themselves to their own interests, the time allocated to those activities should be regarded as working time within the meaning of Directive 2003/88, that is to say, for the sole purpose of protecting health and safety at work.

In the light of Articles 111 and 120 of the Romanian Labor Code, the time allocated to participating in team-building activities cannot be included in the working time taken into

  12 C.A.Cluj, S. III c.a.f., Dec. 534/10 March 2017 (www.rolii.ro); 13 As follows from C.A.Ploiesti, S. II c.a.f., judgment No 214/5 December 2017 (www.rolii.ro) 14 HCCJ, S. c.a.f., Dec. No 4206/19 November 2008 (www.scj.ro) 15 HCCJ, S. c.a.f., Dec. No 5041/18 April 2013 (www.scj.ro)

  is worth noting that, in the same case, by a previous decision19 , which quashed the sentence of the court of first instance and referred the case back to it, it was noted in the statement of the facts that '[t]he documents in the file (declarations of the injured party, the16 As it follows from the Trib. Bucharest,S. VIII, c.m.a.s., Judgment No 7792 of 1 October 2012 (www.rolii.ro);

17

As follows from C.A. Suceava, S.I. Civ., Dec. 726 of 13 November 2014; in the present case, the dismissal decision was annulled because the employer did not summon the employee to carry out the disciplinary investigation, without further examination of the merits of the case, the employer relying on the existence of other unreasoned absences (www.rolii.ro);

18

C.A. Bucharest -S. II pen, Dec. No 786/A/18 June 2014 (www.rolii.ro) 19 C.A. Bucureşti, S. I pen., Dec. no. 573/27 March 2013 (www.rolii.ro)

Cass. Soc.,

November 2022, 21-15.208, FR:CCASS:2022:SO01164 (published 'https://www.legifrance.gouv.fr/juri/id/JURITEXT000046555948', accesed 26.11.2022);

account when quantifying the remuneration and those activities cannot be considered as additional work either.

If team-building activities overlap with professional training activities carried out outside the locality where the place of work is located, they follow their regime and that of travel for the purpose of work 29 .


Manon Marquet
email: manon.marquet@ap-hm.fr

Julie Blanc

Claude D'ercole

Xavier Carcopino

Florence Bretelle

Antoine Netter

Does a physiology-based interpretation of cardiotocography allow to dispense with second-line methods? A cross-sectional online survey

Keywords:

Context:

Second line methods are used to help obstetricians to identify abnormalities that reflect foetal acidosis. Since the use of a new technique of cardiotocography (CTG) interpretation based on the pathophysiology of the foetal period, the use of second-line tests has been questioned. Objective: To evaluate the impact of specific training in CTG physiology-based interpretation on professional attitudes towards the use of second-line methods. Methods: This cross-sectional study included 57 French obstetricians divided into two groups: the trained group (obstetricians who had already participated in a training course in physiology-based interpretation of CTG) and the control group. Ten medical records of patients who had abnormal CTG tracings and underwent foetal blood sampling pH measurement during labour were presented to the participants. They were given three choices: use a second-line method, continue labour without using second-line method, or perform a caesarean section. The main outcome measures was the median number of decisions to use second-line method.

Results: Forty participants were included in the trained group and 17 in the control group. The median number of recourses to second-line method was significantly inferior for the trained group (4/10 s-line methods) than for the control group (6/10, p = 0.040). Regarding the 4 records for which a caesarean section was the real outcome, the median number of decisions of continuing labour was significantly superior in the trained group than in the control group (p = 0.032). Conclusions: Participation in a training course in physiology-based interpretation of CTG could be associated with a less frequent use of second-line method at the cost of more frequently continuing labour with the risk compromising foetal and maternal well-being. Additional studies are required to determine whether this change in attitude is safe for the foetal well-being.

Introduction

Electronic foetal monitoring was invented in the 1960s, and cardiotocography (CTG) has since become the primary means of monitoring foetal well-being during labour in developed countries [START_REF] Hon | Observations on fetal heart rate and fetal biochemistry: I. Base deficit[END_REF][START_REF] Ayres-De-Campos | Electronic fetal monitoring or cardiotocography, 50 years later: what's in a name?[END_REF]. CTG interpretation has an excellent negative predictive value but carries the drawback of a mediocre positive predictive value [START_REF] Fleischer | The development of fetal acidosis in the presence of an abnormal fetal heart rate tracing. I. The average for gestational age fetus[END_REF]. Thus, the interpretation of an abnormal CTG is challenging, and misinterpretations are frequent with the implicit risk of performing excessive operative deliveries or conversely, to wrongly abstain from an intervention that would have been necessary to preserve foetal well-being [START_REF] Nelson | Uncertain value of electronic fetal monitoring in predicting cerebral palsy[END_REF][START_REF] Parer | Fetal heart rate monitoring: is it salvageable?[END_REF]. CTG is therefore an imperfect tool to be used alone to make decisions with potentially serious consequences, often in emergency situations. In this context, second-line methods have found their use in cases of abnormal CTG and they allow us to differentiate abnormalities that reflect foetal acidosis from those that do not have an impact on foetal well-being [START_REF] Haverkamp | A controlled trial of the differential effects of intrapartum fetal monitoring[END_REF].

This rationale has recently been challenged. Some authors have suggested that foetal monitoring does not inherently have a low positive predictive value and that its diagnostic performance could be improved by a paradigm shift in its interpretation [START_REF] Ugwumadu | Are we (mis)guided by current guidelines on intrapartum fetal heart rate monitoring? Case for a more physiological approach to interpretation[END_REF]. Their claim is that CTG should not be interpreted on a pattern recognition basis but with a pathophysiological approach instead to identify the characteristics of the compensatory response of the foetus [START_REF] Chandraharan | Handbook of CTG interpretation: from patterns to physiology[END_REF][START_REF] Turner | The physiology of intrapartum fetal compromise at term[END_REF][START_REF] Lear | Understanding fetal heart rate patterns that may predict antenatal and intrapartum neural injury[END_REF]. Indeed, traditionally, the interpretation of the CTG is taught by learning distinct criteria of concern (baseline heart rate, absence of accelerations, short-term variability, presence of decelerations) and by the recognition of different patterns of decelerations (early, variable or late; typical or atypical) [START_REF] Ingemarsson | Fetal heart rate monitoring[END_REF]. The new paradigm is based on pathophysiology studies, especially in animals, and promotes the teaching of explanations of the foetal response to various phenomena occurring during labour [START_REF] Chandraharan | Handbook of CTG interpretation: from patterns to physiology[END_REF][START_REF] Lear | Peripheral chemoreflex control of fetal heart rate decelerations overwhelms the baroreflex during brief umbilical cord occlusions in fetal sheep[END_REF]. One of the main purposes of this method is to differentiate between tracings that correspond to a physiological adaptation of the foetus and those that have a decompensatory meaning and require immediate operative deliveries. The underlying implicit goal is to sufficiently improve the positive predictive value of the CTG interpretation to dispense with second-line methods [13 -15]. Since 2017 and the publication of the "Handbook of CTG Interpretation: From Patterns to Physiology", this method of interpretation has been widely promoted, particularly through specific training courses [START_REF] Chandraharan | Handbook of CTG interpretation: from patterns to physiology[END_REF]. Recent literature suggests that this type of analysis has a highest discrimination capacity for neonatal acidaemia than the others CTG guidelines [START_REF] Del Pozo | Diagnostic capacity and interobserver variability in FIGO, ACOG, NICE and Chandraharan cardiotocographic guidelines to predict neonatal acidemia[END_REF]. However, there are no existing studies to determine the value of these teachings on clinical decision-making.

The objective of this study was to evaluate the impact of specific training in CTG physiology-based interpretation on professional attitudes towards the use of second-line methods.

Methods

Study design and participants

We conducted a national cross-sectional study based on an online survey. French obstetricians were invited to participate during congresses and through national networks. Participants could be licenced obstetricians or specialized residents in their fourth year or higher and were required to have had regular practice in obstetrics in the previous year. This study was approved by the local ethics committee (Aix-Marseille University 2021-04-08-06).

Questionnaire

The questionnaire was divided into two parts: The first part included questions about the participant: level of experience, place of work, frequency of use of second-line methods in the maternity hospital where he worked (frequent or infrequent), participation in specific training in physiology-based CTG interpretation and the type of training.

The second part focused on clinical cases. Ten medical records of patients who delivered in our unit and for whom foetal scalp blood sampling was performed during labour were presented with the following information: medical history, notable events during pregnancy, detailed description of the labour with a partograph and CTG. If the complete CTG was too long to be transmitted in its entirety, CTG at the beginning of labour and then at the onset of CTG abnormalities was transmitted. Patients gave their consent for the use of anonymized data from their records. All presented information was anterior to the decision to perform foetal scalp blood sampling: information about what happened after this decision was hidden from the participants on the partograph and the CTG. For each medical record, the participants were given three options: (i) perform a second-line method, (ii) continue labour without performing second-line method, or (iii) perform a caesarean section without performing second-line method.

After completion of the questionnaire, the participants received an email in which the real outcomes (foetal scalp blood sampling, mode of delivery, neonatal status) were presented for each medical record. They could not modify their answers after their completion of the questionnaire.

Selection of medical records

Ten medical records of term pregnant women who delivered in our unit between 2019 and 2020 and presented CTG abnormalities for whom FBS was used were carefully selected amongst forty records. Four reviewers were involved in this selection process and had access to the entire record (before and after foetal scalp blood sampling, including the neonatal status). The four reviewers were experienced obstetricians, including one expert in the court.

They were given the same instructions: For patients for whom a caesarean section was performed, the record could be retained only if the foetal scalp blood sampling was less than 7.20 and if the reviewers deemed that caesarean section was the only reasonable decision to preserve foetal well-being. The record could not be retained if one or more reviewers deemed that another reasonable solution existed to avoid or delay a caesarean section (e.g., begin expulsive efforts, modify oxytocin administration). According to these criteria, four records of patients for whom a caesarean section was performed after foetal scalp blood sampling were retained and presented to the participants.

For patients who had a vaginal delivery, the record could be retained only if the foetal scalp blood sampling was greater than 7.20, if the delivery occurred at least one hour after the foetal scalp blood sampling and if the reviewers deemed that continuing the labour had been a reasonable decision based on the neonatal status. According to these criteria, six records were selected.

The four reviewers had to agree that a medical record met the required criteria for it to be selected. In any case of disagreement amongst the reviewers, the medical record was not retained for presentation. Their judgement was based on the entire medical record, including the neonatal status after delivery.

Groups and endpoints

The participants were divided into two groups: the trained group (obstetricians who participated in a training course in physiologybased interpretation of CTG) and the control group (no participation in such a course declared).

The primary endpoint was the difference between groups in the median number of second line method that the participants would have performed.

The secondary endpoints were the median number of decisions to continue labour without second-line method when the real outcome was a caesarean section and the median number of decisions to perform a caesarean section when the real outcome was a vaginal delivery.

Statistical analyses

The number of participants was calculated to detect an arbitrary median difference between groups of one recourse to second-line method amongst the ten presented records. Given a two-sided test with 90% statistical power and 95% confidence interval (CI), 44 participants needed to be included. Based on this number and with the assumption that 10 to 15 more obstetricians would agree to participate after each monthly reminder, we decided to allow access to the online questionnaire for four months (July to October 2020).

Professional characteristics of the participants and attitudes towards the presented cases were compared between the two groups. Qualitative variables are presented as counts (percentages) and were compared between groups using the x 2 test or Fisher's exact test when appropriate. Continuous variables are presented as the median (interquartile range [IQR]) and were compared using Student's t-test or the Mann-Whitney U test when appropriate.

All of the statistical analyses were two-tailed, and the results were taken to be statistically significant when P values <0.05 were obtained. The analyses were performed using IBM SPSS Statistics version 20.0 (IBM Corporation, Armonk, New York, US).

Results

Characteristics of the participants

The participants' characteristics are reported in Table 1. Fiftyseven obstetricians answered the questionnaire: 40 had already participated in specific training in physiology-based CTG interpretation and were included in the trained group, and 17 participants were included in the control group. The level of experience was the same in both groups (p = 0.623). The majority of participants were residents (in their fourth year or higher) and worked in a university hospital. Participants in the trained group either participated in a twoday master class (27.5%), had a shorter training course (72.5%) or read a book on physiology-based CTG interpretation (25.0%). Fifty percent of the participants of the trained group followed least two different types amongst the aforementioned trainings. Most of the participants in the trained group declared using this teaching in their daily practice (95.0%).

Attitudes towards clinical cases

The participants' decisions towards the clinical cases are summarized in Table 2. amongst the ten medical records, the median number of recourses to second-line method was significantly inferior for the trained group (4 [START_REF] Ayres-De-Campos | Electronic fetal monitoring or cardiotocography, 50 years later: what's in a name?[END_REF][START_REF] Fleischer | The development of fetal acidosis in the presence of an abnormal fetal heart rate tracing. I. The average for gestational age fetus[END_REF][START_REF] Nelson | Uncertain value of electronic fetal monitoring in predicting cerebral palsy[END_REF][START_REF] Parer | Fetal heart rate monitoring: is it salvageable?[END_REF][START_REF] Haverkamp | A controlled trial of the differential effects of intrapartum fetal monitoring[END_REF] second-line method on 10 records) than for the control group (6 [4-7]; p = 0.040). The median number of decisions to continue labour without using second-line method was significantly superior in the trained group than in the control group (3 [2-5] vs. 2 [START_REF] Hon | Observations on fetal heart rate and fetal biochemistry: I. Base deficit[END_REF][START_REF] Ayres-De-Campos | Electronic fetal monitoring or cardiotocography, 50 years later: what's in a name?[END_REF][START_REF] Fleischer | The development of fetal acidosis in the presence of an abnormal fetal heart rate tracing. I. The average for gestational age fetus[END_REF]; p = 0.015). The median number of decisions to perform a caesarean section without using second-line method was similar between groups (2 [START_REF] Hon | Observations on fetal heart rate and fetal biochemistry: I. Base deficit[END_REF][START_REF] Ayres-De-Campos | Electronic fetal monitoring or cardiotocography, 50 years later: what's in a name?[END_REF][START_REF] Fleischer | The development of fetal acidosis in the presence of an abnormal fetal heart rate tracing. I. The average for gestational age fetus[END_REF][START_REF] Nelson | Uncertain value of electronic fetal monitoring in predicting cerebral palsy[END_REF] vs. 2 [1-3.5]; p = 0.788). amongst the 4 records for which a caesarean section was in fact performed after the foetal scalp blood sampling, the median number of decisions of continuing labour without using second-line method was significantly superior in the trained group than in the control group (1 [0 -1] decision of continuing labour on 4 records vs. 0 [0-1]; p = 0.032). amongst the 6 records for which the patient actually delivered vaginally after the result of the foetal scalp blood sampling, the median number of decisions of performing a caesarean section without using second-line method was not significantly different between groups (0 [0-2] caesarean sections on 6 records vs. 1 [0-2]; p = 0.641). amongst 4 records for which the result of foetal scalp blood sampling was superior to 7.30, the median number of decisions to perform second-line method was not significantly different for both groups (0 [0 -1] vs. 0 [0-1]; p = 0.921).

Examples of medical records

The description of the medical records with the answers from the participants can be found in Table 3. We also provide a detailed description of the two medical records for which the rates of inconsistent answers with regard to the real outcome were the greatest (Fig. 1):

Medical Record #7: A 24-year-old woman, gravida 1, para 0, presented at 38 weeks of gestation with oligohydramnios and decreased active foetal movements in the setting of gestational diabetes with foetal macrosomia (estimated foetal weight above the 99th percentile). Induction of labour was achieved with oxytocin under epidural anaesthesia. CTG abnormalities appeared at 9 cm of cervical dilatation and led to foetal scalp blood sampling (Fig. 1a). The result was 7.27, and the obstetrician decided to continue labour with iterative foetal scalp blood sampling. One hour after the first sampling, the patient vaginally delivered a 3800 gram newborn boy. The Apgar scores were 10, 10, and 10 at 1, 5 and 10 min, respectively, and the umbilical cord pH was 7.17.

Regarding this medical record, 42% of participants decided to perform a caesarean section without using second-line method (38% of the participants in the trained group and 53% of the participants in the control group). Only 3 participants (7%) from the trained group decided to continue labour without using second-line method, and no participant from the control group decided to continue labour.

Medical Record #9: A 38-year-old woman, gravida 1, para 0, presented in labour at 39 gestational weeks in the setting of gestational diabetes without foetal macrosomia. CTG abnormalities appeared at 6 cm of cervical dilatation and led to foetal scalp blood sampling (Fig. 1b). The result was 7.16, and the obstetrician decided to perform a caesarean section. The newborn boy weighed 2605 gs and had Apgar scores of 8, 9, and 9 at 1, 5 and 10 min, respectively, with an umbilical cord pH of 7.14. He was admitted to the neonatal intensive care unit for respiratory distress and required continuous positive airway pressure for 24 h. Regarding this medical record, 47% of participants would have decided to continue labour without using second-line method (55% of the participants in the trained group and 29% of participants in the control group). Only two participants (5%) from the trained group would have chosen to perform a caesarean section without using a second-line method, and one from the control group (6%) would have chosen to perform a caesarean section.

Discussion

Interpretation of main findings

To date and to our knowledge, this is the first study to evaluate the influence of specific training in physiology-based CTG Abbreviations: # = number of the medical record; GW= Gestational weeks V = Vaginal delivery; C = cesarean section; 2nd Line = Second line method; Continue = Continuing labor without a second line method; cesarean = cesarean section without a second line method. interpretation on professional attitudes towards recourse to secondline method. Our results suggest that obstetricians who underwent this type of training would less often decide to use second-line method when confronted with CTG abnormalities. This advantage would come at the cost of more often deciding to continue labour in situations that would have required a caesarean section to preserve neonatal well-being. Conversely, the obstetricians who did not undergo this training did not seem to opt more often for a caesarean section when the patient actually delivered vaginally.

Strengths and limitations

The main strength of this study was the careful selection of medical records. Ten medical records were selected amongst forty others by four reviewers, including one expert in court. Clear instructions were given beforehand to the reviewers to only retain records whose outcome was unequivocal. In other words, the four reviewers had to agree that the actual mode of delivery (either a caesarean section or a vaginal delivery) was the best possible outcome in the clinical context with knowledge of the entire medical record, including the results of the foetal scalp blood sampling and the neonatal status. This rigorous selection process legitimises the claim that choosing an alternative mode of delivery without using second-line method and pH estimation would at least result in a nonoptimal outcome for the patient or her newborn. The exhaustive and careful presentation of all the information necessary for the participants to make a decision should also be emphasized. Real CTGs were presented either entirely since the beginning of labour or partially since before the beginning of CTG abnormalities (when the tracings exceeded three hours). Hence, this online questionnaire allowed an original simulation of real clinical situations, and we believe that it is a reliable evaluation of the participants' professional attitudes.

However, several considerations mitigate the conclusions that can be drawn from the results of this study. Despite the aforementioned precautions, it is impossible to assert with absolute certainty the outcome of an alternative scenario. Although we consider it unlikely, it is not formally impossible that amongst the 4 records that resulted in a caesarean section, one or more records could have ended differently. Several participants also pointed out that reducing the choice to three options was too restrictive and did not give a fair representation of reality. In particular, it is possible that some participants would have opted to continue labour only for some time before ultimately performing a caesarean section or a second-line method . Similarly, some participants suggested that other options were available, such as positioning the patient differently or stopping oxytocic administration. As stated before, although four reviewers deemed that the actual outcome was the best possible option, alternative scenarios cannot formally be excluded.

In addition, there is no way of verifying that the participants would have actually made the stated decision in a real-life situation. It is possible that the context of the anonymous questionnaire, devoid of any stress related to the consequences and presented as a test, encouraged participants to take more risks in their decision-making. It is also worth mentioning that the majority of the participants of this online survey were residents. Although we only included residents in their fourth year or higher who are ordinarily already selfreliant in obstetrical decision-making, we can hardly extrapolate the results to more experienced physicians.

Furthermore, all modes of training for the CTG physiology-based interpretation were placed on an equal footing in the trained group. The number of participants was insufficient to provide subgroup analysis for each type of training. Although the vast majority of the participants from the trained group declared that they used the precepts of CTG physiology-based interpretation in their daily practice, it is possible that our results are biased by the insufficient training of some participants.

Validity of results

The underlying goal of physiology-based CTG interpretation is to dispense with second-line methods14,15. In a 2014 review, Edwin Chandraharan pointed out the absence of evidence supporting second-line method during labour13. This critique was enriched with a detailed list of pathophysiological inconsistencies associated with the use of this test; in particular, a sample of blood from nonessential peripheral tissue (foetal scalp) is being used to assess the acid-base status of essential central organs. His-conclusion was that foetal scalp blood sampling was an outdated practice and that it should no longer be recommended. This review provoked a debate amongst various authors whose responses were just as interesting as the original article, essentially discussing the pathophysiological basis of foetal scalp blood sampling [START_REF] Steer | Fetal scalp blood sampling during labour: is it a useful diagnostic test or a historical test which has no longer a place in modern clinical obstetrics[END_REF][START_REF] Nzewi | Fetal scalp blood sampling during labour: is it a useful diagnostic test or a historical test that no longer has a place in modern clinical obstetrics?[END_REF][START_REF] Sholapurkar | Re: fetal scalp blood sampling during labour: is it a useful diagnostic test or a historical test that no longer has a place in modern clinical obstetrics [corrected]?[END_REF]. These expert debates are enlightening, but no pathophysiological analysis can ever replace the evidence provided by a well-conducted clinical study. Since 2014, despite this article, which should have encouraged research on this matter, little has been done to demonstrate the usefulness of second-line methods, which are still widely used despite this lack of evidence [START_REF] Wattar | Evaluating the value of intrapartum fetal scalp blood sampling to predict adverse neonatal outcomes: a UK multicentre observational study[END_REF][START_REF] East | The addition of fetal scalp blood lactate measurement as an adjunct to cardiotocography to reduce caesarean sections during labour: the Flamingo randomised controlled trial[END_REF].

The same reasoning could easily be applied to physiology-based CTG interpretation training. There is no doubt that pathophysiological teaching leads to a deeper understanding of medical phenomena and should be encouraged. Recent studies showed that training programmes based on foetal physiology led to a long-term improvement in CTG interpretation and to homogenization of obstetrical decisions in simulated situations [START_REF] Dupuis | Evaluation and impact of fetal physiology training on fetal heart rate analysis[END_REF][START_REF] Zhu | Fetal physiology cardiotocography training, a regional evaluation[END_REF]. However, there is a strong need for clinical evidence regarding the teaching of this method before totally discouraging second-line methods. As suggested by our results, overconfidence in the interpretation of CTG could lead to wrong decisions and it should therefore be taught with humility and by stressing the importance of being cautious when in doubt. The present article is up to date and, to our knowledge, is the only attempt to analyse the effect of physiology-based CTG interpretation training on obstetrical practice. Although our work is clearly insufficient on its own to substantiate the benefits or shortcomings of this teaching, it does have the merits of raising the issue of the lack of evidence and should encourage further research.

Conclusions

Our results suggest that participation in a training course in physiology-based interpretation of CTG could be associated with a less frequent use of second-line method at the cost of more frequently continuing labour with the risk compromising foetal and maternal well-being. Neither this study nor the current state of the literature allows us to recommend abandoning second-line methods in favour of an enhanced CTG interpretation. The same methodology could be used on a larger scale to confirm or refute these results.

Fig. 1 .

 1 Fig. 1. Examples of medical records. Left side: Partograph; Right side: Cardiotocograph. 1A: Medical Record #7 before foetal scalp blood sampling. The result was 7.27, and the obstetrician decided to continue labour with iterative foetal scalp blood sampling. The patient delivered vaginally. 1B: Medical Record #9 before the foetal scalp blood sampling. The result was 7.16, and the obstetrician decided to perform a caesarean section. The newborn was admitted to the neonatal intensive care unit for respiratory distress and required continuous positive airway pressure for 24 h.

Table 1

 1 Characteristics of the participants.

		Control group Training group P value
		n = 17	n = 40
	Level of experiences, n/N (%)		0.623
	Residents	13/17 (76.5%) 26/40 (65.0%)
	Fellow	2/17 (11.8%)	5/40 (12.5%)
	Attending physician	2/17 (11.8%)	9/40 (22.5%)
	Place of work, n/N (%)		0.802
	University hospital	14/17 (82.4%) 34/40 (85.0%)
	Public Hospital	3/17 (17.6%)	6/40 (15.0%)
	Frequent use of second-line methods	12/17 (70.6%) 30/40 (75.0%)
	in the maternity, n/N (%)
	Type of CTG-training, n/N (%)
	CTG Masterclass (2 days)	-	11/40 (27.5%)
	Other shorter training (less than a	-	29/40 (72.5%)
	day)
	Reading the book "CTG	-	10/40 (25.0%)
	interpretation"
	Date of the CTG-training, n/N (%)		-
	More than 6 months	-	30/38 (78.9%)
	Less than 6 months	-	8/38 (21.1%)
	Use of the precepts taught in the	-	38/40 (95.0%)
	CTG-training in current practice

Table 2

 2 Comparison of attitudes towards clinical cases between the two groups.

		Control group Training group P value
		n = 17	n = 40
	Responses to the ten clinical cases,
	median (IQR)
	Continue labour without using a	2 (1 -3)	3 (2 -5)	0.015*
	second-line method
	Perform a second-line method	6 (4 -7)	4 (2 -6)	0.040*
	Perform a caesarean section with-	2 (1 -3.5)	2 (1 -4)	0.788
	out using a second-line method
	Attitudes inconsistent with the real
	outcome, median (IQR)
	Caesarean section when the real	1 (0 -2)	0 (0 -2)	0.641
	outcome was a vaginal delivery (6
	medical records)
	Continuing labour when the real	0 (0 -1)	1 (0 -1)	0.032*
	outcome was a caesarean section
	(4 medical records)
	Cumulative inconsistent attitudes	1 (0,5 -2)	1 (1 -3)	0.490
	(10 medical records)
	Attitudes consistent with the real
	outcome, median (IQR)
	Caesarean section when the real	2 (0 -2)	2 (1 -2)	0.641
	outcome was a caesarean section
	(4 medical records)
	Continuing labour when the real	2 (0.5 -2)	2.5 (1 -4)	0.042*
	outcome was a vaginal delivery (6
	medical records)
	Cumulative consistent attitudes	3 (2 -4)	4 (2 -6)	0.039*
	(10 medical records)
	Second-line method performed	0 (0 -1)	0 (0 -1)	0.921
	when the pH was ≥ 7,30 (4 medi-
	cal records), median, IQR

* p <0.050.

Table 3

 3 Description of the medical records and detailed answers from the participants.

	#	Age,	Parity, n Gestational	Cervical	scalp pH Actual	Answers from all participants, n/N (%)	Answers from the training group, n/N (%) Answers from the control group, n/N (%)
		years		age, GW	dilatation,		outcome
					cm
								2nd Line	continue	caesarean	2nd Line	continue	caesarean	2nd Line	continue	caesarean
	1	38	0	39	8	7.35	V	35/57 (62%) 19/57 (33%) 3/57 (5%)	22/40 (55%) 16/40 (40%) 2/40 (5%)	13/17 (76%)	3/17 (18%)	1/17 (6%)
	2	34	0	40	6	7.19	C	21/57 (37%) 5/57 (9%)	31/57 (54%) 13/40 (33%) 4/40 (10%)	23/40 (57%) 8/17 (47%)	1/17 (6%)	8/17 (47%)
	3	38	0	41	9	7.29	V	23/57 (40%) 33/57 (58%) 1/57 (2%)	12/40 (30%) 27/40 (67%) 1/40 (3%)	11/17 (65%)	6/17 (35%)	0/17 (0%)
	4	18	0	39	9	7.31	V	25/57 (44%) 21/57 (37%) 11/57 (19%) 17/40 (42%) 14/40 (35%) 9/40 (23%)	8/17 (47%)	7/17 (41%)	2/17 (12%)
	5	32	0	40	9	7.35	V	19/57 (33%) 27/57 (48%) 11/57 (19%) 12/40 (30%) 22/40 (55%) 6/40 (15%)	7/17 (42%)	5/17 (29%)	5/17 (29%)
	6	30	0	38	4	7.17	C	25/57 (44%) 5/57 (9%)	27/57 (47%) 16/40 (40%) 4/40 (10%)	20/40 (50%) 9/17 (53%)	1/17 (6%)	7/17 (41%)
	7	24	0	38	9	7.27	V	30/57 (53%) 3/57 (5%)	24/57 (42%) 22/40 (55%) 3/40 (7%)	15/40 (38%) 8/17 (47%)	0/17 (0%)	9/17 (53%)
	8	25	0	38	8	7.16	C	27/57 (47%) 2/57 (4%)	28/57 (49%) 17/40 (42%) 2/40 (5%)	21/40 (52%) 10/17 (59%)	0/17 (0%)	7/17 (41%)
	9	38	0	39	6	7.16	C	27/57 (47%) 27/57 (47%) 3/57 (5%)	16/40 (40%) 22/40 (55%) 2/40 (5%)	11/17 (65%)	5/17 (29%)	1/17 (6%)
	10	35	3	40	7	7.33	V	29/57 (51%) 27/57 (47%) 1/57 (2%)	19/40 (47%) 20/40 (%)	1/40 (3%)	10/17 (59%)	7/17 (41%)	0/17 (0%)

Acknowledgements

We thank Mr. D'Ercole and Mr. Carcopino for having accepted that this work be carried out within their service. We thank Mr. Netter and Mrs. Blanc for helping us to choose the files to use. Mr. D'Ercole and Ms. Bretelle subsequently corrected the questionnaire.

Ms. Marquet wrote the questionnaire and took care of its distribution, and Mr. Netter and Ms. Blanc carried out the statistical analyses.

Ms. Marquet and Mr. Netter wrote the final paper and all the coauthors helped to edit the final paper.

Funding information, financial and maternal support None

Declaration of Competing Interest

The authors declare no conflict of interest related to this study.