Use of a hysterometer to measure the head–perineum distance before an operative delivery: a prospective study

Use of a hysterometer to measure the head–perineum distance before an operative delivery: a prospective study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Use of a hysterometer to measure the head–perineum distance before an operative delivery: a prospective study Thibaud Quibel, Marion Chesnais, Marie-Anne Joly, Lea Tettamanti, and 6 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-7603641/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Introduction: Many studies have investigated the contribution of transperineal ultrasound in determining the fetal head station during the management of the second stage of delivery. The head–perineum distance (HPD) remains 1 of the most studied measures.We hypothesized that a HPD measured “clinically” with a hysterometer might correlate with that measured by transperineal ultrasound and could be used to predict the risk of cesarean delivery. STUDY DESIGN: This was a unicentric prospective observational study that occurred between February 10, 2022, and June 30, 2024. Women with a singleton fetus in the cephalic presentation at term (≥37 weeks of gestation) who had an operative delivery (vaginal operative birth or cesarean delivery during the second stage) were eligible for this study. Women were included during the second stage if an operative delivery was expected. The HPD was measured using 2 devices: transperineal ultrasound (HPDus) and a hysterometer (HPDhys). Correlations and agreement were calculated, and receiver-operating characteristic curve analysis was conducted to evaluate the performance of each method in predicting cesarean delivery. RESULTS The final population comprised 671 women who underwent both HPDhys and HPDus. Pearson correlational analysis showed good agreement between both methods: r = .85 (95% confidence interval [CI] .84–.88). Correlations were independent of the level of the fetus head station and head position. The area-under-the-curve values were high for both methods: 0.87 (95% CI 82.8–92.1) for clinical HPDhys and 0.83 (95% CI 0.78–0.89) for HPDus ( P = .006). CONCLUSIONS HPD measured with a hysterometer is accessible to all practitioners and correlates well with HPD measured with transperineal ultrasound. HPD has potential as a tool to help clinicians select the appropriate indications for instrumental deliveries. It is hoped that this easily accessible technique will be used widely, especially in countries where ultrasound resources may be limited. Further studies are needed to confirm the results of this study. Health sciences/Health care Health sciences/Medical research cesarean delivery head–perineum distance hysterometer transperineal ultrasound Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction Studies have highlighted the decline in the use of vacuum delivery in favor of cesarean delivery performed during the second stage of labor. 1 – 3 These findings are concerning given the potential complications of a cesarean delivery performed during the second stage of labor. 4 , 5 The fear of vacuum extraction failure, which is associated with an increase in maternal and perinatal morbidity, may explain this decline in its use. 6 Vaginal examination remains the key assessment for deciding on the need for an operative vaginal birth or cesarean delivery in the second stage of labor in cases involving a prolonged second stage of labor or suspicion of immediate or potential fetal compromise. This examination can be used to determine the fetal head position and head station. However, the significant variability in determining the head position and station has led professional societies to recommend supplementing the examination with an ultrasound to determine the fetal position accurately before performing an operative vaginal birth. 7 ,- 11 Since the publication of Kalache et al in 2009, transperineal ultrasound during the second stage of labor has emerged as a promising tool for predicting failed operative vaginal birth or cesarean deliveries. 12 – 14 The contribution of transperineal ultrasound in determining the fetal head station during second-stage management has been reported 15 , 16 , and the head–perineum distance (HPD) remains 1 of the most studied methods. A recent meta-analysis involving 6 studies that examined the ability of HPD to predict the success of vaginal delivery highlighted this measurement as a useful predictor 17 . The use of ultrasound in the labor ward may be limited by local resources and the lack of training of some physicians. Here, we hypothesized that the HPD measured “clinically” with a hysterometer might correlate with that measured by transperineal ultrasound. We also hypothesized that HPD measured with a hysterometer could be used to predict a cesarean delivery as well as HPD measured transperineally when an expeditive delivery is expected. Materials and methods This was a prospective observational study that occurred between February 10, 2022, and June 30, 2024 at the University Maternity of Poissy Saint-Germain, Poissy, France. The ethics committee (Comité de Protection des Personnes OUEST III, France) approved the study protocol (number LL/JT/FB/2021/147). All participants provided written informed consent. Eligibility criteria Women with a singleton fetus in the cephalic presentation at term (≥37 weeks of gestation) who had an operative delivery (vaginal operative birth or cesarean delivery during the second stage) were eligible for inclusion in this study. Women were included if, during the second stage, an operative delivery was expected, and the HPD was measured using both devices: transperineal ultrasound (HPDus) and hysterometer (HPDhys). The exclusion criteria were multiple pregnancy, noncephalic presentation, spontaneous vaginal delivery, suspicion of immediate or potential fetal compromise, lack of use of epidural anesthesia, and lack of both HPD measurements. Local procedures When a prolonged second stage of labor was diagnosed, the caregiver was asked to perform the vaginal examination by measuring the HPD with a single-use hysterometer, which was introduced horizontally (coronal plane) until it touched gently against the fetal skull scalp.(Fig. 1 ) The HPD was defined as the shortest distance from the outer bony limit of the skull to the perineum. The fetal head station was assessed clinically by digital vaginal examination according to the classification of the American College of Obstetricians and Gynecology and in relation to the outlet (i.e., high, mid, or low). Suprapubic ultrasound was then performed before considering or performing instrumental delivery. The HPD was then measured using the transverse transperineal approach from the fetal skull to the transducer as described by Eggebo. 18 The sonographer was blinded to the HPD measured with the hysterometer. Operative deliveries were performed by residents under the supervision of the attending obstetrician. Local policy recommends use of a vacuum extractor as the instrument of first choice when an operative vaginal delivery is indicated. If vacuum extraction fails, the attending senior obstetrician must choose between using forceps or performing a cesarean delivery. The following demographic and obstetric data were recorded prospectively: maternal age, parity, prepregnancy body mass index, and history of a previous cesarean delivery; gestational age at delivery; mode of onset of labor (spontaneous or induced labor); duration of the second stage of labor; clinical station of the fetal head; failed vacuum extraction; final mode of delivery (forceps or cesarean); mediolateral episiotomy; and neonatal weight. Ultrasound data for fetal head position on ultrasound and angle of progression were recorded. Data on the following maternal and neonatal morbidity outcomes were collected: maternal anal sphincter injury and postpartum hemorrhage; 5-min Apgar score < 7; arterial cord pH < 7.10 at delivery; and newborn birthweight. Statistical analysis Qualitative variables are presented as the percentage and absolute count. Continuous variables are presented as the median and interquartile range or as the mean and standard deviation (SD), depending on the distribution of the data. For comparisons of qualitative variables between groups, the chi-squared test or Fisher’s exact test was used as appropriate. Continuous variables were compared using Student’s t test for normally distributed data or the Mann–Whitney U test for nonnormally distributed data. To identify correlations between the measurements, Pearson or Spearman correlational analysis was used depending on whether the data were normally distributed. The agreement of both methods was visualized using the Bland–Altman plot, 19 in which 2 additional horizontal lines representing the limits of agreement at ±1.96 SDs from the mean difference were included to represent the range within which 95% of the differences should fall if the 2 methods are in agreement. Concordance analysis was calculated using intraclass correlation coefficient (ICC), which was used to assess the reliability of measurements obtained with the 2 methods. Receiver-operating characteristic (ROC) curve analysis was conducted for each HPD measurement method to evaluate the performance of HPD in predicting cesarean delivery. To construct the ROC curve, the HPD distance was plotted against the sensitivity and 1-specificity. The area under the curve (AUC) and its 95% confidence interval (CI) were calculated to quantify the discriminative ability of HPD. The optimal threshold for HPD was identified using the Youden index, which maximizes the sum of sensitivity and specificity. The performance of the HPD of each method was also compared using the DeLong test to assess whether the AUC values differed significantly. 20 A significance level of P < .05 was set for all comparisons. Results During the study period, 10,370 women with a singleton fetus in a cephalic presentation at term were admitted to the labor ward for a planned vaginal delivery. Among them, 1875 women had a vaginal examination during the second stage of labor before an operative delivery (i.e., vaginal operative delivery or cesarean delivery) because of a prolonged second stage of labor. Clinical and ultrasound HPD measurements were performed in 671 women, who comprised the final population for this study. The maternal and ultrasound characteristics of the population are summarized in Table 1 . Women were mostly nulliparous, and a high percentage (42%) underwent induction of labor. At the time of inclusion, a fetal head station of + 2 was observed in 66.5% of women and below + 2 in about 25% of women. The mean HPDhys was 39.3 (±14.2) mm. The positions of occiput anterior (OA) and occiput posterior (OP) were found by ultrasound in 81.5% and 16.0% of births, respectively. The mean HPDus was 41.5 (±12.8) mm. The mean difference in HPD between the 2 methods was 1.51 (±7.1) mm. The correlations between both methods of measuring HPD are shown in Figs. 2 and 3 . Pearson correlational analysis showed good agreement between both methods: r = .85 (95% CI .84–.88). The Bland–Altman plot also showed good agreement for HPD regardless of the HPD values. The ICC was .85 (95% CI .82–.87]. The correlations and agreements were good for the OA and OP/occiput transverse positions. The ability of both HPD methods to predict cesarean delivery are illustrated in Fig. 4 . The AUC values were .87 (95% CI .83–.92) for clinical HPDhys and .83 (95% CI 0.78–0.89) for HPDus ( P = .006). The optimal HPD cutoff was 47.5 mm and 44.5 mm for HPDhys and HPDus, respectively. The HPDhys for predicting CD had a sensitivity of 88%, specificity of 71%, positive predictive value (PPV) of 20% and negative predictive value (PNV) of 98%. The HPDus had a sensitivity of 86.5%, specificity of 63.2%, PPV of 16.2%, and PNV of 98.2%. Comment Principal findings In this study, the HPD was measured easily during a vaginal examination using a hysterometer, and this value correlated highly with HPD measured by ultrasound. The correlations between HPD measured using the 2 methods were independent of the level of the fetus head station and the fetal head position. Results in the context of what is known We examined the measurement of the HPD using a hysterometer during a vaginal examination. Our results are encouraging and suggest that a simple measurement with a single-use hysterometer correlates well with the same measurement taken by ultrasound. Transperineal ultrasound performed in the delivery room, especially before the decision for an operative delivery is made, is of interest to clinical practice. The first reason for this interest is the reproducibility of ultrasound measurement of both the angle of progression and head probe distance, which provide a certain degree of consistency in contrast to the heterogeneity of vaginal examination. 21 The high reproducibility of the HPD measurement, even in cases involving a high fetal presentation, has been demonstrated. 22;23 In our study, HPDhys correlated well with HPDus, even when the fetal head station was high in the pelvis. There are now automatic methods of measurement that strongly correlate with manual HPD measurements obtained via ultrasound. Patients tend to be more satisfied when the fetal head station and position are assessed by ultrasound, as this procedure is non-intrusive. 24 The predictive value of this examination for anticipating success or failure of instrumental delivery appears promising. These preliminary encouraging results justify further investigation of HPDhys using the same indications as ultrasound, particularly before induction or during labor monitoring. In a comparative systematic review and meta-analysis, Skinner et al evaluated the performance of ultrasound measures for predicting failed or complicated operative vaginal deliveries. 17 They found that HPD had moderate to excellent accuracy for predicting failed or complicated operative vaginal deliveries (AUC = 0.747 for 8 studies). However, a limitation of this meta-analysis was that many of the included studies involved fetal presentations at + 2 or lower, for which the measurement’s benefit is more limited. By contrast, in a recent study that included only cephalic presentations considered high (0 or + 1), Nallet et al noted that a long head probe distance (≥+ 2 z -score) was associated with an increased risk of failed instrumental vaginal delivery. These authors also found that in cases involving a fetal height evaluation at + 0, the head probe distance was the only factor associated with the risk of instrumental vaginal delivery failure. In this study, using a threshold of 55 mm resulted in a sensitivity of .90 (95% CI .83–.95), specificity of .19 (95% CI .14–0.25), PPV of .36 (95% CI .30–.42), and NPV of .80 (95% CI .66–.90). These results suggest a real clinical benefit of HPD measurement. 24 Clinical implications The clinical implication of our results is that measuring the HPD using a hysterometer is accessible to all and allows practitioners to avoid the need for costly resources such as ultrasound. Given the potential of HPD to assist clinicians in selecting the appropriate indications for instrumental deliveries, we hope that this technique will be applied widely, especially in low-to-middle resource countries. Strengths and limitations The HPD is the only transperineal ultrasound measurement that can be directly translated into a clinical measurement, and ours is the first study to evaluate the use of HPDhys. All data were collected prospectively, and sonographers were used to measure HPDus. The main limitation of our study is its monocentric design. The ability of HPD to predict cesarean delivery, as shown here, should be interpreted with caution because HPDus was not blinded to the medical team, which could have influenced the choice of delivery method. Due to the lack of consistent data on HPD, the mode of delivery was decided based on clinical assessment of the fetal head station, and no specific cutoff in HPD was established prior to choosing the operative delivery mode. Another limitation concerns the fact that the two measurements may be considered different. Indeed, HPDhys involves taking the tip of the cephalic presentation outline as the reference point for the height of the presentation, which may differ from the ultrasound-based HPD measurement, where the reference point corresponds to the end of the cranial box, without accounting for an eventual caput. Thus, the hysterometer does not allow for its assessment, even though it is not clear whether the extent of the caput measurement impacts the success of instrumental extraction. 26 , 27 Evaluation of the inter- and intraobserver reproducibility of the HPDhys is therefore required. However, this evaluation would have required a third party to measure HPDhys, which was not desirable because it required an extra person in the delivery room. Conclusions HPD has potential as a tool to help clinicians select the appropriate indications for instrumental deliveries. Future studies should be aligned with those conducted using ultrasound, and the optimal cutoff values for successful instrumental and spontaneous vaginal delivery should be determined. Further studies are needed to confirm the results of this study in low-to-middle income settings. Declarations Disclosure statement : The authors report no conflict of interest Funding There is no funding to report for this study. Author Contribution TQ, MC, CT, PB, PR conceived the study question. MAJ, SF, LT, LB collected the data. CD performed the statistical analyses, and TQ drafted the first version of the manuscript that was revised by PR and CT.All the authors approved the manuscript. Data Availability Data is provided within the manuscript or supplementary information files References Bailey, P. E. The disappearing art of instrumental delivery: time to reverse the trend. Int. J. Gynecol. Obstet. 91 (1), 89–96 (2005). Hirshberg, A. & Srinivas, S. K. 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Gynecol. 233 (1), 68. 10.1016/j.ajog.2024.12.022 (2025). Epub 2024 Dec 20. PMID: 39710223. Bultez, T. et al. Angle of fetal head progression measured using transperineal ultrasound as a predictive factor of vacuum extraction failure. Ultrasound Obstet. Gynecol. 48 (1), 86–91. 10.1002/uog.14951 (2016). Epub 2016 Jun 10. PMID: 26183426. Contributorship. Thibaud Quibel*. 1,2 , Marion Chesnais 3 , Marie-Anne Joly 4 ,Lea Tettamanti 1 , Clémence Duvillier 1 , Paul Berveiller 1,5 , Claire Thuillier 2,6 , Laure Benoit 7 , Patrick Rozenberg 2,6 . TQ, M. C. & CT, P. B. PR conceived the study question. MAJ, SF, LT, LB collected the data. CD performed the statistical analyses, and TQ drafted the first version of the manuscript that was revised by PR and CT. All the authors approved the manuscript. Tables Tables 1 and 2 are available in the Supplementary Files section. Additional Declarations No competing interests reported. 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13:44:45","extension":"html","order_by":13,"title":"","display":"","copyAsset":false,"role":"acdc-reference","size":95374,"visible":true,"origin":"","legend":"","description":"","filename":"earlyproof.html","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/fcacee3f9555767697336fb3.html"},{"id":100722041,"identity":"6be6e9c4-d214-46f1-b6f2-b3112fde114f","added_by":"auto","created_at":"2026-01-20 19:51:48","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":397028,"visible":true,"origin":"","legend":"\u003cp\u003eDescription of head perineum distance (HPD) measured with a hysterometer and HPD measured with a transperineal ultrasound\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/e296c1f80c27776adcbed5f6.png"},{"id":100857747,"identity":"07aaf97a-0e8e-41ed-87cd-db28c03d385b","added_by":"auto","created_at":"2026-01-22 07:21:33","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":161064,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eCorrelation between head perineum distance (HPD) measured with the hysterometer and HPD measured during transperineal ultrasound\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eClinically head perineum distance (HPD) was measured with a a single-use hysterometer and ultrasound HPD was measured during a transperineal ultrasound (\u003cem\u003er\u003c/em\u003e=.85 (95% CI .84–.88).\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/b31c6cfdef7d2a889469c362.png"},{"id":100721883,"identity":"c238ddec-b8e7-45d5-b3ac-67a3777a125e","added_by":"auto","created_at":"2026-01-20 19:50:17","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":170283,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eAgreement between a clinically and ultrasonographic measurement of head perineum distance\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eBland–Altman plot showing high agreement between ultrasonographic head perineum distance (HPD) \u0026nbsp;and a clinically HPD measured with a single-use hysterometer (ICC .85 [95% CI .82–.87]).\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/dde44cebd0444b5706240a19.png"},{"id":100721403,"identity":"8634283f-fb34-4bf3-9727-930c0cefeb27","added_by":"auto","created_at":"2026-01-20 19:47:24","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":63470,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003ePerformance of head perineum distance to predict cesarean delivery\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eROC curves for the 2 methods for predicting cesarean delivery. The blue curve relates to ultrasound HPD (HPDus) and the red curve to clinical HPD measured with a single-use hysterometer (HPDhys). The AUCs were for .87 (95% CI .83-.92) for HPDhys and .83 (95% CI .78–.89) for HPDus (\u003cem\u003eP\u003c/em\u003e=.006).\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/7a8d547edfa67128d6fff5bc.png"},{"id":108505957,"identity":"57c07396-6f2c-4259-a9d8-510b785a8d94","added_by":"auto","created_at":"2026-05-05 11:42:05","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1207566,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/4ab9bc94-46c6-48bf-865a-d32579f999d2.pdf"},{"id":100721778,"identity":"325c1dc7-420b-4ba7-a352-503052e7cb06","added_by":"auto","created_at":"2026-01-20 19:49:48","extension":"xlsx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":573814,"visible":true,"origin":"","legend":"","description":"","filename":"HPDcesar.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/5e30b2a306eb088b4b5b2d4f.xlsx"},{"id":100722357,"identity":"cc24f4d9-57d6-4d95-837d-f24f0535c911","added_by":"auto","created_at":"2026-01-20 19:54:18","extension":"docx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":18613,"visible":true,"origin":"","legend":"","description":"","filename":"Tables.docx","url":"https://assets-eu.researchsquare.com/files/rs-7603641/v1/00118990af7eb99d77ffb8fb.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Use of a hysterometer to measure the head–perineum distance before an operative delivery: a prospective study","fulltext":[{"header":"Introduction","content":"\u003cp\u003eStudies have highlighted the decline in the use of vacuum delivery in favor of cesarean delivery performed during the second stage of labor.\u003csup\u003e\u003cspan additionalcitationids=\"CR2\" citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e These findings are concerning given the potential complications of a cesarean delivery performed during the second stage of labor.\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e,\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e\u003c/sup\u003e The fear of vacuum extraction failure, which is associated with an increase in maternal and perinatal morbidity, may explain this decline in its use.\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eVaginal examination remains the key assessment for deciding on the need for an operative vaginal birth or cesarean delivery in the second stage of labor in cases involving a prolonged second stage of labor or suspicion of immediate or potential fetal compromise. This examination can be used to determine the fetal head position and head station. However, the significant variability in determining the head position and station has led professional societies to recommend supplementing the examination with an ultrasound to determine the fetal position accurately before performing an operative vaginal birth.\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e,-\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eSince the publication of Kalache et al in 2009, transperineal ultrasound during the second stage of labor has emerged as a promising tool for predicting failed operative vaginal birth or cesarean deliveries.\u003csup\u003e\u003cspan additionalcitationids=\"CR13\" citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u003c/sup\u003e The contribution of transperineal ultrasound in determining the fetal head station during second-stage management has been reported\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e,\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e\u003c/sup\u003e, and the head\u0026ndash;perineum distance (HPD) remains 1 of the most studied methods. A recent meta-analysis involving 6 studies that examined the ability of HPD to predict the success of vaginal delivery highlighted this measurement as a useful predictor\u003csup\u003e\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe use of ultrasound in the labor ward may be limited by local resources and the lack of training of some physicians. Here, we hypothesized that the HPD measured \u0026ldquo;clinically\u0026rdquo; with a hysterometer might correlate with that measured by transperineal ultrasound. We also hypothesized that HPD measured with a hysterometer could be used to predict a cesarean delivery as well as HPD measured transperineally when an expeditive delivery is expected.\u003c/p\u003e"},{"header":"Materials and methods","content":"\u003cp\u003eThis was a prospective observational study that occurred between February 10, 2022, and June 30, 2024 at the University Maternity of Poissy Saint-Germain, Poissy, France. The ethics committee (Comit\u0026eacute; de Protection des Personnes OUEST III, France) approved the study protocol (number LL/JT/FB/2021/147). All participants provided written informed consent.\u003c/p\u003e \u003cp\u003eEligibility criteria\u003c/p\u003e \u003cp\u003eWomen with a singleton fetus in the cephalic presentation at term (\u0026ge;37 weeks of gestation) who had an operative delivery (vaginal operative birth or cesarean delivery during the second stage) were eligible for inclusion in this study. Women were included if, during the second stage, an operative delivery was expected, and the HPD was measured using both devices: transperineal ultrasound (HPDus) and hysterometer (HPDhys). The exclusion criteria were multiple pregnancy, noncephalic presentation, spontaneous vaginal delivery, suspicion of immediate or potential fetal compromise, lack of use of epidural anesthesia, and lack of both HPD measurements.\u003c/p\u003e \u003cp\u003eLocal procedures\u003c/p\u003e \u003cp\u003eWhen a prolonged second stage of labor was diagnosed, the caregiver was asked to perform the vaginal examination by measuring the HPD with a single-use hysterometer, which was introduced horizontally (coronal plane) until it touched gently against the fetal skull scalp.(Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) The HPD was defined as the shortest distance from the outer bony limit of the skull to the perineum. The fetal head station was assessed clinically by digital vaginal examination according to the classification of the American College of Obstetricians and Gynecology and in relation to the outlet (i.e., high, mid, or low). Suprapubic ultrasound was then performed before considering or performing instrumental delivery. The HPD was then measured using the transverse transperineal approach from the fetal skull to the transducer as described by Eggebo.\u003csup\u003e\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e\u003c/sup\u003e The sonographer was blinded to the HPD measured with the hysterometer.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eOperative deliveries were performed by residents under the supervision of the attending obstetrician. Local policy recommends use of a vacuum extractor as the instrument of first choice when an operative vaginal delivery is indicated. If vacuum extraction fails, the attending senior obstetrician must choose between using forceps or performing a cesarean delivery.\u003c/p\u003e \u003cp\u003eThe following demographic and obstetric data were recorded prospectively: maternal age, parity, prepregnancy body mass index, and history of a previous cesarean delivery; gestational age at delivery; mode of onset of labor (spontaneous or induced labor); duration of the second stage of labor; clinical station of the fetal head; failed vacuum extraction; final mode of delivery (forceps or cesarean); mediolateral episiotomy; and neonatal weight. Ultrasound data for fetal head position on ultrasound and angle of progression were recorded. Data on the following maternal and neonatal morbidity outcomes were collected: maternal anal sphincter injury and postpartum hemorrhage; 5-min Apgar score\u0026thinsp;\u0026lt;\u0026thinsp;7; arterial cord pH\u0026thinsp;\u0026lt;\u0026thinsp;7.10 at delivery; and newborn birthweight.\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eQualitative variables are presented as the percentage and absolute count. Continuous variables are presented as the median and interquartile range or as the mean and standard deviation (SD), depending on the distribution of the data. For comparisons of qualitative variables between groups, the chi-squared test or Fisher\u0026rsquo;s exact test was used as appropriate. Continuous variables were compared using Student\u0026rsquo;s \u003cem\u003et\u003c/em\u003e test for normally distributed data or the Mann\u0026ndash;Whitney \u003cem\u003eU\u003c/em\u003e test for nonnormally distributed data.\u003c/p\u003e \u003cp\u003eTo identify correlations between the measurements, Pearson or Spearman correlational analysis was used depending on whether the data were normally distributed. The agreement of both methods was visualized using the Bland\u0026ndash;Altman plot,\u003csup\u003e19\u003c/sup\u003e in which 2 additional horizontal lines representing the limits of agreement at \u0026plusmn;1.96 SDs from the mean difference were included to represent the range within which 95% of the differences should fall if the 2 methods are in agreement. Concordance analysis was calculated using intraclass correlation coefficient (ICC), which was used to assess the reliability of measurements obtained with the 2 methods.\u003c/p\u003e \u003cp\u003eReceiver-operating characteristic (ROC) curve analysis was conducted for each HPD measurement method to evaluate the performance of HPD in predicting cesarean delivery. To construct the ROC curve, the HPD distance was plotted against the sensitivity and 1-specificity. The area under the curve (AUC) and its 95% confidence interval (CI) were calculated to quantify the discriminative ability of HPD. The optimal threshold for HPD was identified using the Youden index, which maximizes the sum of sensitivity and specificity. The performance of the HPD of each method was also compared using the DeLong test to assess whether the AUC values differed significantly.\u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e\u003c/sup\u003e A significance level of \u003cem\u003eP\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;.05 was set for all comparisons.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eDuring the study period, 10,370 women with a singleton fetus in a cephalic presentation at term were admitted to the labor ward for a planned vaginal delivery. Among them, 1875 women had a vaginal examination during the second stage of labor before an operative delivery (i.e., vaginal operative delivery or cesarean delivery) because of a prolonged second stage of labor. Clinical and ultrasound HPD measurements were performed in 671 women, who comprised the final population for this study.\u003c/p\u003e\n\u003cp\u003eThe maternal and ultrasound characteristics of the population are summarized in Table \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e. Women were mostly nulliparous, and a high percentage (42%) underwent induction of labor. At the time of inclusion, a fetal head station of +\u0026thinsp;2 was observed in 66.5% of women and below +\u0026thinsp;2 in about 25% of women. The mean HPDhys was 39.3 (\u0026plusmn;14.2) mm. The positions of occiput anterior (OA) and occiput posterior (OP) were found by ultrasound in 81.5% and 16.0% of births, respectively. The mean HPDus was 41.5 (\u0026plusmn;12.8) mm. The mean difference in HPD between the 2 methods was 1.51 (\u0026plusmn;7.1) mm.\u003c/p\u003e\n\u003cp\u003eThe correlations between both methods of measuring HPD are shown in Figs. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e and \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e. Pearson correlational analysis showed good agreement between both methods: \u003cem\u003er\u003c/em\u003e\u0026thinsp;=\u0026thinsp;.85 (95% CI .84\u0026ndash;.88). The Bland\u0026ndash;Altman plot also showed good agreement for HPD regardless of the HPD values. The ICC was .85 (95% CI .82\u0026ndash;.87]. The correlations and agreements were good for the OA and OP/occiput transverse positions.\u003c/p\u003e\n\u003cp\u003eThe ability of both HPD methods to predict cesarean delivery are illustrated in Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003e. The AUC values were .87 (95% CI .83\u0026ndash;.92) for clinical HPDhys and .83 (95% CI 0.78\u0026ndash;0.89) for HPDus (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;.006). The optimal HPD cutoff was 47.5 mm and 44.5 mm for HPDhys and HPDus, respectively. The HPDhys for predicting CD had a sensitivity of 88%, specificity of 71%, positive predictive value (PPV) of 20% and negative predictive value (PNV) of 98%. The HPDus had a sensitivity of 86.5%, specificity of 63.2%, PPV of 16.2%, and PNV of 98.2%.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eComment\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003ePrincipal findings\u003c/p\u003e\n\u003cp\u003eIn this study, the HPD was measured easily during a vaginal examination using a hysterometer, and this value correlated highly with HPD measured by ultrasound. The correlations between HPD measured using the 2 methods were independent of the level of the fetus head station and the fetal head position.\u003c/p\u003e\n\u003ch3\u003eResults in the context of what is known\u003c/h3\u003e\n\u003cp\u003eWe examined the measurement of the HPD using a hysterometer during a vaginal examination. Our results are encouraging and suggest that a simple measurement with a single-use hysterometer correlates well with the same measurement taken by ultrasound. Transperineal ultrasound performed in the delivery room, especially before the decision for an operative delivery is made, is of interest to clinical practice. The first reason for this interest is the reproducibility of ultrasound measurement of both the angle of progression and head probe distance, which provide a certain degree of consistency in contrast to the heterogeneity of vaginal examination.\u003csup\u003e\u003cspan class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e The high reproducibility of the HPD measurement, even in cases involving a high fetal presentation, has been demonstrated. \u003csup\u003e22;23\u003c/sup\u003eIn our study, HPDhys correlated well with HPDus, even when the fetal head station was high in the pelvis. There are now automatic methods of measurement that strongly correlate with manual HPD measurements obtained via ultrasound. Patients tend to be more satisfied when the fetal head station and position are assessed by ultrasound, as this procedure is non-intrusive. \u003csup\u003e24\u003c/sup\u003e The predictive value of this examination for anticipating success or failure of instrumental delivery appears promising. These preliminary encouraging results justify further investigation of HPDhys using the same \u003cstrong\u003eindications\u003c/strong\u003e as ultrasound, particularly before induction or during labor monitoring.\u003c/p\u003e\n\u003cp\u003eIn a comparative systematic review and meta-analysis, Skinner et al evaluated the performance of ultrasound measures for predicting failed or complicated operative vaginal deliveries.\u003csup\u003e\u003cspan class=\"CitationRef\"\u003e17\u003c/span\u003e\u003c/sup\u003e They found that HPD had moderate to excellent accuracy for predicting failed or complicated operative vaginal deliveries (AUC\u0026thinsp;=\u0026thinsp;0.747 for 8 studies). However, a limitation of this meta-analysis was that many of the included studies involved fetal presentations at +\u0026thinsp;2 or lower, for which the measurement\u0026rsquo;s benefit is more limited. By contrast, in a recent study that included only cephalic presentations considered high (0 or +\u0026thinsp;1), Nallet et al noted that a long head probe distance (\u0026ge;+\u0026thinsp;2 \u003cem\u003ez\u003c/em\u003e-score) was associated with an increased risk of failed instrumental vaginal delivery. These authors also found that in cases involving a fetal height evaluation at +\u0026thinsp;0, the head probe distance was the only factor associated with the risk of instrumental vaginal delivery failure. In this study, using a threshold of 55 mm resulted in a sensitivity of .90 (95% CI .83\u0026ndash;.95), specificity of .19 (95% CI .14\u0026ndash;0.25), PPV of .36 (95% CI .30\u0026ndash;.42), and NPV of .80 (95% CI .66\u0026ndash;.90). These results suggest a real clinical benefit of HPD measurement.\u003csup\u003e\u003cspan class=\"CitationRef\"\u003e24\u003c/span\u003e\u003c/sup\u003e\u003c/p\u003e\n\u003cp\u003eClinical implications\u003c/p\u003e\n\u003cp\u003eThe clinical implication of our results is that measuring the HPD using a hysterometer is accessible to all and allows practitioners to avoid the need for costly resources such as ultrasound. Given the potential of HPD to assist clinicians in selecting the appropriate indications for instrumental deliveries, we hope that this technique will be applied widely, especially in low-to-middle resource countries.\u003c/p\u003e\n\u003cp\u003eStrengths and limitations\u003c/p\u003e\n\u003cp\u003eThe HPD is the only transperineal ultrasound measurement that can be directly translated into a clinical measurement, and ours is the first study to evaluate the use of HPDhys. All data were collected prospectively, and sonographers were used to measure HPDus. The main limitation of our study is its monocentric design. The ability of HPD to predict cesarean delivery, as shown here, should be interpreted with caution because HPDus was not blinded to the medical team, which could have influenced the choice of delivery method. Due to the lack of consistent data on HPD, the mode of delivery was decided based on clinical assessment of the fetal head station, and no specific cutoff in HPD was established prior to choosing the operative delivery mode. Another limitation concerns the fact that the two measurements may be considered different. Indeed, HPDhys involves taking the tip of the cephalic presentation outline as the reference point for the height of the presentation, which may differ from the ultrasound-based HPD measurement, where the reference point corresponds to the end of the cranial box, without accounting for an eventual caput. Thus, the hysterometer does not allow for its assessment, even though it is not clear whether the extent of the caput measurement impacts the success of instrumental extraction.\u003csup\u003e\u003cspan class=\"CitationRef\"\u003e26\u003c/span\u003e,\u003cspan class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e Evaluation of the inter- and intraobserver reproducibility of the HPDhys is therefore required. However, this evaluation would have required a third party to measure HPDhys, which was not desirable because it required an extra person in the delivery room.\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eHPD has potential as a tool to help clinicians select the appropriate indications for instrumental deliveries. Future studies should be aligned with those conducted using ultrasound, and the optimal cutoff values for successful instrumental and spontaneous vaginal delivery should be determined. Further studies are needed to confirm the results of this study in low-to-middle income settings.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eDisclosure statement :\u003c/h2\u003e\n\u003cp\u003eThe authors report no conflict of interest\u003c/p\u003e\n\u003ch2\u003eFunding\u003c/h2\u003e \u003cp\u003eThere is no funding to report for this study.\u003c/p\u003e\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eTQ, MC, CT, PB, PR conceived the study question. MAJ, SF, LT, LB collected the data. CD performed the statistical analyses, and TQ drafted the first version of the manuscript that was revised by PR and CT.All the authors approved the manuscript.\u003c/p\u003e\u003ch2\u003eData Availability\u003c/h2\u003e\u003cp\u003e Data is provided within the manuscript or supplementary information files\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eBailey, P. E. 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Ramirez Zegarra R(2), Mazellier S(1), Dall'asta A(2), Puyraveau M(3), Lallemant M(1), Ramanah R(4), Riethmuller D(5), Ghi T(6), Mottet N(4) Head-to-perineum distance measured transperineally as a predictor of failed midcavity vacuum-assisted delivery. \u003cem\u003eAm. J. Obstet. Gynecol. MFM\u003c/em\u003e. \u003cb\u003e1\u003c/b\u003e (2), 100827. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003e10.1016/j.ajogmf.2022.100827\u003c/span\u003e\u003cspan address=\"10.1016/j.ajogmf.2022.100827\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e (2023). Epub 2022 Dec 1.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFalcone, V. et al. Vacuum extraction is successful in 95% of cases with an occiput posterior position: the results of a prospective, multicenter study. \u003cem\u003eAm. J. Obstet. Gynecol.\u003c/em\u003e \u003cb\u003e233\u003c/b\u003e (1), 68. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003e10.1016/j.ajog.2024.12.022\u003c/span\u003e\u003cspan address=\"10.1016/j.ajog.2024.12.022\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e (2025). Epub 2024 Dec 20. PMID: 39710223.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBultez, T. et al. Angle of fetal head progression measured using transperineal ultrasound as a predictive factor of vacuum extraction failure. \u003cem\u003eUltrasound Obstet. Gynecol.\u003c/em\u003e \u003cb\u003e48\u003c/b\u003e (1), 86\u0026ndash;91. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003e10.1002/uog.14951\u003c/span\u003e\u003cspan address=\"10.1002/uog.14951\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e (2016). Epub 2016 Jun 10. PMID: 26183426.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eContributorship.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eThibaud Quibel*. \u003csup\u003e1,2\u003c/sup\u003e, Marion Chesnais\u003csup\u003e3\u003c/sup\u003e, Marie-Anne Joly \u003csup\u003e4\u003c/sup\u003e,Lea Tettamanti\u003csup\u003e1\u003c/sup\u003e, Cl\u0026eacute;mence Duvillier\u003csup\u003e1\u003c/sup\u003e, Paul Berveiller\u003csup\u003e1,5\u003c/sup\u003e, Claire Thuillier \u003csup\u003e2,6\u003c/sup\u003e, Laure Benoit\u003csup\u003e7\u003c/sup\u003e, Patrick Rozenberg\u003csup\u003e2,6\u003c/sup\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTQ, M. C. \u0026amp; CT, P. B. PR conceived the study question. MAJ, SF, LT, LB collected the data. CD performed the statistical analyses, and TQ drafted the first version of the manuscript that was revised by PR and CT.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAll the authors approved the manuscript.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1 and 2 are available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"cesarean delivery, head–perineum distance, hysterometer, transperineal ultrasound","lastPublishedDoi":"10.21203/rs.3.rs-7603641/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-7603641/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eIntroduction:\u003c/h2\u003e \u003cp\u003eMany studies have investigated the contribution of transperineal ultrasound in determining the fetal head station during the management of the second stage of delivery. The head\u0026ndash;perineum distance (HPD) remains 1 of the most studied measures.We hypothesized that a HPD measured \u0026ldquo;clinically\u0026rdquo; with a hysterometer might correlate with that measured by transperineal ultrasound and could be used to predict the risk of cesarean delivery.\u003c/p\u003e\u003ch2\u003eSTUDY DESIGN:\u003c/h2\u003e \u003cp\u003eThis was a unicentric prospective observational study that occurred between February 10, 2022, and June 30, 2024. Women with a singleton fetus in the cephalic presentation at term (\u0026ge;37 weeks of gestation) who had an operative delivery (vaginal operative birth or cesarean delivery during the second stage) were eligible for this study. Women were included during the second stage if an operative delivery was expected. The HPD was measured using 2 devices: transperineal ultrasound (HPDus) and a hysterometer (HPDhys). Correlations and agreement were calculated, and receiver-operating characteristic curve analysis was conducted to evaluate the performance of each method in predicting cesarean delivery.\u003c/p\u003e\u003ch2\u003eRESULTS\u003c/h2\u003e \u003cp\u003eThe final population comprised 671 women who underwent both HPDhys and HPDus. Pearson correlational analysis showed good agreement between both methods: \u003cem\u003er\u003c/em\u003e\u0026thinsp;=\u0026thinsp;.85 (95% confidence interval [CI] .84\u0026ndash;.88). Correlations were independent of the level of the fetus head station and head position. The area-under-the-curve values were high for both methods: 0.87 (95% CI 82.8\u0026ndash;92.1) for clinical HPDhys and 0.83 (95% CI 0.78\u0026ndash;0.89) for HPDus (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;.006).\u003c/p\u003e\u003ch2\u003eCONCLUSIONS\u003c/h2\u003e \u003cp\u003eHPD measured with a hysterometer is accessible to all practitioners and correlates well with HPD measured with transperineal ultrasound. HPD has potential as a tool to help clinicians select the appropriate indications for instrumental deliveries. It is hoped that this easily accessible technique will be used widely, especially in countries where ultrasound resources may be limited. Further studies are needed to confirm the results of this study.\u003c/p\u003e","manuscriptTitle":"Use of a hysterometer to measure the head–perineum distance before an operative delivery: a prospective study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-01-20 16:41:13","doi":"10.21203/rs.3.rs-7603641/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"cc2a8556-8612-46be-9227-baba90c5d60e","owner":[],"postedDate":"January 20th, 2026","published":true,"recentEditorialEvents":[{"type":"decision","content":"Rejected","date":"2026-05-05T11:29:49+00:00","index":"","fulltext":""}],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":61315723,"name":"Health sciences/Health care"},{"id":61315724,"name":"Health sciences/Medical research"}],"tags":[],"updatedAt":"2026-05-05T11:41:34+00:00","versionOfRecord":[],"versionCreatedAt":"2026-01-20 16:41:13","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-7603641","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-7603641","identity":"rs-7603641","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}