Abstract
Background:
Since its introduction nine years ago, gasless transaxillary thyroidectomy with robotic assistance (RT) has achieved a relatively limited application in North America. This study aimed to assess the outcomes of RT in a recent large, diverse North American population.
Methods:
Consenting patients were selected for the RT approach from November 2010 to July 2015 based on patient preference, and their perioperative data were retrospectively reviewed.
Results:
Of 301 robotic thyroidectomies completed in 281 patients, 160 were total thyroidectomy and 141 were lobectomy. Women predominated (98.9%), with a mean age of 41 years (range 17–74 years) and a mean follow-up of 24 months (range 3–71 months). The mean body mass index (BMI) was 25.7 kg/m2 (range 17–44 kg/m2). However, 33.3% of patients had a BMI 25–29.9 kg/m2, 12.4% had a BMI 30–34.9 kg/m2, 3.5% had a BMI 35–39.9 kg/m2, and 0.7% had a BMI ≥40 kg/m2. Excluding 20 completion lobectomy, the indications for surgery were indeterminate cytology (53%), malignant cytology (10%), growth (18%), Graves' disease (12%), and other (5%). The mean size of the largest resected nodule was 2.5 cm (range 0.7–6.4 cm). Mean operating time for robotic lobectomy and total thyroidectomy was 81 and 109 minutes, respectively. One patient was converted to standard cervicotomy for failure to progress endoscopically. Complications included temporary dysphonia (6.0%), permanent recurrent laryngeal nerve deficit (1.3%), hypocalcemia (temporary 8.2%, permanent 1.1%), seroma (0.7%), and hematoma requiring reoperation (0.3%). Complications did not differ in patients with a BMI ≥25 kg/m2 compared to those with a BMI <25 kg/m2 or with respect to nodules >3 cm or surgery for Graves' thyroiditis. One patient developed grade II arm lymphedema ipsilateral to the axillary incision at two years, which resolved with conservative management. No patient had a surgical site infection or brachial plexopathy. Cancer was present histologically in 133 (48%) patients. Among 91 patients with cancer of the index nodule, 48.4% had papillary, 44.0% follicular variant papillary, 2.2% minimally invasive follicular carcinoma, and 5.5% minimally invasive Hürthle cell carcinoma. One patient had sclerosing variant thyroid paraganglioma. To date, all patients are without evidence of tumor recurrence.
Conclusions:
At a high-volume center, gasless transaxillary endoscopic thyroid surgery done with robotic assistance is a safe, efficient, and effective approach in a diverse North American patient population.
Introduction
S
The American Thyroid Association (ATA) Statement on Remote-Access Thyroid Surgery acknowledged several barriers to implementation, including a limited published experience for the several remote access techniques, many of which utilize a robotic platform (17). In the studies detailing experience with the transaxillary approach, the average patient body mass index (BMI) was higher and the average nodule size was larger than that of the robotic Korean experience (5,7,17). To date, the utility of the transaxillary approach in a diverse North American patient population has been unclear, and there is a need for additional clinical data to define the role of this alternative access approach to thyroid surgery better.
This study aimed to assess the outcomes of RT in a recent large and diverse North American population.
Methods
RT implementation
After institutional quality assurance/quality improvement approval (QI0001198), the perioperative course of all patients who had robotic thyroidectomy (RT) from November 2010 to July 2015 was retrospectively reviewed. Patient demographics, indication for surgery, preoperative radiology findings, operative reports, pathology, postoperative imaging, laboratory data, and clinical long term follow-up documentation were examined. Operative time was defined as the time from initial skin incision to the point of final closure. Temporary recurrent laryngeal nerve (RLN) deficit was documented by an independent laryngologist, and permanent RLN deficit was defined as persistent deficit six months or more from surgery. Temporary hypoparathyroidism was defined by symptomatic hypocalcemia requiring calcitriol and calcium supplements in the immediate postoperative period, and permanent hypoparathyroidism was defined by low or undetectable parathyroid hormone level requiring calcitriol and calcium supplements six months or more from surgery.
Utilizing a framework for safe implementation at an academic center (18,19), one surgeon from the authors' group (M.T.S.) was selected to adapt new technology by observing intraoperatively in November 2009 the methodology of RT by Dr. W.Y. Chung et al. at Yonsei University Health System, Seoul, South Korea. The RT surgeon then underwent human cadaveric training at Hackensack University Medical Center (Hackensack, NJ) and Memorial Hermann Texas Medical Center (Houston, TX) prior to clinical application. The initial three surgical cases were precepted by a senior surgical oncologist with extensive robotic surgery experience (D.L.B.), as well as a senior endocrine surgeon with experience in minimally invasive video assisted thyroidectomy (S.E.C.).
Patient selection for RT
At presentation to an academic endocrine surgery program, where surgical management of thyroid nodules and/or differentiated thyroid cancer was conducted using the 2009 ATA guidelines (20), counseling was routinely provided about the conduct, risks, and alternatives of RT and conventional cervicotomy. Patients were selected for RT consideration based on their expressed preference for that approach. Additional inclusion criteria were medical health appropriate for general anesthesia and an evident understanding of the detailed consenting discussion. At the start, favorable habitus for transaxillary access, including a BMI of <30, no limitations in the range of motion of the neck or ipsilateral shoulder, and a normal gland size (20–25 mg estimated), were also required. With experience, the restrictions for body habitus and thyroid nodule or gland size were slowly liberalized to include patients with a higher BMI, mild degree of limitation in neck extension, and larger glands or nodules without typically exceeding >3 cm in an anterior to posterior (AP) dimension that would limit the AP working space.
Patients were excluded from consideration for RT for preoperatively diagnosed vocal cord paralysis; prior carotid, cervical disc, or parathyroid surgery; known cervical disc disease; severely limited neck or arm mobility; ultrasound evidence of extrathyroidal extension (ETE); or lateral neck lymphadenopathy. Two patients with remote history of thyroid lobectomy (L) surgery via cervicotomy elected to have RT for completion thyroidectomy. In both cases, the previous scar was imperceptible, and it was the patients' ardent preference to avoid a second neck incision.
Surgical methodology
The approach to RT was similar to that described by Kang et al. (21). The patient was placed supine on a mildly sloping pillow, allowing for gentle neck extension. The arm ipsilateral to the side of axillary approach was placed into a Krause arm board, maintaining internal rotation of the arm and wrist, and extended superiorly, with meticulous attention to avoid extension beyond 30° from full superior abduction and to minimize any traction on the inferior brachial plexus. The initial 12 cases included the use of a second paramedian incision on the anterior chest wall along the medial aspect of the ipsilateral breast crease for the 8 mm Prograsp. With the 13th operative case, all further surgeries were performed with all four ports placed in the single axillary incision as described (22). A postoperative drain was left for the initial six operative cases and was removed on the first postoperative morning. With the seventh case, all further surgeries did not involve placement of an operative drain, except for one case of operative takeback for hematoma formation.
L procedures were approached from the side ipsilateral to the lobe of the thyroid being resected. Total thyroidectomy (TT) procedures were approached from the right axilla irrespective of the side of the thyroid lesion. In the initial experience, TT was approached with the right thyroid lobe and isthmus being resected first, followed by the left thyroid lobe. The robot was undocked, and the patient's bed was then rotated to the right side approximately 10–20° to improve visualization of the contralateral left tracheoesophageal groove and RLN. After 108 robotic TT cases and in current practice, TT was universally approached from the right axilla. However, the RT procedure was adapted to resect first the side with the lesion, followed by completion of the thyroidectomy only after confirmation of normal RLN stimulation (i.e., left thyroid lobe resected first for a left-sided lesion from a right axillary approach, followed by removal of the right thyroid lobe). The routine use of intraoperative nerve monitoring was introduced after 34 cases. Prophylactic central compartment lymph node dissection (CCLND) was done for cases with suspicious for cancer (Bethesda V) or positive for malignancy (Bethesda VI) thyroid cytology (23).
Statistics
A chi-square test was used to examine associations between categorical variables, and an unpaired two-tailed Student's t-test was used to identify the correlation between continuous variables.
Results
Demographics
Between November 2010 and July 2015, 302 RTs were performed in 282 patients. One case of attempted RT was converted to standard cervicotomy (without complication) for failure to progress endoscopically. Thus, 281 unique patients underwent successful RT.
Of the 282 study patients, the majority were female (279/282; 98.9%), with a mean age of 41 years (range 17–74 years). The mean clinical follow-up was 24 months (range 3–71 months). The mean BMI was 25.7 kg/m2 (range 17–44 kg/m2), with 141/282 (50.0%) patients having a BMI <25 kg/m2. Among patients with a BMI ≥25 kg/m2, 94/282 (33.3%) had a BMI 25–29.9 kg/m2, 35/282 (12.4%) had a BMI 30–34.9 kg/m2, 10/282 (3.5%) had a BMI 35–39.9 kg/m2, and 2/282 (0.7%) had a BMI ≥40 kg/m2 (Table 1).
Clinical Characteristics
BMI, body mass index.
Among the 281 patients who had successful RT, there were 301 robotic thyroid surgeries comprised of TT in 160/301 (53.2%) and L in 141/301 (46.8%). Of the 141 L, 20 cases represented completion thyroidectomy following initial robotic L for cancer on the contralateral side, and two patients represented completion thyroidectomy after remote conventional thyroidectomy via cervicotomy. The mean operative time for robotic L was 81 minutes (range 33–172 minutes), and for TT it was 109 minutes (range 56–240 minutes). Operative times decreased progressively with surgeon experience (Supplementary Fig. S1; Supplementary Data are available online at
Excluding the 20 cases of completion thyroidectomy for cancer, the indications for initial RT were indeterminate cytology (Bethesda III, IV, and V) for 150/281 (53.4%), malignant cytology (Bethesda VI) for 28/281 (10.0%), nodule growth for 51/281 (18.1%), Graves' disease for 35/281(12.5%), non-diagnostic cytology (Bethesda I) for 2/281 (0.7%), toxic adenoma for 10/281 (3.6%), recurrent thyroid cyst for 3/281 (1.1%), and toxic multinodular goiter for 2/281 (0.7%). Among cases done for thyroid nodular disease, the mean size of the largest nodule by preoperative ultrasound was 2.5 cm (range 0.7–6.4 cm). More than one third of RT cases (36.7%) involved a nodule that was ≥3 cm. Assessed as a surrogate marker for the gland volume, the mean resected gland weight was 14.3 g for thyroid lobes and 22.7 g for total thyroid specimens. Examining Graves' disease glands separately, the mean gland weight was slightly larger at 27.7 mg compared to all other TT specimens with mean gland weight of 21.3 mg (Table 1).
Cancer outcomes
Cancer was histologically present in 133/281 (47.3%) RT patients. Of these, the pathologic cancer represented the index nodule identified by cytology in only 91/281 (32.4%), with the remaining 42 cases being an incidental microcarcinoma. Most incidental microcarcinomas were papillary thyroid cancer (PTC). However, one patient had incidental finding of a 4 mm medullary microcarcinoma. Among 91 patients with cancer found in the index nodule, histology subtype is summarized in Table 2. Of the 84 cases of PTC identified in the index nodule, 16 (19.0%) had minimal ETE, which was not evident intraoperatively or on preoperative ultrasound. Tumor multifocality was identified in 52/133 (39.0%) of cancer cases, including those with incidental microPTC.
Pathologic Characteristics
Tall-cell variant = 5; cribiform morular variant = 2, infiltrative Warthin variant = 1.
Well demarcated or encapsulated = 39; infiltrative pattern = 1.
Excluding incidental microPTC.
One patient was pathologic TX but presumed PTC due to finding of N1a PTC.
PTC, papillary thyroid carcinoma; FVPTC, follicular variant PTC; FCC, follicular cell carcinoma; HCC, Hürthle cell carcinoma; CCLND, central compartment lymph node dissection.
Intentional central compartment (Level VI) lymph node dissection was performed in 40 cases and yielded an average of 6.7 lymph nodes on final pathology (range 0–17), with 31/40 (77.5%) having four or more lymph nodes on final pathology. For patients who went on to receive adjuvant radioactive iodine (RAI) treatment (n = 44), the mean RAI uptake was 1.5% (range 0.00–6.9%). One RT patient had a 2.4 cm sclerosing variant thyroid paraganglioma on final pathology. During the time frame of this study, the diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) was not yet in use (24). However, since then, four follicular variant PTC cases have been found to be consistent with a NIFTP diagnosis. To date, all study patients are without biochemical or ultrasound evidence of tumor recurrence.
Complications
Surgical complications in the 281 patients with successful RT included temporary dysphonia in 18/301 (6.0%), permanent RLN deficit in 4/301 (1.3%), seroma in 2/301 (0.7%), and hematoma requiring reoperation in 1/301 (0.3%; Table 3). Symptomatic postoperative hypocalcemia was seen temporarily in 15/182 (8.2%) TT robotic surgeries or completion thyroidectomy, and was found to represent permanent hypoparathyroidism in 2/182 (1.1%).
Complications
RLN, recurrent laryngeal nerve.
Complications of RLN deficit (temporary and permanent) or hypoparathyroidism (temporary and permanent) did not differ for patients with a BMI ≥25 kg/m2, a BMI ≥30 kg/m2, or a BMI ≥35 kg/m2 versus a BMI <25 kg/m2 (Table 4). Similarly, the complication rates did not differ for L versus TT for other clinical variables, including Graves' disease, thyroiditis, nodule ≥3 cm, macrocarcinomas, or concurrent CCLND (Table 4).
Surgery Complications and Clinical Variables
Inclusive of initial lobectomy and completion thyroidectomy.
Inclusive of incidental T1a microcarcinoma.
Inclusive of initial total thyroidectomy surgeries.
One patient with a BMI of 27.1 kg/m2 developed grade II arm lymphedema ipsilateral to the axillary incision at two years, which resolved with physical therapy and conservative management. No patient had a surgical site infection. Although chyle leak, brachial plexopathy, carotid artery injury, Horner's syndrome, and axillary skin flap perforation have been reported with RT, they did not occur in this series (4 –7).
Discussion
The RT approach has been prolifically pursued at some clinical centers and today represents a robust clinical experience of >3000 patients (4). The reported RT surgical experience, however, is mostly outside the United States. From 2009 to 2011, there was an initial growth in the number of robotic thyroid surgeries being performed in the United States, with a preponderance of RT cases being done at a few high-volume centers (25,26). However, with the withdrawal of material support by industry for the RT approach in 2011, the number of RT cases declined, and the majority of encounters shifted to low-volume centers doing <10 yearly (26). The initial North American experiences were subject to considerable criticism of the relatively high rate of complications, prompting some experts to abandon the procedure (27). This highlights the importance of understanding the clinical role of new technology as it is safely implemented. The authors' institution has extensive experience with robotic-assisted complex surgery with extensive existing equipment and a monitoring peer-review committee to oversee such implementation (28). Despite the technologic hurdles, the reported advantages of RT include perception of more desirable cosmetic outcome and increased patient satisfaction for those who choose it (19,29). Thus, use of RT was adopted in informed, consenting patients, and herein the series and experience are presented.
In using RT, low complication rates were observed for permanent RLN deficit and permanent hypoparathyroidism. These rates are congruent with published reports of non-robotic thyroidectomy-specific complications (30,31). Furthermore, no specific clinical variable was associated with a higher incidence of complications. These findings are in contrast to the suggestions of the ATA position statement on RT, which proposed as relative contraindications the presence of “excessive body fat” along the flap trajectory, nodules >3 cm, or underlying thyroid pathology with thyroiditis (17). In the authors' hands, RT was safe and reasonable, even if these conditions were present. For example, for patients with a BMI >25 kg/m2, with proper positioning, the soft tissue over the clavipectoral fascia is easily elevated, especially with the benefit of static retraction using the retractor described by Cho et al. (32). In the authors' opinion, patients with a higher BMI may actually have more laxity in the soft tissue over the flap trajectory and provide for a larger working space during RT.
Another selection criteria that was suggested by the ATA group is to limit the RT approach to nodules that are <3 cm in size (17). In the current study, however, more than one third of thyroid nodules were >3 cm, and such size was not associated with higher complication risk. In the authors' experience, the limiting factor in resecting larger nodules tends to be the AP working space. Many nodules are oblong in nature, and the largest ultrasonographic measurement tends to represent the longitudinal axis. In general, the authors do not offer robotic thyroid surgery to patients with nodules >3 cm in the AP dimension.
Today, there is still a paucity of data about robotic thyroid surgery in the context of Graves' disease (33,34). The present study included 35 cases of RT for Graves' disease, and there was no difference in the rates of RLN injury or permanent hypoparathyroidism compared to RT without Graves' disease. Comparison would ideally be made to the outcomes of propensity matched patients with Graves' disease done via conventional cervicotomy. However, the current study was not designed to address this. Here, the mean gland weight was 28 g, which was significantly less than in the study by Park et al. (77 g). Thus, there may be a selection effect in the current study.
Cost is a significant criticism of RT (35,36). Despite the use of numerous expensive robot-associated operative consumables and the amortized cost of the robot itself, one of the main drivers of cost is operative time (36). However, in the authors' hands, RT was relatively efficient, with a mean operative time of 81 minutes for L and 109 minutes for TT. The observed operative times are certainly above the threshold of 68 minutes established by Cabot et al. for cost equivalence. Yet, they compare favorably to even that of standard cervicotomy used in the cost analysis (69 minutes L, 106 minutes TT) (36).
To summarize, in the authors' experience, the following steps are important to adopt RT safely in a diverse North American population: adequate training and proctoring in robotic-assisted surgery, high-volume expertise and proven excellent outcomes as a conventional thyroid surgeon (37,38), appropriate institutional support and oversight, a consistent dedicated operative team, and a motivated and informed patient. During the initial adoption of this surgical approach, careful selection of patients per the ATA position statement is recommended (17). However, it is reasonable to expand the criteria carefully as experience accrues.
In addition to the limitations discussed above, this was a retrospective data review and thus has intrinsic potential for missed or biased information. Also, although this report represents the largest single surgeon series of RT performed in North America, it is likely underpowered to exclude a possible link of clinical variables to operative complications completely. In addition, inherent to the safe implementation of any new technology, patients were carefully selected for approachable and likely indolent disease. Thus, their long-term oncologic outcomes compared to conventional thyroidectomy will need continued evaluation.
Conclusion
RT can be a safe and effective surgical approach within the context of a diverse North American patient population with low-risk thyroid cancer. This study adds to the limited data on RT experience outside of Korea, details technical considerations and outcomes, and informs RT selection criteria relating to patient BMI, nodule size, and presence of thyroiditis.
Footnotes
Acknowledgments
We thank Michaele Armstrong, PhD, for help in the quality assurance/quality improvement regulatory process and Naomi Chen, MD, for her contributions in some of the original data acquisition.
Author Disclosure Statement
The authors attest that they do not have any commercial association that might create a conflict of interest in connection with this submitted manuscript.
