ORIGINAL ARTICLE
Gasless Transaxillary Endoscopic Thyroidectomy: A Decade On Nor Azham Hakim Darail, MD, So Hee Lee, MD, Sang-Wook Kang, MD, Jong Ju Jeong, MD, Kee-Hyun Nam, MD, and Woong Youn Chung, MD
Purpose: In 2001, the authors developed a novel method of gasless transaxillary endoscopic thyroidectomy (ET) and have now performed >1000 operations. This review was performed to document surgical outcomes after 10 years of experience with this technique and to determine what the role of ET has in the current era. Patients and Methods: All patients who underwent elective ET using the gasless transaxillary approach from November 2001 to December 2010 were evaluated. Patient demographics, surgical data, histologic analysis results, and complications were recorded and analyzed. Results: A total of 1085 patients underwent ET during the study period. Mean patient age was 36.9 ± 9.7 years; the gender ratio was 1:49 (male:female). There were 228 benign thyroid tumor cases and 857 thyroid malignancies. Trend analysis showed a progressive increase in case numbers per month until the end of 2007, followed by a steady decline. There were 175 total thyroidectomy cases and 910 cases of less-than-total thyroidectomy. Mean overall operating time was 132.92 ± 48.6 minutes, and the overall complication rate was 13.5%. The most common complications were: transient hypocalcemia (6.3%), transient hoarseness (3.9%), hematoma (0.4%), permanent hypocalcemia (0.1%), and permanent recurrent laryngeal nerve injury (0.2%). Conclusions: Gasless ET is comparable to open thyroidectomy in terms of early surgical outcomes and complications, and it bridges the gap between conventional open surgery and robotic transaxillary thyroidectomy. Key Words: endoscopic thyroidectomy, gasless, transaxillary
(Surg Laparosc Endosc Percutan Tech 2014;24:e211–e215)
T
hyroidectomy has evolved from a dreaded procedure with high morbidity and mortality into one of the safest of commonly performed surgical procedures.1 Conventional open thyroidectomy has become the standard surgical treatment for thyroid diseases, but surgeons continue to search for new surgical techniques that could improve outcomes. Advances in medical technologies have enabled the incorporation of endoscopic instruments in thyroid surgery. Gagner2 paved the way with the first endoscopic parathyroidectomy, followed by Huscher et al3 with endoscopic thyroidectomy (ET). Spurred by possible advantages afforded by the endoscopic approach, various ET techniques have since been introduced.4–11 Received for publication March 20, 2013; accepted August 27, 2013. From the Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea. The authors declares no conflicts of interest. Reprints: Sang-Wook Kang, MD, Department of Surgery, Yonsei University College of Medicine, C.P.O. Box 8044, 250 Seongsanno, Seodaemun-gu, Seoul 120-752, Korea (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Gasless transaxillary ET is the technique that was developed and adopted by the Department of Surgery, Yonsei University College of Medicine. Previously, we reported our early experiences and stressed the safety and completeness of this procedure, particularly for the treatment of low-risk thyroid cancer.12,13 In this report, we look back for some perspective of where we are 10 years after its introduction and to determine where ET fits into the current management of thyroid cancers.
PATIENTS AND METHODS Patients All patients who underwent gasless transaxillary ET between November 1, 2001 and December 31, 2010 at Department of Surgery, Yonsei University of Medicine were included. However, between September 2003 and August 2005, no ET was performed as the primary surgeon was training overseas. The period of observation was subdivided into 3 consecutive phases as follows: (1) phase I— November 1, 2001 to August 31, 2003, (2) phase II— September 1, 2005 to December 31, 2007, and (3) phase III—January 1, 2008 to December 31, 2010. Preoperatively, patients underwent thyroid ultrasonography, ultrasound-guided fine-needle aspiration biopsy (FNAB), contrast-enhanced computed tomography of the neck, and thyroid function testing. In cases with malignant thyroid nodules, patients were evaluated for tumor size, capsular invasiveness, multiplicity, bilaterality, cervical lymph node status, and distant metastases by preoperative staging ultrasonography. Indications for ET were as follows: (1) a thyroid tumor not >5 cm diagnosed by FNAB either as benign or as a follicular neoplasm, or (2) a diagnosis of a well-differentiated thyroid carcinoma of size r2 cm. Contraindications included wide or definite extracapsular soft tissue invasion, multiple lateral neck node metastases or perinodal infiltration of metastatic lymph nodes, or the presence of distant metastases by preoperative imaging. Cases with a lesion situated at the posterior capsular area (dorsal surface) of the thyroid, especially adjacent to the tracheoesophageal groove, and advanced cases, such as, patients with conglomerated central compartment lymph nodes and those with recurrent laryngeal nerve (RLN) invasion, were also excluded. Extent of surgery was determined in accordance with the guidelines of the American Thyroid Association.14 Patients with multiple and bilateral lesions and those found to have thyroid capsular invasion intraoperatively underwent total thyroidectomy. Ipsilateral prophylactic central compartment lymph node dissection (CCND) was performed routinely, with the exception of the first few cases at
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the beginning of the series. Modified radical neck dissection (MRND) was performed limitedly in the few cases found preoperatively to have 1 to 2 lateral neck lymph node metastases without evidence of perinodal infiltration. Data analyzed included patient characteristics, types of surgical procedure, operation times, postoperative hospital stays, postoperative complications, histopathologic characteristics (size, capsular invasion, multiplicity, bilaterality, and central and lateral neck lymph node metastases), and TNM stage according to the sixth edition of the American Joint Committee on Cancer and the International Union Against Cancer (AJCC/UICC) staging system.15 Data were obtained from a prospectively enrolled database maintained in the department. Postoperatively, all patients diagnosed with thyroid carcinoma were given levothyroxine to suppress thyroid stimulating hormone and were followed up regularly at 3 to 6 month intervals. Patients indicated for radioactive iodine therapy were treated at around 4 to 6 weeks postoperatively and underwent a 131I whole-body scan 2 days after radioactive iodine therapy.
Operation Method The operative technique has been described extensively.11–13 Briefly, ET was performed using a gasless transaxillary double-incision approach. The surgical procedure consists of 2 stages: (1) the creation of a working space (ie, flap dissection from the axilla to the anterior neck and connection of a retractor to an external lifting system) and (2) thyroid dissection.
Creation of Working Space Patients are placed in supine position while under general anesthesia. The neck is slightly extended and the lesion-side arm is raised and fixed to achieve the shortest distance between axilla and anterior neck (Fig. 1). A 4- to 6-cm-sized vertical skin incision is then made in the axilla to allow the insertion of a 45-degree endoscope and endoscopic instruments. The route to the anterior neck area is dissected through the anterior surface of the pectoralis major muscle by electrical cautery under direct vision, until the anterior border of the sternocleidomastoid muscle (SCM) is exposed. Initially, exposition of the thyroid is achieved through the space between the medial border of the SCM and lateral borders of strap muscles. However, since 2006, this dissection has been approached through the space between SCM branches (between the sternal head and the clavicular head) and continued beneath the strap
FIGURE 1. Positioning of the patient.
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FIGURE 2. Approaching route (the space between 2 branches of SCM). SCM indicates sternocleidomastoid muscle.
muscle until the contralateral lobe of the thyroid is exposed (Fig. 2). An external retractor is then inserted through the skin incision in the axilla and the flap is raised using a lifting device to maintain a working space. A second skin incision (0.5 cm in length) is made on the medial side of the anterior chest wall for the insertion of endoscopic instruments on an imaginary horizontal line starting from the lower end of the axillary incision and extending from 5 to 6 cm.
Thyroidectomy The operation is conducted in the same manner as conventional open thyroidectomy. Under endoscopic guidance, the upper pole of the thyroid is drawn downward and the superior thyroid vessels are identified and individually divided [harmonic scalpel (Johnson & Johnson Medical, Cincinnati, OH)] close to the thyroid gland to avoid injuring the external branch of the superior laryngeal nerve. The lower pole is dissected from adipose and cervical thymic tissues, and the inferior thyroid vein is divided close to the thyroid gland for mobilization. The thyroid gland is then retracted medially, and the perithyroidal fascia is divided and sharply dissected using an endoscopic dissector. Dissection is then carefully performed to identify the inferior thyroid artery and the RLN. The inferior thyroid artery is divided close to the thyroid gland using the harmonic scalpel, and the whole cervical course of the RLN is traced. The superior parathyroid gland is identified during dissection and left intact, and the thyroid gland is then dissected from the trachea. Contralateral thyroidectomy is performed using the same method with anteromedial traction of the thyroid. When CCND (prelaryngeal, pretracheal, and paratracheal regions on the tumor side) is required, soft tissue and lymph nodes are detached from the thyrothymic ligament area with superior-medial retraction of the thyroid while monitoring the track of the RLN. Dissection close to the RLN is performed using a fine endoscopic dissector to avoid damage by collateral energy generated by the harmonic scalpel. In cases of MRND (usually performed by posterolateral neck dissection), the same approach method is used and subplatysmal dissection is performed to the midline of the anterior neck, the submandibular gland superiorly, and the trapezius muscle posteriorly. Initially, soft tissue and lymph nodes around the anterior and posterior aspects of r
2014 Lippincott Williams & Wilkins
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Volume 24, Number 6, December 2014
Gasless Transaxillary Endoscopic Thyroidectomy
the SCM are dissected and the carotid artery and internal jugular vein are exposed. The retractor is then placed under the SCM, and dissection is started from the anterior aspect of the carotid artery and jugular vein and continued until the posterior aspect of the internal jugular vein is fully exposed. Dissection of level VB in the posterior neck area is then conducted while preserving the spinal accessory nerve, the phrenic nerve, the thoracic duct, and the brachial nerve plexus. The dissection is then continued up to level II. The resected specimen is extracted through the 4 to 6 cm skin incision. Finally, a 3-mm closed suction drain is inserted through a separate skin incision under the axillary skin incision, and the wound is closed cosmetically. FIGURE 3. Trends in the monthly average of cases done during the observed period.
RESULTS Between November 2001 and December 2010, 1085 cases of ET were performed. There were 228 cases of benign disease and 857 cases of differentiated thyroid cancer. Table 1 provides a breakdown of cases during the 3 phases, namely from November 2001 to August 2003, September 2005 to December 2007, and from January 2008 to December 2010. The overall number of cases increased progressively throughout the study period. However, monthly averages of cases by year showed a progressive increase to a peak of 23.7 cases per month in 2007 followed by a steady decline to about 9.3 cases per month in the 2010 (Fig. 3). The benign to malignant case ratios were 1.3:1 in phase I, 1:3.4 in phase II, and 1:7.8 in phase III, giving an overall ratio of 1:4, which reveals a change from predominantly benign cases initially to almost completely malignant cases in 2010. The mean overall patient age at presentation was 38.9 ± 9.7 years (range, 6 to 68 y) with a male to female ratio of 1:44 (Table 1). Of the 228 benign cases, 189 underwent hemithyroidectomy alone, 37 hemithyroidectomy with contralateral subtotal thyroidectomy, 1 bilateral subtotal thyroidectomy, and 1 bilateral total thyroidectomy. In the 857 patients with thyroid cancer, 316 underwent hemithyroidectomy, 364 hemithyroidectomy with contralateral subtotal thyroidectomy, 174 underwent bilateral total thyroidectomy, and 3 completion thyroidectomy. Excluding the
TABLE 1. Demographic Data
Total Number (%) No. cases Phase I Benign Malignant Total Phase II Benign Malignant Total Phase III Benign Malignant Total Mean age of the patients (y) (range) Sex (female:male) Phase I—November 2001 to August 2003. Phase II—September 2005 to December 2007. Phase III—January 2008 to December 2010.
r
2014 Lippincott Williams & Wilkins
1085 63 (56.7) 48 (43.3) 111 (10.2) 108 (23.0) 362 (77.0) 470 (43.3) 57 447 504 36.9 ± 9.7 1061:24
(11.3) (89.7) (46.5) (6-68) (44.2:1)
first 30 cancer cases, all cancer patients received prophylactic CCND. Twelve patients with a confirmed metastatic lateral neck lymph node from PTC by preoperative FNAB underwent additional endoscopic MRND. Overall mean operating time was 132.9 ± 48.6 minutes (range, 50 to 485 min). A breakdown of operating times by procedure types is provided in Table 2. The most common histopathologic diagnosis was papillary thyroid carcinoma (PTC), which comprised 847 of the 857 (98.8%) malignant cases, and 697 (81.3%) of these were papillary thyroid microcarcinomas. There were 9 (1.1%) cases of follicular thyroid carcinoma and 1 (0.1%) case of poorly differentiated carcinoma. Central compartment lymph node metastases were present in 233 (27.2%) cases, and 12 (1.4%) had lateral cervical lymph node metastases. There were 168 (19.6%) cases of multifocal lesions and 79 (9.2%) cases of bilateral cancer. In the benign group, adenomatous hyperplasia was the most common diagnosis followed by follicular adenoma [156 (68.4%) and 58 (25.4%) cases, respectively]. The overall complication rate was 13.5%. The most common complications were transient hypocalcemia (6.1%), transient RLN injury (3.9%), hematoma (0.4%), permanent hypocalcemia (0.2%), and permanent RLN injury (0.2%) (Table 3). Taking into account only total thyroidectomy cases, the rates of transient hypocalcemia (< 7.5 mg/dL or symptoms of hypocalcemia) and transient RLN injury were 31.4% and 8.0%, respectively. We performed preoperative or postoperative laryngoscopy for the evaluation of vocal cord palsy only as clinically indicated, not routinely.
TABLE 2. Types of Surgical Procedures and Operating Times
N (%) Surgical procedures LTT TT TT with MRND Operating time (min) Overall (range) LTT (range) TT (range) TT with MRND (range)
910 (83.9) 163 (15.0) 12 (1.1) 132.92 ± 48.6 126.20 ± 41.9 156.50 ± 43.4 322.25 ± 91.0
(50-485) (50-365) (86-381) (183-485)
LTT indicates less–than-total thyroidectomy; MRND, modified radical neck dissection; TT, total thyroidectomy.
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TABLE 3. Summary of Data According to the Time Phase No. cases Ratio of benign to malignant Ratio of TT:LTT Mean tumor size (cm) Benign Malignant TNM stage, N (%) I II IVa Mean operating time (min) (range) Postoperative hospital stay in days (range) Complications, N (%) Overall Transient hypocalcemia Permanent hypocalcemia Transient RLN injury Permanent RLN injury Hematoma Others Cancer recurrence Mean period for recurrence (mo)
Phase I
Phase II
Phase III
111 1.3:1 1:110
470 1:3.4 1:5.4
504 1:7.8 1:4.1
2.81 0.98
2.62 0.74
2.26 0.74
45 (93.8) 3 (6.2) 0 (0) 135.4 ± 49.5 (50-365) 3.2 ± 0.7 (3-8)
320 (88.4) 41 (11.3) 1 (0.3) 140 ± 57.0 (58-485) 3.4 ± 1.4 (2-23)
385 (86.1) 61 (13.6) 1 (0.3) 125.7 ± 37.7 (55-318) 3.3 ± 2.9 (2-62)
0 0 0 0 0 0 0
(0) (0) (0) (0) (0) (0) (0) 0
67 22 2 22 0 5 16
(14.3) (4.7) (0.2) (4.7) (0) (1.0) (3.7) 4 40
80 44 0 21 2 0 13
(15.9) (8.7) (0) (4.1) (0.4) (0) (2.7) 1 35
LTT indicates less-than-total thyroidectomy; RLN, recurrent laryngeal nerve; TT, total thyroidectomy.
Of the 174 cancer patients who underwent total thyroidectomy, 12 did not receive radioiodine ablation (RIA), and 21 did not have follow-up data; thus, 141 were analyzed for completeness of surgery. All of these 141 patients underwent a post-RIA whole-body scan and none showed any abnormal 131I activity in the neck area. All of these 141 patients were also evaluated for postoperative second year follow-up serum thyroglobulin level. However, the data of 29 patients were missing, leaving 112 cases for analysis; among these, the mean serum thyroglobulin level was 0.36 ± 1.35 ng/mL (range, 0.1 to 14.4 ng/mL). The mean follow-up period for the malignancy cancer patient was 52.7 ± 20.3 (range, 3 to 128 mo). During follow-up period, there were 5 cases (0.62%) of cancer recurrence among the 803 patients who underwent ET for malignancy [F/U rate was 93.7% (803/857)]. Three patients had recurrences in contralateral remnant thyroid tissue, and 2 had recurrences in the ipsilateral lateral neck compartment. The mean recurrence-free duration was 39 months.
DISCUSSION Almost 15 years have passed since the idea of endoscopic neck surgery was turned into reality by Gagner.2 During this time, various approaches and techniques have been proposed and refined. At present, ET can be broadly divided into direct and indirect approaches.16,17 Examples of the former include minimally invasive video-assisted thyroid surgery (MIVATS) and video-assisted neck surgery (VANS),4,7 whereby the minimally invasive principle is maintained by accessing the thyroid directly via the neck through small incisions. In contrast, the indirect approach allows access to the thyroid through a remote incision and often necessitates more invasive dissection, although freeing the patient from the customary neck scar. Common sites of incision for the latter include axilla, chest, and breast, typically in combination to provide better access to the thyroid gland; examples include the transaxillary approach,
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the axillo-bilateral-breast approach, and the bilateral axilla breast approach.5,6,8–12 These procedures can be further divided into gas or gasless techniques. At our institution, the gasless transaxillary approach has been adopted as the standard ET technique. This approach was developed by Chung and is based on a modification of the original completely endoscopic transaxillary with gas technique devised by Ikeda.5 The natural course of well-differentiated carcinoma makes it difficult to determine the long-term results of new thyroidectomy techniques. Several authors have published reports suggesting the feasibility and safety of ET for the treatment of thyroid cancer, particularly low-risk PTC.13,18,19 In the present study, there were 5 cases of recurrent cancer among 803 ET cases (0.62%). Four patients underwent endoscopic less-than-total thyroidectomy with CCND for PTC and 3 experienced recurrence in remnant thyroid tissue (contralateral lobe) at 31, 38, and 64 months after initial surgery, respectively. Two of the 3 underwent endoscopic completion total thyroidectomy and the other, robotic completion total thyroidectomy. The other patient who underwent endoscopic less-than-total thyroidectomy with CCND for PTC had recurrence in the lateral neck compartment at 35 months postoperatively and underwent robotic completion total thyroidectomy with robotic MRND for the recurrence. The last patient underwent endoscopic total thyroidectomy with CCND for PTC (T2N1aMo) and experienced recurrence in the lateral neck compartment at 27 months postoperatively and subsequently underwent open MRND. Although this study enrolled 10 year’s experience of ET and the oncologic results were acceptable, considering the natural history of thyroid cancer, it would be important to have longer follow-up to assess the long-term results of this procedure compared with standard open surgery. The overall complication rate of ET in this series was B13%. The more common complications were temporary hypocalcemia and transient RLN palsy (6.1% and 4.0%, r
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respectively). In fact, among the bilateral total thyroidectomy cases in our series, the rate of temporary hypocalcaemia was high at 30.9%. However, almost all of these transient complications resolved completely within 2 to 3 months. The rates of permanent hypocalcaemia and RLN injury were 0.1% and 0.2%, respectively, which are comparable with the complication rates of conventional open thyroidectomies. Other complications, such as, hematoma, seroma, and tracheal and esophageal injuries, did occur but were uncommon. The 3 time periods within our study period, namely, phases I, II, and III, represents the evolution of gasless transaxillary ET at our institution. Phase I was a learning period when the procedure was first developed and introduced; cases were carefully chosen from among patients with small benign disease or low-risk papillary thyroid cancer, and procedures were mainly ipsilateral hemithyroidectomies, with only one total thyroidectomy. Central compartment lymph node dissections (CCND) were gradually introduced after the first 30 cancer cases. Phase II represented a period of growth and as experience accumulated, more cases were performed and the proportion of thyroid cancer cases increased. In addition, indications were extended slightly, and selective lymph node dissection and MRND were attempted. In contrast, phase III was a period of maturation and training. The majority of cases were for PTCs, mainly subcentimeter lesions (papillary thyroid microcarcinomas), and cases of benign thyroid disease were only performed occasionally. Selective lymph node and MRND were not performed during this phase, because experience during phase II showed that although these procedures were possible endoscopically, they were simply too taxing in terms of technical difficulty, ergonomics, and operating time to be made routine components of ET. During phase III, ET was incorporated into the training program of trainees in Endocrine surgery at our institution. The present study raises another interesting point. The overall numbers of cases treated in the 3 phases show an increasing trend, but average numbers of ETs per month show a peak of around 24 ET cases per month that reached in the middle of phase II and since then, this has steadily declined to
Gasless Transaxillary Endoscopic Thyroidectomy: A Decade On Nor Azham Hakim Darail, MD, So Hee Lee, MD, Sang-Wook Kang, MD, Jong Ju Jeong, MD, Kee-Hyun Nam, MD, and Woong Youn Chung, MD
Purpose: In 2001, the authors developed a novel method of gasless transaxillary endoscopic thyroidectomy (ET) and have now performed >1000 operations. This review was performed to document surgical outcomes after 10 years of experience with this technique and to determine what the role of ET has in the current era. Patients and Methods: All patients who underwent elective ET using the gasless transaxillary approach from November 2001 to December 2010 were evaluated. Patient demographics, surgical data, histologic analysis results, and complications were recorded and analyzed. Results: A total of 1085 patients underwent ET during the study period. Mean patient age was 36.9 ± 9.7 years; the gender ratio was 1:49 (male:female). There were 228 benign thyroid tumor cases and 857 thyroid malignancies. Trend analysis showed a progressive increase in case numbers per month until the end of 2007, followed by a steady decline. There were 175 total thyroidectomy cases and 910 cases of less-than-total thyroidectomy. Mean overall operating time was 132.92 ± 48.6 minutes, and the overall complication rate was 13.5%. The most common complications were: transient hypocalcemia (6.3%), transient hoarseness (3.9%), hematoma (0.4%), permanent hypocalcemia (0.1%), and permanent recurrent laryngeal nerve injury (0.2%). Conclusions: Gasless ET is comparable to open thyroidectomy in terms of early surgical outcomes and complications, and it bridges the gap between conventional open surgery and robotic transaxillary thyroidectomy. Key Words: endoscopic thyroidectomy, gasless, transaxillary
(Surg Laparosc Endosc Percutan Tech 2014;24:e211–e215)
T
hyroidectomy has evolved from a dreaded procedure with high morbidity and mortality into one of the safest of commonly performed surgical procedures.1 Conventional open thyroidectomy has become the standard surgical treatment for thyroid diseases, but surgeons continue to search for new surgical techniques that could improve outcomes. Advances in medical technologies have enabled the incorporation of endoscopic instruments in thyroid surgery. Gagner2 paved the way with the first endoscopic parathyroidectomy, followed by Huscher et al3 with endoscopic thyroidectomy (ET). Spurred by possible advantages afforded by the endoscopic approach, various ET techniques have since been introduced.4–11 Received for publication March 20, 2013; accepted August 27, 2013. From the Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea. The authors declares no conflicts of interest. Reprints: Sang-Wook Kang, MD, Department of Surgery, Yonsei University College of Medicine, C.P.O. Box 8044, 250 Seongsanno, Seodaemun-gu, Seoul 120-752, Korea (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Gasless transaxillary ET is the technique that was developed and adopted by the Department of Surgery, Yonsei University College of Medicine. Previously, we reported our early experiences and stressed the safety and completeness of this procedure, particularly for the treatment of low-risk thyroid cancer.12,13 In this report, we look back for some perspective of where we are 10 years after its introduction and to determine where ET fits into the current management of thyroid cancers.
PATIENTS AND METHODS Patients All patients who underwent gasless transaxillary ET between November 1, 2001 and December 31, 2010 at Department of Surgery, Yonsei University of Medicine were included. However, between September 2003 and August 2005, no ET was performed as the primary surgeon was training overseas. The period of observation was subdivided into 3 consecutive phases as follows: (1) phase I— November 1, 2001 to August 31, 2003, (2) phase II— September 1, 2005 to December 31, 2007, and (3) phase III—January 1, 2008 to December 31, 2010. Preoperatively, patients underwent thyroid ultrasonography, ultrasound-guided fine-needle aspiration biopsy (FNAB), contrast-enhanced computed tomography of the neck, and thyroid function testing. In cases with malignant thyroid nodules, patients were evaluated for tumor size, capsular invasiveness, multiplicity, bilaterality, cervical lymph node status, and distant metastases by preoperative staging ultrasonography. Indications for ET were as follows: (1) a thyroid tumor not >5 cm diagnosed by FNAB either as benign or as a follicular neoplasm, or (2) a diagnosis of a well-differentiated thyroid carcinoma of size r2 cm. Contraindications included wide or definite extracapsular soft tissue invasion, multiple lateral neck node metastases or perinodal infiltration of metastatic lymph nodes, or the presence of distant metastases by preoperative imaging. Cases with a lesion situated at the posterior capsular area (dorsal surface) of the thyroid, especially adjacent to the tracheoesophageal groove, and advanced cases, such as, patients with conglomerated central compartment lymph nodes and those with recurrent laryngeal nerve (RLN) invasion, were also excluded. Extent of surgery was determined in accordance with the guidelines of the American Thyroid Association.14 Patients with multiple and bilateral lesions and those found to have thyroid capsular invasion intraoperatively underwent total thyroidectomy. Ipsilateral prophylactic central compartment lymph node dissection (CCND) was performed routinely, with the exception of the first few cases at
Volume 24, Number 6, December 2014 www.surgical-laparoscopy.com |
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Hakim Darail et al
Surg Laparosc Endosc Percutan Tech
the beginning of the series. Modified radical neck dissection (MRND) was performed limitedly in the few cases found preoperatively to have 1 to 2 lateral neck lymph node metastases without evidence of perinodal infiltration. Data analyzed included patient characteristics, types of surgical procedure, operation times, postoperative hospital stays, postoperative complications, histopathologic characteristics (size, capsular invasion, multiplicity, bilaterality, and central and lateral neck lymph node metastases), and TNM stage according to the sixth edition of the American Joint Committee on Cancer and the International Union Against Cancer (AJCC/UICC) staging system.15 Data were obtained from a prospectively enrolled database maintained in the department. Postoperatively, all patients diagnosed with thyroid carcinoma were given levothyroxine to suppress thyroid stimulating hormone and were followed up regularly at 3 to 6 month intervals. Patients indicated for radioactive iodine therapy were treated at around 4 to 6 weeks postoperatively and underwent a 131I whole-body scan 2 days after radioactive iodine therapy.
Operation Method The operative technique has been described extensively.11–13 Briefly, ET was performed using a gasless transaxillary double-incision approach. The surgical procedure consists of 2 stages: (1) the creation of a working space (ie, flap dissection from the axilla to the anterior neck and connection of a retractor to an external lifting system) and (2) thyroid dissection.
Creation of Working Space Patients are placed in supine position while under general anesthesia. The neck is slightly extended and the lesion-side arm is raised and fixed to achieve the shortest distance between axilla and anterior neck (Fig. 1). A 4- to 6-cm-sized vertical skin incision is then made in the axilla to allow the insertion of a 45-degree endoscope and endoscopic instruments. The route to the anterior neck area is dissected through the anterior surface of the pectoralis major muscle by electrical cautery under direct vision, until the anterior border of the sternocleidomastoid muscle (SCM) is exposed. Initially, exposition of the thyroid is achieved through the space between the medial border of the SCM and lateral borders of strap muscles. However, since 2006, this dissection has been approached through the space between SCM branches (between the sternal head and the clavicular head) and continued beneath the strap
FIGURE 1. Positioning of the patient.
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FIGURE 2. Approaching route (the space between 2 branches of SCM). SCM indicates sternocleidomastoid muscle.
muscle until the contralateral lobe of the thyroid is exposed (Fig. 2). An external retractor is then inserted through the skin incision in the axilla and the flap is raised using a lifting device to maintain a working space. A second skin incision (0.5 cm in length) is made on the medial side of the anterior chest wall for the insertion of endoscopic instruments on an imaginary horizontal line starting from the lower end of the axillary incision and extending from 5 to 6 cm.
Thyroidectomy The operation is conducted in the same manner as conventional open thyroidectomy. Under endoscopic guidance, the upper pole of the thyroid is drawn downward and the superior thyroid vessels are identified and individually divided [harmonic scalpel (Johnson & Johnson Medical, Cincinnati, OH)] close to the thyroid gland to avoid injuring the external branch of the superior laryngeal nerve. The lower pole is dissected from adipose and cervical thymic tissues, and the inferior thyroid vein is divided close to the thyroid gland for mobilization. The thyroid gland is then retracted medially, and the perithyroidal fascia is divided and sharply dissected using an endoscopic dissector. Dissection is then carefully performed to identify the inferior thyroid artery and the RLN. The inferior thyroid artery is divided close to the thyroid gland using the harmonic scalpel, and the whole cervical course of the RLN is traced. The superior parathyroid gland is identified during dissection and left intact, and the thyroid gland is then dissected from the trachea. Contralateral thyroidectomy is performed using the same method with anteromedial traction of the thyroid. When CCND (prelaryngeal, pretracheal, and paratracheal regions on the tumor side) is required, soft tissue and lymph nodes are detached from the thyrothymic ligament area with superior-medial retraction of the thyroid while monitoring the track of the RLN. Dissection close to the RLN is performed using a fine endoscopic dissector to avoid damage by collateral energy generated by the harmonic scalpel. In cases of MRND (usually performed by posterolateral neck dissection), the same approach method is used and subplatysmal dissection is performed to the midline of the anterior neck, the submandibular gland superiorly, and the trapezius muscle posteriorly. Initially, soft tissue and lymph nodes around the anterior and posterior aspects of r
2014 Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 6, December 2014
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the SCM are dissected and the carotid artery and internal jugular vein are exposed. The retractor is then placed under the SCM, and dissection is started from the anterior aspect of the carotid artery and jugular vein and continued until the posterior aspect of the internal jugular vein is fully exposed. Dissection of level VB in the posterior neck area is then conducted while preserving the spinal accessory nerve, the phrenic nerve, the thoracic duct, and the brachial nerve plexus. The dissection is then continued up to level II. The resected specimen is extracted through the 4 to 6 cm skin incision. Finally, a 3-mm closed suction drain is inserted through a separate skin incision under the axillary skin incision, and the wound is closed cosmetically. FIGURE 3. Trends in the monthly average of cases done during the observed period.
RESULTS Between November 2001 and December 2010, 1085 cases of ET were performed. There were 228 cases of benign disease and 857 cases of differentiated thyroid cancer. Table 1 provides a breakdown of cases during the 3 phases, namely from November 2001 to August 2003, September 2005 to December 2007, and from January 2008 to December 2010. The overall number of cases increased progressively throughout the study period. However, monthly averages of cases by year showed a progressive increase to a peak of 23.7 cases per month in 2007 followed by a steady decline to about 9.3 cases per month in the 2010 (Fig. 3). The benign to malignant case ratios were 1.3:1 in phase I, 1:3.4 in phase II, and 1:7.8 in phase III, giving an overall ratio of 1:4, which reveals a change from predominantly benign cases initially to almost completely malignant cases in 2010. The mean overall patient age at presentation was 38.9 ± 9.7 years (range, 6 to 68 y) with a male to female ratio of 1:44 (Table 1). Of the 228 benign cases, 189 underwent hemithyroidectomy alone, 37 hemithyroidectomy with contralateral subtotal thyroidectomy, 1 bilateral subtotal thyroidectomy, and 1 bilateral total thyroidectomy. In the 857 patients with thyroid cancer, 316 underwent hemithyroidectomy, 364 hemithyroidectomy with contralateral subtotal thyroidectomy, 174 underwent bilateral total thyroidectomy, and 3 completion thyroidectomy. Excluding the
TABLE 1. Demographic Data
Total Number (%) No. cases Phase I Benign Malignant Total Phase II Benign Malignant Total Phase III Benign Malignant Total Mean age of the patients (y) (range) Sex (female:male) Phase I—November 2001 to August 2003. Phase II—September 2005 to December 2007. Phase III—January 2008 to December 2010.
r
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1085 63 (56.7) 48 (43.3) 111 (10.2) 108 (23.0) 362 (77.0) 470 (43.3) 57 447 504 36.9 ± 9.7 1061:24
(11.3) (89.7) (46.5) (6-68) (44.2:1)
first 30 cancer cases, all cancer patients received prophylactic CCND. Twelve patients with a confirmed metastatic lateral neck lymph node from PTC by preoperative FNAB underwent additional endoscopic MRND. Overall mean operating time was 132.9 ± 48.6 minutes (range, 50 to 485 min). A breakdown of operating times by procedure types is provided in Table 2. The most common histopathologic diagnosis was papillary thyroid carcinoma (PTC), which comprised 847 of the 857 (98.8%) malignant cases, and 697 (81.3%) of these were papillary thyroid microcarcinomas. There were 9 (1.1%) cases of follicular thyroid carcinoma and 1 (0.1%) case of poorly differentiated carcinoma. Central compartment lymph node metastases were present in 233 (27.2%) cases, and 12 (1.4%) had lateral cervical lymph node metastases. There were 168 (19.6%) cases of multifocal lesions and 79 (9.2%) cases of bilateral cancer. In the benign group, adenomatous hyperplasia was the most common diagnosis followed by follicular adenoma [156 (68.4%) and 58 (25.4%) cases, respectively]. The overall complication rate was 13.5%. The most common complications were transient hypocalcemia (6.1%), transient RLN injury (3.9%), hematoma (0.4%), permanent hypocalcemia (0.2%), and permanent RLN injury (0.2%) (Table 3). Taking into account only total thyroidectomy cases, the rates of transient hypocalcemia (< 7.5 mg/dL or symptoms of hypocalcemia) and transient RLN injury were 31.4% and 8.0%, respectively. We performed preoperative or postoperative laryngoscopy for the evaluation of vocal cord palsy only as clinically indicated, not routinely.
TABLE 2. Types of Surgical Procedures and Operating Times
N (%) Surgical procedures LTT TT TT with MRND Operating time (min) Overall (range) LTT (range) TT (range) TT with MRND (range)
910 (83.9) 163 (15.0) 12 (1.1) 132.92 ± 48.6 126.20 ± 41.9 156.50 ± 43.4 322.25 ± 91.0
(50-485) (50-365) (86-381) (183-485)
LTT indicates less–than-total thyroidectomy; MRND, modified radical neck dissection; TT, total thyroidectomy.
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TABLE 3. Summary of Data According to the Time Phase No. cases Ratio of benign to malignant Ratio of TT:LTT Mean tumor size (cm) Benign Malignant TNM stage, N (%) I II IVa Mean operating time (min) (range) Postoperative hospital stay in days (range) Complications, N (%) Overall Transient hypocalcemia Permanent hypocalcemia Transient RLN injury Permanent RLN injury Hematoma Others Cancer recurrence Mean period for recurrence (mo)
Phase I
Phase II
Phase III
111 1.3:1 1:110
470 1:3.4 1:5.4
504 1:7.8 1:4.1
2.81 0.98
2.62 0.74
2.26 0.74
45 (93.8) 3 (6.2) 0 (0) 135.4 ± 49.5 (50-365) 3.2 ± 0.7 (3-8)
320 (88.4) 41 (11.3) 1 (0.3) 140 ± 57.0 (58-485) 3.4 ± 1.4 (2-23)
385 (86.1) 61 (13.6) 1 (0.3) 125.7 ± 37.7 (55-318) 3.3 ± 2.9 (2-62)
0 0 0 0 0 0 0
(0) (0) (0) (0) (0) (0) (0) 0
67 22 2 22 0 5 16
(14.3) (4.7) (0.2) (4.7) (0) (1.0) (3.7) 4 40
80 44 0 21 2 0 13
(15.9) (8.7) (0) (4.1) (0.4) (0) (2.7) 1 35
LTT indicates less-than-total thyroidectomy; RLN, recurrent laryngeal nerve; TT, total thyroidectomy.
Of the 174 cancer patients who underwent total thyroidectomy, 12 did not receive radioiodine ablation (RIA), and 21 did not have follow-up data; thus, 141 were analyzed for completeness of surgery. All of these 141 patients underwent a post-RIA whole-body scan and none showed any abnormal 131I activity in the neck area. All of these 141 patients were also evaluated for postoperative second year follow-up serum thyroglobulin level. However, the data of 29 patients were missing, leaving 112 cases for analysis; among these, the mean serum thyroglobulin level was 0.36 ± 1.35 ng/mL (range, 0.1 to 14.4 ng/mL). The mean follow-up period for the malignancy cancer patient was 52.7 ± 20.3 (range, 3 to 128 mo). During follow-up period, there were 5 cases (0.62%) of cancer recurrence among the 803 patients who underwent ET for malignancy [F/U rate was 93.7% (803/857)]. Three patients had recurrences in contralateral remnant thyroid tissue, and 2 had recurrences in the ipsilateral lateral neck compartment. The mean recurrence-free duration was 39 months.
DISCUSSION Almost 15 years have passed since the idea of endoscopic neck surgery was turned into reality by Gagner.2 During this time, various approaches and techniques have been proposed and refined. At present, ET can be broadly divided into direct and indirect approaches.16,17 Examples of the former include minimally invasive video-assisted thyroid surgery (MIVATS) and video-assisted neck surgery (VANS),4,7 whereby the minimally invasive principle is maintained by accessing the thyroid directly via the neck through small incisions. In contrast, the indirect approach allows access to the thyroid through a remote incision and often necessitates more invasive dissection, although freeing the patient from the customary neck scar. Common sites of incision for the latter include axilla, chest, and breast, typically in combination to provide better access to the thyroid gland; examples include the transaxillary approach,
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the axillo-bilateral-breast approach, and the bilateral axilla breast approach.5,6,8–12 These procedures can be further divided into gas or gasless techniques. At our institution, the gasless transaxillary approach has been adopted as the standard ET technique. This approach was developed by Chung and is based on a modification of the original completely endoscopic transaxillary with gas technique devised by Ikeda.5 The natural course of well-differentiated carcinoma makes it difficult to determine the long-term results of new thyroidectomy techniques. Several authors have published reports suggesting the feasibility and safety of ET for the treatment of thyroid cancer, particularly low-risk PTC.13,18,19 In the present study, there were 5 cases of recurrent cancer among 803 ET cases (0.62%). Four patients underwent endoscopic less-than-total thyroidectomy with CCND for PTC and 3 experienced recurrence in remnant thyroid tissue (contralateral lobe) at 31, 38, and 64 months after initial surgery, respectively. Two of the 3 underwent endoscopic completion total thyroidectomy and the other, robotic completion total thyroidectomy. The other patient who underwent endoscopic less-than-total thyroidectomy with CCND for PTC had recurrence in the lateral neck compartment at 35 months postoperatively and underwent robotic completion total thyroidectomy with robotic MRND for the recurrence. The last patient underwent endoscopic total thyroidectomy with CCND for PTC (T2N1aMo) and experienced recurrence in the lateral neck compartment at 27 months postoperatively and subsequently underwent open MRND. Although this study enrolled 10 year’s experience of ET and the oncologic results were acceptable, considering the natural history of thyroid cancer, it would be important to have longer follow-up to assess the long-term results of this procedure compared with standard open surgery. The overall complication rate of ET in this series was B13%. The more common complications were temporary hypocalcemia and transient RLN palsy (6.1% and 4.0%, r
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respectively). In fact, among the bilateral total thyroidectomy cases in our series, the rate of temporary hypocalcaemia was high at 30.9%. However, almost all of these transient complications resolved completely within 2 to 3 months. The rates of permanent hypocalcaemia and RLN injury were 0.1% and 0.2%, respectively, which are comparable with the complication rates of conventional open thyroidectomies. Other complications, such as, hematoma, seroma, and tracheal and esophageal injuries, did occur but were uncommon. The 3 time periods within our study period, namely, phases I, II, and III, represents the evolution of gasless transaxillary ET at our institution. Phase I was a learning period when the procedure was first developed and introduced; cases were carefully chosen from among patients with small benign disease or low-risk papillary thyroid cancer, and procedures were mainly ipsilateral hemithyroidectomies, with only one total thyroidectomy. Central compartment lymph node dissections (CCND) were gradually introduced after the first 30 cancer cases. Phase II represented a period of growth and as experience accumulated, more cases were performed and the proportion of thyroid cancer cases increased. In addition, indications were extended slightly, and selective lymph node dissection and MRND were attempted. In contrast, phase III was a period of maturation and training. The majority of cases were for PTCs, mainly subcentimeter lesions (papillary thyroid microcarcinomas), and cases of benign thyroid disease were only performed occasionally. Selective lymph node and MRND were not performed during this phase, because experience during phase II showed that although these procedures were possible endoscopically, they were simply too taxing in terms of technical difficulty, ergonomics, and operating time to be made routine components of ET. During phase III, ET was incorporated into the training program of trainees in Endocrine surgery at our institution. The present study raises another interesting point. The overall numbers of cases treated in the 3 phases show an increasing trend, but average numbers of ETs per month show a peak of around 24 ET cases per month that reached in the middle of phase II and since then, this has steadily declined to
