Robot-Assisted Endocrine Surgery: Indications and Drawbacks

Abstract

Background:

Over the last few decades, robotic surgery with the da Vinci system has become increasingly prevalent. Endocrine surgeons are witnessing a rapid growth in enthusiasm for robotic approaches for treating thyroid, parathyroid, and adrenal disease. For carefully selected patients, the robotic system may be the preferred technique, although its use remains controversial and indications are in evolution. The goal of this article is to review current robotic procedures for thyroidectomy, parathyroidectomy, and adrenalectomy, and scrutinize the existing literature for application of these approaches.

Methods:

We systematically searched and reviewed relevant articles on PubMed and MEDLINE databases for robotic or robot-assisted thyroidectomy, parathyroidectomy, or adrenalectomy.

Results:

The safety and feasibility for robotic thyroidectomy, parathyroidectomy, and adrenalectomy have been repeatedly demonstrated. Although robotic thyroid and parathyroid surgery offers better cosmetic results compared to the conventional open operation, remote-access techniques introduce new risks. Similar outcomes have been reported for laparoscopic and robotic adrenalectomy, but robot-assisted techniques may extend the capabilities of minimally invasive surgery, particularly performing subtotal adrenalectomy.

Conclusions:

While robotic procedures offer better ergonomics for the endocrine surgeon and improved cosmesis for the patient, the major drawback to the robot system almost universally is the higher cost. With new robotically assisted surgical devices on the way that could drive down costs and speed up innovation, the indications for robotic endocrine surgery may greatly expand.

Introduction

Robot-assisted surgery has been applied to many specialties over the last two decades, and endocrine surgery is no exception. Certain advantages of the robot, including its three-dimensional (3D) imaging, dexterity, and stable platform, have garnered enthusiasm among some surgeons. For thyroid and parathyroid disease, open surgery remains the recommended surgical approach for most patients.

However, remote-access approaches to thyroidectomy and parathyroidectomy are improving the cosmetic outcomes for patients with little if any impact on morbidity and mortality, and growing experience with these techniques is allowing surgeons to expand their indications. On the other hand, for most adrenal operations, minimally invasive surgery is standard. While the safety and feasibility of robot-assisted adrenalectomy is known, the benefits over traditional laparoscopy are less clear and difficult to define. Still, in carefully selected patients the robotic system may be the preferred technique. The goal of this article is to review current robotic procedures for thyroidectomy, parathyroidectomy, and adrenalectomy, and scrutinize the existing literature for application of these approaches.

Robot-Assisted Thyroidectomy

Thyroidectomy is a common surgical procedure associated with a low morbidity in experienced hands. The transverse cervical incision pioneered by Kocher remains the standard access for surgical exposure of the thyroid gland. With the incorporation of coagulating and cutting devices, surgeons were able to reduce the size of the skin incision for thyroidectomy. However, with patients and surgeons motivated to avoid a visible neck scar entirely, remote-access approaches, including endoscopic and robotic techniques, were developed. Remote-access thyroid surgery is mostly driven by the patients' desire to avoid cervical scars. Thus, these approaches are best suited for highly motivated patients, particularly those with increased tendency to form keloid or hyperplastic scars.¹ The high-definition, 3D view and wristed instrumentation provided by the robot system have allowed access to the thyroid gland through incisions made at distant sites, and new techniques are continuing to be developed.

The main drawbacks, however, are increased postoperative pain due to more extensive tissue dissection, longer operative times, and increased cost.² Furthermore, based on the site of incision, each remote-access technique introduces new risks not typically associated with open thyroidectomy. These include, but are not limited to, stretch injury to the brachial plexus, esophageal perforation, and injury to the carotid artery and/or internal jugular vein.³ These risks, along with those associated with the learning curve for a new technology, have led to societal recommendations that remote-access thyroidectomy be performed only by experienced surgeons at high-volume centers.⁴ Given the growing number of publications on this controversial subject, with this review we aim to describe the various advantages and drawbacks for different approaches for robot-assisted thyroid surgery.

Robotic bilateral axillo-breast approach for thyroidectomy

The bilateral axillo-breast approach (BABA) for thyroidectomy is one of the most popular remote-access thyroidectomy techniques, particularly in Southeast Asia.⁵ BABA was introduced in 2007 by Choe et al. and is now widely used for thyroid surgery (using both endoscopic and robotic methods), as it offers outstanding cosmetic results.⁶ BABA robotic thyroidectomy combines the da Vinci robot surgical system with the BABA surgical method, requiring four small incisions at the circumareolar and skin creases of the axilla.⁷ Coupling the BABA procedure with the da Vinci robot system enables the surgeon to complete thyroid resection with optimal visualization of critical structures, namely, the parathyroid glands, the recurrently laryngeal nerves, and the superior or inferior thyroidal vessels. This is facilitated by the 3D magnified view and the highly movable multiarticulated hands of the robot system.

BABA's multidirectional approach allows the surgeon to look down onto the thyroid from the midline providing the view similar to that typically seen in open surgery. Thus, it may provide a symmetric view of the area that is obscured by the trachea. Multiple studies have reported that this approach associates with good oncological completeness, functional safety, and low complication rates.^8–11 Therefore, the BABA robotic thyroidectomy appears to be an oncologic safe procedure and offers cosmetic advantages in patients with papillary thyroid carcinoma. To date, however, BABA robotic thyroidectomy has seldom been performed in patients with lymph node metastasis. Additional studies with long follow-up periods are needed to determine the long-term outcomes of BABA robotic thyroidectomy, specifically, the disease recurrence and patient survival rates.

Robotic transaxillary thyroidectomy

The robotic gasless transaxillary thyroidectomy has emerged as another popular remote-access approach, although not without setbacks and controversy. In East Asia, this technique has been shown to be safe and feasible, with patients actually experiencing less pain and excellent cosmetic outcomes.¹² Yet, the initial experience in the United States was different. This technique was felt to be more challenging in America, where patients are more likely to be overweight or obese,¹³ leading to a diminished interest after the initial enthusiasm for this approach. The surgeons in the United States came to recognize the importance of careful patient selection for remote-access robotic thyroidectomy techniques. Unlike cervical thyroidectomy, there is risk of injury to the brachial nerve plexus with robotic transaxillary surgery. In earlier series, despite use of intraoperative nerve monitoring with surveillance of radial, ulnar, and median nerves, there were cases of temporary brachial plexus injury following transaxillary surgery.¹⁴ However, Zaidi et al. recently published their experiences and noted that there were no cases of temporary or permanent radial, ulnar, or median nerve injuries.¹⁵

While some surgeons have used this technique to perform thyroid lobectomy, the limited visualization of the contralateral recurrent laryngeal nerve and parathyroid glands from a single transaxillary incision has led others to question the safety of this approach for patients requiring total thyroidectomy.¹³ On the other hand, centers in Korea, where there is much more experience with this technique, have used the robotic transaxillary approach to perform modified radical neck dissection safely for patients with differentiated thyroid cancer and clinical lymph node metastasis, without injury to major vessels or nerves and without compromising surgical oncologic principles.¹⁶ As it currently stands, one of the main drawbacks of this technique is that the removal of the contralateral lobe requires significant expertise and can be technically challenging.⁴ Some authors, therefore, recommended a bilateral axillary approach for total thyroidectomy to circumvent the limitations of unilateral transaxillary approach.¹³

Robotic facelift thyroidectomy

The robotic facelift thyroidectomy combines the principles of gasless surgery with the facelift-type incision. This technique affords excellent cosmetic outcomes, with the option for neck-lift surgery.¹⁷ The surgeon makes an incision along the postauricular crease, which is well masked along the hairline and, thus avoids a cervical incision.¹⁸ Removal of the ipsilateral thyroid lobe has been shown to be both safe and feasible, but access to the contralateral lobe is restricted. Because of this, robotic facelift surgery is limited to patients undergoing thyroid lobectomy, although a staged bilateral operation can be performed.¹⁹ In addition to long operative times, some patients experience high levels of postoperative pain and long recovery periods owing to the more extensive dissection.²⁰ There is also risk of injury to the greater auricular nerve, which is exposed early in the operation.¹⁹ Thus, robotic facelift thyroidectomy is currently performed only by highly skilled and experienced surgeons and offered to a very select and highly motivated patients.

Robotic transoral thyroidectomy

The robotic transoral approach, in contrast to other remote-access techniques described earlier in this chapter, completely avoids cutaneous scarring by using a mucosal incision in the oral vestibule. While this technique has required refinement over the last decade, in its most recent version appears to be both safe and feasible.²¹ Because of the short distance between the oral vestibule and the central neck, this technique requires less tissue dissection compared with other remote-access techniques. Importantly, the midline location of this incision makes this technique amendable to central neck dissection and allows for both partial and total thyroidectomy.

Even though transoral thyroid surgery is becoming more accepted, not all patients with thyroid disease meet the criteria for this procedure. By and far the most indispensable criterion for transoral thyroidectomy is that the patient is keen to pursue an optimal cosmetic result.²² Other inclusion criteria originally considered in selecting patients eligible for a transoral operation included the following: (1) thyroid gland less than 10 cm in diameter; (2) benign tumor, such as single or multinodular goiter; (3) follicular neoplasm; (4) Graves' disease; (5) papillary carcinoma without any evidence of metastasis.^23,24 Some distinct exclusion criteria include (1) patient unfit for surgery; (2) previous surgery or radiation in the area of the neck; (3) evidence of invasion or metastasis; and (4) infected lesions. However, there is considerable variation in the literature in which inclusion and exclusion criteria are used for this operation, and, as surgeons gain more experience with this technique these criteria continue to change.^25,26 Most recently, Anuwong et al. expanded their inclusion criteria, making more patients, including those with substernal goiters or history of surgery or radiation on the neck, eligible for this operation.²⁷

With the high-definition view and precise movement afforded by the robot, the robotic transoral thyroidectomy incorporates visualization and protection of the recurrent laryngeal nerve and parathyroid glands.²¹ The operative time is longer, and there are complications unique to transoral surgery not seen with cervical thyroidectomy, including lower lip hypoesthesia and weakness, tear of the lateral commissure, and perforation of the chin skin. Still, this technique shows promise for a select group of patients. The mean operative time in the current literature ranges anywhere between 60 to 265 minutes, although these times include both robotic and other endoscopic platforms.²⁸ However, most of the “extra” time for this operation is spent creating the working space. Kim et al. report that the learning curve stabilizes after only 12 consecutive cases.²⁹ It is likely that as surgeons gain experience, robotic operative time would approach that of conventional surgical approaches.

Despite its increasing popularity, robotic thyroidectomy remains controversial. Importantly, robotic thyroidectomy entails new risks not previously encountered in the open technique, such as brachial plexus neuropathy and tracheal injury. However, robotic thyroidectomy in carefully selected patients appears to have some short-term outcomes similar to open thyroidectomy. Ideally, a prospective, multi-institutional clinical trial could better evaluate short- and long-term clinical and economic outcomes of robotic versus open thyroidectomy for both benign and malignant thyroid disease.

Robot-Assisted Parathyroidectomy

When a solitary parathyroid adenoma has been localized preoperatively, alternatives to open parathyroidectomy are viable options for surgical resection. Many techniques have been described in the literature including endoscopic, robotic, and video-assisted approaches, yet none have been shown to be superior.³⁰ Robotic parathyroidectomy is the latest of the minimally invasive approaches to parathyroidectomy to be performed. As with other minimally invasive techniques, robotic parathyroidectomy avoids creating a neck scar by concealing the operative incisions either within the axilla or infraclavicular region. The first description of the technique used an ipsilateral infraclavicular incision and three small incisions in the ipsilateral anterior axillary line, along with placement of the inferior trocar through an ipsilateral periareolar incision.³¹ Another study describes robotic parathyroidectomy through a single transaxillary port incision.³² There are no formal indications for selecting a robotic approach over other minimally invasive or traditional open approaches to parathyroidectomy. A variety of exclusion criteria have been identified in the literature as representing a higher likelihood of failure or complication if undertaken robotically. Among these contraindications for robotic parathyroidectomy are significant thyroiditis, bulky thyroid disease, previous neck surgery, previous neck radiation, suspicion of malignancy, and high body-mass index.^30,31,33 Large body habitus occasionally requires conversion to an open operation, and hence is included as one of the exclusion criteria for selection of a robotic versus open approach.³¹ Despite varying exclusion criteria, the patients in all studies had their parathyroid adenoma preoperatively localized, and several studies made note of the need for concordance among imaging modalities used to preoperatively localize the adenoma.³⁰

The robotic approach to targeted parathyroidectomy is more technically challenging than conventional open cervical exploration. But it is more favorable than the traditional endoscopic approach with nonarticulated instruments.^30,34,35 The operative times were initially longer for robotic operations compared to open. However, as is often the case with other robotic surgeries, operative time decreases with increasing case numbers.^30,32 Successful excision of the parathyroid gland with identification and protection of the recurrent laryngeal nerve occurred in all studies describing the robotic parathyroidectomy technique.^30,36 These high rates of success on the two most important metrics for parathyroid excision are potentially the result of robotic magnification of the operative field and precise instrumentation.³² Tolley et al.³¹ performed the largest study to date, which was also the first to be reported. Eleven patients with primary hyperparathyroidism, undergoing robotic parathyroidectomy, were retrospectively evaluated. The authors reported high rates of satisfaction across numerous quality of life measures (pain, voice satisfaction, and scar cosmesis)^30,31 demonstrating that the robotic approach is feasible for targeted parathyroidectomy. However, the high cost of robotic approach is undisputed, and it is important to take into account the financial burden on patients when selecting the operative approach.

Given the limited number of case series in the current literature, the advantages of the robotic platform for transaxillary or infraclavicular parathyroidectomy have not yet been adequately delineated. The main advantage of robotic parathyroidectomy over the conventional transcervical approach is an improved cosmetic outcome. At present, the best candidates for robotic parathyroidectomy are patients presenting with a history of hypertrophic scar/keloid formation and a solitary cervical gland identified on localizing studies. Careful patient selection at experienced centers is therefore warranted for a successful outcome.

Robot-Assisted Adrenalectomy

Laparoscopic adrenalectomy has become a preferred approach for removal of most benign and some malignant adrenal tumors. This includes hormonally active adrenal tumors (pheochromocytoma, aldosteronoma, and Cushing's disease), large or enlarging tumors suspicious for malignancy, and isolated adrenal metastases from a distant primary malignancy. The appropriate use of laparoscopy continues to expand as minimally invasive surgery is more desired by patients with adrenal disease.^37,38 On the contrary, open adrenalectomy is still recommended by most societies, at least in the United States, for resection of invasive adrenocortical carcinoma.³⁹ In general, the laparoscopic approach is associated with a shorter hospital stay, less postoperative pain, and an improved recovery when compared with an open adrenalectomy.

The two most common laparoscopic approaches are lateral transabdominal (LT) and posterior retroperitoneal (PR) adrenalectomy. Robot-assisted adrenalectomy has emerged as an alternative minimally invasive approach to adrenal surgery, and both LT and PR robotic approaches have been described.⁴⁰ Recently, these techniques were compared directly using retrospective data.⁴¹ The PR approach was associated with a shorter operating time, even adjusting for differences in tumor size. However, there were no significant differences between these techniques when comparing rates of open conversion, estimated blood loss, or postoperative complications. Robot-assisted adrenalectomy appears to be safe and feasible in centers experienced in both laparoscopic and robotic surgery.

Morino et al. were the first to prospectively compare laparoscopic to robot-assisted LT adrenalectomy.^42,43 Since that time, multiple studies including several systematic reviews and meta-analysis have been performed comparing different laparoscopic and robotic techniques.^38,44,45 Overall laparoscopic and robot-assisted surgery were associated with similar clinical outcomes. There is some evidence that robotic operations result in shorter hospital stays, which could be a cost-saving feature, and are associated with less blood loss, although this difference is not actually clinically significant. On the other hand, comparisons on operative times are conflicting, and training and increased expense appear to be two major drawbacks for robotic adrenalectomy when compared with standard laparoscopy.

Robotic LT adrenalectomy

Laparoscopic LT adrenalectomy is a widely adopted technique. The operative view is most familiar to endocrine surgeons, but this approach appears to provide additional advantages. It is clearly preferred when there is the need for other simultaneous abdominal procedures. Further, this method is preferred in the morbidly obese population and for resection of large tumors, as it allows greater working space compared with the retroperitoneal approach. The indications for robotic LT adrenalectomy are largely the same as its laparoscopic counterpart. The robotic system appears to be well adapted to more difficult adrenalectomies.⁴⁶ In particular, laparoscopic resection of large adrenal tumors can be challenging because of the risk of complications and concerns about malignancy from capsular disruption. However, there is a growing opinion that the robotic system may represent a superior treatment option for these particular patients. When compared against laparoscopy for adrenal tumors greater than 5 cm the use of robot assistance was found to shorten operative times and decrease the rate of open conversion.^47,48 This is largely attributed to the wristed component of the robot and the excellent visualization of adrenal tumors and adjacent structures provided by its 3D view. These features appeared to make the dissection faster and more accurate. Morelli et al. published similar findings when they demonstrated a shorter mean operative time with the robotic approach for tumors ≥6 cm.⁴⁹

Overall, the currently available data demonstrate that there are some benefits to use the robotic system in these patients and suggest that this approach could avoid conversion to laparotomy and corresponding increase in postoperative morbidity. In fact, it appears that larger tumors are more frequently being considered suitable for robotic surgery. A recent publication from the Swedish nationwide database revealed that patients with large tumors were more likely to undergo robot-assisted adrenalectomy compared with laparoscopic operation.⁵⁰

Robotic PR adrenalectomy

The PR approach for minimally invasive adrenalectomy offers some distinct advantages over a transabdominal operation. The posterior approach is preferred for patients requiring bilateral adrenalectomy, as it obviates the need for repositioning of the patient. Most patients who require synchronous bilateral adrenalectomy have adrenocorticotropin hormone (ACTH)-dependent Cushing's syndrome, with less common indications including adrenocortical hyperplasia, bilateral adrenocortical adenoma, bilateral pheochromocytoma (as can occur with MEN2 and VHL), adrenal gland metastasis, and congenital adrenal hyperplasia.⁵¹ Further, the posterior approach provides direct access to the adrenal gland without need for visceral mobilization or lysis of adhesions, and thus is well suited for patients with prior abdominal operations or a hostile abdomen.⁵²

The main drawback to the retroperitoneal approach is the limited intraoperative workspace. Because this operation frequently requires dissection using angled instruments, some authors have advocated that the 3D optics and articulating instrumentation provided by robotic surgery make this a superior technique for this approach. Berber et al. published the first case series comparing robotic retroperitoneal adrenalectomy to laparoscopic surgery, and concluded that the robot overcame the limitations of laparoscopic surgery and was considered to be a refinement of the technique.⁵³ Further, this group demonstrated that once the learning curve has been achieved, which generally requires at least 20 cases, the robotic PR could shorten the operative time compared with the laparoscopic approach.⁵⁴

Single-port robotic-assisted adrenalectomy

Single-port adrenalectomy has evolved concurrently with other single-site surgical procedures, although its use remains limited to high volume centers experienced with this technique. The main attraction of these techniques is the improved cosmetic outcome. While the technique inherently adds difficulty to the operation, the robotic system appears to, at least partially, overcome some of these challenges. Arghami et al. reported a case series of 16 patients who underwent single-port robot-assisted adrenalectomy.⁵⁵ They found no significant difference in operating time and reported less postoperative pain in this cohort.

Pheochromocytoma and paragangliomas

Minimally invasive adrenalectomy is the recommended approach for most pheochromocytomas, and can also be performed for small noninvasive paragangliomas in surgically favorable locations by experienced laparoscopic surgeons.⁵⁶ However, there is some concern for tumor rupture and local recurrence with using minimally invasive techniques for these tumors, especially when pheochromocytomas are large or invasive. Similarly, paragangliomas are more likely to be malignant, thus are more likely to require an open resection. In addition to complete resection, the main principles of surgery for pheochromocytomas include minimal tumor manipulation to avoid hypertensive crisis. There is some suggestion that the robot-assisted technique is well-suited, and perhaps more appropriate, for resection of these tumors, although the evidence supporting this claim is currently lacking.

The robotic approach for resection of these tumors has been reported in several cases series and retrospective reports.⁵⁷ In one small case series of patients undergoing robot-assisted adrenalectomy, about one-fifth of these patients underwent an operation for pheochromocytoma.⁵⁸ There was one intra-operative complication, a capsule tear in a patient with a 6 cm pheochromocytoma, and one mortality due to development of a fatal arrhythmia postoperatively. Another group examined the perioperative outcomes for patients with pheochromoctyoma undergoing laparoscopic versus robot-assisted adrenalectomy. Notably, there were three patients in the laparoscopic arm who experienced cardiac arrhythmia, but no adverse cardiac events in the robot-assisted group were observed.⁵⁷ Notably, no cardiac events following robotic-assisted adrenalectomy were observed. Further, there was no evidence of local recurrence in the robotic group. In the authors' opinion, the dissection was faster with the articulating instruments of the robot. Together with the 3D view and more stable camera platform, the adrenalectomy was felt to be expedited with the robotic technique.

Partial adrenalectomy has been described for pheochromocytoma, including patients with hereditary syndrome that predispose patients to multiple adrenal lesions, and this represents a promising application of the robot system.⁵⁹ The safety and feasibility of robot-assisted partial adrenalectomy has been reported.⁶⁰ There have been no direct comparisons between robotic and laparoscopic partial adrenalectomy, and this technique requires validation with a larger series. However, based on currently available data, the operative time for the robot appears comparable to the conventional laparoscopic partial adrenalectomy. Further, some surgeons feel that the robotic platform is particularly helpful when performing a partial adrenalectomy as the articulation of the robotic instruments allowed circumferential dissection around the tumor deep within the adrenal with minimal manipulation of the normal adrenal gland.⁵⁹ Thus, the maneuverability of the robot, along with its superior visualization, may assist with preservation of the cortical remnant and represent an improvement on this operation.

Overall, the primary benefits of the robotic system including additional degrees of articulation and a 3D camera also extend to performing adrenalectomy, and this appears to provide some benefit when operating on the adrenal glands for certain indications. Whether these differences lead to improved patient outcomes is not easily demonstrated. The primary disadvantage to robot-assisted adrenalectomy remains cost and limited availability.

Conclusion

Over the last decade, developments in technology have led to a rapid progress in robotic surgery. Safety and effectiveness of robotic adrenalectomy, parathyroidectomy, and thyroidectomy have been proven. The robotic technology offers better ergonomics for the surgeon, while providing similar outcomes when compared with laparoscopic adrenalectomy and better cosmetic results when compared with open parathyroidectomy and thyroidectomy. Even though the robotic approach for adrenalectomy has been popularized, robotic parathyroidectomy and thyroidectomy have not been widely accepted by the surgical community. The main advantage of robotic parathyroidectomy over the conventional transcervical approach is an improved cosmetic outcome. However, given the limited number of case series in the current literature, the advantages of the robotic platform for transaxillary or infraclavicular parathyroidectomy have not yet been adequately validated. Robotic thyroidectomy in carefully selected patients appears to have some short-term outcomes similar to open thyroidectomy. Still, this technology entails new risks not previously encountered in the open technique and its use remains controversial.

Regardless of operation, the major drawback to the robot almost universally is the cost. With new robotically assisted surgical devices on the way, we may see these limitations go away.

Footnotes

Acknowledgments

The authors would like to thank Drs. Konstantin Umanskiy and Ciro Andolfi for their assistance with review of this article.

Disclosure Statement

No competing financial interests exist.

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