Cumulative sum analysis for evaluating learning curve of endoscopic lateral neck dissection | 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 Cumulative sum analysis for evaluating learning curve of endoscopic lateral neck dissection Zhen-Xin Chen, Xin-Ran Zhao, Jie-Min Deng, Ying Cao, Jing-Bao Chen, and 5 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4259154/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 26 Nov, 2024 Read the published version in BMC Surgery → Version 1 posted 4 You are reading this latest preprint version Abstract Objectives Endoscopic lateral neck dissection (LND) can be a scarless procedure if a surgeon has performed a sufficient number of operations to become skilled at the techniques involved. Here, we examine the learning curve for a surgeon who performed 53 endoscopic LND procedures via chest approach. Methods Surgical outcomes for 53 patients with papillary thyroid carcinoma who underwent endoscopic LND via chest approach between February 2017 and November 2022 were retrospectively reviewed. The surgeon’s learning curve was evaluated using a cumulative sum graphic model (CUSUM). Results A CUSUM analysis was applied to 53 patients (10 males, 43 females) with a mean age of 41.4 y who underwent endoscopic LND via chest approach. The best model for the curve was determined to be a third-order polynomial equation as follows: CUSUM OT = − 0.007×patient number 3 -0.666×patient number 2 + 55.721×patient number − 72.964. This equation has a high R 2 value of 0.929. The peak operative time (OT) occurred at the 30th case. Consequently, the learning curve model was divided into two phases: phase 1 (1–30 cases) and phase 2 (31–53 cases). OT (307.9 ± 63.8 min vs. 232.4 ± 44.2 min, respectively; p < 0.001), blood loss (50 mL vs. 20 mL, respectively; p = 0.001), and complications (43.3% vs. 13.0%, respectively; p = 0.038) decreased significantly in phase 2 compared to phase 1. Conclusions The learning curve of endoscopic LND via chest approach was found to involve 30 cases. With greater experience, the surgery was completed with shorter OT and fewer complications. This approach is an alternative for patients who desire cosmesis. Furthermore, the present data and experience insights regarding endoscopic LND via chest approach may help other surgeons to pass the learning phase more safely. Papillary thyroid carcinoma Endoscopic lateral neck dissection Chest approach Learning Curve Cumulative sum graphic model Figures Figure 1 Figure 2 Figure 3 Introduction In 1996, endoscopic parathyroidectomy was first reported[1]. Since then, various endoscopic and robotic approaches have been developed and improved to achieve less visible scars and better cosmetic results. Most recently, endoscopic and robotic approaches are commonly used to perform total thyroidectomy and central lymph node dissection[2, 3]. Over 30% of papillary thyroid carcinoma (PTC) patients have been diagnosed with cervical lateral lymph node metastasis[4–8]. For these patients, lateral neck dissection (LND) is an effective treatment to improve prognosis[9, 10]. However, complete endoscopic LND is a technically challenging procedure, and has only been reported in a few studies[11–13]. Here, we demonstrate the feasibility of endoscopic LND via chest approach by summarizing early cases of our previous study[14]. Due to the complexity and difficulty of performing endoscopic LND, surgeons need sufficient experience with the procedure to attain proficiency. An alternative approach to obtaining surgical experience is to study the learning curve of a procedure. To date, little attention has been focused on the learning curve for endoscopic LND via chest approach. Cumulative sum (CUSUM) is an analytic technique for detecting change. Here, the CUSUM was applied to evaluate a learning curve for endoscopic LND via chest approach with a graphic model. These data may help other surgical teams’ progress through the learning phase more safely and rapidly. Materials and Methods 2.1 Patients and inclusion criteria This study was approved by the Institutional Review Board (IRB) for ethics at the Guangdong Provincial Hospital of Traditional Chinese Medicine (Guangdong, China). Clinical data for 53 patients with PTC who underwent endoscopic LND via chest approach at our center between February 2017 and November 2022 were retrospectively assessed. All 53 patients were operated on by the same surgical team, with You Qin serving as the main surgeon. This surgical team completed over 2000 cases of endoscopic thyroidectomy in total. An early study on endoscopic LND has been published[14]. Inclusion criteria for the present study were: 1) confirmed case of PTC with metastatic lymph nodes at levels II, III, or IV based on ultrasonography, computed tomography, fine needle aspiration cytology, or intra-operative exploration; and 2) patients elected to undergo endoscopic surgery. Exclusion criteria were: 1) invasion of surrounding tissues; 2) level I/V metastatic lymph nodes; 3) distant metastasis; 4) past medical history of neck surgery or radiotherapy; and 5) inability to tolerate anesthesia or surgery. 2.2 Operative procedure Briefly, a 12-mm incision was initially made parasternally at nipple level before a 10-mm trocar was inserted through the incision. A 5-mm trocar was set at the 10–11 o’clock position on the left side of the areola, while another 5-mm trocar was set at the 1–2 o’clock position on the right side of the areola (Fig. 1 ). CO 2 gas was insufflated at 6 mmHg pressure with high flow. A 10-mm 30° laparoscope was inserted through the 10-mm trocar. Next, subcutaneous loose connective tissue was separated to establish an initial working space, and to conduct a total thyroidectomy and central lymph node dissection. After completing these steps, endoscopic LND was performed. A working space was established from the posterior border of the sternocleidomastoid (SCM) laterally to the posterior belly of the digastric muscle superiorly. Then, a longitudinal incision in the SCM at the site between its sternal head and the clavicular head was made. The incision extended to the level of the carotid bifurcation superiorly. With assistance from two retractors pulling on the sternal head and clavicular head of the SCM, respectively, the lymph nodes between the SCM and sternohyoid muscle were dissected. Next, the internal jugular vein (IJV) was cautiously dissected to the cricoid cartilage superiorly and the venous angle inferiorly, followed by exposure of the omohyoid. An assistant then pulled the IJV and sternal head of the SCM to the tracheal side with a retractor, while another assistant pulled the clavicular head to the opposite side. Level IV lymph nodes were cleaned. To continue lymph node dissection, the assistants moved up the retractors and pulled both the sternal head and clavicular head of the SCM as described above. Level III lymph nodes were then exposed and cleaned. At this point, the assistant turned to pull the sternum head of the SCM away from the trachea, and the space between the cervical anterior muscles and the SCM were dissected to expose and clean the lymph nodes at the carotid triangle. The final step of the lymph node dissection involved sequential cleaning of the lymph nodes at levels IIa and IIb. Lymph nodes in this compartment to the lower edge of the digastric muscle superiorly and to the posterior border of the SCM laterally were dissected as well. Precautions observed for each surgical step of the endoscopic LND procedure have previously been described[14]. All of the resected lymph nodes were taken out from the observation hole in a specimen bag. After the operative field was rinsed with distilled water and drainage tubes were placed (Fig. 1 ), both linea alba cervicalis and chest incisions were closed with absorbable sutures. 2.3 Learning curve analysis The OT for each patient was documented chronologically from the first case to the last case to evaluate the progress of endoscopic LND. The CUSUM OT for the first patient was calculated according to the difference between the OT of the first patient and the mean OT of all the enrolled patients. The CUSUM OT for the second patient was the CUSUM OT of the first patient plus the difference between the OT of the second patient and the mean OT of all the enrolled patients. Similarly, the CUSUM OT for the remaining patients were determined. CUSUM analysis was used to analyze the learning curve. 2.4 Statistical Analysis Data were analyzed using SPSS 18.0 software. To analyze frequency differences between the groups, the Chi-square test or Fisher’s exact test was applied to categorical data. The Wilcoxon rank sum test or independent Student’s t -test was applied to continuous data. A p-value less than 0.05 was considered statistically significant and all statistical tests were two-sided. Results Patient Cohort and Surgery Outcomes All 53 of the enrolled PTC patients successfully underwent endoscopic LND (including endoscopic total thyroidectomy and central neck dissection). In addition, none required conversion to open surgery. Of the 53 patients, 43 (81.1%) were female and the average age of the cohort was 41.4 ± 12.7 y. Mean tumor size was 1.6 ± 1.0 cm and the numbers of lymph nodes retrieved from the lateral and central compartments were 21.9 ± 8.9 and 8.7 ± 6.5, respectively. The average OT for all of the cases was 275.1 ± 67.3 min. Mean blood loss was 42.0 ± 44.2 mL. Postoperatively, the mean hospital stay after surgery was 5.7 ± 1.5 d. Lymphatic leakage and accessory nerve injury were observed in 2 (3.8%) and 3 (5.7%) patients, respectively. Eight patients (15.1%) had cervical plexus injury, one patient (1.9%) had hypoglossal nerve injury, and three patients (5.7%) had IJV injury. Postoperative bleeding, carotid artery injury, or phrenic nerve injury were not reported (Table 1 ). During the follow-up period of 38.8 ± 15.7 months, tumor recurrence was not detected. Table 1 Clinical outcomes of PTC patients who underwent endoscopic LND via chest approach. Variable Value Age 41.4 ± 12.7 Gender (Female/Male) 43 / 10 Tumor size (cm) 1.6 ± 1.0 Hospital stay (d) 5.7 ± 1.5 Blood loss (mL) 42.0 ± 44.2 Operative time (min) 275.1 ± 67.3 No. of retrieved lymph nodes 30.5 ± 11.3 Lateral 21.9 ± 8.9 Central 8.7 ± 6.5 Complications of lateral neck dissection 17 Lymphatic leakage 2 Cervical plexus injury a 8 Accessory nerve injury 3 Hypoglossal nerve injury 1 Internal jugular vein injury Other complications b 3 0 a Identification of cervical plexus injury is based on intraoperative cervical plexus transection; b including phrenic nerve injury, carotid artery injury and postoperative bleeding. Learning Curve Analysis OTs for the individual PTC patients were plotted according to the chronological sequence of their cases (Fig. 2 ). CUSUM analysis was subsequently performed to establish a learning curve for endoscopic LND based on these cases (Fig. 3 ). The best model for the curve was determined to be a third-order polynomial equation as follows: CUSUM OT = − 0.007×patient number 3 -0.666×patient number 2 + 55.721×patient number − 72.964. This equation has a high R 2 value of 0.929. The CUSUM OT revealed a curve exhibiting a positive slope from the initial case to case 30, while a negative slope after case 31 was observed. Thus, the curve helped identify a learning phase (cases 1–30) and a mature phase (cases 31–53), according to slope. Differences in Clinical Outcome According to Phases determined by CUSUM Learning Curve Analysis Clinical outcomes between phase 1 and phase 2 are presented in Table 2 . No significant differences in age, gender, tumor size, hospital stay after surgery, and/or number of retrieved lymph nodes between the two phases were observed. However, greater blood loss (p = 0.001), longer OT (p < 0.001), and a greater number of complications (p = 0.038) occurred in phase 1. Table 2 Comparison of clinical outcomes between phases. Variable Phase 1 (n = 30) Phase 2 (n = 23) p -value Age 41.0 ± 12.8 42.0 ± 12.9 0.782 Gender (Female/Male) 23 / 7 20 / 3 0.552 Tumor size (cm) 1.15 (0.2, 4.3) 1.2 (0.15, 3) 0.336 Hospital stay (d) 5.5 (4, 11) 5 (3, 9) 0.089 Blood loss (mL) 50 (10, 300) 20 (5, 100) 0.001 Operative time (min) 307.9 ± 63.8 232.4 ± 44.2 < 0.001 No. of retrieved lymph nodes 32.1 ± 12.0 28.3 ± 10.3 0.221 Lateral 22.9 ± 8.8 20.6 ± 9.0 0.348 Central 9.2 ± 7.3 8.0 ± 5.4 0.523 Complications of lateral neck dissection 13 a 3 0.038 Lymphatic leakage 1 1 1.000 Cervical plexus injury 7 1 0.127 Accessory nerve injury 3 0 0.249 Hypoglossal nerve injury 1 0 1.000 Internal jugular vein injury 2 1 1.000 a One patient experienced cervical plexus injury and accessory nerve injury. Discussion Neck appearance after open LND has been shown to negatively impact patient quality of life[15, 16]. Therefore, many different approaches for achieving “scarless” LND have been reported, including robotic approaches[17–19]and endoscopic approaches[20, 21]. However, due to the high cost of robotic instruments, the former have had limited application. In contrast, endoscopic LND via a chest approach is currently the most popular method among endoscopic approaches[11, 14, 20, 22]. Since the learning curve has not been examined for the latter approach, CUSUM was applied in this study. The mature phase on the CUSUM curve indicates that the learning curve for the procedure has been overcome. Moreover, it was observed that surgeons needed to have completed 30 cases to gain proficiency with endoscopic LND. When comparing phase 1 and phase 2 of the CUSUM curve in the present study, the incidence of complications and volume of blood loss decreased significantly in phase 2. Thus, a sufficient number of surgical cases (in this study, 30 cases) are needed for surgeons to achieve shorter OTs and reduce possible complications. While the OT in phase 1 was longer, there was no significant difference in the number of retrieved lymph nodes in phase 1 compared with phase 2. In addition, recurrence did not occur during phase 1. Taken together, these data reveal that even for beginners, as long as they exhibit sufficient patience and adherence to the techniques required to complete LND, oncological safety can be achieved during the learning phase. Yan et al.[12] previously reported 155 cases of endoscopic LND via chest approach. The OT in the present study (275.1 ± 67.3 min) versus in Yan’s study (278.2 ± 38.6 min), as well as the number of retrieved lateral lymph nodes (21.9 ± 8.9 vs. 22.9 ± 9.9, respectively), are similar. However, the incidence of lymphatic leakage (3.8% vs. 2.6%, respectively) and accessory nerve injury (5.7% vs. 3.9%, respectively) in the present study were slighter higher than in Yan’s study. We hypothesize that a lack of experience during the learning phase of a procedure leads to a high incidence of complications. As the number of surgical cases increases, the incidence of complications should gradually decrease. The conclusions of this study support this hypothesis. Regarding the management of postoperative complications, we provide some of our methods for reference. For lymphatic leakage, we usually apply a pressure bandage to the site of leakage. If this conservative treatment fails, ligation of the thoracic duct is performed. When dealing with IJV injuries, we use a 5 − 0 prolene suture for endoscopic vascular repair. While this is a rather challenging approach, all three cases of IJV injuries have been successfully repaired. Regarding nerve injury, the primary treatment is administration of neurotrophic drugs following surgery. Use of prolene suture to perform nerve repair endoscopically has also been undertaken. However, neither of these methods have achieved satisfactory results. Our further suggestions regarding endoscopic LND are as follows. First, from early experience, we conclude that the risk of complications increases during hemostasis. However, as proficiency improves, both blood loss and complications are significantly reduced. Therefore, we advocate that surgeons in their early experience pay attention to the protection of thick vessels, such as facial vein, IJV, and communicating branches of the internal and external jugular veins. Second, a fixed surgical team can facilitate advancing the learning curve as safely as possible. Finally, we suggest that endoscopic LND should be performed at centers with experience in endoscopic thyroidectomy via chest approach. The procedures required for endoscopic LND are complex and difficult. It is nearly impossible for a completely inexperienced surgeon to calmly respond to emergencies that may arise during surgery, and patient safety must be of utmost concern. Serious complications can also affect the confidence of a surgeon while completing the operation. Dr. You Qin performed the first endoscopic thyroid surgery via chest approach in 2006, and is also an expert in endoscopic gastrointestinal surgery and endoscopic hernia surgery. Thus, he possesses proficient techniques in endoscopic surgery. In summary, endoscopic LND requires a fixed surgical team to accumulate experience by which the feasibility and safety of a procedure can be determined. Based on the present data, we demonstrate that a main surgeon with previous experience in endoscopic thyroid surgery can overcome the learning curve of endoscopic LND after 30 cases. It is anticipated that our experience may help other surgical teams to progress through the learning curve of endoscopic LND more smoothly and safely. Abbreviations lateral neck dissection (LND) cumulative sum (CUSUM) operative time (OT) papillary thyroid carcinoma (PTC) Institutional Review Board (IRB) sternocleidomastoid (SCM) internal jugular vein (IJV) Declarations Ethics approval and consent to participate The study protocol was approved by the Institutional Review Board for ethics at the Guangdong Provincial Hospital of Traditional Chinese Medicine. The research reported in this paper was in compliance with the Helsinki Declaration. Informed Consent to participate was given by all patients. Consent for publication Written consent to participate included permission to access specimens and clinical details, and to publish findings. Availability of data and materials The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request. Competing interests The authors declare no competing interest. Funding None. Contributions ZXC and XRZ designed the concept of this study. JMD, YC, JBC, FSP, ZHL and XBZ collected the datasets. ZXC and XRZ analyzed the data and wrote the manuscript. BX and YQ revised the manuscript. All authors have read and approved the manuscript. Acknowledgments The authors thank Medjaden Bioscience Limited for linguistic revision of the manuscript. References Gagner M (1996) Endoscopic subtotal parathyroidectomy in patients with primary hyperparathyroidism. Br J Surg 83 : 875 Kim YS, Joo KH, Park SC, Kim KH, Ahn CH, Kim JS (2014) Endoscopic thyroid surgery via a breast approach: a single institution's experiences. 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Arch Otolaryngol Head Neck Surg 132 : 662-666 Shah S, Har-El G, Rosenfeld RM (2001) Short-term and long-term quality of life after neck dissection. Head Neck 23 : 954-961 Kim JK, Lee CR, Kang SW, Jeong JJ, Nam KH, Chung WY (2022) Robotic transaxillary lateral neck dissection for thyroid cancer: learning experience from 500 cases. Surg Endosc 36 : 2436-2444 Lira RB, Chulam TC, Kowalski LP (2018) Variations and results of retroauricular robotic thyroid surgery associated or not with neck dissection. Gland Surg 7 : S42-S52 He Q, Zhu J, Zhuang D, Fan Z, Zheng L, Zhou P, Yu F, Wang G, Ni G, Dong X, Wang M, Li X, Liu C, Wang D, Yue T, Hou L, Wang M, Li D (2020) Robotic lateral cervical lymph node dissection via bilateral axillo-breast approach for papillary thyroid carcinoma: a single-center experience of 260 cases. 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Cite Share Download PDF Status: Published Journal Publication published 26 Nov, 2024 Read the published version in BMC Surgery → Version 1 posted Editorial decision: Revision requested 08 May, 2024 Editor assigned by journal 08 May, 2024 Submission checks completed at journal 25 Apr, 2024 First submitted to journal 12 Apr, 2024 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. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. 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-4259154","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":295423213,"identity":"5c794157-9798-45f0-8d7d-4c796d8a3c1a","order_by":0,"name":"Zhen-Xin Chen","email":"","orcid":"","institution":"First Affiliated Hospital of Jinan University","correspondingAuthor":false,"prefix":"","firstName":"Zhen-Xin","middleName":"","lastName":"Chen","suffix":""},{"id":295423215,"identity":"53ca64c4-3349-49a6-8fbf-01d25b78956c","order_by":1,"name":"Xin-Ran Zhao","email":"","orcid":"","institution":"The Second Affiliated Hospital of Guangzhou 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Qin","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAu0lEQVRIiWNgGAWjYJCCAyCCn5n58APStEi2s6UZkGaVwXkeBQmiVMr7H954uLDNJnHzYR4GA4Yam2iCWgwPHCs4PLMtLXHbYd4DDxiOpeU2ENTS2GNwmLftMFALX4IBY8NhIrQ080C0bAYyJIjSIs8G1bKBmVgtBjxsBYd5zqUZzzgMDOQEYvwi339482eeMhvZ/v7Dhx98qLEhwpYDwKBlZIPyEggpB9vSANTC8IcYpaNgFIyCUTBiAQCoFEDimFqK8wAAAABJRU5ErkJggg==","orcid":"","institution":"The Second Affiliated Hospital of Guangzhou University of Chinese Medicine (Guangdong Provincial Hospital of TCM)","correspondingAuthor":true,"prefix":"","firstName":"You","middleName":"","lastName":"Qin","suffix":""}],"badges":[],"createdAt":"2024-04-12 17:29:26","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4259154/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4259154/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s12893-024-02666-y","type":"published","date":"2024-11-26T15:56:59+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":55765130,"identity":"62cb11c6-1bb1-400f-9348-a303693f5a07","added_by":"auto","created_at":"2024-05-02 20:05:56","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":2522629,"visible":true,"origin":"","legend":"\u003cp\u003eEndoscopic LND via chest approach. A) Design of trocar placement before surgery; B) Drainage tube placement after surgery; C-H) Photos taken during surgery.\u003c/p\u003e","description":"","filename":"Fig.1.png","url":"https://assets-eu.researchsquare.com/files/rs-4259154/v1/ffc2e00989ce100c10beb80e.png"},{"id":55765129,"identity":"7da696ac-9d0e-40c5-9f65-1d6c70ea5c98","added_by":"auto","created_at":"2024-05-02 20:05:56","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":71477,"visible":true,"origin":"","legend":"\u003cp\u003eOT of endoscopic LND plotted according to cases examined in chronological sequence.\u003c/p\u003e","description":"","filename":"Fig.2.png","url":"https://assets-eu.researchsquare.com/files/rs-4259154/v1/1b855c607ef6d8d24b9a2fbe.png"},{"id":55765131,"identity":"1bedd777-e677-4428-b989-390e4cd672f7","added_by":"auto","created_at":"2024-05-02 20:05:56","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":80283,"visible":true,"origin":"","legend":"\u003cp\u003eLearning curve for endoscopic LND according to the CUSUM method.\u003c/p\u003e","description":"","filename":"Fig.3.png","url":"https://assets-eu.researchsquare.com/files/rs-4259154/v1/393efdceb90eee91fce82af6.png"},{"id":70381786,"identity":"f1c64a81-c826-477c-8e45-100545a95232","added_by":"auto","created_at":"2024-12-02 16:14:47","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":4168294,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4259154/v1/02ca76be-c2c1-46c9-aa6d-3d7c4a57430e.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Cumulative sum analysis for evaluating learning curve of endoscopic lateral neck dissection","fulltext":[{"header":"Introduction","content":"\u003cp\u003eIn 1996, endoscopic parathyroidectomy was first reported[1]. Since then, various endoscopic and robotic approaches have been developed and improved to achieve less visible scars and better cosmetic results. Most recently, endoscopic and robotic approaches are commonly used to perform total thyroidectomy and central lymph node dissection[2, 3].\u003c/p\u003e \u003cp\u003eOver 30% of papillary thyroid carcinoma (PTC) patients have been diagnosed with cervical lateral lymph node metastasis[4\u0026ndash;8]. For these patients, lateral neck dissection (LND) is an effective treatment to improve prognosis[9, 10]. However, complete endoscopic LND is a technically challenging procedure, and has only been reported in a few studies[11\u0026ndash;13]. Here, we demonstrate the feasibility of endoscopic LND via chest approach by summarizing early cases of our previous study[14].\u003c/p\u003e \u003cp\u003eDue to the complexity and difficulty of performing endoscopic LND, surgeons need sufficient experience with the procedure to attain proficiency. An alternative approach to obtaining surgical experience is to study the learning curve of a procedure. To date, little attention has been focused on the learning curve for endoscopic LND via chest approach.\u003c/p\u003e \u003cp\u003eCumulative sum (CUSUM) is an analytic technique for detecting change. Here, the CUSUM was applied to evaluate a learning curve for endoscopic LND via chest approach with a graphic model. These data may help other surgical teams\u0026rsquo; progress through the learning phase more safely and rapidly.\u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003e2.1 Patients and inclusion criteria\u003c/h2\u003e \u003cp\u003e This study was approved by the Institutional Review Board (IRB) for ethics at the Guangdong Provincial Hospital of Traditional Chinese Medicine (Guangdong, China). Clinical data for 53 patients with PTC who underwent endoscopic LND via chest approach at our center between February 2017 and November 2022 were retrospectively assessed. All 53 patients were operated on by the same surgical team, with You Qin serving as the main surgeon. This surgical team completed over 2000 cases of endoscopic thyroidectomy in total. An early study on endoscopic LND has been published[14]. Inclusion criteria for the present study were: 1) confirmed case of PTC with metastatic lymph nodes at levels II, III, or IV based on ultrasonography, computed tomography, fine needle aspiration cytology, or intra-operative exploration; and 2) patients elected to undergo endoscopic surgery. Exclusion criteria were: 1) invasion of surrounding tissues; 2) level I/V metastatic lymph nodes; 3) distant metastasis; 4) past medical history of neck surgery or radiotherapy; and 5) inability to tolerate anesthesia or surgery.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003e2.2 Operative procedure\u003c/h2\u003e \u003cp\u003eBriefly, a 12-mm incision was initially made parasternally at nipple level before a 10-mm trocar was inserted through the incision. A 5-mm trocar was set at the 10\u0026ndash;11 o\u0026rsquo;clock position on the left side of the areola, while another 5-mm trocar was set at the 1\u0026ndash;2 o\u0026rsquo;clock position on the right side of the areola (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). CO\u003csub\u003e2\u003c/sub\u003e gas was insufflated at 6 mmHg pressure with high flow. A 10-mm 30\u0026deg; laparoscope was inserted through the 10-mm trocar. Next, subcutaneous loose connective tissue was separated to establish an initial working space, and to conduct a total thyroidectomy and central lymph node dissection. After completing these steps, endoscopic LND was performed. A working space was established from the posterior border of the sternocleidomastoid (SCM) laterally to the posterior belly of the digastric muscle superiorly. Then, a longitudinal incision in the SCM at the site between its sternal head and the clavicular head was made. The incision extended to the level of the carotid bifurcation superiorly. With assistance from two retractors pulling on the sternal head and clavicular head of the SCM, respectively, the lymph nodes between the SCM and sternohyoid muscle were dissected. Next, the internal jugular vein (IJV) was cautiously dissected to the cricoid cartilage superiorly and the venous angle inferiorly, followed by exposure of the omohyoid. An assistant then pulled the IJV and sternal head of the SCM to the tracheal side with a retractor, while another assistant pulled the clavicular head to the opposite side. Level IV lymph nodes were cleaned. To continue lymph node dissection, the assistants moved up the retractors and pulled both the sternal head and clavicular head of the SCM as described above. Level III lymph nodes were then exposed and cleaned. At this point, the assistant turned to pull the sternum head of the SCM away from the trachea, and the space between the cervical anterior muscles and the SCM were dissected to expose and clean the lymph nodes at the carotid triangle. The final step of the lymph node dissection involved sequential cleaning of the lymph nodes at levels IIa and IIb. Lymph nodes in this compartment to the lower edge of the digastric muscle superiorly and to the posterior border of the SCM laterally were dissected as well. Precautions observed for each surgical step of the endoscopic LND procedure have previously been described[14]. All of the resected lymph nodes were taken out from the observation hole in a specimen bag. After the operative field was rinsed with distilled water and drainage tubes were placed (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), both linea alba cervicalis and chest incisions were closed with absorbable sutures.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003e2.3 Learning curve analysis\u003c/h2\u003e \u003cp\u003eThe OT for each patient was documented chronologically from the first case to the last case to evaluate the progress of endoscopic LND. The CUSUM\u003csub\u003eOT\u003c/sub\u003e for the first patient was calculated according to the difference between the OT of the first patient and the mean OT of all the enrolled patients. The CUSUM\u003csub\u003eOT\u003c/sub\u003e for the second patient was the CUSUM\u003csub\u003eOT\u003c/sub\u003e of the first patient plus the difference between the OT of the second patient and the mean OT of all the enrolled patients. Similarly, the CUSUM\u003csub\u003eOT\u003c/sub\u003e for the remaining patients were determined. CUSUM analysis was used to analyze the learning curve.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003e2.4 Statistical Analysis\u003c/h2\u003e \u003cp\u003eData were analyzed using SPSS 18.0 software. To analyze frequency differences between the groups, the Chi-square test or Fisher\u0026rsquo;s exact test was applied to categorical data. The Wilcoxon rank sum test or independent Student\u0026rsquo;s \u003cem\u003et\u003c/em\u003e-test was applied to continuous data. A p-value less than 0.05 was considered statistically significant and all statistical tests were two-sided.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003ePatient Cohort and Surgery Outcomes\u003c/h2\u003e \u003cp\u003eAll 53 of the enrolled PTC patients successfully underwent endoscopic LND (including endoscopic total thyroidectomy and central neck dissection). In addition, none required conversion to open surgery. Of the 53 patients, 43 (81.1%) were female and the average age of the cohort was 41.4\u0026thinsp;\u0026plusmn;\u0026thinsp;12.7 y. Mean tumor size was 1.6\u0026thinsp;\u0026plusmn;\u0026thinsp;1.0 cm and the numbers of lymph nodes retrieved from the lateral and central compartments were 21.9\u0026thinsp;\u0026plusmn;\u0026thinsp;8.9 and 8.7\u0026thinsp;\u0026plusmn;\u0026thinsp;6.5, respectively. The average OT for all of the cases was 275.1\u0026thinsp;\u0026plusmn;\u0026thinsp;67.3 min. Mean blood loss was 42.0\u0026thinsp;\u0026plusmn;\u0026thinsp;44.2 mL.\u003c/p\u003e \u003cp\u003ePostoperatively, the mean hospital stay after surgery was 5.7\u0026thinsp;\u0026plusmn;\u0026thinsp;1.5 d. Lymphatic leakage and accessory nerve injury were observed in 2 (3.8%) and 3 (5.7%) patients, respectively. Eight patients (15.1%) had cervical plexus injury, one patient (1.9%) had hypoglossal nerve injury, and three patients (5.7%) had IJV injury. Postoperative bleeding, carotid artery injury, or phrenic nerve injury were not reported (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). During the follow-up period of 38.8\u0026thinsp;\u0026plusmn;\u0026thinsp;15.7 months, tumor recurrence was not detected.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eClinical outcomes of PTC patients who underwent endoscopic LND via chest approach.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"2\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eVariable\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eValue\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAge\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e41.4\u0026thinsp;\u0026plusmn;\u0026thinsp;12.7\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGender (Female/Male)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e43 / 10\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTumor size (cm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.6\u0026thinsp;\u0026plusmn;\u0026thinsp;1.0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHospital stay (d)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5.7\u0026thinsp;\u0026plusmn;\u0026thinsp;1.5\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBlood loss (mL)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e42.0\u0026thinsp;\u0026plusmn;\u0026thinsp;44.2\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOperative time (min)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e275.1\u0026thinsp;\u0026plusmn;\u0026thinsp;67.3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNo. of retrieved lymph nodes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e30.5\u0026thinsp;\u0026plusmn;\u0026thinsp;11.3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLateral\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e21.9\u0026thinsp;\u0026plusmn;\u0026thinsp;8.9\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCentral\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8.7\u0026thinsp;\u0026plusmn;\u0026thinsp;6.5\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eComplications of lateral neck dissection\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e17\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLymphatic leakage\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCervical plexus injury\u003csup\u003ea\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAccessory nerve injury\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHypoglossal nerve injury\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eInternal jugular vein injury\u003c/p\u003e \u003cp\u003eOther complications\u003csup\u003eb\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"2\"\u003e\u003csup\u003ea\u003c/sup\u003e Identification of cervical plexus injury is based on intraoperative cervical plexus transection; \u003csup\u003eb\u003c/sup\u003e including phrenic nerve injury, carotid artery injury and postoperative bleeding.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eLearning Curve Analysis\u003c/h2\u003e \u003cp\u003eOTs for the individual PTC patients were plotted according to the chronological sequence of their cases (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). CUSUM analysis was subsequently performed to establish a learning curve for endoscopic LND based on these cases (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The best model for the curve was determined to be a third-order polynomial equation as follows: CUSUM\u003csub\u003eOT\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;\u0026minus;\u0026thinsp;0.007\u0026times;patient number\u003csup\u003e3\u003c/sup\u003e-0.666\u0026times;patient number\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;+\u0026thinsp;55.721\u0026times;patient number\u0026thinsp;\u0026minus;\u0026thinsp;72.964. This equation has a high R\u003csup\u003e2\u003c/sup\u003e value of 0.929. The CUSUM\u003csub\u003eOT\u003c/sub\u003e revealed a curve exhibiting a positive slope from the initial case to case 30, while a negative slope after case 31 was observed. Thus, the curve helped identify a learning phase (cases 1\u0026ndash;30) and a mature phase (cases 31\u0026ndash;53), according to slope.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eDifferences in Clinical Outcome According to Phases determined by CUSUM Learning Curve Analysis\u003c/h2\u003e \u003cp\u003eClinical outcomes between phase 1 and phase 2 are presented in Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e. No significant differences in age, gender, tumor size, hospital stay after surgery, and/or number of retrieved lymph nodes between the two phases were observed. However, greater blood loss (p\u0026thinsp;=\u0026thinsp;0.001), longer OT (p\u0026thinsp;\u0026lt;\u0026thinsp;0.001), and a greater number of complications (p\u0026thinsp;=\u0026thinsp;0.038) occurred in phase 1.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eComparison of clinical outcomes between phases.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eVariable\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePhase 1\u003c/p\u003e \u003cp\u003e(n\u0026thinsp;=\u0026thinsp;30)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePhase 2\u003c/p\u003e \u003cp\u003e(n\u0026thinsp;=\u0026thinsp;23)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cem\u003ep\u003c/em\u003e-value\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAge\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e41.0\u0026thinsp;\u0026plusmn;\u0026thinsp;12.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e42.0\u0026thinsp;\u0026plusmn;\u0026thinsp;12.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.782\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGender (Female/Male)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e23 / 7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e20 / 3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.552\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTumor size (cm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.15 (0.2, 4.3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.2 (0.15, 3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.336\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHospital stay (d)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5.5 (4, 11)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e5 (3, 9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.089\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBlood loss (mL)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003e50 (10, 300)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e20 (5, 100)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOperative time (min)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003e307.9\u0026thinsp;\u0026plusmn;\u0026thinsp;63.8\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e232.4\u0026thinsp;\u0026plusmn;\u0026thinsp;44.2\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNo. of retrieved lymph nodes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e32.1\u0026thinsp;\u0026plusmn;\u0026thinsp;12.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e28.3\u0026thinsp;\u0026plusmn;\u0026thinsp;10.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.221\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLateral\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e22.9\u0026thinsp;\u0026plusmn;\u0026thinsp;8.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e20.6\u0026thinsp;\u0026plusmn;\u0026thinsp;9.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.348\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCentral\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e9.2\u0026thinsp;\u0026plusmn;\u0026thinsp;7.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.0\u0026thinsp;\u0026plusmn;\u0026thinsp;5.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.523\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eComplications of lateral neck dissection\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003e13\u003c/b\u003e\u003csup\u003e\u003cb\u003ea\u003c/b\u003e\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e3\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.038\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLymphatic leakage\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1.000\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCervical plexus injury\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.127\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAccessory nerve injury\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.249\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHypoglossal nerve injury\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1.000\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eInternal jugular vein injury\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1.000\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003e\u003csup\u003ea\u003c/sup\u003e One patient experienced cervical plexus injury and accessory nerve injury.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eNeck appearance after open LND has been shown to negatively impact patient quality of life[15, 16]. Therefore, many different approaches for achieving \u0026ldquo;scarless\u0026rdquo; LND have been reported, including robotic approaches[17\u0026ndash;19]and endoscopic approaches[20, 21]. However, due to the high cost of robotic instruments, the former have had limited application. In contrast, endoscopic LND via a chest approach is currently the most popular method among endoscopic approaches[11, 14, 20, 22]. Since the learning curve has not been examined for the latter approach, CUSUM was applied in this study. The mature phase on the CUSUM curve indicates that the learning curve for the procedure has been overcome. Moreover, it was observed that surgeons needed to have completed 30 cases to gain proficiency with endoscopic LND.\u003c/p\u003e \u003cp\u003eWhen comparing phase 1 and phase 2 of the CUSUM curve in the present study, the incidence of complications and volume of blood loss decreased significantly in phase 2. Thus, a sufficient number of surgical cases (in this study, 30 cases) are needed for surgeons to achieve shorter OTs and reduce possible complications. While the OT in phase 1 was longer, there was no significant difference in the number of retrieved lymph nodes in phase 1 compared with phase 2. In addition, recurrence did not occur during phase 1. Taken together, these data reveal that even for beginners, as long as they exhibit sufficient patience and adherence to the techniques required to complete LND, oncological safety can be achieved during the learning phase.\u003c/p\u003e \u003cp\u003eYan et al.[12] previously reported 155 cases of endoscopic LND via chest approach. The OT in the present study (275.1\u0026thinsp;\u0026plusmn;\u0026thinsp;67.3 min) versus in Yan\u0026rsquo;s study (278.2\u0026thinsp;\u0026plusmn;\u0026thinsp;38.6 min), as well as the number of retrieved lateral lymph nodes (21.9\u0026thinsp;\u0026plusmn;\u0026thinsp;8.9 vs. 22.9\u0026thinsp;\u0026plusmn;\u0026thinsp;9.9, respectively), are similar. However, the incidence of lymphatic leakage (3.8% vs. 2.6%, respectively) and accessory nerve injury (5.7% vs. 3.9%, respectively) in the present study were slighter higher than in Yan\u0026rsquo;s study. We hypothesize that a lack of experience during the learning phase of a procedure leads to a high incidence of complications. As the number of surgical cases increases, the incidence of complications should gradually decrease. The conclusions of this study support this hypothesis.\u003c/p\u003e \u003cp\u003eRegarding the management of postoperative complications, we provide some of our methods for reference. For lymphatic leakage, we usually apply a pressure bandage to the site of leakage. If this conservative treatment fails, ligation of the thoracic duct is performed. When dealing with IJV injuries, we use a 5\u0026thinsp;\u0026minus;\u0026thinsp;0 prolene suture for endoscopic vascular repair. While this is a rather challenging approach, all three cases of IJV injuries have been successfully repaired. Regarding nerve injury, the primary treatment is administration of neurotrophic drugs following surgery. Use of prolene suture to perform nerve repair endoscopically has also been undertaken. However, neither of these methods have achieved satisfactory results.\u003c/p\u003e \u003cp\u003eOur further suggestions regarding endoscopic LND are as follows. First, from early experience, we conclude that the risk of complications increases during hemostasis. However, as proficiency improves, both blood loss and complications are significantly reduced. Therefore, we advocate that surgeons in their early experience pay attention to the protection of thick vessels, such as facial vein, IJV, and communicating branches of the internal and external jugular veins. Second, a fixed surgical team can facilitate advancing the learning curve as safely as possible. Finally, we suggest that endoscopic LND should be performed at centers with experience in endoscopic thyroidectomy via chest approach. The procedures required for endoscopic LND are complex and difficult. It is nearly impossible for a completely inexperienced surgeon to calmly respond to emergencies that may arise during surgery, and patient safety must be of utmost concern. Serious complications can also affect the confidence of a surgeon while completing the operation. Dr. You Qin performed the first endoscopic thyroid surgery via chest approach in 2006, and is also an expert in endoscopic gastrointestinal surgery and endoscopic hernia surgery. Thus, he possesses proficient techniques in endoscopic surgery.\u003c/p\u003e \u003cp\u003eIn summary, endoscopic LND requires a fixed surgical team to accumulate experience by which the feasibility and safety of a procedure can be determined. Based on the present data, we demonstrate that a main surgeon with previous experience in endoscopic thyroid surgery can overcome the learning curve of endoscopic LND after 30 cases. It is anticipated that our experience may help other surgical teams to progress through the learning curve of endoscopic LND more smoothly and safely.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003elateral neck dissection (LND)\u003c/p\u003e\n\u003cp\u003ecumulative sum (CUSUM)\u003c/p\u003e\n\u003cp\u003eoperative time (OT)\u003c/p\u003e\n\u003cp\u003epapillary thyroid carcinoma (PTC)\u003c/p\u003e\n\u003cp\u003eInstitutional Review Board (IRB)\u003c/p\u003e\n\u003cp\u003esternocleidomastoid (SCM)\u003c/p\u003e\n\u003cp\u003einternal jugular vein (IJV)\u003c/p\u003e"},{"header":"Declarations","content":"\n\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe study protocol was approved by the Institutional Review Board for ethics at the Guangdong Provincial Hospital of Traditional Chinese Medicine. The research reported in this paper was in compliance with the Helsinki Declaration.\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003eInformed Consent to participate was given by all patients.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWritten consent to participate included permission to access specimens and clinical details, and to publish findings.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNone.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eContributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eZXC and XRZ designed the concept of this study. JMD, YC, JBC, FSP, ZHL and XBZ collected the datasets. ZXC and XRZ analyzed the data and wrote the manuscript. BX and YQ revised the manuscript. All authors have read and approved the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors thank Medjaden Bioscience Limited for linguistic revision of the manuscript.\u003cstrong\u003e\u003c/strong\u003e\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eGagner M (1996) Endoscopic subtotal parathyroidectomy in patients with primary hyperparathyroidism. Br J Surg 83\u003cstrong\u003e:\u003c/strong\u003e875\u003c/li\u003e\n \u003cli\u003eKim YS, Joo KH, Park SC, Kim KH, Ahn CH, Kim JS (2014) Endoscopic thyroid surgery via a breast approach: a single institution\u0026apos;s experiences. BMC Surg 14\u003cstrong\u003e:\u003c/strong\u003e49\u003c/li\u003e\n \u003cli\u003eLee KE, Koo do H, Kim SJ, Lee J, Park KS, Oh SK, Youn YK (2010) Outcomes of 109 patients with papillary thyroid carcinoma who underwent robotic total thyroidectomy with central node dissection via the bilateral axillo-breast approach. Surgery 148\u003cstrong\u003e:\u003c/strong\u003e1207-1213\u003c/li\u003e\n \u003cli\u003eHu D, Zhou J, He W, Peng J, Cao Y, Ren H, Mao Y, Dou Y, Xiong W, Xiao Q, Su X (2018) Risk factors of lateral lymph node metastasis in cN0 papillary thyroid carcinoma. World J Surg Oncol 16\u003cstrong\u003e:\u003c/strong\u003e30\u003c/li\u003e\n \u003cli\u003eCracchiolo JR, Wong RJ (2018) Management of the lateral neck in well differentiated thyroid cancer. Eur J Surg Oncol 44\u003cstrong\u003e:\u003c/strong\u003e332-337\u003c/li\u003e\n \u003cli\u003eDucoudray R, Tresallet C, Godiris-Petit G, Tissier F, Leenhardt L, Menegaux F (2013) Prophylactic lymph node dissection in papillary thyroid carcinoma: is there a place for lateral neck dissection? World J Surg 37\u003cstrong\u003e:\u003c/strong\u003e1584-1591\u003c/li\u003e\n \u003cli\u003eMulla MG, Knoefel WT, Gilbert J, McGregor A, Schulte KM (2012) Lateral cervical lymph node metastases in papillary thyroid cancer: a systematic review of imaging-guided and prophylactic removal of the lateral compartment. Clin Endocrinol (Oxf) 77\u003cstrong\u003e:\u003c/strong\u003e126-131\u003c/li\u003e\n \u003cli\u003eIto Y, Tomoda C, Uruno T, Takamura Y, Miya A, Kobayashi K, Matsuzuka F, Kuma K, Miyauchi A (2005) Ultrasonographically and anatomopathologically detectable node metastases in the lateral compartment as indicators of worse relapse-free survival in patients with papillary thyroid carcinoma. World J Surg 29\u003cstrong\u003e:\u003c/strong\u003e917-920\u003c/li\u003e\n \u003cli\u003eHaugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L (2016) 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid 26\u003cstrong\u003e:\u003c/strong\u003e1-133\u003c/li\u003e\n \u003cli\u003eStack BC, Jr., Ferris RL, Goldenberg D, Haymart M, Shaha A, Sheth S, Sosa JA, Tufano RP, American Thyroid Association Surgical Affairs C (2012) American Thyroid Association consensus review and statement regarding the anatomy, terminology, and rationale for lateral neck dissection in differentiated thyroid cancer. Thyroid 22\u003cstrong\u003e:\u003c/strong\u003e501-508\u003c/li\u003e\n \u003cli\u003eGuo Y, Qu R, Huo J, Wang C, Hu X, Chen C, Liu D, Chen W, Xiong J (2019) Technique for endoscopic thyroidectomy with selective lateral neck dissection via a chest-breast approach. Surg Endosc 33\u003cstrong\u003e:\u003c/strong\u003e1334-1341\u003c/li\u003e\n \u003cli\u003eYan HC, Xiang C, Wang Y, Wang P (2020) Scarless endoscopic thyroidectomy (SET) lateral neck dissection for papillary thyroid carcinoma through breast approach: 10 years of experience. 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Surg Endosc 34\u003cstrong\u003e:\u003c/strong\u003e5274-5282\u003c/li\u003e\n \u003cli\u003eLin P, Liang F, Cai Q, Han P, Chen R, Xiao Z, Wang J, Huang X (2021) Comparative study of gasless endoscopic selective lateral neck dissection via the anterior chest approach versus conventional open surgery for papillary thyroid carcinoma. Surg Endosc 35\u003cstrong\u003e:\u003c/strong\u003e693-701\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"
[email protected]","identity":"bmc-surgery","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bsur","sideBox":"Learn more about [BMC Surgery](http://bmcsurg.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bsur/default.aspx","title":"BMC Surgery","twitterHandle":"@BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Papillary thyroid carcinoma, Endoscopic lateral neck dissection, Chest approach, Learning Curve, Cumulative sum graphic model","lastPublishedDoi":"10.21203/rs.3.rs-4259154/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4259154/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eObjectives\u003c/h2\u003e \u003cp\u003eEndoscopic lateral neck dissection (LND) can be a scarless procedure if a surgeon has performed a sufficient number of operations to become skilled at the techniques involved. Here, we examine the learning curve for a surgeon who performed 53 endoscopic LND procedures via chest approach.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eSurgical outcomes for 53 patients with papillary thyroid carcinoma who underwent endoscopic LND via chest approach between February 2017 and November 2022 were retrospectively reviewed. The surgeon\u0026rsquo;s learning curve was evaluated using a cumulative sum graphic model (CUSUM).\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eA CUSUM analysis was applied to 53 patients (10 males, 43 females) with a mean age of 41.4 y who underwent endoscopic LND via chest approach. The best model for the curve was determined to be a third-order polynomial equation as follows: CUSUM\u003csub\u003eOT\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;\u0026minus;\u0026thinsp;0.007\u0026times;patient number\u003csup\u003e3\u003c/sup\u003e-0.666\u0026times;patient number\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;+\u0026thinsp;55.721\u0026times;patient number\u0026thinsp;\u0026minus;\u0026thinsp;72.964. This equation has a high R\u003csup\u003e2\u003c/sup\u003e value of 0.929. The peak operative time (OT) occurred at the 30th case. Consequently, the learning curve model was divided into two phases: phase 1 (1\u0026ndash;30 cases) and phase 2 (31\u0026ndash;53 cases). OT (307.9\u0026thinsp;\u0026plusmn;\u0026thinsp;63.8 min vs. 232.4\u0026thinsp;\u0026plusmn;\u0026thinsp;44.2 min, respectively; p\u0026thinsp;\u0026lt;\u0026thinsp;0.001), blood loss (50 mL vs. 20 mL, respectively; p\u0026thinsp;=\u0026thinsp;0.001), and complications (43.3% vs. 13.0%, respectively; p\u0026thinsp;=\u0026thinsp;0.038) decreased significantly in phase 2 compared to phase 1.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eThe learning curve of endoscopic LND via chest approach was found to involve 30 cases. With greater experience, the surgery was completed with shorter OT and fewer complications. This approach is an alternative for patients who desire cosmesis. Furthermore, the present data and experience insights regarding endoscopic LND via chest approach may help other surgeons to pass the learning phase more safely.\u003c/p\u003e","manuscriptTitle":"Cumulative sum analysis for evaluating learning curve of endoscopic lateral neck dissection","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-05-02 20:05:51","doi":"10.21203/rs.3.rs-4259154/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-05-08T13:54:47+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-05-08T13:25:19+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-04-25T12:45:27+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Surgery","date":"2024-04-12T17:21:27+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"
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