JOURNAL OF LAPAROENDOSCOPIC & ADVANCED SURGICAL TECHNIQUES Volume 25, Number 6, 2015 ª Mary Ann Liebert, Inc. DOI: 10.1089/lap.2015.0026
Complete Endoscopic Thyroidectomy via Oral Vestibular Approach Versus Areola Approach for Treatment of Thyroid Diseases Jingge Yang, MD,1 Cunchuan Wang, MD, PhD,1 Jinyi Li, MD,1 Wah Yang, MD,1 Guo Cao, MD,1 Hong-meng Wong, MD,1 Hening Zhai, MD,1 and Weijun Liu, MD 2
Abstract
Background: Natural orifice translumenal endoscopic surgery (NOTES; American Society for Gastrointestinal Endoscopy [Oak Brook, IL] and Society of American Gastrointestinal and Endoscopic Surgeons [Los Angeles, CA]) is gaining interest because it allows operations without skin incisions. The aim of this study was to evaluate the feasibility, safety, and cosmetic results of endoscopic thyroidectomy via the oral vestibular approach (ETOVA) compared with endoscopic thyroidectomy via the areola approach (ETAA) in patients with thyroid diseases. Materials and Methods: Eighty-two patients with thyroid diseases were randomized to receive either ETOVA (n = 41) or ETAA (n = 41). Perioperative and follow-up data were assessed. Results: The surgery was completed in all cases, and all patients were followed up for at least 1 year. There were no differences between the two groups in operation time, blood loss, or postoperative hospital stay. Respective pain scores were 1.7 versus 2.1 and 0.6 versus 0.8 on Days 1 and 3, respectively, postoperatively. The white blood cell counts and C-reactive protein levels were not significantly different between the two groups. Complications were the same in both groups. Oral incision scars were invisible in the ETOVA group. Rates of skin traction sensation on the surgical field were lower in the ETOVA group than in the ETAA group at 3 and 6 months postoperatively (53.7% versus 80.5% and 24.4% versus 46.3%, respectively). The respective satisfaction score was 9.61 versus 9.22 (P = .021). No recurrent cases were observed in the study. Conclusions: Both the ETOVA and the ETAA procedures are feasible for thyroid diseases. The ETOVA eliminated skin incision scars and gained better cosmetic results in the short-term follow-ups, and the trauma was the same between the two approaches. However, more cases and longer-term follow-ups are needed for confirmation.
Introduction
S
ince the first case of endoscopic thyroidectomy was performed successfully in 1997 by Huscher et al.,1 surgeons and patients have favored this innovative technique because of the excellent cosmetic results. Currently, endoscopic thyroidectomy techniques include the cervical approach,2 the small anterior cervical incision approach,3 the subclavian approach,4 the axillary approach,5 the areola and cleavage approach,6 and the areola approach.7 With the development of this technology, the incision is smaller and less apparent. However, to those patients with higher cosmetic requirements, the skin incision still affects their appearance and is unacceptable. Natural orifice translumenal endoscopic surgery (NOTES; American Society for Gastrointestinal Endoscopy [Oak Brook, IL] and Society of American Gastrointestinal and Endo-
scopic Surgeons [Los Angeles, CA]) is gaining interest because it allows operations without skin incisions. Kalloo et al.8 first reported in 2004 an endoscopic examination and liver biopsy through the abdominal cavity, and increasing numbers of NOTES surgeries have been conducted in animals or humans.9–11 In 2008, Witzel et al.12 reported an endoscopic thyroidectomy via the sublingual transoral access approach, and in 2013, Nakajo et al.13 reported an endoscopic thyroidectomy by the buccal cavity. In 2011, our hospital began performing endoscopic thyroidectomy via the oral vestibular approach (ETOVA) with good treatment and cosmetic results.14 Based on preliminary studies, we conducted a further clinical study to compare the safety, degree of trauma, and cosmetic results of the ETOVA and the endoscopic thyroidectomy via the areola approach (ETAA) procedures.
Departments of 1General Surgery and 2Stomatology, First Affiliated Hospital of Jinan University, Guangzhou, China.
470
COMPARISON OF TWO THYROIDECTOMY APPROACHES
471
Materials and Methods Study design and preoperative management
This study was performed in the Department of General Surgery of the First Affiliated Hospital of Jinan University (Guangzhou, China) from July 2012 to July 2014. The hospital ethics committee approved the study design, and patients who fitted the inclusion criteria were enrolled. Inclusion criteria were as follows: 18–50 years old; maximum tumor diameter less than 5 cm; hyperthyroidism not exceeding degree II; suspicious cancer cases without metastasis in cervical lymph nodes; and endoscopic surgery required for the patient. Exclusion criteria were as follows: less than 18 or more than 50 years old; maximum tumor diameter greater than 5 cm; degree III hyperthyroidism; suspicious cancer cases with metastasis in cervical lymph nodes; infected lesions like oral ulcers; history of lower jaw, neck, or breast surgeries; and substernal goiter. Eighty-two patients who met the study criteria were informed of the risks and benefits of endoscopic thyroidectomy and issued consent forms during their preoperative consultation. The patients were randomly grouped, and the information was sealed in envelopes in their medical records. Thyroid function, parathyroid hormone, calcium, white blood cell (WBC) counts, and C-reaction protein (CRP) levels were tested preoperatively. Vocal cord activities were examined pre- and postoperatively. Size and location of nodules were detected by color Doppler ultrasonography and computed tomography scan. Biopsies were not routinely performed in patients with suspected malignancy, but other examinations were performed to exclude cervical lymph node metastases. Hyperthyroidism patients were administered antithyroid drug therapy and preoperative iodine preparation to ensure the heart rate was less than 90 beats/minute and that the thyroid function was normal. All patients received chlorhexidine mouthwash. The group designation envelope was opened in the operating room, and if the subject was in the ETOVA group, prophylactic antibiotics were given before anesthesia. Interventions ETOVA: working space. Patients received anesthesia through nasal intubation in a supine position with slightly padded shoulders and a fully reclined head. The cephalic surgeon stood beside the patient’s head, and the laparoscope holder and the assistant stood on either side of the surgeon. Just before surgery, full-mouth disinfection was performed twice with chlorhexidine. Then, adrenaline expansion saline solution (1 mg/500 mL) was injected subcutaneously from the middle of the lower lip mucosa to the midline of the mandible. A 10-mm midline incision was made in the mucosa of the vestibule. Blunt dissection of the lower jaw midline subcutaneously was made to perform a tunnel to the neck. During the separation, a suture was used to hang the submental skin for easy access to the cervical space and avoiding skin perforation. A 10-mm trocar was placed as an observation port. Two 5-mm incisions were made in front of the second lower canines, and two 5-mm trocars were placed under endoscopic surveillance as the operation ports (Fig. 1). CO2 infused through the observation port maintained a pressure of 6 mm Hg to preserve an appropriate operating space together with the anterior suture hanging of the cervical
FIG. 1. Placement of trocars in endoscopic thyroidectomy via the oral vestibular approach. skin. An ultrasonic scalpel was used to dissect the subcutaneous space from the sternum notch to the cricoid cartilage and both sides of the central sternocleidomastoid. The midline of the infrahyoid muscles was opened, and a suture was made to suspend infrahyoid muscles for revealing the thyroid. After these steps, the operative space was accomplished. Then, the isthmus was incised to locate the trachea, which is an important anatomical landmark in an endoscopic thyroidectomy (Fig. 2A). Thyroidectomy. The specific surgical procedure was conducted based on the patient’s condition. For a unilateral benign goiter, unilateral total resection was performed. For bilateral benign goiters, near-total resection on both sides or near-total resection on one side and total resection on the other side were performed. Bilateral subtotal resection was used for hyperthyroidism. Bilateral total resection was used for papillary thyroid carcinoma (PTC). First, gland and infrahyoid muscles adhesions were separated, and muscles were stretched as much as possible to expose the gland by suture suspending. Then, the upper thyroid artery was isolated and was cut by an ultrasonic scalpel closely to the gland after solidification (Fig. 2B). Ligation was required when the artery was coarse. Berry’s ligament was cut, and the gland was separated close to the intrinsic capsule to reveal the outer side and to resect the vein. Then, glands were retracted inwardly to reveal the back, and the gland and surrounding structures received blunt dissection. The upper parathyroid nerve and the recurrent laryngeal nerve (RLN) were carefully identified and further separated. A small amount of gland attached to the trachea was left for near-total or subtotal resection. Afterward, the gland was retracted inside to free the lower part of the lobe. The lower parathyroid was identified, and then the vasculature was cut at the site close to the gland after artery solidification. Lastly, the lobe was resected, and the contralateral lobe was resected in a similar manner. All the specimens were placed in a specimen bag to pull out through the observation port for intraoperative frozen pathology. Central lymph node dissection. If PTC was detected, bilateral glands were totally excised, and the central lymph
472
YANG ET AL.
into the thorax (Fig. 2C). Parathyroid glands and their blood vessels were retained in situ as much as possible during the surgery. When the resected tissues were suspected to be parathyroid glands, a small piece was collected and sent for frozen biopsy. The remaining tissues were cut into 1–2-mmdiameter slices and then transplanted into the sternocleidomastoid in once they were confirmed as parathyroid glands. The specimen was also placed in the specimen bag and pulled out through the observation port. The surgical field was then rinsed and checked for any active bleeding signs. The linea alba was interrupted sutured with with 3-0 polyglactin 910 (Vicryl; Ethicon, Somerville, NJ) suture, followed by excluding gas and 4-0 Vicryl interrupted sutures for the oral mucosa incisions. After that, the mouth was rinsed with chlorhexidine, and the jaw and chin were compressively bandaged. No drainage tube was placed in the surgical field. ETAA. Patients received anesthesia through oral intubation in a supine position with all limbs spread outward and slightly padded shoulders and a fully reclined head. The cephalic surgeon stood between the patient’s legs, and the laparoscope holder and assistant stood to the right and left sides of the patient. A 10-mm curved incision was made at two to four points of the right-hand edge of the areola, and 50 mL of ‘‘inflation liquid’’ was injected subcutaneously into the deep fascia below the suprasternal notch. Then, the upper sternum and neck subcutaneous space were blunt-dissected, and a 10-mm trocar was placed as an observation port. CO2 was injected to maintain a pressure of 6 mm Hg. On the edge of the left- and right-side areolas, 5-mm incisions were made for inserting the 5-mm trocars as operating ports. The subcutaneous space was separated by an ultrasonic scalpel, to the lower end of the sternum, the upper edge of the cricoid cartilage, and laterally to the midline of the sternocleidomastoid. Gland removal was in accordance with the order of upward and outward depending on the disease. For frozen biopsy of PTC, central lymph node dissection was conducted. The dissection range and method for protecting the RLN and parathyroid were the same as those described by Wang et al.7 The drainage tube was placed after surgery regularly.
FIG. 2. Endoscopic thyroidectomy via the oral vestibule approach. (A) Subcutaneous space. LA, linea alba; SF, suprasternal fossa; SM, sternocleidomastoid muscle. (B) Craniocaudal view. The superior thyroid artery (STA), trachea, and isthmus were separated from the right lobe. (C) Separating the recurrent laryngeal nerve (RLN) during right central lymph node dissection. node clearance was carried out on the same side. The infrahyoid muscles were stretched to the outside as much as possible by the suture. If necessary, the sternum thyroid muscle attachment points were cut in the thyroid cartilage, to fully expose the operative field. From the inside of the carotid sheath to the tracheoesophageal groove, and from the cricoid cartilage plane to the upper edge of thymus, lymph nodes and adipose tissue were excised by an ultrasonic scalpel. The lymph nodes and adipose tissue in the front of the throat, trachea, and paratracheal area were cleared simultaneously. The RLN was fully revealed by blunt dissection until it goes
Postoperative management and follow-up. An oral antibiotic was administered, and rinsing the mouth with chlorhexidine was recommended three times daily for 3 days postoperatively. The drainage tube in the ETAA group was usually removed at 24 hours postsurgery or when there was less than 50 mL of drainage. All patients in both groups had a liquid diet the day of surgery and began a normal diet the first day after surgery. Pain scores were recorded at Days 1 and 3 postoperatively. WBC and CRP levels were measured at Day 3 after surgery. The patients’ postoperative hospital stay was also documented. Levothyroxine was administered for patients with diagnosis of nodular goiter and was also used in hyperthyroidism patients according to the thyroid function after surgery. For patients with PTC, if there was lymph node metastasis according to the pathology, 131I treatment was given 1 month after surgery, followed by long-term use of levothyroxine. All patients were followed up for more than 1 year, and the data were collected at 3, 6, and 12 months postoperatvely. The thyroid function, parathyroid function, and calcium phosphorus levels were checked every time, and
COMPARISON OF TWO THYROIDECTOMY APPROACHES
color Doppler ultrasonography was used to identify recurrence. RLN paralysis was checked by the vocal cord test. Patients with hypoparathyroidism were given appropriate treatments. The wound scars and the skin traction sensation in the surgical area were also checked, and the patients’ cosmetic satisfaction was recorded. Statistics
Chi-squared and t tests were used to compare the difference between the ETOVA group and the ETAA group. Continuous variables were presented as mean (standard deviation) values, and ratios were expressed as a percentage. A two-tailed P value of < .05 indicated a statistically significant difference for all tests. All analyses were performed with SPSS version 17.0 software (SPSS Inc., Chicago, IL). Results
Eighty-two cases were randomized to receive the ETOVA (n = 41) or ETAA (n = 41) procedure. The two groups were comparable in age, sex, and diameter of the biggest tumor (Table 1). Tumor diameters were measured by the same doctor using the same color Doppler ultrasound equipment. Operations
Surgeries were successfully completed in all cases, and no cases were converted to the open procedure. The surgical outcomes are shown in Table 2. There were no differences of operation time (ETOVA versus ETAA, 72.1 versus 66.1 minutes), intraoperative estimated blood loss (11.1 versus 11.2 mL), or postoperative hospital stay (5.0 versus 4.6 days). The surgical procedure included lobectomy, near-total or subtotal resection, and total resection with central lymph node dissection. Pathological diagnoses of thyroid adenoma, nodular goiter, hyperthyroidism, and PTC were reported postoperatively. The cases of PTC were not different in the number of central lymph nodes (10.8 versus 10.4), and each group had 1 patient with central lymph node metastasis (2/10 and 1/9). The wounds healed without incision infection, seroma, or abscess in both groups. The ETOVA group had 5 cases of complications (14.3%), including 2 cases of lower jaw skin ecchymosis, 1 case of skin pierced under the chin, 1 case of anterior skin burn, and 1 case
Table 1. Baseline Characteristics of the Endoscopic Thyroidectomy via the Oral Vestibular Approach and the Endoscopic Thyroidectomy via the Areola Approach Groups
Age (years) Sex (F:M) Diameter of the biggest tumor (cm)
ETOVA (n = 41)
ETAA (n = 41)
Pa
31.9 – 8.8 33:8 3.5 – 0.67
31.0 – 8.9 30:11 3.4 – 0.86
.646 .432 .530
Data are mean – standard deviation values or number of patients, as indicated. a P < .05 is considered statistically significant. ETAA, endoscopic thyroidectomy via the areola approach; ETOVA, endoscopic thyroidectomy via the oral vestibular approach; F, female; M, male.
473
Table 2. Operative Results of the Endoscopic Thyroidectomy via the Oral Vestibular Approach and the Endoscopic Thyroidectomy via the Areola Approach Groups ETVOA (n = 41)
ETAA (n = 41)
Pa
Operation time (minutes) 72.1 – 19.5 66.1 – 23.2 .212 Estimated blood loss (mL) 11.1 – 7.1 11.2 – 7.3 .951 Postoperative 5.0 – 1.4 4.6 – 1.0 .130 hospital stay (days) Diseases Benign goiter 34 32 .577 Hyperthyroidism 3 4 1.000 Papillary carcinoma 4 5 1.000 Operation Lobectomy 19 23 .377 Subtotal or near-total 18 13 .255 resection Total resection + CLND 4 5 1.000 Number of central 10.8 – 2.2 10.4 – 2.3 .824 lymph nodes Complications (%) 14.3 9.8 .767 Data are mean – standard deviation values, number of patients or nodes, or percentages, as indicated. a P < .05 is considered statistically significant. CLND, central lymph node dissection; ETAA, endoscopic thyroidectomy via the areola approach; ETOVA, endoscopic thyroidectomy via the oral vestibular approach.
of transient RLN palsy. The ETAA group had 4 cases of complications (9.8%), including 1 case of transient RLN palsy, 1 case of temporary hypoparathyroidism, and 1 case of chest wall ecchymosis. Additionally, 1 case of PTC had symptoms of right-side miosis and eyelid ptosis after center lymph node dissection, which was diagnosed as Horner’s syndrome. After steroids and neurotrophic therapy for 7 days, the symptoms were relieved. Other complications self-healed in 7 days to 6 months. Trauma assessment
Pain scoring, WBC counts, and CRP levels were used to assess surgical trauma. The Day 1 pain score in the ETOVA group was significantly lower than that in the ETAA group (1.7 versus 2.1 [P = .016]). Moreover, the Day 3 pain scores were significantly lower than the Day 1 scores (2.24 versus 0.61 [P < .001] for ETOVA; 2.1 versus 0.8 [P < .001] for ETAA). WBC and CRP 3 days postoperatively were significantly increased compared with the preoperative level, but there was no significant difference between the two groups (Table 3). Follow-up and cosmetic satisfaction score. All patients had a follow-up duration of at least 1 year. The follow-up rate was 100%. Thyroid function test and color Doppler ultrasonography examination were administered to the patients. One PTC case in each group needed 131I therapy according to the guidelines of the American Thyroid Association.15–17 There were no recurrent cases in either group in 1 year of follow-up. The patients with transient RLN palsy and hypoparathyroidism recovered in 3–6 months. No persistent RLN palsy or hypoparathyroidism was observed in either group.
474
YANG ET AL.
Table 3. Postoperative Trauma Assessment and Skin Traction Sensation Rate
WBC ( · 109/L)b Preoperative 3 days CRP (mg/L)b Preoperative 3 days Pain score 1 day 3 days
ETOVA (n = 41)
ETAA (n = 41)
Pa
5.9 – 1.1 6.5 – 1.1
5.5 – 0.9 6.4 – 1.1
.071 .687
0.5 – 0.1 3.9 – 0.7
0.5 – 0.2 3.7 – 0.3
.856 .181
1.7 – 0.7 0.6 – 0.7
2.1 – 0.8 0.8 – 0.7
.016 .270
a
P < .05 is considered statistically significant. White blood cell (WBC) counts and C-reactive protein (CRP) levels before and after surgery in each group were not significantly different (P < .001). ETAA, endoscopic thyroidectomy via the areola approach; ETOVA, endoscopic thyroidectomy via the oral vestibular approach. b
Sensation of skin traction in the surgical field was observed at 3 months, 6 months, and 12 months postoperatively. The rate of skin traction sensation was significantly different between the ETOVA and ETAA groups at 3 months (53.7% versus 80.5% [P = .010]) and 6 months (24.4% versus 46.3% [P = .038]), but it was the same at 12 months (4.9% versus 7.3% [P = 1.000]). For the ETOVA group, the incision was completely healed 1 month after surgery, and no scars were seen in the mouth cavity (Fig. 3). Three small scars could be seen in the ETAA group around the areola, but the trend was not apparent. At 12 months after surgery, the cosmetic satisfaction score was higher in the ETOVA group than in the ETAA group (9.61 – 0.67 versus 9.22 – 0.82 [P = .021]). Discussion
Currently, there are some reports on transoral endoscopic thyroid/parathyroid surgery, including the sublingual transoral access,12 the transoral vestibular approach,14 and a combination of both or the small-incision transoral vestibular approach.13 Most studies focused on the study of animals or human cadavers rather than living patients, making the surgical techniques controversial.18–20 In our hospital, we began using the ETOVA in 2011 with good results. We conducted the present study to further compare the safety and feasibility of this approach with the ETAA procedure. Prior to this study, we performed the ETOVA in more than 40 cases as a learning curve. Because we previously found that ETOVA should not be used in patients with tumors in the upper lobe, those patients were excluded. In order to prevent surgical field infection by oral bacteria, patients used chlorhexidine to rinse their mouths before and during. This group received intravenous antibiotics 30 minutes before anesthesia induction, and oral antibiotics were used for 3 days postoperatively. In the present study, no patient had an infection. Compared with those in the ETAA group, the WBC count was not different, indicating the same sterile surgical effect. Using pigs and other animals, Karakas et al.18 conducted transoral endoscopic thyroidectomy and also found that postoperative wound microbiological testing was negative. Therefore, by taking appropriate measures in the perioperative period, surgical-site infection can be prevented.
FIG. 3. Intraoral wound in endoscopic thyroidectomy via the oral vestibular approach group patients: (A) 2 days after operation and (B) an invisible scar 1 month postoperatively. Wilhelm and Metzig21 reported that 3 cases of sublingual endoscopic thyroidectomy needed to be converted to the open procedure to remove specimens due to the narrow operation space. Nakajo et al.13 reported 8 cases of small-incision premandible endoscopic thyroidectomy where an incision of 2.5 cm was made in the oral vestibule to separate the large spaces to reach the thyroid area, resulting in much trauma. Because the jaw in Chinese people is relatively flat, our complete transoral vestibular approach with a 1-cm observation port and 0.5-cm operating ports was feasible and easy to access to the thyroid area through narrow tunnels with minimal invasion. In this approach, all of the operation space occurred through the subcutaneous tunnels in front of the mandible and subplatysma layer of the anterior cervical region, which is a layer of loose connective tissue with no important nerves, blood vessels, submandibular glands, or other structures, reducing the chance of vice injury. In the ETAA procedure, the path from the areola incision to the thyroid gland is long. The ETOVA procedure, however, has a significantly shorter path, suggesting a decrease of surgical trauma in the ETOVA. It is still controversial whether endoscopic thyroidectomy is a minimally invasive surgery.20,22 Wilhelm and Kru¨ger20 believed oral thyroid surgery is minimally invasive, but Henry22 thought that a
COMPARISON OF TWO THYROIDECTOMY APPROACHES
minimally invasive surgery does not depend on the length of incision. When the invasiveness of ETOVA and ETAA was compared in this study, the results showed that CRP and WBC were not significantly different. Although the separation range in the ETOVA group was smaller, the degree of trauma was not different between the two groups. Furthermore, patients in the ETAA group had more obvious pain on the first postoperative day, which is related to the bigger range of separation and drainage tube placement in these patients. According to the 1-year follow-up data, the skin traction sensation rate in the ETOVA group was significantly lower than that in the ETAA group 6 months after surgery. In a study using the oral vestibule endoscopic assistant method, Nakajo et al.13 reported that all patients had significant lower jaw numbness after 6 months due to the larger separation range. Overall, ETOVA had fewer traumas than ETAA, but whether ETOVA is a true minimally invasive surgery needs to be compared with more open surgeries.22 Emergency complications of thyroid surgery, including bleeding and glottis closure caused by bilateral RLN injury, did not occur in either group of patients in this study. During the operation, an ultrasonic scalpel was fully used. For glands and small blood vessels, the ultrasonic scalpel has a good obstruction effect. For hyperthyroidism and other conditions with blood vessels greater than 5 mm, the vessels were sutured with 3-0 Vicryl before cutting. If postoperative bleeding occurred without asphyxia by tracheal compression, hemostasis could be done under endoscope. Previous reports showed that for postoperative bleeding in the anterior jugular venous and residual gland, endoscopic hemostasis through the original path can work well.7 Subcutaneous tunnel bleeding manifested as subcutaneous ecchymosis is a unique complication in endoscopic thyroidectomy and is likely to occur in both the ETOVA and the ETAA procedures. In this study, 2 cases in the ETOVA group and 1 case in the ETAA group had subcutaneous ecchymosis. The ETOVA subcutaneous bleeding site is generally in the lower jaw. Careful observation was required at the end of the procedure. Some small veins that bleed during surgery can be closed by gas compression, but after the gas pressure is lifted they may re-open. A compressively bandaged jaw can be useful for preventing subcutaneous delayed bleeding. ETAA tunnel bleeding is often too deep in the mammary glands and can be treated with suture in the surgery. RLN paralysis occurs mostly due to heat damage by the ultrasonic scalpel in endoscopic surgery, so it is necessary to keep a safe distance between the scalpel and the RLN of more than 5 mm. The lower thyroid artery is usually cut close to the gland in order to reduce accidental nerve injury. During the central lymph node dissection, the whole RLN needs to be revealed to minimize the possibility of injury. Injury of superior laryngeal nerve is rare.23 In practice, our experience to protect the superior laryngeal nerve is to cut the superior artery close to the gland. Hypoparathyroidism may occur when it is mistakenly resected or the blood supply is affected. Close attention must be paid to protect the nutrient vessels when exposed the gland. Suspicious mistaken resection should be verified by intraoperative frozen biopsy, and residual glands should be cut into pieces and transplanted in the sternocleidomastoid. Other less common complications, such as skin puncture wounds and burns, occurred in the ETOVA group, which might
475
be due to the small operation space in this approach. This situation can be avoided by trocar penetration under direct supervision and lifting the submental skin. In addition, 1 patient in the ETAA group had Horner’s syndrome, which was alleviated after 7 days of symptomatic treatment. Previous reports showed that in thyroid surgery, traction of the cervical sympathetic chain rear to the carotid sheath could cause Horner’s syndrome, which commonly occurs in lymph node dissection cases.24 In endoscopic surgery, less pulling of the carotid artery decreases the chance of Horner’s syndrome. However, Horner’s syndrome can also be caused by heat damage from the ultrasonic scalpel during dissection of the lymph nodes surrounding the artery. From a therapeutic perspective, patients in the two groups had no significant differences in the operative time, blood loss, or postoperative hospital stay. During the 1-year followup, there were no recurrences, and the skin traction sensation at the surgical site disappeared. The absence of surface scars, as well as less postoperative pain and traction sensation, resulted in patients’ higher satisfaction in the ETOVA group. For patients with differentiated thyroid carcinoma, the suitability of the endoscopic thyroidectomy approach is still controversial. In this study, both the ETOVA and ETAA procedures were efficient at central lymph node dissection. In ETAA, some lymph nodes behind the sternum were difficult to remove, which required pulling the lymph nodes together with the fat tissues to reveal the thymus. Close attention should also be paid to avoid thoracic duct damage. If not, there may be postoperative lymphatic leakage. In ETOVA, the upside-down perspective makes it relatively easy to reveal the lymph nodes right behind the sternum. Endoscopic lymph node dissection for the lateral neck area was also reported.25 However, the effects of ETOVA are not yet known. Therefore, in cases of suspicious thyroid carcinoma and lateral neck lymph node metastasis, we do not recommend endoscopic surgery. The American Thyroid Association15–17– recommended 131I therapy and levothyroxine replacement therapy were conducted after surgery. During the follow-up, color Doppler ultrasonography and emission computed tomography found no residual lymph node or tumor recurrence. This confirms the good therapeutic results of ETOVA and ETAA in thyroid diseases, including thyroid carcinoma. Conclusions
Based on our study, the ETOVA and ETAA procedures are both feasible and safe approaches that result in good cosmetic effects. In a year-long follow-up study, patients in the ETOVA group had less postoperative pain and discomfort than those in the ETAA group. In addition, because of its excellent cosmetic results, the ETOVA procedure is a worthy approach. However, more cases and longer follow-up time are still needed to further study the traumatic and long-term effects. Acknowledgments
This work was supported by the Medical Science Fund Project of Guangdong Province, China (grant B2012192). Disclosure Statement
No competing financial interests exist.
476
YANG ET AL.
References
1. Huscher CS, Chiodini S, Napolitano C, Recher A. Endoscopic right thyroid lobectomy. Surg Endosc 1997;11:877. 2. Walz MK, Lederbogen S, Limmer JC, Peitgen K, Mann K. Video-assisted hemithyroidectomy: Surgical technique and early results. Chirurg 2001;72:1054–1057. 3. Miccoli P, Berti P, Raffaelli M, Conte M, Materazzi G, Galleri D. Minimally invasive video-assisted thyroidectomy. Am J Surg 2001;181:567–570. 4. Shimizu K, Akira S, Tanaka S. Video-assisted neck surgery: Endoscopic resection of benign thyroid tumor aiming at scarless surgery on the neck. J Surg Oncol 1998;69:178–180. 5. Ikeda Y, Takami H, Sasaki Y, Kan S, Niimi M. Endoscopic neck surgery by the axillary approach. J Am Coll Surg 2000;191:336–340. 6. Ohgami M, Ishii S, Arisawa Y, Ohmori T, Noga K, Furukawa T, Kitajima M. Scarless endoscopic thyroidectomy: Breast approach for better cosmesis. Surg Laparosc Endosc Percutan Tech 2000;10:1–4. 7. Wang C, Feng Z, Li J, Yang W, Zhai H, Choi N, Yang J, Hu Y, Pan Y, Cao G. Endoscopic thyroidectomy via areola approach: Summary of 1,250 cases in a single institution. Surg Endosc 2015;29:192–201. 8. Kalloo AN, Singh VK, Jagannath SB, Niiyama H, Hill SL, Vaughn CA, Magee CA, Kantsevoy SV. Flexible transgastric peritoneoscopy: A novel approach to diagnostic and therapeutic interventions. Gastrointest Endosc 2004;60: 114–117. 9. Zorron R, Phillips HN, Wynn G, Neto MP, Coelho D, Vassallo RC. ‘‘Down-to-up’’ transanal NOTES total mesorectal excision for rectal cancer: Preliminary series of 9 patients. J Minim Access Surg 2014;10:144–150. 10. Wang Z, Zhang XM, Zhou HT, Liang JW, Zhou ZX. New technique of intracorporeal anastomosis and transvaginal specimen extraction for laparoscopic sigmoid colectomy. Asian Pac J Cancer Prev 2014;15:6733–6736. 11. Federlein M, Mu¨ller VA, Fritze-Bu¨ttner F, Burghardt J, Gra¨ber S, Gellert K, Borchert DH. Transvaginal cholecystectomy: Results of a randomized study. Chirurg 2014;85: 825–832. 12. Witzel K, von Rahden BH, Kaminski C, Stein HJ. Transoral access for endoscopic thyroid resection. Surg Endosc 2008;22:1871–1875. 13. Nakajo A, Arima H, Hirata M, Mizoguchi T, Kijima Y, Mori S, Ishigami S, Ueno S, Yoshinaka H, Natsugoe S. Trans-oral video-assisted neck surgery (TOVANS). A new transoral technique of endoscopic thyroidectomy with gasless premandible approach. Surg Endosc 2013;27:1105–1110. 14. Wang C, Zhai H, Liu W, Li J, Yang J, Hu Y, Huang J, Yang W, Pan Y, Ding H. Thyroidectomy: A novel endoscopic oral vestibular approach. Surgery 2014;155:33–38. 15. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM. Revised
16.
17.
18.
19. 20.
21. 22. 23.
24. 25.
American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19:1167–1214. Erratum in Thyroid 2010;20:942 and Thyroid 2010;20:674–675. Smith BR, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Sherman SI, Tuttle RM; American Thyroid Association Guidelines Taskforce. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2006;16:109–142. Singer PA, Cooper DS, Daniels GH, Ladenson PW, Greenspan FS, Levy EG, Braverman LE, Clark OH, McDougall IR, Ain KV, Dorfman SG. Treatment guidelines for patients with thyroid nodules and well-differentiated thyroid cancer. American Thyroid Association. Arch Intern Med 1996;156:2165–2172. Karakas E, Steinfeldt T, Gockel A, Schlosshauer T, Dietz C, Ja¨ger J, Westermann R, Sommer F, Richard HR, Exner C, Sesterhenn AM, Bartsch DK. Transoral thyroid and parathyroid surgery—Development of a new transoral technique. Surgery 2011;150:108–115. Karakas E, Steinfeldt T, Gockel A, Mangalo A, Sesterhenn A, Bartsch DK. Transoral parathyroid surgery—A new alternative or nonsense? Langenbecks Arch Surg 2014;399:741–745. Wilhelm T, Kru¨ger J. Ultrasound studies on the shift of cervical tissues in different head and neck positions—Impact on transoral endoscopic, minimally invasive and conventional thyroid surgery. Ultrasound Med Biol 2011;37:1430–1435. Wilhelm T, Metzig A. Endoscopic minimally invasive thyroidectomy (eMIT): A prospective proof-of-concept study in humans. World J Surg 2011;35:543–551. Henry JF. Minimally invasive thyroid and parathyroid surgery is not a question of length of the incision. Langenbecks Arch Surg 2008;393:621–626. Barczyn´ski M, Konturek A, Hubalewska-Dydejczyk A, Go1kowski F, Nowak W. Randomized clinical trial of bilateral subtotal thyroidectomy versus total thyroidectomy for Graves’ disease with a 5-year follow-up. Br J Surg 2012;99:515–522. Ying X, Dandan G, Bin C. Postoperative Horner’s syndrome after video-assisted thyroidectomy: A report of two cases. World J Surg Oncol 2013; 11:315. Li Z, Wang P, Wang Y, Xu S, Cao L, Que R, Zhou F. Endoscopic lateral neck dissection via breast approach for papillary thyroid carcinoma: A preliminary report. Surg Endosc 2011;25:890–896.
Address correspondence to: Cunchuan Wang, MD, PhD Jinan University No. 613, West Huangpu Avenue Tianhe District, Guangzhou 510630 China E-mail: [email protected]
Copyright of Journal of Laparoendoscopic & Advanced Surgical Techniques is the property of Mary Ann Liebert, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
Complete Endoscopic Thyroidectomy via Oral Vestibular Approach Versus Areola Approach for Treatment of Thyroid Diseases Jingge Yang, MD,1 Cunchuan Wang, MD, PhD,1 Jinyi Li, MD,1 Wah Yang, MD,1 Guo Cao, MD,1 Hong-meng Wong, MD,1 Hening Zhai, MD,1 and Weijun Liu, MD 2
Abstract
Background: Natural orifice translumenal endoscopic surgery (NOTES; American Society for Gastrointestinal Endoscopy [Oak Brook, IL] and Society of American Gastrointestinal and Endoscopic Surgeons [Los Angeles, CA]) is gaining interest because it allows operations without skin incisions. The aim of this study was to evaluate the feasibility, safety, and cosmetic results of endoscopic thyroidectomy via the oral vestibular approach (ETOVA) compared with endoscopic thyroidectomy via the areola approach (ETAA) in patients with thyroid diseases. Materials and Methods: Eighty-two patients with thyroid diseases were randomized to receive either ETOVA (n = 41) or ETAA (n = 41). Perioperative and follow-up data were assessed. Results: The surgery was completed in all cases, and all patients were followed up for at least 1 year. There were no differences between the two groups in operation time, blood loss, or postoperative hospital stay. Respective pain scores were 1.7 versus 2.1 and 0.6 versus 0.8 on Days 1 and 3, respectively, postoperatively. The white blood cell counts and C-reactive protein levels were not significantly different between the two groups. Complications were the same in both groups. Oral incision scars were invisible in the ETOVA group. Rates of skin traction sensation on the surgical field were lower in the ETOVA group than in the ETAA group at 3 and 6 months postoperatively (53.7% versus 80.5% and 24.4% versus 46.3%, respectively). The respective satisfaction score was 9.61 versus 9.22 (P = .021). No recurrent cases were observed in the study. Conclusions: Both the ETOVA and the ETAA procedures are feasible for thyroid diseases. The ETOVA eliminated skin incision scars and gained better cosmetic results in the short-term follow-ups, and the trauma was the same between the two approaches. However, more cases and longer-term follow-ups are needed for confirmation.
Introduction
S
ince the first case of endoscopic thyroidectomy was performed successfully in 1997 by Huscher et al.,1 surgeons and patients have favored this innovative technique because of the excellent cosmetic results. Currently, endoscopic thyroidectomy techniques include the cervical approach,2 the small anterior cervical incision approach,3 the subclavian approach,4 the axillary approach,5 the areola and cleavage approach,6 and the areola approach.7 With the development of this technology, the incision is smaller and less apparent. However, to those patients with higher cosmetic requirements, the skin incision still affects their appearance and is unacceptable. Natural orifice translumenal endoscopic surgery (NOTES; American Society for Gastrointestinal Endoscopy [Oak Brook, IL] and Society of American Gastrointestinal and Endo-
scopic Surgeons [Los Angeles, CA]) is gaining interest because it allows operations without skin incisions. Kalloo et al.8 first reported in 2004 an endoscopic examination and liver biopsy through the abdominal cavity, and increasing numbers of NOTES surgeries have been conducted in animals or humans.9–11 In 2008, Witzel et al.12 reported an endoscopic thyroidectomy via the sublingual transoral access approach, and in 2013, Nakajo et al.13 reported an endoscopic thyroidectomy by the buccal cavity. In 2011, our hospital began performing endoscopic thyroidectomy via the oral vestibular approach (ETOVA) with good treatment and cosmetic results.14 Based on preliminary studies, we conducted a further clinical study to compare the safety, degree of trauma, and cosmetic results of the ETOVA and the endoscopic thyroidectomy via the areola approach (ETAA) procedures.
Departments of 1General Surgery and 2Stomatology, First Affiliated Hospital of Jinan University, Guangzhou, China.
470
COMPARISON OF TWO THYROIDECTOMY APPROACHES
471
Materials and Methods Study design and preoperative management
This study was performed in the Department of General Surgery of the First Affiliated Hospital of Jinan University (Guangzhou, China) from July 2012 to July 2014. The hospital ethics committee approved the study design, and patients who fitted the inclusion criteria were enrolled. Inclusion criteria were as follows: 18–50 years old; maximum tumor diameter less than 5 cm; hyperthyroidism not exceeding degree II; suspicious cancer cases without metastasis in cervical lymph nodes; and endoscopic surgery required for the patient. Exclusion criteria were as follows: less than 18 or more than 50 years old; maximum tumor diameter greater than 5 cm; degree III hyperthyroidism; suspicious cancer cases with metastasis in cervical lymph nodes; infected lesions like oral ulcers; history of lower jaw, neck, or breast surgeries; and substernal goiter. Eighty-two patients who met the study criteria were informed of the risks and benefits of endoscopic thyroidectomy and issued consent forms during their preoperative consultation. The patients were randomly grouped, and the information was sealed in envelopes in their medical records. Thyroid function, parathyroid hormone, calcium, white blood cell (WBC) counts, and C-reaction protein (CRP) levels were tested preoperatively. Vocal cord activities were examined pre- and postoperatively. Size and location of nodules were detected by color Doppler ultrasonography and computed tomography scan. Biopsies were not routinely performed in patients with suspected malignancy, but other examinations were performed to exclude cervical lymph node metastases. Hyperthyroidism patients were administered antithyroid drug therapy and preoperative iodine preparation to ensure the heart rate was less than 90 beats/minute and that the thyroid function was normal. All patients received chlorhexidine mouthwash. The group designation envelope was opened in the operating room, and if the subject was in the ETOVA group, prophylactic antibiotics were given before anesthesia. Interventions ETOVA: working space. Patients received anesthesia through nasal intubation in a supine position with slightly padded shoulders and a fully reclined head. The cephalic surgeon stood beside the patient’s head, and the laparoscope holder and the assistant stood on either side of the surgeon. Just before surgery, full-mouth disinfection was performed twice with chlorhexidine. Then, adrenaline expansion saline solution (1 mg/500 mL) was injected subcutaneously from the middle of the lower lip mucosa to the midline of the mandible. A 10-mm midline incision was made in the mucosa of the vestibule. Blunt dissection of the lower jaw midline subcutaneously was made to perform a tunnel to the neck. During the separation, a suture was used to hang the submental skin for easy access to the cervical space and avoiding skin perforation. A 10-mm trocar was placed as an observation port. Two 5-mm incisions were made in front of the second lower canines, and two 5-mm trocars were placed under endoscopic surveillance as the operation ports (Fig. 1). CO2 infused through the observation port maintained a pressure of 6 mm Hg to preserve an appropriate operating space together with the anterior suture hanging of the cervical
FIG. 1. Placement of trocars in endoscopic thyroidectomy via the oral vestibular approach. skin. An ultrasonic scalpel was used to dissect the subcutaneous space from the sternum notch to the cricoid cartilage and both sides of the central sternocleidomastoid. The midline of the infrahyoid muscles was opened, and a suture was made to suspend infrahyoid muscles for revealing the thyroid. After these steps, the operative space was accomplished. Then, the isthmus was incised to locate the trachea, which is an important anatomical landmark in an endoscopic thyroidectomy (Fig. 2A). Thyroidectomy. The specific surgical procedure was conducted based on the patient’s condition. For a unilateral benign goiter, unilateral total resection was performed. For bilateral benign goiters, near-total resection on both sides or near-total resection on one side and total resection on the other side were performed. Bilateral subtotal resection was used for hyperthyroidism. Bilateral total resection was used for papillary thyroid carcinoma (PTC). First, gland and infrahyoid muscles adhesions were separated, and muscles were stretched as much as possible to expose the gland by suture suspending. Then, the upper thyroid artery was isolated and was cut by an ultrasonic scalpel closely to the gland after solidification (Fig. 2B). Ligation was required when the artery was coarse. Berry’s ligament was cut, and the gland was separated close to the intrinsic capsule to reveal the outer side and to resect the vein. Then, glands were retracted inwardly to reveal the back, and the gland and surrounding structures received blunt dissection. The upper parathyroid nerve and the recurrent laryngeal nerve (RLN) were carefully identified and further separated. A small amount of gland attached to the trachea was left for near-total or subtotal resection. Afterward, the gland was retracted inside to free the lower part of the lobe. The lower parathyroid was identified, and then the vasculature was cut at the site close to the gland after artery solidification. Lastly, the lobe was resected, and the contralateral lobe was resected in a similar manner. All the specimens were placed in a specimen bag to pull out through the observation port for intraoperative frozen pathology. Central lymph node dissection. If PTC was detected, bilateral glands were totally excised, and the central lymph
472
YANG ET AL.
into the thorax (Fig. 2C). Parathyroid glands and their blood vessels were retained in situ as much as possible during the surgery. When the resected tissues were suspected to be parathyroid glands, a small piece was collected and sent for frozen biopsy. The remaining tissues were cut into 1–2-mmdiameter slices and then transplanted into the sternocleidomastoid in once they were confirmed as parathyroid glands. The specimen was also placed in the specimen bag and pulled out through the observation port. The surgical field was then rinsed and checked for any active bleeding signs. The linea alba was interrupted sutured with with 3-0 polyglactin 910 (Vicryl; Ethicon, Somerville, NJ) suture, followed by excluding gas and 4-0 Vicryl interrupted sutures for the oral mucosa incisions. After that, the mouth was rinsed with chlorhexidine, and the jaw and chin were compressively bandaged. No drainage tube was placed in the surgical field. ETAA. Patients received anesthesia through oral intubation in a supine position with all limbs spread outward and slightly padded shoulders and a fully reclined head. The cephalic surgeon stood between the patient’s legs, and the laparoscope holder and assistant stood to the right and left sides of the patient. A 10-mm curved incision was made at two to four points of the right-hand edge of the areola, and 50 mL of ‘‘inflation liquid’’ was injected subcutaneously into the deep fascia below the suprasternal notch. Then, the upper sternum and neck subcutaneous space were blunt-dissected, and a 10-mm trocar was placed as an observation port. CO2 was injected to maintain a pressure of 6 mm Hg. On the edge of the left- and right-side areolas, 5-mm incisions were made for inserting the 5-mm trocars as operating ports. The subcutaneous space was separated by an ultrasonic scalpel, to the lower end of the sternum, the upper edge of the cricoid cartilage, and laterally to the midline of the sternocleidomastoid. Gland removal was in accordance with the order of upward and outward depending on the disease. For frozen biopsy of PTC, central lymph node dissection was conducted. The dissection range and method for protecting the RLN and parathyroid were the same as those described by Wang et al.7 The drainage tube was placed after surgery regularly.
FIG. 2. Endoscopic thyroidectomy via the oral vestibule approach. (A) Subcutaneous space. LA, linea alba; SF, suprasternal fossa; SM, sternocleidomastoid muscle. (B) Craniocaudal view. The superior thyroid artery (STA), trachea, and isthmus were separated from the right lobe. (C) Separating the recurrent laryngeal nerve (RLN) during right central lymph node dissection. node clearance was carried out on the same side. The infrahyoid muscles were stretched to the outside as much as possible by the suture. If necessary, the sternum thyroid muscle attachment points were cut in the thyroid cartilage, to fully expose the operative field. From the inside of the carotid sheath to the tracheoesophageal groove, and from the cricoid cartilage plane to the upper edge of thymus, lymph nodes and adipose tissue were excised by an ultrasonic scalpel. The lymph nodes and adipose tissue in the front of the throat, trachea, and paratracheal area were cleared simultaneously. The RLN was fully revealed by blunt dissection until it goes
Postoperative management and follow-up. An oral antibiotic was administered, and rinsing the mouth with chlorhexidine was recommended three times daily for 3 days postoperatively. The drainage tube in the ETAA group was usually removed at 24 hours postsurgery or when there was less than 50 mL of drainage. All patients in both groups had a liquid diet the day of surgery and began a normal diet the first day after surgery. Pain scores were recorded at Days 1 and 3 postoperatively. WBC and CRP levels were measured at Day 3 after surgery. The patients’ postoperative hospital stay was also documented. Levothyroxine was administered for patients with diagnosis of nodular goiter and was also used in hyperthyroidism patients according to the thyroid function after surgery. For patients with PTC, if there was lymph node metastasis according to the pathology, 131I treatment was given 1 month after surgery, followed by long-term use of levothyroxine. All patients were followed up for more than 1 year, and the data were collected at 3, 6, and 12 months postoperatvely. The thyroid function, parathyroid function, and calcium phosphorus levels were checked every time, and
COMPARISON OF TWO THYROIDECTOMY APPROACHES
color Doppler ultrasonography was used to identify recurrence. RLN paralysis was checked by the vocal cord test. Patients with hypoparathyroidism were given appropriate treatments. The wound scars and the skin traction sensation in the surgical area were also checked, and the patients’ cosmetic satisfaction was recorded. Statistics
Chi-squared and t tests were used to compare the difference between the ETOVA group and the ETAA group. Continuous variables were presented as mean (standard deviation) values, and ratios were expressed as a percentage. A two-tailed P value of < .05 indicated a statistically significant difference for all tests. All analyses were performed with SPSS version 17.0 software (SPSS Inc., Chicago, IL). Results
Eighty-two cases were randomized to receive the ETOVA (n = 41) or ETAA (n = 41) procedure. The two groups were comparable in age, sex, and diameter of the biggest tumor (Table 1). Tumor diameters were measured by the same doctor using the same color Doppler ultrasound equipment. Operations
Surgeries were successfully completed in all cases, and no cases were converted to the open procedure. The surgical outcomes are shown in Table 2. There were no differences of operation time (ETOVA versus ETAA, 72.1 versus 66.1 minutes), intraoperative estimated blood loss (11.1 versus 11.2 mL), or postoperative hospital stay (5.0 versus 4.6 days). The surgical procedure included lobectomy, near-total or subtotal resection, and total resection with central lymph node dissection. Pathological diagnoses of thyroid adenoma, nodular goiter, hyperthyroidism, and PTC were reported postoperatively. The cases of PTC were not different in the number of central lymph nodes (10.8 versus 10.4), and each group had 1 patient with central lymph node metastasis (2/10 and 1/9). The wounds healed without incision infection, seroma, or abscess in both groups. The ETOVA group had 5 cases of complications (14.3%), including 2 cases of lower jaw skin ecchymosis, 1 case of skin pierced under the chin, 1 case of anterior skin burn, and 1 case
Table 1. Baseline Characteristics of the Endoscopic Thyroidectomy via the Oral Vestibular Approach and the Endoscopic Thyroidectomy via the Areola Approach Groups
Age (years) Sex (F:M) Diameter of the biggest tumor (cm)
ETOVA (n = 41)
ETAA (n = 41)
Pa
31.9 – 8.8 33:8 3.5 – 0.67
31.0 – 8.9 30:11 3.4 – 0.86
.646 .432 .530
Data are mean – standard deviation values or number of patients, as indicated. a P < .05 is considered statistically significant. ETAA, endoscopic thyroidectomy via the areola approach; ETOVA, endoscopic thyroidectomy via the oral vestibular approach; F, female; M, male.
473
Table 2. Operative Results of the Endoscopic Thyroidectomy via the Oral Vestibular Approach and the Endoscopic Thyroidectomy via the Areola Approach Groups ETVOA (n = 41)
ETAA (n = 41)
Pa
Operation time (minutes) 72.1 – 19.5 66.1 – 23.2 .212 Estimated blood loss (mL) 11.1 – 7.1 11.2 – 7.3 .951 Postoperative 5.0 – 1.4 4.6 – 1.0 .130 hospital stay (days) Diseases Benign goiter 34 32 .577 Hyperthyroidism 3 4 1.000 Papillary carcinoma 4 5 1.000 Operation Lobectomy 19 23 .377 Subtotal or near-total 18 13 .255 resection Total resection + CLND 4 5 1.000 Number of central 10.8 – 2.2 10.4 – 2.3 .824 lymph nodes Complications (%) 14.3 9.8 .767 Data are mean – standard deviation values, number of patients or nodes, or percentages, as indicated. a P < .05 is considered statistically significant. CLND, central lymph node dissection; ETAA, endoscopic thyroidectomy via the areola approach; ETOVA, endoscopic thyroidectomy via the oral vestibular approach.
of transient RLN palsy. The ETAA group had 4 cases of complications (9.8%), including 1 case of transient RLN palsy, 1 case of temporary hypoparathyroidism, and 1 case of chest wall ecchymosis. Additionally, 1 case of PTC had symptoms of right-side miosis and eyelid ptosis after center lymph node dissection, which was diagnosed as Horner’s syndrome. After steroids and neurotrophic therapy for 7 days, the symptoms were relieved. Other complications self-healed in 7 days to 6 months. Trauma assessment
Pain scoring, WBC counts, and CRP levels were used to assess surgical trauma. The Day 1 pain score in the ETOVA group was significantly lower than that in the ETAA group (1.7 versus 2.1 [P = .016]). Moreover, the Day 3 pain scores were significantly lower than the Day 1 scores (2.24 versus 0.61 [P < .001] for ETOVA; 2.1 versus 0.8 [P < .001] for ETAA). WBC and CRP 3 days postoperatively were significantly increased compared with the preoperative level, but there was no significant difference between the two groups (Table 3). Follow-up and cosmetic satisfaction score. All patients had a follow-up duration of at least 1 year. The follow-up rate was 100%. Thyroid function test and color Doppler ultrasonography examination were administered to the patients. One PTC case in each group needed 131I therapy according to the guidelines of the American Thyroid Association.15–17 There were no recurrent cases in either group in 1 year of follow-up. The patients with transient RLN palsy and hypoparathyroidism recovered in 3–6 months. No persistent RLN palsy or hypoparathyroidism was observed in either group.
474
YANG ET AL.
Table 3. Postoperative Trauma Assessment and Skin Traction Sensation Rate
WBC ( · 109/L)b Preoperative 3 days CRP (mg/L)b Preoperative 3 days Pain score 1 day 3 days
ETOVA (n = 41)
ETAA (n = 41)
Pa
5.9 – 1.1 6.5 – 1.1
5.5 – 0.9 6.4 – 1.1
.071 .687
0.5 – 0.1 3.9 – 0.7
0.5 – 0.2 3.7 – 0.3
.856 .181
1.7 – 0.7 0.6 – 0.7
2.1 – 0.8 0.8 – 0.7
.016 .270
a
P < .05 is considered statistically significant. White blood cell (WBC) counts and C-reactive protein (CRP) levels before and after surgery in each group were not significantly different (P < .001). ETAA, endoscopic thyroidectomy via the areola approach; ETOVA, endoscopic thyroidectomy via the oral vestibular approach. b
Sensation of skin traction in the surgical field was observed at 3 months, 6 months, and 12 months postoperatively. The rate of skin traction sensation was significantly different between the ETOVA and ETAA groups at 3 months (53.7% versus 80.5% [P = .010]) and 6 months (24.4% versus 46.3% [P = .038]), but it was the same at 12 months (4.9% versus 7.3% [P = 1.000]). For the ETOVA group, the incision was completely healed 1 month after surgery, and no scars were seen in the mouth cavity (Fig. 3). Three small scars could be seen in the ETAA group around the areola, but the trend was not apparent. At 12 months after surgery, the cosmetic satisfaction score was higher in the ETOVA group than in the ETAA group (9.61 – 0.67 versus 9.22 – 0.82 [P = .021]). Discussion
Currently, there are some reports on transoral endoscopic thyroid/parathyroid surgery, including the sublingual transoral access,12 the transoral vestibular approach,14 and a combination of both or the small-incision transoral vestibular approach.13 Most studies focused on the study of animals or human cadavers rather than living patients, making the surgical techniques controversial.18–20 In our hospital, we began using the ETOVA in 2011 with good results. We conducted the present study to further compare the safety and feasibility of this approach with the ETAA procedure. Prior to this study, we performed the ETOVA in more than 40 cases as a learning curve. Because we previously found that ETOVA should not be used in patients with tumors in the upper lobe, those patients were excluded. In order to prevent surgical field infection by oral bacteria, patients used chlorhexidine to rinse their mouths before and during. This group received intravenous antibiotics 30 minutes before anesthesia induction, and oral antibiotics were used for 3 days postoperatively. In the present study, no patient had an infection. Compared with those in the ETAA group, the WBC count was not different, indicating the same sterile surgical effect. Using pigs and other animals, Karakas et al.18 conducted transoral endoscopic thyroidectomy and also found that postoperative wound microbiological testing was negative. Therefore, by taking appropriate measures in the perioperative period, surgical-site infection can be prevented.
FIG. 3. Intraoral wound in endoscopic thyroidectomy via the oral vestibular approach group patients: (A) 2 days after operation and (B) an invisible scar 1 month postoperatively. Wilhelm and Metzig21 reported that 3 cases of sublingual endoscopic thyroidectomy needed to be converted to the open procedure to remove specimens due to the narrow operation space. Nakajo et al.13 reported 8 cases of small-incision premandible endoscopic thyroidectomy where an incision of 2.5 cm was made in the oral vestibule to separate the large spaces to reach the thyroid area, resulting in much trauma. Because the jaw in Chinese people is relatively flat, our complete transoral vestibular approach with a 1-cm observation port and 0.5-cm operating ports was feasible and easy to access to the thyroid area through narrow tunnels with minimal invasion. In this approach, all of the operation space occurred through the subcutaneous tunnels in front of the mandible and subplatysma layer of the anterior cervical region, which is a layer of loose connective tissue with no important nerves, blood vessels, submandibular glands, or other structures, reducing the chance of vice injury. In the ETAA procedure, the path from the areola incision to the thyroid gland is long. The ETOVA procedure, however, has a significantly shorter path, suggesting a decrease of surgical trauma in the ETOVA. It is still controversial whether endoscopic thyroidectomy is a minimally invasive surgery.20,22 Wilhelm and Kru¨ger20 believed oral thyroid surgery is minimally invasive, but Henry22 thought that a
COMPARISON OF TWO THYROIDECTOMY APPROACHES
minimally invasive surgery does not depend on the length of incision. When the invasiveness of ETOVA and ETAA was compared in this study, the results showed that CRP and WBC were not significantly different. Although the separation range in the ETOVA group was smaller, the degree of trauma was not different between the two groups. Furthermore, patients in the ETAA group had more obvious pain on the first postoperative day, which is related to the bigger range of separation and drainage tube placement in these patients. According to the 1-year follow-up data, the skin traction sensation rate in the ETOVA group was significantly lower than that in the ETAA group 6 months after surgery. In a study using the oral vestibule endoscopic assistant method, Nakajo et al.13 reported that all patients had significant lower jaw numbness after 6 months due to the larger separation range. Overall, ETOVA had fewer traumas than ETAA, but whether ETOVA is a true minimally invasive surgery needs to be compared with more open surgeries.22 Emergency complications of thyroid surgery, including bleeding and glottis closure caused by bilateral RLN injury, did not occur in either group of patients in this study. During the operation, an ultrasonic scalpel was fully used. For glands and small blood vessels, the ultrasonic scalpel has a good obstruction effect. For hyperthyroidism and other conditions with blood vessels greater than 5 mm, the vessels were sutured with 3-0 Vicryl before cutting. If postoperative bleeding occurred without asphyxia by tracheal compression, hemostasis could be done under endoscope. Previous reports showed that for postoperative bleeding in the anterior jugular venous and residual gland, endoscopic hemostasis through the original path can work well.7 Subcutaneous tunnel bleeding manifested as subcutaneous ecchymosis is a unique complication in endoscopic thyroidectomy and is likely to occur in both the ETOVA and the ETAA procedures. In this study, 2 cases in the ETOVA group and 1 case in the ETAA group had subcutaneous ecchymosis. The ETOVA subcutaneous bleeding site is generally in the lower jaw. Careful observation was required at the end of the procedure. Some small veins that bleed during surgery can be closed by gas compression, but after the gas pressure is lifted they may re-open. A compressively bandaged jaw can be useful for preventing subcutaneous delayed bleeding. ETAA tunnel bleeding is often too deep in the mammary glands and can be treated with suture in the surgery. RLN paralysis occurs mostly due to heat damage by the ultrasonic scalpel in endoscopic surgery, so it is necessary to keep a safe distance between the scalpel and the RLN of more than 5 mm. The lower thyroid artery is usually cut close to the gland in order to reduce accidental nerve injury. During the central lymph node dissection, the whole RLN needs to be revealed to minimize the possibility of injury. Injury of superior laryngeal nerve is rare.23 In practice, our experience to protect the superior laryngeal nerve is to cut the superior artery close to the gland. Hypoparathyroidism may occur when it is mistakenly resected or the blood supply is affected. Close attention must be paid to protect the nutrient vessels when exposed the gland. Suspicious mistaken resection should be verified by intraoperative frozen biopsy, and residual glands should be cut into pieces and transplanted in the sternocleidomastoid. Other less common complications, such as skin puncture wounds and burns, occurred in the ETOVA group, which might
475
be due to the small operation space in this approach. This situation can be avoided by trocar penetration under direct supervision and lifting the submental skin. In addition, 1 patient in the ETAA group had Horner’s syndrome, which was alleviated after 7 days of symptomatic treatment. Previous reports showed that in thyroid surgery, traction of the cervical sympathetic chain rear to the carotid sheath could cause Horner’s syndrome, which commonly occurs in lymph node dissection cases.24 In endoscopic surgery, less pulling of the carotid artery decreases the chance of Horner’s syndrome. However, Horner’s syndrome can also be caused by heat damage from the ultrasonic scalpel during dissection of the lymph nodes surrounding the artery. From a therapeutic perspective, patients in the two groups had no significant differences in the operative time, blood loss, or postoperative hospital stay. During the 1-year followup, there were no recurrences, and the skin traction sensation at the surgical site disappeared. The absence of surface scars, as well as less postoperative pain and traction sensation, resulted in patients’ higher satisfaction in the ETOVA group. For patients with differentiated thyroid carcinoma, the suitability of the endoscopic thyroidectomy approach is still controversial. In this study, both the ETOVA and ETAA procedures were efficient at central lymph node dissection. In ETAA, some lymph nodes behind the sternum were difficult to remove, which required pulling the lymph nodes together with the fat tissues to reveal the thymus. Close attention should also be paid to avoid thoracic duct damage. If not, there may be postoperative lymphatic leakage. In ETOVA, the upside-down perspective makes it relatively easy to reveal the lymph nodes right behind the sternum. Endoscopic lymph node dissection for the lateral neck area was also reported.25 However, the effects of ETOVA are not yet known. Therefore, in cases of suspicious thyroid carcinoma and lateral neck lymph node metastasis, we do not recommend endoscopic surgery. The American Thyroid Association15–17– recommended 131I therapy and levothyroxine replacement therapy were conducted after surgery. During the follow-up, color Doppler ultrasonography and emission computed tomography found no residual lymph node or tumor recurrence. This confirms the good therapeutic results of ETOVA and ETAA in thyroid diseases, including thyroid carcinoma. Conclusions
Based on our study, the ETOVA and ETAA procedures are both feasible and safe approaches that result in good cosmetic effects. In a year-long follow-up study, patients in the ETOVA group had less postoperative pain and discomfort than those in the ETAA group. In addition, because of its excellent cosmetic results, the ETOVA procedure is a worthy approach. However, more cases and longer follow-up time are still needed to further study the traumatic and long-term effects. Acknowledgments
This work was supported by the Medical Science Fund Project of Guangdong Province, China (grant B2012192). Disclosure Statement
No competing financial interests exist.
476
YANG ET AL.
References
1. Huscher CS, Chiodini S, Napolitano C, Recher A. Endoscopic right thyroid lobectomy. Surg Endosc 1997;11:877. 2. Walz MK, Lederbogen S, Limmer JC, Peitgen K, Mann K. Video-assisted hemithyroidectomy: Surgical technique and early results. Chirurg 2001;72:1054–1057. 3. Miccoli P, Berti P, Raffaelli M, Conte M, Materazzi G, Galleri D. Minimally invasive video-assisted thyroidectomy. Am J Surg 2001;181:567–570. 4. Shimizu K, Akira S, Tanaka S. Video-assisted neck surgery: Endoscopic resection of benign thyroid tumor aiming at scarless surgery on the neck. J Surg Oncol 1998;69:178–180. 5. Ikeda Y, Takami H, Sasaki Y, Kan S, Niimi M. Endoscopic neck surgery by the axillary approach. J Am Coll Surg 2000;191:336–340. 6. Ohgami M, Ishii S, Arisawa Y, Ohmori T, Noga K, Furukawa T, Kitajima M. Scarless endoscopic thyroidectomy: Breast approach for better cosmesis. Surg Laparosc Endosc Percutan Tech 2000;10:1–4. 7. Wang C, Feng Z, Li J, Yang W, Zhai H, Choi N, Yang J, Hu Y, Pan Y, Cao G. Endoscopic thyroidectomy via areola approach: Summary of 1,250 cases in a single institution. Surg Endosc 2015;29:192–201. 8. Kalloo AN, Singh VK, Jagannath SB, Niiyama H, Hill SL, Vaughn CA, Magee CA, Kantsevoy SV. Flexible transgastric peritoneoscopy: A novel approach to diagnostic and therapeutic interventions. Gastrointest Endosc 2004;60: 114–117. 9. Zorron R, Phillips HN, Wynn G, Neto MP, Coelho D, Vassallo RC. ‘‘Down-to-up’’ transanal NOTES total mesorectal excision for rectal cancer: Preliminary series of 9 patients. J Minim Access Surg 2014;10:144–150. 10. Wang Z, Zhang XM, Zhou HT, Liang JW, Zhou ZX. New technique of intracorporeal anastomosis and transvaginal specimen extraction for laparoscopic sigmoid colectomy. Asian Pac J Cancer Prev 2014;15:6733–6736. 11. Federlein M, Mu¨ller VA, Fritze-Bu¨ttner F, Burghardt J, Gra¨ber S, Gellert K, Borchert DH. Transvaginal cholecystectomy: Results of a randomized study. Chirurg 2014;85: 825–832. 12. Witzel K, von Rahden BH, Kaminski C, Stein HJ. Transoral access for endoscopic thyroid resection. Surg Endosc 2008;22:1871–1875. 13. Nakajo A, Arima H, Hirata M, Mizoguchi T, Kijima Y, Mori S, Ishigami S, Ueno S, Yoshinaka H, Natsugoe S. Trans-oral video-assisted neck surgery (TOVANS). A new transoral technique of endoscopic thyroidectomy with gasless premandible approach. Surg Endosc 2013;27:1105–1110. 14. Wang C, Zhai H, Liu W, Li J, Yang J, Hu Y, Huang J, Yang W, Pan Y, Ding H. Thyroidectomy: A novel endoscopic oral vestibular approach. Surgery 2014;155:33–38. 15. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM. Revised
16.
17.
18.
19. 20.
21. 22. 23.
24. 25.
American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19:1167–1214. Erratum in Thyroid 2010;20:942 and Thyroid 2010;20:674–675. Smith BR, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Sherman SI, Tuttle RM; American Thyroid Association Guidelines Taskforce. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2006;16:109–142. Singer PA, Cooper DS, Daniels GH, Ladenson PW, Greenspan FS, Levy EG, Braverman LE, Clark OH, McDougall IR, Ain KV, Dorfman SG. Treatment guidelines for patients with thyroid nodules and well-differentiated thyroid cancer. American Thyroid Association. Arch Intern Med 1996;156:2165–2172. Karakas E, Steinfeldt T, Gockel A, Schlosshauer T, Dietz C, Ja¨ger J, Westermann R, Sommer F, Richard HR, Exner C, Sesterhenn AM, Bartsch DK. Transoral thyroid and parathyroid surgery—Development of a new transoral technique. Surgery 2011;150:108–115. Karakas E, Steinfeldt T, Gockel A, Mangalo A, Sesterhenn A, Bartsch DK. Transoral parathyroid surgery—A new alternative or nonsense? Langenbecks Arch Surg 2014;399:741–745. Wilhelm T, Kru¨ger J. Ultrasound studies on the shift of cervical tissues in different head and neck positions—Impact on transoral endoscopic, minimally invasive and conventional thyroid surgery. Ultrasound Med Biol 2011;37:1430–1435. Wilhelm T, Metzig A. Endoscopic minimally invasive thyroidectomy (eMIT): A prospective proof-of-concept study in humans. World J Surg 2011;35:543–551. Henry JF. Minimally invasive thyroid and parathyroid surgery is not a question of length of the incision. Langenbecks Arch Surg 2008;393:621–626. Barczyn´ski M, Konturek A, Hubalewska-Dydejczyk A, Go1kowski F, Nowak W. Randomized clinical trial of bilateral subtotal thyroidectomy versus total thyroidectomy for Graves’ disease with a 5-year follow-up. Br J Surg 2012;99:515–522. Ying X, Dandan G, Bin C. Postoperative Horner’s syndrome after video-assisted thyroidectomy: A report of two cases. World J Surg Oncol 2013; 11:315. Li Z, Wang P, Wang Y, Xu S, Cao L, Que R, Zhou F. Endoscopic lateral neck dissection via breast approach for papillary thyroid carcinoma: A preliminary report. Surg Endosc 2011;25:890–896.
Address correspondence to: Cunchuan Wang, MD, PhD Jinan University No. 613, West Huangpu Avenue Tianhe District, Guangzhou 510630 China E-mail: [email protected]
Copyright of Journal of Laparoendoscopic & Advanced Surgical Techniques is the property of Mary Ann Liebert, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
