ORIGINAL ARTICLE
Clinical Application of Endoscopic Thyroidectomy Via an Anterior Chest Wall Approach Xiaoyuan Wang, MD, Wei Yang, MD, and Yueming Sun, MD
Background: Endoscopic minimally invasive surgery of the cervical region is currently used to treat benign thyroid disease. The aim of this study was to evaluate the safety, feasibility, and inflammatory response to endoscopic thyroidectomy (ET) via an anterior chest wall approach. Methods: Between January 2007 and January 2012, 320 patients underwent sub-total/total thyroidectomy. Of these, 160 had endoscopic surgery through an anterior chest wall approach (ET, group A) and 160 had traditional open surgery (group B). Demographics, operation time, intraoperative blood loss, complications, hospital stay, cost, and postoperative outcomes were compared between the 2 groups. Serum Interleukin-6 and C-reactive protein levels were measured preoperatively and at 2, 12, 24, and 48 hours postoperatively. Results: Patient demographics, tumor size, operation time, and pathologic diagnoses were similar in both groups. There was no difference in procedure time and postoperative complication rates. Intraoperative blood loss and length of hospital stay were significantly lower in group A (P < 0.05), but cost was higher (P < 0.05). Serum Interleukin-6 and C-reactive protein levels increased significantly after both procedures, with levels at the 24hour and 48-hour time points higher in group B (P < 0.05). Two cases in group A and 1 in group B developed a transient hoarse voice postoperatively, which recovered 7.5 days (range, 5 to 12 d) later. There were no serious complications during the 2-year follow-up. Conclusions: ET through an anterior chest wall approach is safe and feasible for benign thyroid disease, and offers the advantage of no visible scar.
demonstrated a remarkable disadvantage for the detrimental incision on the neck, which can result into prominently scarring to develop into a keloid. As a result, the patients with thyroid tumors may put the open surgery approach aside due to its detrimental effects on cosmic outcomes. In the sequence, ET was introduced with an attempt to compromise the cosmic defect of open surgery by the minimally invasive management of ET.1 It was for the first time that Hu¨scher et al2 described a case report on endoscopic right lobectomy of thyroid gland in 1997. Thereafter, Ikeda et al3 and Ohgami et al4 reported that the minimally invasive operation may further improve the cosmetic result by ET through an transaxillary approach. Recently, ET has obtained a widespread acceptance by skilled surgeons with the technique and skill developments of endoscopic approach. However, with regard to the more extensive tissue dissection with ET, ET could be characterized as a minimally invasive approach to reach the satisfactory level of tissue dissection.5 Owing to the scarcity of large-scale trials evaluating the degree of injury arising from ET, our controlled trial was designed and undertaken in the laparoscopic center of our hospital. Three hundred twenty patients were selected and divided into 2 groups: 160 performed the ET (ET, group A), whereas 160 were required to perform the traditional open surgery (OS, group B), between January 2007 and January 2012. The aim of the study was to investigate the safety, feasibility, and inflammatory response of ET as compared with OS.
Key Words: endoscopy, thyroidectomy, anterior chest wall approach
(Surg Laparosc Endosc Percutan Tech 2014;24:254–258)
PATIENTS AND METHODS
E
ndoscopic surgical techniques for thyroid cancer surgery can benefit patients by eliminating the anterior neck incision used in the traditional open approach. In addition to superior cosmetic results, endoscopic thyroidectomy (ET) can reduce postoperative pain and discomfort, shorten hospital stay, and enhance postoperative recovery.1–2 Despite these advantages, ET has technical limitations, including the use of straight, rigid endoscopic instruments without articulation and a 2-dimensional (2D) view. As compared with ET, conventional open thyroidectomy Received for publication August 9, 2012; accepted March 24, 2013. From the Department of Minimally Invasive Surgery, The First Affiliated Hospital of Nanjing Medical University, Jiangsu, China. The authors declare no conflicts of interest. Reprints: Yueming Sun, MD, Department of Minimally Invasive Surgery, the First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Road, Nanjing, Jiangsu 210029, China (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins
254 | www.surgical-laparoscopy.com
Patients This is characterized as a prospective trial. From January 2007 to January 2012, a total of 320 consecutive patients with pathologically confirmed benign thyroid nodules were enrolled into the study and randomly assigned to undergoing ET (n = 160) or OS (n = 160). ET group included 116 female and 44 male at the age of 47.6 ± 13.8 years, whereas 110 female and 50 male at the age of 51.3 ± 18.7 years were assigned to undergo OS. All recruited patients were assessed by the mean of ultrasonography of the thyroid gland. The maximal diameter of the largest nodule ranged from 1.5 to 5.2 cm (mean 3.9 cm). Sixteen patients had compressive symptoms pertinent to an inflated multinodular goiter. Exclusion criteria included a history of neck surgery or radiotherapy, thyroiditis, or hyperthyroidism, or the presence of a thyroid nodule with a diameter of >6 cm, or coexisting immune system disease. All informed written consents were obtained before surgery. The clinical trial was approved by the ethics and academic committees of the hospital.
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Operative Technique The endoscopic surgical approach has been described previously.6 Both ET and OS thyroidectomies were performed by an experienced surgeon (Y.S.) at our hospital. Under general anesthesia, the patient was placed at the lithotomy position with the neck extended by a sandbag under the neck. Three incisions were made, a 12-mm benign tumor-spared skin incision was made to insert the laparoscope (A), and two 5-mm trocars (B) were then inserted into the subcutaneous tissue with a distance of approximately 3 to 5 cm from the lower margin of the ipsilateral clavicle. A postoperative drainage tube was positioned through the incisions (B; Fig. 1). We established a subcutaneous space by subcutaneously injecting 20 mL of 1% epinephrine solution, an expanding dilator and carbon dioxide (CO2) with a pressure of 8 mm Hg. We then adjusted the locations of the trocars according to the size of benign tumor. To ensure a correct subcutaneous plane, the avascular areolar tissue was visualized during the initial dissection (Fig. 1B). A longitudinal incision of the linea alba cervicalis was deemed as necessary to expose and explore the thyroid gland (Fig. 1C). Subtotal or total lobectomy was performed according to the characteristics of the neoplasm.7 It is important to protect the parathyroid glands and the recurrent laryngeal nerve (RLN) (Fig. 1D). The thyroid tumor-involved lobe was retracted forward and inward, after ligation of the middle vein with an ultracision harmonic scalpel, and the parathyroid gland was identified and carefully protected from injury (Fig. 1E). Then, the linea alba cervicalis was sutured (Fig. 1F). Conventional
Endoscopic Thyroidectomy Via Anterior Chest Wall
thyroidectomy was performed through a 6 cm transverse incision on the neck. Subplatysmal flaps were freed with a superior margin of the thyroid cartilage and inferior margin to the suprasternal notch. The lesion was then exposed to perform the open thyroidectomy. Patients were seen at the clinic every 3 months and underwent a complete examination, including neck computed tomography or magnetic resonance image and thyroid gland function test every year. Other examinations were performed whenever they were clinically indicated.
Preparation of Blood Samples and Assays Blood samples were obtained 2 days before surgery and 2, 12, 24, and 48 hours after surgery. They were centrifuged at 1500 g for 15 minutes to separate the serum and then stored at 701C until assay. Interleukin-6 (IL-6) levels were measured with an enzyme-linked immunosorbent assay (ELISA) kit (R&D Systems, Minneapolis, MN), according to manufacturer’s instructions. The system used a solid-phase monoclonal antibody and an enzyme-linked polyclonal antibody against human IL-6. All analyses and calibrations were performed in duplicate using 100-mL serum for each analysis. Absorbance at 450 nm was acceptable. C-reactive protein (CRP) levels were measured automatically by nephelometry (BN II; Dade Behring, Marburg, Germany), according to the manufacturer’s instructions. The levels of IL-6 and CRP in blood samples can reflect the postoperative inflammatory response to operative trauma, which can be helpful in evaluating the prognosis of thyroid gland disease.
FIGURE 1. A, For the anterior anterosternal approach, a 12-mm medial skin incision is made for insertion of a laparoscope (A). Two 5 mm trocars (B) are then inserted into the subcutaneous tissue approximately 3 to 5 cm below the inferior border of the ipsilateral clavicle. A postoperative drainage tube is inserted through the incisions (B). B, For a correct subcutaneous plane, the avascular areolar tissue is visualized during the initial dissection. C, Once the muscles are retracted, a round of preliminary blunt dissection lateral to the thyroid is performed to mobilize the lobe thoroughly. D, Videoscopic surgery facilitates a clearer delineation of the anatomy. After retracting the thyroid lobe in an anterior and medial direction, the fascia is opened by gentle retraction with the spatula. The recurrent laryngeal nerve can be seen lying in the thyrotracheal groove. Arrow D shows the recurrent laryngeal nerve which should be handled with scrupulous care during the operation. E, The thyroid lobe is retracted in an anterior and medial direction, after ligation of the middle vein with an ultracision harmonic scalpel, and the parathyroid gland is identified. Arrow E shows the parathyroid gland which should also be handled with caution during the operation. F, The cervical line alba is closed by an interrupted suture with vicryl. r
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Statistical Analyses Patient age, sex, tumor size, blood loss, and duration of surgery are expressed as mean ± SD. Differences in these parameters between the 2 groups were analyzed using the Student t test. Differences in changes in levels of IL-6 and CRP between the 2 groups were analyzed using a nonparametric test. A P-value 0.05). Levels of IL-6 and CRP increased significantly after both procedures compared to preoperative levels, and levels of IL-6 and CRP at the 24-hour and 48-hour time points were higher in group B than in group A (P < 0.05). A significant rise in IL-6 levels was induced by surgery, reaching a peak at 24 hours after the operation. Levels of CRP increased later than IL-6 levels. The rise in IL-6 and CRP levels was less in group A than in group B.
DISCUSSION The past decade has seen dramatic developments in minimally invasive approaches. Laparoscopic surgery is
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now preferred for benign disease. Since it is introduced as a surgical technique for operations on the parathyroid8 and thyroid glands,2 endoscopic surgery has become an attractive surgery all over the world. Indeed, some surgeons perform ET for well-differentiated thyroid carcinoma and Graves disease,9,10 as well as benign thyroid tumors. The endoscopic techniques can be classified depending on the a manageable space creation by gas insufflation and introduction of trocars through the cervical or anterior chest wall, or breast or the use of axillary approaches. The trans-axillary approach offers a better cosmetic advantage as compared with the trans-cervical or anterior chest wall approaches.11 However, all operative approaches have their related advantages and disadvantages (Table 2). We chose the anterior chest wall approach for our study as we had previous experience of endoscopic parathyroidectomy using this method.6 We have stringent indications of performing endoscopic procedure: a thyroid nodule of r6 cm, no prior neck radiation or surgery, and no evidence of hyperthyroidism. In addition, cases of micropapillary carcinoma found coincidentally during resection for multinodular goiter were excluded. Conventional open thyroidectomy is a safe, effective, and well-tolerated therapy modality for the various thyroid diseases. In contrast, ET is an innovative procedure with satisfactory cosmetic results. Despite the untouchable management of ET, our results relied on the great experience of endoscopic surgeries performed by the expert surgeon in our institution, reducing iatrogenic injury due to the manageable inexperience. In our study, intraoperative blood loss and length of hospital stay were significantly lower in the ET group as compared with those in the OS group. However, the mean operation time and postoperative complication rates were similar for both. It indicated that ET displayed the superiority of postoperative recovery and did not increase the risk for postoperative complications. Postoperative complications included 3 cases of transient RLN palsy, 2 in group A and 1 in group B. The potential to identify and preserve the nerve during surgery has subsequently helped to prevent the occurrence of transient RLN palsy. During the operative procedures, it is alert that electrocautery and ultrasonic scalpel may yield the RLN injury due to the regional hyperthermia. Postoperative bleeding is defined as a fatal complication. In our study, bleeding from the trocar incision was observed in 1 case of group A, and another 1 in group B with bleeding
TABLE 1. Comparison of Clinical Data Between the 2 Groups Age (y) Sex (M/F) Maximal tumor size (cm) Duration of the operation (min) Surgical procedures (subtotal/total) Intraoperative blood loss (mL) Postoperative bleeding (case, %) Transient hoarseness (case, %) Hypocalcemia Hypercapnia Subcutaneous emphysema Pathology (adenoma/nodular goiter) Cost (Yuan) Postoperative hospital stay (d)
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Group A
Group B
P
47.6 ± 13.8 44/116 3.8 ± 1.3 92.5 ± 24.1 116/44 12.6 ± 10.9 1, 0.6 2, 1.2% — — — 34/126 9534 ± 1053 4.2 ± 1.8
51.3 ± 18.7 50/110 4.2 ± 1.1 87.8 ± 33.5 130/30 27.2 ± 17.4 1, 0.6% 1, 0.6 — — — 44/116 7892 ± 838 6.8 ± 1.3
> 0.05 > 0.05 > 0.05 > 0.05 > 0.05 < 0.05 > 0.05 > 0.05
r
> 0.05 < 0.05 < 0.05
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Endoscopic Thyroidectomy Via Anterior Chest Wall
TABLE 2. The Advantages and Disadvantages of Different Endoscopic Thyroidectomy Approaches
ET (Approach) Cosmesis Difficulty of anatomy and dissection Unilateral/bilateral thyroidectomy
Traditional OS
Axillary
Cervical
Anterior Chest Wall
Breast
Bilateral
++++ ++++ Unilateral
+ + Bilateral
++ ++ Bilateral
+++ +++ Bilateral
ET indicates endoscopic thyroidectomy; + , difficult degrees;
, no means in the OS.
from residual thyroid tissue. Both patients required further surgery to govern the hemorrhage. Besides, other complications included numbness, wound discomfort, and mild pain with neck movement or swallowing, which resolved 1 to 2 months after the operation. No late complications were observed. However, the rates of postoperative complications were similar in 2 groups, suggesting that ET can yield the therapeutic efficacy similar to that from OS. IL-6 and CRP are predictive of inflammatory response and acute phase of inflammatory responses after surgery.12–14 To evaluate the extent of trauma after ET, we examined the levels of IL-6 and CRP over time in both groups. Serum IL-6 and CRP levels at the 24-hour and 48-hour time points were higher in group B than in group A (Chart 1). The dissective area in the anterior chest wall and neck is significantly larger than that required by OS. Nevertheless, it seemed that a larger dissective area is not necessary to improve the operative outcomes. The concept of endoscopic subcutaneous surgery has been introduced before, and it has also been confirmed in animal models to cause fewer traumas.15 In the view of an anatomic point, there is a potential space (the fascia cleft) between the superficial fascia and muscular fascia in the neck and in the anterior chest region.16 In our series, we created a working space along
CHART 1. Serum IL-6 (pg/mL) and CRP (mg/L) levels preoperatively/postoperatively. CRP indicates C-reactive protein; IL, interleukin. r
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this layer. As long as the dissection is in the right surgical plane, the degree of invasiveness will not necessarily increase significantly even though the dissection area is larger. The single shorter incision is ascribed to the less disturbance to the integrity of anatomic structures. In addition, endoscopic amplification of the visual field and the use of a harmonic scalpel enabled a more accurate resection and a reduction in hemorrhage.17–19 Blood loss in the endoscopic group was significantly lower than that in the conventional group. Both, the length of the incision and total blood loss are important factors for surgical outcomes.20–22 Thus, it follows that ET is advantageous over conventional thyroidectomy for reducing surgical trauma. Based on our subjective and objective evidence, we conclude that ET is a minimally invasive approach for treating benign thyroid disease.
REFERENCES 1. Ikeda Y, Takami H, Sasaki Y, et al. Comparative study of thyroidectomies: endoscopic surgery versus conventional open surgery. Surg Endosc. 2002;16:1741–1745. 2. Hu¨scher CS, Chiodini S, Napolitano C, et al. Endoscopic right thyroid lobectomy. Surg Endosc. 1997;11:877. 3. Ikeda Y, Takami H, Sasaki Y, et al. Endoscopic neck surgery by the axillary approach. J Am Coll Surg. 2000;191:336–340. 4. Ohgami M, Ishii S, Arisawa Y, et al. Scarless endoscopic thyroidectomy: breast approach for better cosmesis. Surg Laparosc Endosc Percutan Tech. 2000;10:1–4. 5. Tan CT, Cheah WK, Delbridge L. “Scarless” (in the neck) endoscopic thyroidectomy (SET): an evidence-based review of published techniques. World J Surg. 2008;32:1349–1357. 6. Sun Y, Cai H, Bai J, et al. Endoscopic total parathyroidectomy and partial parathyroid tissue autotransplantation for patients with secondary hyperparathyroidism: a new surgical approach. World J Surg. 2009;33:1674–1679. 7. Shimizu K, Kitagawa W, Akasu H, et al. Video-assisted minimally invasive endoscopic thyroid surgery using a gasless neck skin lifting method—153 cases of benign thyroid tumors and applicability for large tumors. Biomed Pharmacother. 2002;56(suppl 1):88s–91s. 8. Gagner M. Endoscopic subtotal parathyroidectomy in patients with primary hyperparathyroidism. Br J Surg. 1996;83:875. 9. Kang SW, Park JH, Jeong JS, et al. Prospects of robotic thyroidectomy using a gasless, transaxillary approach for the management of thyroid carcinoma. Surg Laparosc Endosc Percutan Tech. 2011;21:223–229. 10. Sasaki A, Nitta H, Otsuka K, et al. Endoscopic subtotal thyroidectomy: the procedure of choice for Graves’ disease? World J Surg. 2009;33:67–71. 11. Yeung GH. Endoscopic thyroid surgery today: a diversity of surgical strategies. Thyroid. 2002;12:703–706. 12. Kristiansson M, Saraste L, Soop M, et al. Diminished interleukin-6 and C-reactive protein responses to laparoscopic versus open cholecystectomy. Acta Anaesthesiol Scand. 1999; 43:146–152.
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13. Grande M, Tucci GF, Adorisio O, et al. Systemic acute-phase response after laparoscopic and open cholecystectomy. Surg Endosc. 2002;16:313–316. 14. Karayiannakis AJ, Makri GG, Mantzioka A, et al. Systemic stress response after laparoscopic or open cholecystectomy: a randomized trial. Br J Surg. 1997;84:467–471. 15. Kronowitz SJ. Endoscopic subcutaneous surgery: a new surgical approach. Ann Plast Surg. 1999;42:357–364. 16. Abu-Hijleh MF, Roshier AL, Al-Shboul Q, et al. The membranous layer of superficial fascia: evidence for its widespread distribution in the body. Surg Radiol Anat. 2006; 28:606–619. 17. Jeong JJ, Kang SW, Yun JS, et al. Comparative study of endoscopic thyroidectomy versus conventional open thyroidectomy in papillary thyroid microcarcinoma (PTMC) patients. J Surg Oncol. 2009;100:477–480.
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18. Slotema ET, Sebag F, Henry JF. What is the evidence for endoscopic thyroidectomy in the management of benign thyroid disease? World J Surg. 2008;32:1325–1332. 19. Shimizu K, Tanaka S. Asian perspective on endoscopic thyroidectomy—a review of 193 cases. Asian J Surg. 2003;26: 92–100. 20. Ishibashi S, Takeuchi H, Fujii K, et al. Length of laparotomy incision and surgical stress assessed by serum IL-6 level. Injury. 2006;37:247–251. 21. Huang TJ, Hsu RW, Li YY, et al. Less systemic cytokine response in patients following microendoscopic versus open lumbar discectomy. J Orthop Res. 2005;23:406–411. 22. Schietroma M, Carlei F, Franchi L, et al. A comparison of serum interleukin-6 concentrations in patients treated by cholecystectomy via laparotomy or laparoscopy. Hepatogastroenterology. 2004;51:1595–1599.
r
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Clinical Application of Endoscopic Thyroidectomy Via an Anterior Chest Wall Approach Xiaoyuan Wang, MD, Wei Yang, MD, and Yueming Sun, MD
Background: Endoscopic minimally invasive surgery of the cervical region is currently used to treat benign thyroid disease. The aim of this study was to evaluate the safety, feasibility, and inflammatory response to endoscopic thyroidectomy (ET) via an anterior chest wall approach. Methods: Between January 2007 and January 2012, 320 patients underwent sub-total/total thyroidectomy. Of these, 160 had endoscopic surgery through an anterior chest wall approach (ET, group A) and 160 had traditional open surgery (group B). Demographics, operation time, intraoperative blood loss, complications, hospital stay, cost, and postoperative outcomes were compared between the 2 groups. Serum Interleukin-6 and C-reactive protein levels were measured preoperatively and at 2, 12, 24, and 48 hours postoperatively. Results: Patient demographics, tumor size, operation time, and pathologic diagnoses were similar in both groups. There was no difference in procedure time and postoperative complication rates. Intraoperative blood loss and length of hospital stay were significantly lower in group A (P < 0.05), but cost was higher (P < 0.05). Serum Interleukin-6 and C-reactive protein levels increased significantly after both procedures, with levels at the 24hour and 48-hour time points higher in group B (P < 0.05). Two cases in group A and 1 in group B developed a transient hoarse voice postoperatively, which recovered 7.5 days (range, 5 to 12 d) later. There were no serious complications during the 2-year follow-up. Conclusions: ET through an anterior chest wall approach is safe and feasible for benign thyroid disease, and offers the advantage of no visible scar.
demonstrated a remarkable disadvantage for the detrimental incision on the neck, which can result into prominently scarring to develop into a keloid. As a result, the patients with thyroid tumors may put the open surgery approach aside due to its detrimental effects on cosmic outcomes. In the sequence, ET was introduced with an attempt to compromise the cosmic defect of open surgery by the minimally invasive management of ET.1 It was for the first time that Hu¨scher et al2 described a case report on endoscopic right lobectomy of thyroid gland in 1997. Thereafter, Ikeda et al3 and Ohgami et al4 reported that the minimally invasive operation may further improve the cosmetic result by ET through an transaxillary approach. Recently, ET has obtained a widespread acceptance by skilled surgeons with the technique and skill developments of endoscopic approach. However, with regard to the more extensive tissue dissection with ET, ET could be characterized as a minimally invasive approach to reach the satisfactory level of tissue dissection.5 Owing to the scarcity of large-scale trials evaluating the degree of injury arising from ET, our controlled trial was designed and undertaken in the laparoscopic center of our hospital. Three hundred twenty patients were selected and divided into 2 groups: 160 performed the ET (ET, group A), whereas 160 were required to perform the traditional open surgery (OS, group B), between January 2007 and January 2012. The aim of the study was to investigate the safety, feasibility, and inflammatory response of ET as compared with OS.
Key Words: endoscopy, thyroidectomy, anterior chest wall approach
(Surg Laparosc Endosc Percutan Tech 2014;24:254–258)
PATIENTS AND METHODS
E
ndoscopic surgical techniques for thyroid cancer surgery can benefit patients by eliminating the anterior neck incision used in the traditional open approach. In addition to superior cosmetic results, endoscopic thyroidectomy (ET) can reduce postoperative pain and discomfort, shorten hospital stay, and enhance postoperative recovery.1–2 Despite these advantages, ET has technical limitations, including the use of straight, rigid endoscopic instruments without articulation and a 2-dimensional (2D) view. As compared with ET, conventional open thyroidectomy Received for publication August 9, 2012; accepted March 24, 2013. From the Department of Minimally Invasive Surgery, The First Affiliated Hospital of Nanjing Medical University, Jiangsu, China. The authors declare no conflicts of interest. Reprints: Yueming Sun, MD, Department of Minimally Invasive Surgery, the First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Road, Nanjing, Jiangsu 210029, China (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins
254 | www.surgical-laparoscopy.com
Patients This is characterized as a prospective trial. From January 2007 to January 2012, a total of 320 consecutive patients with pathologically confirmed benign thyroid nodules were enrolled into the study and randomly assigned to undergoing ET (n = 160) or OS (n = 160). ET group included 116 female and 44 male at the age of 47.6 ± 13.8 years, whereas 110 female and 50 male at the age of 51.3 ± 18.7 years were assigned to undergo OS. All recruited patients were assessed by the mean of ultrasonography of the thyroid gland. The maximal diameter of the largest nodule ranged from 1.5 to 5.2 cm (mean 3.9 cm). Sixteen patients had compressive symptoms pertinent to an inflated multinodular goiter. Exclusion criteria included a history of neck surgery or radiotherapy, thyroiditis, or hyperthyroidism, or the presence of a thyroid nodule with a diameter of >6 cm, or coexisting immune system disease. All informed written consents were obtained before surgery. The clinical trial was approved by the ethics and academic committees of the hospital.
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Operative Technique The endoscopic surgical approach has been described previously.6 Both ET and OS thyroidectomies were performed by an experienced surgeon (Y.S.) at our hospital. Under general anesthesia, the patient was placed at the lithotomy position with the neck extended by a sandbag under the neck. Three incisions were made, a 12-mm benign tumor-spared skin incision was made to insert the laparoscope (A), and two 5-mm trocars (B) were then inserted into the subcutaneous tissue with a distance of approximately 3 to 5 cm from the lower margin of the ipsilateral clavicle. A postoperative drainage tube was positioned through the incisions (B; Fig. 1). We established a subcutaneous space by subcutaneously injecting 20 mL of 1% epinephrine solution, an expanding dilator and carbon dioxide (CO2) with a pressure of 8 mm Hg. We then adjusted the locations of the trocars according to the size of benign tumor. To ensure a correct subcutaneous plane, the avascular areolar tissue was visualized during the initial dissection (Fig. 1B). A longitudinal incision of the linea alba cervicalis was deemed as necessary to expose and explore the thyroid gland (Fig. 1C). Subtotal or total lobectomy was performed according to the characteristics of the neoplasm.7 It is important to protect the parathyroid glands and the recurrent laryngeal nerve (RLN) (Fig. 1D). The thyroid tumor-involved lobe was retracted forward and inward, after ligation of the middle vein with an ultracision harmonic scalpel, and the parathyroid gland was identified and carefully protected from injury (Fig. 1E). Then, the linea alba cervicalis was sutured (Fig. 1F). Conventional
Endoscopic Thyroidectomy Via Anterior Chest Wall
thyroidectomy was performed through a 6 cm transverse incision on the neck. Subplatysmal flaps were freed with a superior margin of the thyroid cartilage and inferior margin to the suprasternal notch. The lesion was then exposed to perform the open thyroidectomy. Patients were seen at the clinic every 3 months and underwent a complete examination, including neck computed tomography or magnetic resonance image and thyroid gland function test every year. Other examinations were performed whenever they were clinically indicated.
Preparation of Blood Samples and Assays Blood samples were obtained 2 days before surgery and 2, 12, 24, and 48 hours after surgery. They were centrifuged at 1500 g for 15 minutes to separate the serum and then stored at 701C until assay. Interleukin-6 (IL-6) levels were measured with an enzyme-linked immunosorbent assay (ELISA) kit (R&D Systems, Minneapolis, MN), according to manufacturer’s instructions. The system used a solid-phase monoclonal antibody and an enzyme-linked polyclonal antibody against human IL-6. All analyses and calibrations were performed in duplicate using 100-mL serum for each analysis. Absorbance at 450 nm was acceptable. C-reactive protein (CRP) levels were measured automatically by nephelometry (BN II; Dade Behring, Marburg, Germany), according to the manufacturer’s instructions. The levels of IL-6 and CRP in blood samples can reflect the postoperative inflammatory response to operative trauma, which can be helpful in evaluating the prognosis of thyroid gland disease.
FIGURE 1. A, For the anterior anterosternal approach, a 12-mm medial skin incision is made for insertion of a laparoscope (A). Two 5 mm trocars (B) are then inserted into the subcutaneous tissue approximately 3 to 5 cm below the inferior border of the ipsilateral clavicle. A postoperative drainage tube is inserted through the incisions (B). B, For a correct subcutaneous plane, the avascular areolar tissue is visualized during the initial dissection. C, Once the muscles are retracted, a round of preliminary blunt dissection lateral to the thyroid is performed to mobilize the lobe thoroughly. D, Videoscopic surgery facilitates a clearer delineation of the anatomy. After retracting the thyroid lobe in an anterior and medial direction, the fascia is opened by gentle retraction with the spatula. The recurrent laryngeal nerve can be seen lying in the thyrotracheal groove. Arrow D shows the recurrent laryngeal nerve which should be handled with scrupulous care during the operation. E, The thyroid lobe is retracted in an anterior and medial direction, after ligation of the middle vein with an ultracision harmonic scalpel, and the parathyroid gland is identified. Arrow E shows the parathyroid gland which should also be handled with caution during the operation. F, The cervical line alba is closed by an interrupted suture with vicryl. r
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Statistical Analyses Patient age, sex, tumor size, blood loss, and duration of surgery are expressed as mean ± SD. Differences in these parameters between the 2 groups were analyzed using the Student t test. Differences in changes in levels of IL-6 and CRP between the 2 groups were analyzed using a nonparametric test. A P-value 0.05). Levels of IL-6 and CRP increased significantly after both procedures compared to preoperative levels, and levels of IL-6 and CRP at the 24-hour and 48-hour time points were higher in group B than in group A (P < 0.05). A significant rise in IL-6 levels was induced by surgery, reaching a peak at 24 hours after the operation. Levels of CRP increased later than IL-6 levels. The rise in IL-6 and CRP levels was less in group A than in group B.
DISCUSSION The past decade has seen dramatic developments in minimally invasive approaches. Laparoscopic surgery is
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now preferred for benign disease. Since it is introduced as a surgical technique for operations on the parathyroid8 and thyroid glands,2 endoscopic surgery has become an attractive surgery all over the world. Indeed, some surgeons perform ET for well-differentiated thyroid carcinoma and Graves disease,9,10 as well as benign thyroid tumors. The endoscopic techniques can be classified depending on the a manageable space creation by gas insufflation and introduction of trocars through the cervical or anterior chest wall, or breast or the use of axillary approaches. The trans-axillary approach offers a better cosmetic advantage as compared with the trans-cervical or anterior chest wall approaches.11 However, all operative approaches have their related advantages and disadvantages (Table 2). We chose the anterior chest wall approach for our study as we had previous experience of endoscopic parathyroidectomy using this method.6 We have stringent indications of performing endoscopic procedure: a thyroid nodule of r6 cm, no prior neck radiation or surgery, and no evidence of hyperthyroidism. In addition, cases of micropapillary carcinoma found coincidentally during resection for multinodular goiter were excluded. Conventional open thyroidectomy is a safe, effective, and well-tolerated therapy modality for the various thyroid diseases. In contrast, ET is an innovative procedure with satisfactory cosmetic results. Despite the untouchable management of ET, our results relied on the great experience of endoscopic surgeries performed by the expert surgeon in our institution, reducing iatrogenic injury due to the manageable inexperience. In our study, intraoperative blood loss and length of hospital stay were significantly lower in the ET group as compared with those in the OS group. However, the mean operation time and postoperative complication rates were similar for both. It indicated that ET displayed the superiority of postoperative recovery and did not increase the risk for postoperative complications. Postoperative complications included 3 cases of transient RLN palsy, 2 in group A and 1 in group B. The potential to identify and preserve the nerve during surgery has subsequently helped to prevent the occurrence of transient RLN palsy. During the operative procedures, it is alert that electrocautery and ultrasonic scalpel may yield the RLN injury due to the regional hyperthermia. Postoperative bleeding is defined as a fatal complication. In our study, bleeding from the trocar incision was observed in 1 case of group A, and another 1 in group B with bleeding
TABLE 1. Comparison of Clinical Data Between the 2 Groups Age (y) Sex (M/F) Maximal tumor size (cm) Duration of the operation (min) Surgical procedures (subtotal/total) Intraoperative blood loss (mL) Postoperative bleeding (case, %) Transient hoarseness (case, %) Hypocalcemia Hypercapnia Subcutaneous emphysema Pathology (adenoma/nodular goiter) Cost (Yuan) Postoperative hospital stay (d)
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Group A
Group B
P
47.6 ± 13.8 44/116 3.8 ± 1.3 92.5 ± 24.1 116/44 12.6 ± 10.9 1, 0.6 2, 1.2% — — — 34/126 9534 ± 1053 4.2 ± 1.8
51.3 ± 18.7 50/110 4.2 ± 1.1 87.8 ± 33.5 130/30 27.2 ± 17.4 1, 0.6% 1, 0.6 — — — 44/116 7892 ± 838 6.8 ± 1.3
> 0.05 > 0.05 > 0.05 > 0.05 > 0.05 < 0.05 > 0.05 > 0.05
r
> 0.05 < 0.05 < 0.05
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Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
Endoscopic Thyroidectomy Via Anterior Chest Wall
TABLE 2. The Advantages and Disadvantages of Different Endoscopic Thyroidectomy Approaches
ET (Approach) Cosmesis Difficulty of anatomy and dissection Unilateral/bilateral thyroidectomy
Traditional OS
Axillary
Cervical
Anterior Chest Wall
Breast
Bilateral
++++ ++++ Unilateral
+ + Bilateral
++ ++ Bilateral
+++ +++ Bilateral
ET indicates endoscopic thyroidectomy; + , difficult degrees;
, no means in the OS.
from residual thyroid tissue. Both patients required further surgery to govern the hemorrhage. Besides, other complications included numbness, wound discomfort, and mild pain with neck movement or swallowing, which resolved 1 to 2 months after the operation. No late complications were observed. However, the rates of postoperative complications were similar in 2 groups, suggesting that ET can yield the therapeutic efficacy similar to that from OS. IL-6 and CRP are predictive of inflammatory response and acute phase of inflammatory responses after surgery.12–14 To evaluate the extent of trauma after ET, we examined the levels of IL-6 and CRP over time in both groups. Serum IL-6 and CRP levels at the 24-hour and 48-hour time points were higher in group B than in group A (Chart 1). The dissective area in the anterior chest wall and neck is significantly larger than that required by OS. Nevertheless, it seemed that a larger dissective area is not necessary to improve the operative outcomes. The concept of endoscopic subcutaneous surgery has been introduced before, and it has also been confirmed in animal models to cause fewer traumas.15 In the view of an anatomic point, there is a potential space (the fascia cleft) between the superficial fascia and muscular fascia in the neck and in the anterior chest region.16 In our series, we created a working space along
CHART 1. Serum IL-6 (pg/mL) and CRP (mg/L) levels preoperatively/postoperatively. CRP indicates C-reactive protein; IL, interleukin. r
2014 Lippincott Williams & Wilkins
this layer. As long as the dissection is in the right surgical plane, the degree of invasiveness will not necessarily increase significantly even though the dissection area is larger. The single shorter incision is ascribed to the less disturbance to the integrity of anatomic structures. In addition, endoscopic amplification of the visual field and the use of a harmonic scalpel enabled a more accurate resection and a reduction in hemorrhage.17–19 Blood loss in the endoscopic group was significantly lower than that in the conventional group. Both, the length of the incision and total blood loss are important factors for surgical outcomes.20–22 Thus, it follows that ET is advantageous over conventional thyroidectomy for reducing surgical trauma. Based on our subjective and objective evidence, we conclude that ET is a minimally invasive approach for treating benign thyroid disease.
REFERENCES 1. Ikeda Y, Takami H, Sasaki Y, et al. Comparative study of thyroidectomies: endoscopic surgery versus conventional open surgery. Surg Endosc. 2002;16:1741–1745. 2. Hu¨scher CS, Chiodini S, Napolitano C, et al. Endoscopic right thyroid lobectomy. Surg Endosc. 1997;11:877. 3. Ikeda Y, Takami H, Sasaki Y, et al. Endoscopic neck surgery by the axillary approach. J Am Coll Surg. 2000;191:336–340. 4. Ohgami M, Ishii S, Arisawa Y, et al. Scarless endoscopic thyroidectomy: breast approach for better cosmesis. Surg Laparosc Endosc Percutan Tech. 2000;10:1–4. 5. Tan CT, Cheah WK, Delbridge L. “Scarless” (in the neck) endoscopic thyroidectomy (SET): an evidence-based review of published techniques. World J Surg. 2008;32:1349–1357. 6. Sun Y, Cai H, Bai J, et al. Endoscopic total parathyroidectomy and partial parathyroid tissue autotransplantation for patients with secondary hyperparathyroidism: a new surgical approach. World J Surg. 2009;33:1674–1679. 7. Shimizu K, Kitagawa W, Akasu H, et al. Video-assisted minimally invasive endoscopic thyroid surgery using a gasless neck skin lifting method—153 cases of benign thyroid tumors and applicability for large tumors. Biomed Pharmacother. 2002;56(suppl 1):88s–91s. 8. Gagner M. Endoscopic subtotal parathyroidectomy in patients with primary hyperparathyroidism. Br J Surg. 1996;83:875. 9. Kang SW, Park JH, Jeong JS, et al. Prospects of robotic thyroidectomy using a gasless, transaxillary approach for the management of thyroid carcinoma. Surg Laparosc Endosc Percutan Tech. 2011;21:223–229. 10. Sasaki A, Nitta H, Otsuka K, et al. Endoscopic subtotal thyroidectomy: the procedure of choice for Graves’ disease? World J Surg. 2009;33:67–71. 11. Yeung GH. Endoscopic thyroid surgery today: a diversity of surgical strategies. Thyroid. 2002;12:703–706. 12. Kristiansson M, Saraste L, Soop M, et al. Diminished interleukin-6 and C-reactive protein responses to laparoscopic versus open cholecystectomy. Acta Anaesthesiol Scand. 1999; 43:146–152.
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13. Grande M, Tucci GF, Adorisio O, et al. Systemic acute-phase response after laparoscopic and open cholecystectomy. Surg Endosc. 2002;16:313–316. 14. Karayiannakis AJ, Makri GG, Mantzioka A, et al. Systemic stress response after laparoscopic or open cholecystectomy: a randomized trial. Br J Surg. 1997;84:467–471. 15. Kronowitz SJ. Endoscopic subcutaneous surgery: a new surgical approach. Ann Plast Surg. 1999;42:357–364. 16. Abu-Hijleh MF, Roshier AL, Al-Shboul Q, et al. The membranous layer of superficial fascia: evidence for its widespread distribution in the body. Surg Radiol Anat. 2006; 28:606–619. 17. Jeong JJ, Kang SW, Yun JS, et al. Comparative study of endoscopic thyroidectomy versus conventional open thyroidectomy in papillary thyroid microcarcinoma (PTMC) patients. J Surg Oncol. 2009;100:477–480.
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18. Slotema ET, Sebag F, Henry JF. What is the evidence for endoscopic thyroidectomy in the management of benign thyroid disease? World J Surg. 2008;32:1325–1332. 19. Shimizu K, Tanaka S. Asian perspective on endoscopic thyroidectomy—a review of 193 cases. Asian J Surg. 2003;26: 92–100. 20. Ishibashi S, Takeuchi H, Fujii K, et al. Length of laparotomy incision and surgical stress assessed by serum IL-6 level. Injury. 2006;37:247–251. 21. Huang TJ, Hsu RW, Li YY, et al. Less systemic cytokine response in patients following microendoscopic versus open lumbar discectomy. J Orthop Res. 2005;23:406–411. 22. Schietroma M, Carlei F, Franchi L, et al. A comparison of serum interleukin-6 concentrations in patients treated by cholecystectomy via laparotomy or laparoscopy. Hepatogastroenterology. 2004;51:1595–1599.
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