Robotic-assisted ectopic mediastinal parathyroidectomy: a single institution experience and operative review for the thoracic surgeon

Introduction

Primary hyperparathyroidism (PHPT) is a condition in which one or more of the parathyroid glands (PTGs) secretes excess parathyroid hormone (PTH) which increases blood calcium levels. PHPT is the leading cause of hypercalcemia in the United States, affecting an estimated 0.1–0.5% of the population and up to 1% of individuals over 70 years of age (1). The majority of patients are asymptomatic or only experience minor manifestations related to hypercalcemia, including fatigue, reduced appetite, excessive thirst, nausea, constipation, mild depression, or loss of concentration (2). Despite advancements in medical therapies, parathyroidectomy remains the only definitive cure for individuals with PHPT.

The majority of PHPT cases arise from solitary parathyroid adenomas, with a small proportion attributed to multiple adenomas or glandular hyperplasia (3). Localization studies, such as neck ultrasonography (US), nuclear scintigraphy with Tc-99m sestamibi, or computed tomography (CT), facilitate focused surgical exploration. Typically, the paired superior PTGs are situated behind the upper and middle lobes of the thyroid gland, while the inferior PTGs are commonly found within 1 cm of the intersection between the inferior thyroid artery and recurrent laryngeal nerve (4). However, ectopic PTGs are common with an incidence of up to 25%, and between 1% and 2% of ectopic glands are located in the mediastinum (5).

When an ectopic mediastinal adenoma is in the anterior superior mediastinum, it is often within the thyrothymic ligament or thymus itself and amenable to removal via a standard cervical approach. When faced with a PTG that is either very inferior in the anterior mediastinum or in the posterior mediastinum, surgeons have traditionally utilized open approaches, such as sternotomy and thoracotomy, to achieve adequate exposure and ensure localization of the offending gland. Due to the significant postoperative morbidity up to 21%, pain, and extended length of stay associated with these procedures, minimally invasive parathyroidectomy using a robotic-assisted thoracic surgery (RATS) approach has emerged as an alternative surgical option (6). The purpose of our study was to share our institution’s experience with robotic-assisted mediastinal parathyroidectomy including intra- and perioperative management and provide a review of the literature regarding mediastinal parathyroidectomy with the aim of educating thoracic surgeons who may be engaged in such patient management. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1920/rc).

Methods

Ethical oversight

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Colorado Multiple Institutional Review Board which oversees the University of Colorado Anschutz Medical Campus (COMIRB; IRB Organization Number IORG0000433) (IRB Approval COMIRB #22-0713) and individual consent for this retrospective analysis was waived.

Study design

This was a single-center, 5-year retrospective cohort study at the University of Colorado Anschutz Medical Campus from 3/2018–4/2023. All patients who underwent mediastinal mass resection (MMR) using a minimally invasive RATS approach for PHPT at our tertiary academic referral center were targeted for inclusion. Patient cases were reviewed for basic demographic information, medical history, operative procedures, laboratory values, and postoperative course.

Statistical analysis

Summary statistics are presented as frequency and percentage for categorical variables and median [interquartile range (IQR)] for continuous variables. No comparative analysis was performed.

Preoperative workup

Preoperative workup including history and physical examination, as well as laboratory and localization studies, were performed by an endocrine surgeon prior to referral to a board-certified thoracic surgeon. Imaging workup included formal neck US performed by sonographer. Where indicated Tc-99m scintigraphy (sestamibi scan) coupled with CT was performed for further localization.

RATS operative technique for anterior mediastinal resection and intraoperative monitoring

After safe induction of general anesthesia and placement of a dual-lumen endotracheal tube, the patient is positioned in a left or right partial lateral decubitus position based on location of the tumor; patients with an adenoma at the level of the ascending aorta and to the right are positioned in a supine position and approached from the right; patients with an adenoma to the left of the ascending aorta or in the aorto-pulmonary window are approached from the left. The patient is then prepped and draped in sterile manner. Prior to incision, a baseline PTH is collected.

The chest is entered via a 1 cm transverse incision in the 6th intercostal space of the anterior axillary line. The video thoracoscope is introduced and confirms ipsilateral lung isolation and contralateral single lung ventilation. Three additional working ports are placed via 1 cm transverse incisions 2-rib intervals superiorly and 2-rib intervals inferiorly to the camera, and at the nipple line just above the diaphragm. Trocars are placed under direct visualization bluntly and docked to the da Vinci Xi robot (Intuitive Surgical, Sunnyvale, CA, USA). Carbon dioxide insufflation at 12 cmH₂O is helpful, and can be delivered either via the assistant ports, or in the case of the da Vinci Xi robot, the robotic arm ports.

The anterior mediastinal fat-pad overlying the pericardium is incised from 1 cm medial to the phrenic nerve from the mid pericardium up to the innominate vein and aortic arch, then superiorly to the posterior sternum just medial to the internal mammary artery and vein, and then inferiorly along the internal mammary artery and vein to the mid pericardium. Dissection is carried laterally to medially until the innominate vein is identified. The soft tissue is skeletonized from the vein using clips to divide and ligate draining veins. The thymic horns are dissected out from over the top of the innominate vein. All the soft tissue overlying the pericardium, the aortic arch, and the innominate vein are resected en bloc. The resected soft tissue is placed in a retrieval bag and removed from the chest.

Following specimen removal, intraoperative parathyroid hormone (ioPTH) levels are checked within 5 minutes, and then again 10–20 minutes after resection. In the meantime, frozen pathologic evaluation is used to determine the presence of parathyroid tissue. If the patient has a history of prior parathyroidectomy, a portion of the mediastinal parathyroid tissue is sent for cryopreservation. The dissection bed is examined for hemostasis. After ensuring a PTH decrease of at least 50%, the trocars are undocked from the robot and sequentially removed under direct visualization. A 24-French chest tube is placed, and dual-lung ventilation is resumed. Muscle layers, subcutaneous tissue and skin are closed. Perioperative pain control is achieved with either an intercostal nerve block performed by the surgeon, or an erector spinae nerve block performed by the anesthesiologist.

Successful surgical management was defined as an ioPTH drop of 50% or more at 10–20 minutes post-resection, and successful cure of PHPT was defined as a normal calcium level 6 months following resection in those with preoperative hypercalcemia, or a normal PTH level 6 months following resection in those with preoperative normocalcemia.

Results

A total of eight patients and cases were reviewed, five of which (63%) were female. All patients were white (100%) and non-Hispanic (100%). Median age was 59 (IQR, 47–66) years old and median body mass index was 28.0 (IQR, 26.9–31.4) kg/m².

All patients were diagnosed with PHPT based on biochemical evidence indicative of elevated PTH [median 76.5 (IQR, 65.4–113.5) pg/mL; normal PTH 15–65 pg/mL] and high/normal serum calcium [median 10.9 (IQR, 10.2–11.3) mg/dL]. Patients were deemed a candidate for surgical management based on their symptoms meeting National Institutes of Health (NIH) criteria for surgery (7-9) including either nephrolithiasis (5/8, 63%), urine calcium >400 mg/24 hours (3/8, 38%), osteoporosis on dual-energy X-ray absorptiometry (DEXA) (2/8, 25%), fragility fractures (1/8, 13%) and/or severe subjective symptomatology of excessive fatigue, myalgias/arthralgias and mood disorders (1/8, 13%). On physical exam, no patients had evidence of palpable masses. All patients underwent ultrasound and the majority of patients (6/8, 75%) underwent sestamibi scan, less than half (3/8, 37%) underwent 4D CT scan. Based on initial workup, 6/8 (75%) of adenomas were initially localized to the anterior mediastinum and 25% to one of the PTGs. Results of initial workup and initial localization are shown in Table 1.

Figure 1 demonstrates the operative approach of each patient. Of the 6/8 (75%) of patients that were initially localized to the anterior mediastinum, five were immediately referred to thoracic surgery for direct RATS-MMR (5/8, 63%). Patients A, B, C and D all underwent RATS-MMR and were noted to have a >50% drop in iPTH upon resection of the thymus indicating successful removal of the hypersecretory gland (72 to 9, 128 to 20, 69 to 11 and 94 to 12 pg/dL, respectively). Patient E underwent RATS-MMR however did not experience the expected iPTH drop >50% (135 to 72 pg/dL), as such this patient concurrently underwent a neck exploration by the endocrine surgeon with resection of the right superior gland, and at this time had appropriate PTH drop >50% (135 to 32 pg/dL). This suggests likely double adenoma, and was confirmed on final pathology. Patient F was not immediately referred to thoracic surgery and instead underwent resection of the adenoma via a cervical approach. This was ultimately aborted due to inability to safely visualize the thymus and suspected ectopic gland. This patient was subsequently referred to thoracic surgery and underwent a successful RATS-MMR 1 month later with expected PTH drop >50% (176 to 71 pg/dL).

Figure 1 Initial localization and operative strategy by patient. Letters indicate each individual patient. RATS, robotic-assisted thoracic surgery; ioPTH, intraoperative parathyroid hormone.

Of the 2/8 (25%) of patients who were initially localized to one of the native PTGs (patients G and H), each underwent a subtotal parathyroidectomy with bilateral neck exploration. Patient G had an appropriate PTH drop >50% (147 to 51 pg/dL) however had recurrence of disease 20 months later. This patient then underwent repeat workup with sestamibi scan which demonstrated signal in the anterior mediastinum. They were referred to thoracic surgery and ultimately underwent successful RATS resection with PTH drop 210 to 13 pg/dL. Patient H also underwent subtotal parathyroidectomy; however, an appropriate PTH drop >50% was not observed (162 to 94 pg/dL), as such the patient was referred for further diagnostic workup upon which a sestamibi scan revealed a signal in the anterior mediastinum. The patient was referred to thoracic surgery and underwent successful RATS-MMR 11 months later with expected PTH drop (109 to 9 pg/dL). Final pathology confirmed intrathymic parathyroid tissue on all eight patients. Operative data and final pathology are shown in Table 2.

Overall, eight patients underwent RATS anterior mediastinal resection by three thoracic surgeons. Median operative time was 178 (IQR, 138–213) minutes. Following resection, patients were admitted to the hospital with median length of stay of 2.0 (IQR, 1.5–2.0) days. Patient A experienced a complication on the index admission of a chylothorax requiring dietary modification only, Clavien-Dindo Grade 1, indicating morbidity in 1/8 patients. Outside of this, there were no 30-day complications or readmissions.

All patients were discharged using a parathyroidectomy calcium supplement protocol, including discharge with directions to take two tablets of Citracal Maximum three times daily (one tablet contains calcium citrate 315 mg with 250 IU vitamin D3) with plans for close follow-up for outpatient laboratory monitoring. All patients achieved cure of PHPT, defined as a normal calcium level 6 months following resection in those with preoperative hypercalcemia, or a normal PTH level 6 months following resection in those with preoperative normocalcemia.

Discussion

Here, we present our single-institution experience with RATS mediastinal parathyroidectomy in a series of eight patients who all underwent successful treatment of their PHPT. We demonstrate that the RATS approach is safe with low morbidity and associated length of stay. While the incidence of ectopic PTGs varies in the literature, mediastinal parathyroid tissue is rare. Nevertheless, thoracic surgeons should be familiar with the diagnostic workup and key management principles, including the importance of preoperative localization techniques, operative approaches and intra- and perioperative management. Prior to this study, the RATS approach to resection of a mediastinal parathyroid adenoma remained an infrequently studied intervention. Our review of the literature identified three other reports of RATS mediastinal parathyroidectomy ranging from single case studies to small series with the largest containing eight patients, similar to ours (10-13).

In our study, the majority of patients were female, consistent with the observation that PHPT is 2–3 times more common in women, and its incidence rises with advancing age (8,14). All of our patients presented with biochemical evidence of elevated PTH and elevated serum calcium, often with symptoms of kidney stones, osteoporosis and subjective symptoms of fatigue and mood disorder. In general, surgical intervention for PHPT is recommended for symptomatic patients (kidney stones, fragility fractures, hypercalcemic crisis and hypercalcemia pancreatitis). In asymptomatic patients, parathyroidectomy is recommended for those presenting with calcium levels greater than 1 mg/dL above normal, objective evidence of renal involvement [nephrolithiasis, hypercalciuria (24-hour calcium level >250 mg in woman and 300 in men), glomerular filtration rate <60 mL/min], decreased bone mineral density T <−2.5], individuals less than 50 years old, those unable or unlikely to undergo regular follow-up monitoring, or patients who prefer surgical management (7,8). Each of our patients met at least one criterion for undergoing parathyroidectomy.

Following decision to operate, our patients underwent localization workup. All of our patients underwent formal neck US. While neck US is the mainstay of diagnosis for cervical PTGs (14), this study will be negative in almost all cases involving mediastinal parathyroid adenomas due to its inability to visualize glands positioned behind bony or air-filled structures (4). This is concordant with our findings of uniformly negative US studies in our patient population. The majority of our patients then went on to receive nuclear scintigraphy with Tc-99m sestamibi radiotracer or dual isotope (Tc-99m sestamibi plus iodine-123), which helps identify ectopic mediastinal parathyroid adenomas not visualized by US. Abnormal parathyroid tissue exhibits increased uptake of Tc-99m sestamibi, achieving a sensitivity of 86% for glands larger than 1 g and even up to 100% for glands surpassing 2 g (6). Of our 6/8 patients who underwent sestamibi scan prior to first course operative treatment, 5 were immediately localized to the anterior mediastinum.

The importance of accurate preoperative localization is paramount, especially when considering the use of a minimally invasive approach. This is illustrated with patients G and H in our series, both of whom did not have a sestamibi scan prior to their first course of surgical therapy, and ultimately needed additional workup and resection. In addition to sestamibi scan, choline PET-CT has shown favorable results in detection of hyperfunctioning parathyroid tissue and may be used in place of conventional sestamibi scintigraphy in preoperative planning of parathyroid (15). While not applied in this series, there is encouraging evidence in the utilization of near-infrared fluorescence (NIRF) imaging using indocyanine green (ICG) for intraoperative PTG localization. ICG has been shown to reliably locate PTGs at a rate of 92.9% (16). At least one study has reported the successful identification of an intrathymic PTG using ICG (17), and similarly, intra-arterial methylene blue and indigo carmine have been used (18,19). Localization techniques like this may be useful in reducing operative time and limiting need for total thymectomy when intrathymic. However, a higher volume of applications or multi-institutional study are needed to provide such an analysis.

There are numerous theories postulating the potential mechanisms underlying the development of mediastinal ectopic parathyroid tissue, often focusing on embryologic factors and migration (20). Originating from the third branchial cleft pouch, the inferior PTGs may descend into the anterior mediastinum along with the thymus. Additionally, PTGs may migrate to the thoracic cavity throughout life as enlargement secondary to adenoma or hyperplasia in the neck may predispose descent into the mediastinum due to the augmented weight, impact of swallowing, and negative intrathoracic pressure (20). Specific to mediastinal glands, a retrospective analysis by Said et al. found that 45% of ectopic mediastinal glands were intrathymic, 21% located in the aortopulmonary window, and the remaining 33% situated in other intrathoracic sites (21).

In general, anterior mediastinal PTGs that are situated within 6 cm of the superior aspect of the clavicular head can safely excised using a transcervical approach (22,23). A multidisciplinary discussion between the parathyroid surgeon and thoracic surgeon can be very useful in determining whether a primary cervical or thoracic approach is most appropriate. In some cases, a combined approach may be indicated. When lesions are positioned more distally within the mediastinum, a transthoracic approach is often necessary because this technique allows for the comprehensive excision of mediastinal fat and thymus, ensuring that the culprit lesion is removed en bloc without capsular rupture (22). Described transthoracic approaches include open, video-assisted thoracoscopic surgery (VATS), and RATS. Traditional open approaches to mediastinal parathyroidectomy result in notable postoperative morbidity, pain, and prolonged hospital stays. Since the first reported thoracoscopic removal of an ectopic mediastinal PTG in 1994 by Prinz (24), there has been a growing adoption of minimally invasive mediastinal parathyroidectomy due to preliminary data indicating comparable outcomes to open surgery but with fewer complications (21). The Said et al. study remains the only comparative study with a cohort of 11 open resections versus 9 VATS approaches (21). Besides this, comparative studies are lacking likely due to the rarity of this condition. This provides an opportunity for further study through a multicentered retrospective analysis. While our study too is limited by lack of comparison group, we demonstrated low rates of overall morbidity with only one patient experiencing a postoperative complication that notably did not require further intervention beyond dietary modification. This low morbidity was accompanied by short hospital length of stay. We recommend the use of the RATS approach when possible to reduce morbidity, enhance postoperative recovery, with the added benefit of improved cosmesis over sternotomy. Additionally, RATS approaches have improved visualization of the surgical field and enhanced dexterity enabled by articulation of the instruments, facilitating safe dissection in areas that are relatively difficult to access using conventional thoracoscopy, such as the narrow aortopulmonary window (25).

Regardless of approach, surgical management is guided by intraoperative monitoring of PTH levels. Given the short, 3–5-minute half-life of PTH, intraoperative monitoring can be used to guide completeness of targeted mediastinal parathyroidectomy. At our institution, we employ peripheral venous measurement of serum PTH before incision as well as 5, 10, and 20 minutes after resection. A reduction in iPTH of more than 50% from the baseline at 10 minutes from resection the parathyroid, known as the “50% rule”, serves as confirmation of successful resection. This is supported by the Miami criterion which states that a 50% decline in iPTH from the highest pre-incision or pre-excision measurement obtained 10 minutes after excision is nearly 100% predictive of surgical cure (26).

Conclusions

While this is a relatively rare presentation of PHPT, with only 1% to 2% of ectopic parathyroid adenomas existing in the lower mediastinum, it is important for thoracic surgeons to possess a comprehensive understanding of the anatomy, embryology, preoperative work-up, operative approach and postoperative management of mediastinal PTGs in order to maximize their chances of curing PHPT. While our study is limited by a small sample size, our findings demonstrates that the RATS approach offers a minimally invasive approach with low morbidity and hospital length of stay, with success in surgically curing PHPT. The results of our study and recommendations should however be interpreted with limitations in mind, including the lack of direct comparative group. Additionally, we recognize that there are other considerations in adopting new surgical techniques, including the experiential learning curve and economic considerations to adoption.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1920/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1920/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1920/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-23-1920/coif). J.D.M. serves as an unpaid editorial board member of Journal of Thoracic Disease from April 2022 to March 2024. J.D.M. reports that he consults for Intuitive, Inc. C.M.S. receives salary support, in part, by the National Institutes of Health, under Ruth L. Kirschstein National Research Service Award T32CA17468. R.A.M. reports that he consults for Medtronic, Inc. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Colorado Multiple Institutional Review Board which oversees University of Colorado Anschutz Medical Campus (COMIRB; IRB Organization Number IORG0000433) (IRB Approval COMIRB #22-0713) and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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