Five-Year Outcomes of Transoral Laser Microsurgery for Early-Stage Glottic Cancer: A Single-Center Retrospective Study

Five-Year Outcomes of Transoral Laser Microsurgery for Early-Stage Glottic Cancer: A Single-Center Retrospective 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 Research Article Five-Year Outcomes of Transoral Laser Microsurgery for Early-Stage Glottic Cancer: A Single-Center Retrospective Study Thanh Tuan Nguyen This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-6706063/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 Background This study aimed to evaluate the clinical and functional outcomes of patients with early-stage glottic laryngeal cancer treated by transoral laser microsurgery (TLM) at Ho Chi Minh City ENT Hospital over a five-year period. Methods Ninety-six patients diagnosed with T1-T2N0M0 glottic squamous cell carcinoma and treated exclusively with TLM between 2018 and 2020 were included. Surgical procedures were performed according to the European Laryngological Society classification of endoscopic cordectomies. Outcomes assessed included local control, overall survival (OS), disease-specific survival (DSS), postoperative complications, and functional voice and swallowing preservation over a minimum follow-up of 5 years. Results The 5-year local control rate was 91.7%, with an overall survival rate of 89.6% and disease-specific survival of 100%. Postoperative complications were minimal and manageable, with no permanent tracheostomy or feeding tubes required. The majority of patients maintained satisfactory voice and swallowing function. Conclusions Transoral laser microsurgery (TLM) demonstrates favorable oncologic efficacy and functional preservation in the treatment of early-stage glottic laryngeal cancer. The ability to achieve organ preservation without compromising oncologic safety highlights TLM as a preferred therapeutic option for patients with T1-T2 glottic carcinoma. Glottic cancer Transoral laser microsurgery Organ preservation Figures Figure 1 Figure 2 Figure 3 Figure 4 1. BACKGROUND The larynx plays a vital role in essential physiological functions such as respiration, phonation, and swallowing. Consequently, treatment strategies for laryngeal cancer prioritize organ preservation to maintain these critical functions. Current therapeutic options include transoral laser microsurgery, open surgical techniques, and primary radiotherapy, all of which have been extensively studied and debated in the literature[ 1 ]. Among these modalities, transoral laser microsurgery has gained prominence as a preferred treatment approach. This preference is largely due to its advantages, including lower morbidity, favorable functional outcomes, reduced healthcare costs, and shorter hospitalization durations, while demonstrating comparable rates of local control and overall survival to other established treatments[ 2 ]. This study aims to evaluate the clinical outcomes of patients with early-stage glottic laryngeal cancer treated at Ho Chi Minh City ENT Hospital over a five-year period. Specifically, we seek to analyze the effectiveness of different treatment modalities in terms of local control, overall survival, and functional preservation, as well as to identify factors influencing prognosis and treatment-related complications. 2. METHODS This retrospective study included patients diagnosed with early-stage glottic laryngeal cancer (T1-T2) who received treatment at Ho Chi Minh City ENT Hospital between 2018 and 2020. Only patients with complete clinical data and a minimum follow-up period of 5 years post-treatment were included to ensure comprehensive assessment of long-term outcomes. The research protocol was was approved by the Ethics Committee in Biomedical Research of the University of Medicine and Pharmacy, Ho Chi Minh City, according to Decision [No. 379/ĐHYD-HĐĐĐ]. Patient demographic data, tumor characteristics, treatment modalities, and clinical outcomes were collected from medical records. All patients included in this study were treated exclusively with transoral laser microsurgery (Fig. 1). The treatment protocol was standardized, according to the European Laryngological Society Classification of Endoscopic Cordectomies[ 3 ]. Surgical Margin Assessment with frozen section: Resection the tumor en bloc for frozen section; mark the margins anterior, posterior, external, left and right vocal cord, and dye the deep cut area with suture knots and ink. Evaluation the margins when the frozen section results are obtained, choose a safety margin of 2 mm on the tissue sample to submit to the pathology. The margins were evaluated by visual examination through the operating microscope (Carl Zeiss, Germany), and by palpation with microforceps (Fig. 2 ). If the result is positive, cordectomy will continue to enlarge until all margins are negative. The primary endpoints were local control rate, overall survival (OS), and disease-free survival (DFS) assessed at 5 years post-treatment. Secondary endpoints included treatment-related complications and functional outcomes such as voice quality and swallowing function. Statistical analysis was performed using SPSS version XX. Survival rates were estimated using the Kaplan-Meier method, and differences between groups were assessed by the log-rank test. A p-value < 0.05 was considered statistically significant. 3. RESULTS A total of 96 patients with early-stage glottic laryngeal cancer (T1-T2) treated exclusively by transoral laser microsurgery were included in this study. The median age of the cohort was 61 ± 9 years olds, the youngest was 33 years old, the oldest was 89 years old; The most affected age is from 51 to 60 years old (43.8%); with a male predominance accounting for 96.9% of cases. Regarding risk factors for laryngeal cancer, the vast majority of patients (97.9%) had a history of smoking, while only 2 patients (2.1%) reported no history of tobacco use. In terms of clinical characteristics: All patients presented with hoarseness, which was the sole functional symptom observed. Notably, 81.3% of patients sought medical consultation within 6 months of symptom onset. Concerning tumor staging, 85.4% of patients were diagnosed with stage T1N0M0 laryngeal cancer. Among these, 83.3% were classified specifically as T1bN0M0, while only 6 patients (6.25%) had stage T2N0M0 disease at the time of surgery. Treatment outcomes: All patients underwent standardized transoral laser cordectomy based on the European Laryngological Society Classification of Endoscopic Cordectomies[ 3 ]. Regarding the surgical techniques applied (Fig. 3 ), the distribution of cordectomy types was as follows: 43 patients (44.8%) underwent Type III cordectomy, 36 patients (37.5%) received Type IV, 11 patients (11.5%) underwent Type Va, and 6 patients (6.3%) were treated with Type Vb cordectomy. The median follow-up period was 60 months (range: 60–72 months), ensuring a minimum follow-up duration of five years for all cases. All patients were confirmed to have squamous cell carcinoma (100%) on histopathology, with grade 2 tumors accounting for the majority (59.4%). Negative resection margins were achieved in 72,9% of cases; close or positive margins were found in the remainder but were managed by second-look procedures where indicated. Oncologic outcomes: At 5 years, the local control rate was 91.7%, with 8 patients (8.3%) experiencing local recurrence. All recurrences were managed with total laryngectomy. This corresponds to a larynx-preservation rate of 100%. The 5-year overall survival (OS) rate was 89.6%, and disease-specific survival (DSS) was 100%. Postoperative Complications (Fig. 4 ): Among the 96 patients, we observed four cases of postoperative bleeding at the surgical site (4.17%). These included one patient with a posterior vocal cord injury extending from the glottis, one patient following a Type Va cordectomy, and two patients after Type Vb procedures. All cases were successfully managed with electrocauterization at the resection site. Subcutaneous emphysema occurred in three patients (3.13%). These cases presented with mild emphysema localized around the thyroid cartilage immediately postoperatively and resolved spontaneously within one week under observation. Severe inflammatory granulation tissue developed in ten patients (10.4%) during follow-up, all of whom required surgical excision. Additionally, four patients (4.2%) developed significant laryngeal scarring, which also required surgical intervention for symptomatic relief and airway patency. Functional and postoperative outcomes: Most patients reported satisfactory voice and swallowing function at follow-up. No permanent tracheostomy or feeding tube was required. Transient postoperative complications, such as mild edema or pain, were observed in a minority of cases. Subgroup analysis: T2N0M0 patients showed a slightly higher recurrence rate than T1, echoing trends in international cohorts where local control in T2 disease remains more challenging. However, no statistically significant differences in survival or larynx preservation were observed. 4. DISCUSSION Transoral laser microsurgery (TLM) is indicated for patients who can tolerate direct rigid laryngoscopy under general anesthesia. One of the primary technical challenges lies in adequately exposing tumors involving the anterior commissure. During TLM, tumor resection is performed with the goal of achieving negative surgical margins, often guided by intraoperative frozen section analysis; however, the definition of a safe margin remains a subject of ongoing debate[ 4 ]. Consequently, the success of TLM largely depends on the surgeon’s expertise and intraoperative judgment in determining the appropriate extent of cordectomy. The mean age of patients at diagnosis was 61 years, ranging from 33 to 89 years, with the majority (43.8%) falling within the 51–60 age group. This distribution aligns closely with findings reported by Hartl[ 5 ] and Peretti[ 6 ], reflecting the typical onset of laryngeal cancer during middle age, a period when cumulative exposure to risk factors such as tobacco and alcohol reaches a critical threshold. Regarding gender distribution, males constituted the overwhelming majority of cases, a pattern that differs from studies by Bocciolini[ 7 ] and Remacle[ 8 ], where female representation was comparatively higher. This discrepancy may be attributed to variations in smoking and alcohol consumption prevalence among women across different countries, including a historically lower rate in Vietnam, although recent trends suggest these patterns are evolving. Regarding lesion classification and surgical indications, the majority of our cases were stage T1a (85.4%), followed by 8.3% at T1b, and only 6 patients (6.3%) with stage T2N0M0 disease. In comparison, Giovanni Motta’s study[ 9 ], which analyzed CO2 laser surgery outcomes in 719 patients, reported a distribution of 432 T1, 236 T2, and 51 T3 tumors. Early in our study period, due to limited experience and suboptimal equipment, we primarily restricted surgical indications to T1 glottic cancers and selected early T2 cases. Nevertheless, it remains essential to proceed cautiously to maintain oncologic safety and ensure appropriate lesion selection. In our cohort, Type III cordectomy was performed in 44.8% of patients, followed by Type IV in 37.5%, Type Va in 11.5%, and Type Vb in 6.3%. Compared to the findings of Sigston et al.[ 10 ], our study shows a higher proportion of Type IV and Va cordectomies among patients with stage T1 disease, which may be attributable to the greater incidence of lesions involving the anterior commissure in our population. The utilization of Type Va cordectomy in our series aligns with Peretti’s description[ 6 ] for lesions extending across the anterior commissure of the vocal cords. This surgical approach entails removal of the entire ipsilateral vocal cord, the anterior commissure, and a portion of the contralateral vocal cord, along with dissection of the perichondrium on the inner aspect of the thyroid cartilage at the anterior commissure. However, the indication for endoscopic cordectomy in cases with anterior commissure involvement remains controversial, as noted by both Peretti[ 6 ] and Steiner[ 11 ], due to concerns regarding oncologic safety and functional outcomes. In our study, all patients were diagnosed with squamous cell carcinoma (100%), with grade 2 tumors representing the majority (59.4%). During cordectomy, careful assessment of tumor extension is critical for planning the resection to ensure complete removal while minimizing the risk of residual disease. Therefore, establishing an adequate safety margin around the tumor is essential. In this study, intraoperative frozen section analysis was routinely performed to confirm clear margins. We adopted a safety margin of 2 mm, in accordance with criteria proposed by Crespo[ 12 ] and Remacle[ 8 ]. If a positive margin was identified, the resection was extended until all surgical margins were confirmed to be free of tumor. Our 5-year follow-up demonstrated a high local control rate of 91.7%, which is within the range reported in the international literature (2.3–10.8% recurrence) and comparable to other large cohort studies Parker et al.[ 13 ] and Ansarin et al.[ 14 ]. The absence of total laryngectomy or adjuvant radiotherapy in managing recurrences underlines the effectiveness of TLM in organ preservation, reflected in our larynx-preservation rate of 100%. Survival outcomes were favorable, with a 5-year overall survival of 89.6% and disease-specific survival of 100%. These findings are consistent with previously published data Choi et al.[ 15 ] and Jones et al[ 16 ] supporting TLM as an oncologically sound and functionally preservative treatment modality for early glottic cancer. In this study, surgical site bleeding was observed in 4.2% of patients, while subcutaneous emphysema occurred in 3.1%. Granulation tissue formation was noted in 14.6% of cases, with 7.3% progressing to laryngeal stenosis. Among these, four patients with severe stenosis underwent laryngoplasty, and three with mild stenosis were managed conservatively through follow-up. At the final assessment, 35.4% of patients retained normal voice quality, and an additional 52.1% experienced only mild to moderate voice changes. Respiratory and swallowing functions were well preserved across the cohort, with no cases requiring tracheostomy or feeding tube placement. Previous studies have reported various intraoperative and postoperative complications associated with CO2 laser surgery, including dental injury, bleeding, thermal burns, and difficulties in lesion removal. For instance, Preuss[ 17 ] et al. documented a complication rate of 5.8% among 275 patients, and Wan[ 18 ] et al. reported 6.6% in a cohort of 500 patients. Although the overall incidence of complications related to CO2 laser surgery remains low, occasional severe events such as endotracheal perforation, bleeding, and respiratory distress have been documented. To minimize TLM-related complications, it is crucial to adhere strictly to laser safety protocols, carefully plan tumor resection with clearly defined anatomical landmarks, and ensure thorough surgical training and experience. 5. CONCLUSION Transoral laser microsurgery demonstrates favorable oncologic efficacy and functional preservation in the treatment of early-stage glottic laryngeal cancer. Our five-year follow-up confirms a high local control rate, favorable overall and disease-specific survival, and minimal postoperative complications. The ability to achieve organ preservation without compromising oncologic safety highlights TLM as a preferred therapeutic option for patients with T1-T2 glottic carcinoma. Careful patient selection, adherence to standardized surgical protocols, and intraoperative margin assessment are essential to optimize outcomes. Declarations ETHICS APPROVAL AND CONSENT TO PARTICIPATE This study was approved by the Ethics Committee in Biomedical Research of the University of Medicine and Pharmacy, Ho Chi Minh City, according to Decision No. 379/ĐHYD-HĐĐĐ. Informed consent was waived due to the retrospective nature of the study and the use of anonymized patient data. FUNDING This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The funding body had no role in the design of the study, collection, analysis, interpretation of data, or writing of the manuscript. Author Contribution N.T.T. conceived the study, collected and analyzed data, and wrote the manuscript. Acknowledgement The authors would like to thank the staff of the Ear Nose Throat Hospital, Ho Chi Minh City, for their support and assistance during the study. Special thanks to the patients who participated in this research. References Reddy SP et al (2007) Effect of tumor bulk on local control and survival of patients with T1 glottic cancer: a 30-year experience. 69(5):1389–1394 Bradley P et al (2009) Consensus statement on management in the UK: transoral laser assisted microsurgical resection of early glottic cancer. Clin Otolaryngol 34(4):367–373 Remacle M et al (2007) Proposal for revision of the European Laryngological Society classification of endoscopic cordectomies. European archives of oto-rhino-laryngology. 264(5):499–504 Hans S et al (2021) Oncological and Surgical Outcomes of Patients Treated by Transoral CO2 Laser Cordectomy for Early-Stage Glottic Squamous Cell Carcinoma: A Retrospective Chart Review. 100(1suppl):33S–37S Hartl DM et al (2007) Treatment of early-stage glottic cancer by transoral laser resection. Annals Otology Rhinology Laryngology 116(11):832–836 Peretti G et al (2003) Vocal outcome after endoscopic cordectomies for Tis and T1 glottic carcinomas. 112(2):174–179 Bocciolini C, Presutti L (2005) J.A.o.i. Laudadio, Oncological outcome after CO2 laser cordectomy for early-stage glottic carcinoma . 25(2):86 Remacle M et al (2010) Is frozen section reliable in transoral CO 2 laser-assisted cordectomies? 267(3):397–400 Motta G et al (1997) T1-T2-T3 glottic tumors: fifteen years experience with CO2 laser. Acta Otolaryngol 117(sup527):155–159 Sigston E et al (2006) Early-stage glottic cancer: oncological results and margins in laser cordectomy. 132(2):147–152 Steiner W et al (2003) Transoral laser microsurgery for squamous cell carcinoma of the base of the tongue. Archives Otolaryngology–Head Neck Surg 129(1):36–43 Crespo AN et al (2006) Role of margin status in recurrence after CO2 laser endoscopic resection of early glottic cancer. Acta Otolaryngol 126(3):306–310 Parker NP et al (2021) KTP laser treatment of early glottic cancer: a multi-institutional retrospective study. Annals of Otology, Rhinology & Laryngology, 130(1): pp. 47–55 Ansarin M et al (2017) Retrospective analysis of factors influencing oncologic outcome in 590 patients with early-intermediate glottic cancer treated by transoral laser microsurgery. Head Neck 39(1):71–81 Choi SY et al (2023) Oncologic Outcomes of T1–T2N0 Glottic Cancer Treatment: Single Center Experiences of 417 Patients Over 20 Years. J Korean Soc Laryngology Phoniatrics Logopedics 34(2):36–44 Jones H, Ross E, Jose J (2021) TLM outcomes in elderly patients with glottic pre-malignancy and early malignancy; A 12-year retrospective study. Annals of Otology, Rhinology & Laryngology, 130(12): pp. 1392–1399 Preuss S et al (2009) Transoral laser surgery for laryngeal cancer: outcome, complications and prognostic factors in 275 patients. 35(3):235–240 Wan G-L, J.-W (2009) .J.S.m.j. Sun, Peri-and post-operative complications after carbon dioxide laser surgery of the larynx . 30(10):1281–1285 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-6706063","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":470200750,"identity":"f2d81163-0c66-4c81-9036-53dceb4b04d9","order_by":0,"name":"Thanh Tuan Nguyen","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABB0lEQVRIiWNgGAWjYPACCTk2+YONDz7+swFyGBsP4FXMxgwiLYz5JZibDWewpYG0NBCjpSJx5gz2NmketsNgQbxazOX7j0n83CFhbHC7sU1yBs95u7Xth4G21NhE49Ji2cbMJtl7RkLO4M7BZosPEreTt51JBGo5lpbbgEOLwTFmNgneNqAtBxIbb84wuJ1sdgCohbHhMF4tkn/bJBI3AFVK8yScSzY7/5CwFmmgLUDvJzZJ8xw4YGd2g6AtycbWskCH8fMcbDac2ZCcYHYDaEsCPr8cPvjw5tu2Ojk29vaHDz422NmbnU9/+OBDjQ1OLRggEawygVjlIGBPiuJRMApGwSgYGQAArQBl3QStFmUAAAAASUVORK5CYII=","orcid":"","institution":"University of Health Sciences, Vietnam National University, Ho Chi Minh City","correspondingAuthor":true,"prefix":"","firstName":"Thanh","middleName":"Tuan","lastName":"Nguyen","suffix":""}],"badges":[],"createdAt":"2025-05-20 09:23:22","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-6706063/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-6706063/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":84777303,"identity":"390f9133-6870-4f08-9141-25e734926d42","added_by":"auto","created_at":"2025-06-17 09:08:35","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":453072,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eTransoral laser microsurgical resection of glottic cancer\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eA. Pre-operation \u0026nbsp;B. Post-operation\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-6706063/v1/1b71ba9eda5ff77be321cbe2.png"},{"id":84777349,"identity":"f4813b8a-a2d6-42ea-a020-b83c01b821ea","added_by":"auto","created_at":"2025-06-17 09:08:37","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":229360,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eFrozen section sample\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-6706063/v1/f0e2b91c916ff8fbec09ad5a.png"},{"id":84777310,"identity":"ebf5b447-5409-41dc-b982-5958a4047340","added_by":"auto","created_at":"2025-06-17 09:08:35","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":21256,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eType of cordectomy according to T-stage\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-6706063/v1/9fdfa098b7107091d9e3bda6.png"},{"id":84777351,"identity":"03e80383-8fb5-46e6-9c99-c25c44797712","added_by":"auto","created_at":"2025-06-17 09:08:37","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":176610,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eTLM complications\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-6706063/v1/f7c93e83d65007f7902f5d4b.png"},{"id":100362466,"identity":"07b3aac6-3eda-478a-b49d-1c422f64fde4","added_by":"auto","created_at":"2026-01-16 07:46:49","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1438643,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-6706063/v1/28cf65d7-a6f2-4387-970b-35c9c6b41d0d.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"\u003cp\u003eFive-Year Outcomes of Transoral Laser Microsurgery for Early-Stage Glottic Cancer: A Single-Center Retrospective Study\u003c/p\u003e","fulltext":[{"header":"1. BACKGROUND","content":"\u003cp\u003eThe larynx plays a vital role in essential physiological functions such as respiration, phonation, and swallowing. Consequently, treatment strategies for laryngeal cancer prioritize organ preservation to maintain these critical functions. Current therapeutic options include transoral laser microsurgery, open surgical techniques, and primary radiotherapy, all of which have been extensively studied and debated in the literature[\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. Among these modalities, transoral laser microsurgery has gained prominence as a preferred treatment approach. This preference is largely due to its advantages, including lower morbidity, favorable functional outcomes, reduced healthcare costs, and shorter hospitalization durations, while demonstrating comparable rates of local control and overall survival to other established treatments[\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eThis study aims to evaluate the clinical outcomes of patients with early-stage glottic laryngeal cancer treated at Ho Chi Minh City ENT Hospital over a five-year period. Specifically, we seek to analyze the effectiveness of different treatment modalities in terms of local control, overall survival, and functional preservation, as well as to identify factors influencing prognosis and treatment-related complications.\u003c/p\u003e"},{"header":"2. METHODS","content":"\u003cp\u003eThis retrospective study included patients diagnosed with early-stage glottic laryngeal cancer (T1-T2) who received treatment at Ho Chi Minh City ENT Hospital between 2018 and 2020. Only patients with complete clinical data and a minimum follow-up period of 5 years post-treatment were included to ensure comprehensive assessment of long-term outcomes. The research protocol was was approved by the Ethics Committee in Biomedical Research of the University of Medicine and Pharmacy, Ho Chi Minh City, according to Decision [No. 379/ĐHYD-HĐĐĐ].\u003c/p\u003e \u003cp\u003ePatient demographic data, tumor characteristics, treatment modalities, and clinical outcomes were collected from medical records. All patients included in this study were treated exclusively with transoral laser microsurgery (Fig.\u0026nbsp;1). The treatment protocol was standardized, according to the European Laryngological Society Classification of Endoscopic Cordectomies[\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eSurgical Margin Assessment with frozen section: Resection the tumor en bloc for frozen section; mark the margins anterior, posterior, external, left and right vocal cord, and dye the deep cut area with suture knots and ink.\u003c/p\u003e \u003cp\u003eEvaluation the margins when the frozen section results are obtained, choose a safety margin of 2 mm on the tissue sample to submit to the pathology. The margins were evaluated by visual examination through the operating microscope (Carl Zeiss, Germany), and by palpation with microforceps (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e2\u003c/span\u003e). If the result is positive, cordectomy will continue to enlarge until all margins are negative.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe primary endpoints were local control rate, overall survival (OS), and disease-free survival (DFS) assessed at 5 years post-treatment. Secondary endpoints included treatment-related complications and functional outcomes such as voice quality and swallowing function.\u003c/p\u003e \u003cp\u003eStatistical analysis was performed using SPSS version XX. Survival rates were estimated using the Kaplan-Meier method, and differences between groups were assessed by the log-rank test. A p-value\u0026thinsp;\u0026lt;\u0026thinsp;0.05 was considered statistically significant.\u003c/p\u003e"},{"header":"3. RESULTS","content":"\u003cp\u003eA total of 96 patients with early-stage glottic laryngeal cancer (T1-T2) treated exclusively by transoral laser microsurgery were included in this study. The median age of the cohort was 61\u0026thinsp;\u0026plusmn;\u0026thinsp;9 years olds, the youngest was 33 years old, the oldest was 89 years old; The most affected age is from 51 to 60 years old (43.8%); with a male predominance accounting for 96.9% of cases. Regarding risk factors for laryngeal cancer, the vast majority of patients (97.9%) had a history of smoking, while only 2 patients (2.1%) reported no history of tobacco use.\u003c/p\u003e \u003cp\u003eIn terms of clinical characteristics: All patients presented with hoarseness, which was the sole functional symptom observed. Notably, 81.3% of patients sought medical consultation within 6 months of symptom onset. Concerning tumor staging, 85.4% of patients were diagnosed with stage T1N0M0 laryngeal cancer. Among these, 83.3% were classified specifically as T1bN0M0, while only 6 patients (6.25%) had stage T2N0M0 disease at the time of surgery.\u003c/p\u003e \u003cp\u003eTreatment outcomes:\u003c/p\u003e \u003cp\u003eAll patients underwent standardized transoral laser cordectomy based on the European Laryngological Society Classification of Endoscopic Cordectomies[\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]. Regarding the surgical techniques applied (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003e), the distribution of cordectomy types was as follows: 43 patients (44.8%) underwent Type III cordectomy, 36 patients (37.5%) received Type IV, 11 patients (11.5%) underwent Type Va, and 6 patients (6.3%) were treated with Type Vb cordectomy. The median follow-up period was 60 months (range: 60\u0026ndash;72 months), ensuring a minimum follow-up duration of five years for all cases.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eAll patients were confirmed to have squamous cell carcinoma (100%) on histopathology, with grade 2 tumors accounting for the majority (59.4%). Negative resection margins were achieved in 72,9% of cases; close or positive margins were found in the remainder but were managed by second-look procedures where indicated.\u003c/p\u003e \u003cp\u003eOncologic outcomes: At 5 years, the local control rate was 91.7%, with 8 patients (8.3%) experiencing local recurrence. All recurrences were managed with total laryngectomy. This corresponds to a larynx-preservation rate of 100%. The 5-year overall survival (OS) rate was 89.6%, and disease-specific survival (DSS) was 100%.\u003c/p\u003e \u003cp\u003ePostoperative Complications (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e4\u003c/span\u003e): Among the 96 patients, we observed four cases of postoperative bleeding at the surgical site (4.17%). These included one patient with a posterior vocal cord injury extending from the glottis, one patient following a Type Va cordectomy, and two patients after Type Vb procedures. All cases were successfully managed with electrocauterization at the resection site. Subcutaneous emphysema occurred in three patients (3.13%). These cases presented with mild emphysema localized around the thyroid cartilage immediately postoperatively and resolved spontaneously within one week under observation. Severe inflammatory granulation tissue developed in ten patients (10.4%) during follow-up, all of whom required surgical excision. Additionally, four patients (4.2%) developed significant laryngeal scarring, which also required surgical intervention for symptomatic relief and airway patency.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eFunctional and postoperative outcomes: Most patients reported satisfactory voice and swallowing function at follow-up. No permanent tracheostomy or feeding tube was required. Transient postoperative complications, such as mild edema or pain, were observed in a minority of cases.\u003c/p\u003e \u003cp\u003eSubgroup analysis: T2N0M0 patients showed a slightly higher recurrence rate than T1, echoing trends in international cohorts where local control in T2 disease remains more challenging. However, no statistically significant differences in survival or larynx preservation were observed.\u003c/p\u003e"},{"header":"4. DISCUSSION","content":"\u003cp\u003eTransoral laser microsurgery (TLM) is indicated for patients who can tolerate direct rigid laryngoscopy under general anesthesia. One of the primary technical challenges lies in adequately exposing tumors involving the anterior commissure. During TLM, tumor resection is performed with the goal of achieving negative surgical margins, often guided by intraoperative frozen section analysis; however, the definition of a safe margin remains a subject of ongoing debate[\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. Consequently, the success of TLM largely depends on the surgeon\u0026rsquo;s expertise and intraoperative judgment in determining the appropriate extent of cordectomy.\u003c/p\u003e \u003cp\u003eThe mean age of patients at diagnosis was 61 years, ranging from 33 to 89 years, with the majority (43.8%) falling within the 51\u0026ndash;60 age group. This distribution aligns closely with findings reported by Hartl[\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e] and Peretti[\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e], reflecting the typical onset of laryngeal cancer during middle age, a period when cumulative exposure to risk factors such as tobacco and alcohol reaches a critical threshold. Regarding gender distribution, males constituted the overwhelming majority of cases, a pattern that differs from studies by Bocciolini[\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e] and Remacle[\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e], where female representation was comparatively higher. This discrepancy may be attributed to variations in smoking and alcohol consumption prevalence among women across different countries, including a historically lower rate in Vietnam, although recent trends suggest these patterns are evolving.\u003c/p\u003e \u003cp\u003eRegarding lesion classification and surgical indications, the majority of our cases were stage T1a (85.4%), followed by 8.3% at T1b, and only 6 patients (6.3%) with stage T2N0M0 disease. In comparison, Giovanni Motta\u0026rsquo;s study[\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e], which analyzed CO2 laser surgery outcomes in 719 patients, reported a distribution of 432 T1, 236 T2, and 51 T3 tumors. Early in our study period, due to limited experience and suboptimal equipment, we primarily restricted surgical indications to T1 glottic cancers and selected early T2 cases. Nevertheless, it remains essential to proceed cautiously to maintain oncologic safety and ensure appropriate lesion selection.\u003c/p\u003e \u003cp\u003eIn our cohort, Type III cordectomy was performed in 44.8% of patients, followed by Type IV in 37.5%, Type Va in 11.5%, and Type Vb in 6.3%. Compared to the findings of Sigston et al.[\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e], our study shows a higher proportion of Type IV and Va cordectomies among patients with stage T1 disease, which may be attributable to the greater incidence of lesions involving the anterior commissure in our population. The utilization of Type Va cordectomy in our series aligns with Peretti\u0026rsquo;s description[\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e] for lesions extending across the anterior commissure of the vocal cords. This surgical approach entails removal of the entire ipsilateral vocal cord, the anterior commissure, and a portion of the contralateral vocal cord, along with dissection of the perichondrium on the inner aspect of the thyroid cartilage at the anterior commissure. However, the indication for endoscopic cordectomy in cases with anterior commissure involvement remains controversial, as noted by both Peretti[\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e] and Steiner[\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e], due to concerns regarding oncologic safety and functional outcomes.\u003c/p\u003e \u003cp\u003eIn our study, all patients were diagnosed with squamous cell carcinoma (100%), with grade 2 tumors representing the majority (59.4%). During cordectomy, careful assessment of tumor extension is critical for planning the resection to ensure complete removal while minimizing the risk of residual disease. Therefore, establishing an adequate safety margin around the tumor is essential. In this study, intraoperative frozen section analysis was routinely performed to confirm clear margins. We adopted a safety margin of 2 mm, in accordance with criteria proposed by Crespo[\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e] and Remacle[\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. If a positive margin was identified, the resection was extended until all surgical margins were confirmed to be free of tumor.\u003c/p\u003e \u003cp\u003eOur 5-year follow-up demonstrated a high local control rate of 91.7%, which is within the range reported in the international literature (2.3\u0026ndash;10.8% recurrence) and comparable to other large cohort studies Parker et al.[\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e] and Ansarin et al.[\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. The absence of total laryngectomy or adjuvant radiotherapy in managing recurrences underlines the effectiveness of TLM in organ preservation, reflected in our larynx-preservation rate of 100%. Survival outcomes were favorable, with a 5-year overall survival of 89.6% and disease-specific survival of 100%. These findings are consistent with previously published data Choi et al.[\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e] and Jones et al[\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e] supporting TLM as an oncologically sound and functionally preservative treatment modality for early glottic cancer.\u003c/p\u003e \u003cp\u003eIn this study, surgical site bleeding was observed in 4.2% of patients, while subcutaneous emphysema occurred in 3.1%. Granulation tissue formation was noted in 14.6% of cases, with 7.3% progressing to laryngeal stenosis. Among these, four patients with severe stenosis underwent laryngoplasty, and three with mild stenosis were managed conservatively through follow-up. At the final assessment, 35.4% of patients retained normal voice quality, and an additional 52.1% experienced only mild to moderate voice changes. Respiratory and swallowing functions were well preserved across the cohort, with no cases requiring tracheostomy or feeding tube placement. Previous studies have reported various intraoperative and postoperative complications associated with CO2 laser surgery, including dental injury, bleeding, thermal burns, and difficulties in lesion removal. For instance, Preuss[\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e] et al. documented a complication rate of 5.8% among 275 patients, and Wan[\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e] et al. reported 6.6% in a cohort of 500 patients. Although the overall incidence of complications related to CO2 laser surgery remains low, occasional severe events such as endotracheal perforation, bleeding, and respiratory distress have been documented. To minimize TLM-related complications, it is crucial to adhere strictly to laser safety protocols, carefully plan tumor resection with clearly defined anatomical landmarks, and ensure thorough surgical training and experience.\u003c/p\u003e"},{"header":"5. CONCLUSION","content":"\u003cp\u003eTransoral laser microsurgery demonstrates favorable oncologic efficacy and functional preservation in the treatment of early-stage glottic laryngeal cancer. Our five-year follow-up confirms a high local control rate, favorable overall and disease-specific survival, and minimal postoperative complications. The ability to achieve organ preservation without compromising oncologic safety highlights TLM as a preferred therapeutic option for patients with T1-T2 glottic carcinoma. Careful patient selection, adherence to standardized surgical protocols, and intraoperative margin assessment are essential to optimize outcomes.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eETHICS APPROVAL AND CONSENT TO PARTICIPATE\u003c/h2\u003e\n\u003cp\u003eThis study was approved by the Ethics Committee in Biomedical Research of the University of Medicine and Pharmacy, Ho Chi Minh City, according to Decision No. 379/ĐHYD-HĐĐĐ. Informed consent was waived due to the retrospective nature of the study and the use of anonymized patient data.\u003c/p\u003e\n\u003ch2\u003eFUNDING\u003c/h2\u003e\n\u003cp\u003eThis research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The funding body had no role in the design of the study, collection, analysis, interpretation of data, or writing of the manuscript.\u003c/p\u003e\n\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\n\u003cp\u003eN.T.T. conceived the study, collected and analyzed data, and wrote the manuscript.\u003c/p\u003e\n\u003ch2\u003eAcknowledgement\u003c/h2\u003e\n\u003cp\u003eThe authors would like to thank the staff of the Ear Nose Throat Hospital, Ho Chi Minh City, for their support and assistance during the study. Special thanks to the patients who participated in this research.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eReddy SP et al (2007) Effect of tumor bulk on local control and survival of patients with T1 glottic cancer: a 30-year experience. 69(5):1389\u0026ndash;1394\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBradley P et al (2009) Consensus statement on management in the UK: transoral laser assisted microsurgical resection of early glottic cancer. Clin Otolaryngol 34(4):367\u0026ndash;373\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRemacle M et al (2007) \u003cem\u003eProposal for revision of the European Laryngological Society classification of endoscopic cordectomies.\u003c/em\u003e European archives of oto-rhino-laryngology. 264(5):499\u0026ndash;504\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHans S et al (2021) Oncological and Surgical Outcomes of Patients Treated by Transoral CO2 Laser Cordectomy for Early-Stage Glottic Squamous Cell Carcinoma: A Retrospective Chart Review. 100(1suppl):33S\u0026ndash;37S\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHartl DM et al (2007) Treatment of early-stage glottic cancer by transoral laser resection. Annals Otology Rhinology Laryngology 116(11):832\u0026ndash;836\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePeretti G et al (2003) Vocal outcome after endoscopic cordectomies for Tis and T1 glottic carcinomas. 112(2):174\u0026ndash;179\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBocciolini C, Presutti L (2005) J.A.o.i. Laudadio, \u003cem\u003eOncological outcome after CO2 laser cordectomy for early-stage glottic carcinoma\u003c/em\u003e. 25(2):86\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRemacle M et al (2010) Is frozen section reliable in transoral CO 2 laser-assisted cordectomies? 267(3):397\u0026ndash;400\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMotta G et al (1997) T1-T2-T3 glottic tumors: fifteen years experience with CO2 laser. Acta Otolaryngol 117(sup527):155\u0026ndash;159\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSigston E et al (2006) Early-stage glottic cancer: oncological results and margins in laser cordectomy. 132(2):147\u0026ndash;152\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSteiner W et al (2003) Transoral laser microsurgery for squamous cell carcinoma of the base of the tongue. Archives Otolaryngology\u0026ndash;Head Neck Surg 129(1):36\u0026ndash;43\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCrespo AN et al (2006) Role of margin status in recurrence after CO2 laser endoscopic resection of early glottic cancer. Acta Otolaryngol 126(3):306\u0026ndash;310\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eParker NP et al (2021) \u003cem\u003eKTP laser treatment of early glottic cancer: a multi-institutional retrospective study.\u003c/em\u003e Annals of Otology, Rhinology \u0026amp; Laryngology, 130(1): pp. 47\u0026ndash;55\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAnsarin M et al (2017) Retrospective analysis of factors influencing oncologic outcome in 590 patients with early-intermediate glottic cancer treated by transoral laser microsurgery. Head Neck 39(1):71\u0026ndash;81\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChoi SY et al (2023) Oncologic Outcomes of T1\u0026ndash;T2N0 Glottic Cancer Treatment: Single Center Experiences of 417 Patients Over 20 Years. J Korean Soc Laryngology Phoniatrics Logopedics 34(2):36\u0026ndash;44\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJones H, Ross E, Jose J (2021) \u003cem\u003eTLM outcomes in elderly patients with glottic pre-malignancy and early malignancy; A 12-year retrospective study.\u003c/em\u003e Annals of Otology, Rhinology \u0026amp; Laryngology, 130(12): pp. 1392\u0026ndash;1399\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePreuss S et al (2009) Transoral laser surgery for laryngeal cancer: outcome, complications and prognostic factors in 275 patients. 35(3):235\u0026ndash;240\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWan G-L, J.-W (2009) .J.S.m.j. Sun, \u003cem\u003ePeri-and post-operative complications after carbon dioxide laser surgery of the larynx\u003c/em\u003e. 30(10):1281\u0026ndash;1285\u003c/span\u003e\u003c/li\u003e\u003c/ol\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":"Glottic cancer, Transoral laser microsurgery, Organ preservation","lastPublishedDoi":"10.21203/rs.3.rs-6706063/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-6706063/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eThis study aimed to evaluate the clinical and functional outcomes of patients with early-stage glottic laryngeal cancer treated by transoral laser microsurgery (TLM) at Ho Chi Minh City ENT Hospital over a five-year period.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eNinety-six patients diagnosed with T1-T2N0M0 glottic squamous cell carcinoma and treated exclusively with TLM between 2018 and 2020 were included. Surgical procedures were performed according to the European Laryngological Society classification of endoscopic cordectomies. Outcomes assessed included local control, overall survival (OS), disease-specific survival (DSS), postoperative complications, and functional voice and swallowing preservation over a minimum follow-up of 5 years.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eThe 5-year local control rate was 91.7%, with an overall survival rate of 89.6% and disease-specific survival of 100%. Postoperative complications were minimal and manageable, with no permanent tracheostomy or feeding tubes required. The majority of patients maintained satisfactory voice and swallowing function.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eTransoral laser microsurgery (TLM) demonstrates favorable oncologic efficacy and functional preservation in the treatment of early-stage glottic laryngeal cancer. The ability to achieve organ preservation without compromising oncologic safety highlights TLM as a preferred therapeutic option for patients with T1-T2 glottic carcinoma.\u003c/p\u003e","manuscriptTitle":"Five-Year Outcomes of Transoral Laser Microsurgery for Early-Stage Glottic Cancer: A Single-Center Retrospective Study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-06-17 09:08:11","doi":"10.21203/rs.3.rs-6706063/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":"d2f153c6-1ecb-4746-95f0-2eb1ca15a824","owner":[],"postedDate":"June 17th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2026-01-12T06:54:13+00:00","versionOfRecord":[],"versionCreatedAt":"2025-06-17 09:08:11","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-6706063","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-6706063","identity":"rs-6706063","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}