Surgery in Primary Hyperparathyroidism: Extensive Personal Experience

Journal of Clinical Densitometry: Assessment of Skeletal Health, vol. 16, no. 1, 54e59, 2013 Ó Copyright 2013 by The International Society for Clinical Densitometry 1094-6950/16:54e59/$36.00 http://dx.doi.org/10.1016/j.jocd.2012.11.007

Original Article

Surgery in Primary Hyperparathyroidism: Extensive Personal Experience Brooks Van Udelsman,1 and Robert Udelsman*,2,3 1

Interdepartmental Program in Vascular Biology and Therapeutics, Yale University School of Medicine, New Haven, CT, USA; 2Yale-New Haven Hospital, New Haven, CT, USA; and 3Department of Surgery, Yale University, School of Medicine, New Haven, CT, USA

Abstract Parathyroidectomy is the optimal treatment for primary hyperparathyroidism (PHPT) and provides a cure in the vast majority of cases. Over the last 2 decades, improvements in preoperative localization and the development of intraoperative parathyroid hormone monitoring have opened the door for new surgical approaches to parathyroidectomy. Minimally invasive parathyroidectomy is performed under regional or local anesthesia. It requires less surgical dissection resulting in decreased trauma to tissues and is more effective and less costly than traditional bilateral cervical exploration. This article reviews our approach reflecting advances in preoperative localization, anesthetic techniques, and intraoperative management of patients undergoing parathyroidectomy for the treatment of PHPT. Key Words: Minimally invasive parathyroidectomy; parathyroid surgery; primary hyperparathyroidism.

uses unilateral neck exploration under regional and/or local anesthesia. Unilateral focused cervical exploration for PHPT was first introduced in 1975 with the side to be explored determined by palpation, esophageal imaging, venography, or arteriography (2e4). The technique was advocated as a means of reducing the cost and morbidity of surgery while maintaining cure rates (5). Today, MIP is performed after preoperative parathyroid localization, including sestamibi scans with single-photon emission computed tomography (SPECT), ultrasonography, and more recently high-quality 4-dimensional computed tomography (4DCT) scans. An intraoperative PTH (IOPTH) assay is used to confirm decreased PTH to ensure the adequacy of the resection. Of note, other nonconventional approaches have also been used including video-assisted, radioguided, and endoscopic parathyroidectomy.

Introduction Mandl (1) performed the first successful parathyroidectomy in 1925. Under local anesthesia and without the aid of preoperative imaging, he identified 3 normal parathyroid glands and removed a single enlarged parathyroid gland, resulting in a dramatic cure. Although in the ensuing decades, standard surgical management came to involve bilateral cervical exploration under general anesthesia, the surgery continued to require identification of all 4 parathyroid glands. However, the realization that the etiology of approx 85% of cases of primary hyperparathyroidism (PHPT) is a single adenoma along with advances in preoperative imaging, regional anesthetic techniques, and the availability of intraoperative parathyroid hormone (PTH) monitoring has opened the door for less invasive techniques. As opposed to bilateral cervical exploration, minimally invasive parathyroidectomy (MIP)

Indications for MIP and Conventional Parathyroidectomy

Accepted 11/18/12. Disclosure Statement: The authors have nothing to disclose. *Address correspondence to: Robert Udelsman, MD, MBA, Department of Surgery, Yale University School of Medicine, P.O. Box 208062, New Haven, CT 06520-8062. E-mail: Robert.Udelsman@ Yale.edu

Indications for parathyroidectomy whether by traditional bilateral cervical exploration or by MIP are symptomatic disease or asymptomatic PHPT with features in accordance with published guidelines (6,7). Symptoms may include subtle 54

Surgery in PHPT neurocognitive dysfunction with fatigue, mood swings, anxiety, and depression (8e10). Multiple studies have shown improvement in neurocognitive function especially in relation to mood and anxiety in patients who undergo successful parathyroidectomy (11e14). A relative contraindication to MIP is documented or suspected familial PHPT. The predilection of this patient population for multiglandular disease often necessitates bilateral cervical neck dissection (15). Similarly, rare cases of suspected parathyroid carcinoma require en bloc resection of the involved hyperfunctioning gland often in conjunction with concomitant ipsilateral thyroid lobectomy to ensure adequate resection (16,17). Previous cervical surgical exploration is not a contraindication to MIP (18).

Preoperative Imaging Over the past 2 decades, the development and refinement of parathyroid imaging (sestamibi-technetium 99m scintigraphy, ultrasonography, and 4DCT) have ushered in an evolution in the surgical approach to PHPT. The most established modality is sestamibi-SPECT, which generates 3-dimensional images (19e21). Initially developed for cardiac scintigraphy, technetium 99m methoxyisobutylisonitrile (sestamibi) was incidentally found to concentrate in enlarged parathyroid glands (22). As a monovalent lipophilic cation, sestamibi is able to diffuse passively through cell membranes, where it accumulates in mitochondria (23). Hyperfunctioning parathyroid glands with increased metabolic rate and density appear brighter on a sestamibi scan (24). Although the reported positive predictive value (PPV) and sensitivity of sestamibi-SPECT vary, a recent metaanalysis found a PPV and sensitivity of 78.9% and 90.7%, respectively (25). Limitations of sestamibi-SPECT include the coexistence of thyroid nodules, especially H€ urthle cell neoplasm or other metabolically active tissue with increased mitochondrial density that can mimic parathyroid adenomas and result in false-positive findings (26,27). Moreover, the size of the adenoma and percentage of oxyphil cells limit the sensitivity. Small adenomas (!600 mg) and those containing few oxyphil cells (!20%) are generally associated with negative scans (28). A false-negative sestamibi-SPECT study is more likely in milder disease with relatively lower elevations in serum calcium (29). In cases of double adenomas or multiglandular hyperplasia, sestamibi-SPECT is only rarely able to detect all abnormal glands (30,31). Ultrasound (US) represents an effective, noninvasive, and inexpensive study in preoperative evaluation of PHPT. A recent meta-analysis reported a PPV of 76.1% and sensitivity of 93.2% (25). The normal parathyroid gland is too small to be routinely detected sonographically, whereas an enlarged parathyroid adenoma is identified as a homogenously hypoechoic extrathyroidal ovoid mass with a hilar blood supply. The main drawback of US is related to its operator dependence resulting in highly variable localization. Some studies suggest improved sensitivity of parathyroid tumor localization with surgeon-performed US (rather than technician- or radiologist-performed US) (32,33). Other studies report Journal of Clinical Densitometry: Assessment of Skeletal Health

55 improved sensitivity of parathyroid tumor localization when US was used in combination with sestamibi-SPECT (27). Limitations of US are its inability to evaluate mediastinal parathyroid glands and difficulty detecting parathyroid abnormality in milder forms of PHPT or in obese patients (34). 4DCT represents a relatively new modality for parathyroid imaging and gland localization. 4DCT derives its name based on its use of CT to track changes in perfusion of contrast over time. Hyperfunctioning parathyroid glands demonstrate a rapid uptake and washout when compared with normal parathyroid glands and other structures in the neck. In studies evaluating the effectiveness of 4DCT, it was found to have increased sensitivity in lateralizing and localizing a hyperfunctioning parathyroid gland to the correct side and quadrant of the neck compared with sestamibi-SPECT and US (35,36). Moreover, 4DCT demonstrated improved sensitivity in the diagnosis of multiglandular disease compared with US and sestamibi-SPECT (36). Limitations of 4DCT include increased radiation exposure, representing approximately a 0.1% risk of subsequent development of thyroid carcinoma in a 20-yr-old female (37). For this reason, 4DCT should be used sparingly in younger patients. The increased cost of 4DCT when compared with sestamibi-SPECT and US must also be considered; however, these costs may be mitigated by reductions in conversion of MIP to bilateral cervical exploration and the associated increases length of hospital stay and complications (38). In cases where the aforementioned techniques result in negative, discordant, or unconvincing preoperative imaging studies, MIP may still be used with excellent cure rates. In patients who require remedial cervical exploration, invasive localization techniques such as selective PTH venous sampling may be indicated. Selective venous sampling performed by an interventional radiologist can uncover subtle, by significant PTH gradients, allowing for localization of hyperfunctioning glands (39). Additionally, ultrasonography can guide preoperative aspiration of a suspected gland from which PTH is measured to confirm that the tissue is a parathyroid gland. As with venous localization, this technique should be reserved for remedial cases (40).

Anesthesia Conventional bilateral cervical parathyroid exploration is performed under general anesthesia with placement of either an endotracheal tube or a laryngeal mask airway. However, at high-volume centers, an increasing number of cases are being performed under monitored anesthesia care with local or regional anesthesia (41). At our institution, the surgeon performs the regional block by injecting 20 mL of 1% lidocaine containing 1:100,000 epinephrine unilaterally at Erb’s point (located on the posterior border of the sternocleidomastoid muscle midway between its attachments to the mastoid process, sternum, and clavicle) and along the anterior border of the sternocleidomastoid muscle on the side of the localized gland (Fig. 1). Intravascular infiltration of local analgesic agents must be avoided. Together, the regional nerve block and local anesthetic at the site of incision provide excellent Volume 16, 2013

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Fig. 1. Cervical block anesthesia. (A) A superficial cervical block is administered posterior and deep to the sternocleidomastoid muscle (1). (B) Local infiltration is also performed along the anterior border of the sternocleidomastoid muscle (2), followed by a local field block (3). (Reprinted with permission from Udelsman (55). Copyright 2002, Lippincott Williams & Wilkins.) analgesia for virtually every case. Intravenous sedation is delivered just before administration of the regional block and is maintained throughout the case reducing patient anxiety while preserving the patient’s ability to phonate. The benefits of regional anesthesia are multifactorial. With a conscious patient, the surgeon may assess the functional status of the recurrent laryngeal nerve in real time. Likewise, the patient is spared the potential complications of general anesthesia and endotracheal intubation, which has been associated with up to a 5% risk of vocal cord changes or damage (42). Avoidance of general anesthesia enhances the ability to perform ambulatory surgery with same-day discharge (18,43e46). In cases in which concomitant thyroid pathology, concern of parathyroid carcinoma, persistently elevated intraoperative PTH levels, difficulty in ensuring safety of the recurrent laryngeal nerve, or patient discomfort are encountered, conversion to general anesthesia may be performed. Conversion is performed in a controlled fashion with protection of the surgical field. In a study of 1037 patients, we reported a conversion rate of approx 10% most commonly because of difficulty of the case and/or ectopic location of the hyperfunctioning glands (18).

Intraoperative PTH Monitoring Intraoperative PTH monitoring was first introduced in 1990 and allowed for a biochemical alternative to 4-gland visualization. Previously, direct visualization of all 4 parathyroid glands was necessary to rule out multiglandular disease. The feasibility of intraoperative PTH monitoring is because of the relatively short half-life of PTH (3e5 min). Journal of Clinical Densitometry: Assessment of Skeletal Health

In the preoperative holding area, an intravenous catheter is inserted in the antecubital fossa to obtain a baseline PTH level. In the operating room, the patient is placed in the semiflower position, and a screen is used to protect the patient’s face from the operative field. Anesthesia personnel maintain access to the intravenous line throughout the procedure and obtain intraoperative PTH levels (Fig. 2). Regional anesthesia is administered, and an abbreviated Kocher incision (approx 3 cm) is made. The anterior compartment of the neck is entered, the median raphe is mobilized, the parathyroid adenoma is visualized, the recurrent laryngeal nerve is protected, and the adenoma is excised (Fig. 3). After excision, serial blood draws are obtained, and the adequacy of resection confirmed when the patient’s preoperative baseline PTH level decreases by at least 50% and returns to the normal range (18,46e48). The importance of intraoperative PTH measurement is highlighted by the increased failure rates seen in series performed without IOPTH (49). If the PTH level fails to appropriately decline after resection, thus indicating residual abnormal parathyroid tissue, further exploration is required. Because parathyroid glands can reside in ectopic sites, the surgeon may need to explore the retroesophageal space, thymus gland, carotid sheaths, and submandibular region for undescended glands. Additional intraoperative adjuncts may be used to localize the parathyroid gland including US or bilateral internal jugular vein sampling. Extensive exploration may necessitate conversion to general anesthesia and traditional bilateral exploration (4,50). In rare cases, a partial sternotomy may be required for removal of parathyroid glands located in the mediastinum (51). Volume 16, 2013

Surgery in PHPT

57 hypocalcemia (4). However, because of the use of regional anesthesia, patients undergoing MIP are spared the complications of endotracheal intubation, which is associated with vocal cord changes and damage (42). In a prospectively collected and retrospectively reviewed series of 1650 consecutive parathyroidectomies performed between 1990 and 2009 (of which 613 were performed in the conventional fashion and 1037 were performed as MIP), we reported the superiority of MIP with a cure rate of 99.4% vs 97.1% in conventional exploration and statistically significant decrease in the complication rate of 1.45% vs 3.10% (18).

Recurrent or Persistent PHPT

Fig. 2. The patient has a large-bore peripheral intravenous line inserted, which is used for medication and fluid administration, as well as sampling for parathyroid hormone levels. That patient is awake, and a fan is used to blow room air gently toward his or her face to minimize the sensation of claustrophobia. (Reprinted with permission from Udelsman (55). Copyright 2002, Lippincott Williams & Wilkins.)

Complications The complications of parathyroidectomy whether by MIP or by traditional bilateral cervical exploration are principally hematomas, recurrently laryngeal nerve injury, and

Despite the high success rate of both MIP and conventional bilateral cervical exploration, a small percentage of patients present with either persistent or recurrent PHPT. Persistent PHPT occurs when hypercalcemia develops within 6 mo of initial parathyroid surgery. When hypercalcemia develops after 6 mo of normocalcemia, this represents recurrent disease (52). In general, persistent PHPT implies inadequate resection, whereas recurrent PHPT indicates development of new disease. Several causes of operative failure exist and include errors in initial diagnosis because of the presence of unrecognized multiglandular disease, parathyroid carcinoma, and surgeon inexperience (52). In cases where hyperparathyroidism is persistent or recurs, the decision to reoperate should be made carefully especially in patients with asymptomatic hypercalcemia. Remedial cases are associated with an overall increase in failure and complication rates, including a 1%e6% risk of permanent injury of

Fig. 3. Excision and removal of parathyroid adenoma. (A) Anterior compartment of the neck is explored with visualization of the recurrent laryngeal nerve, common carotid artery, and blood supply of parathyroid adenoma. (B) The parathyroid adenoma is excised after clipping of its blood supply and visualization and protection of the recurrent laryngeal nerve. (Reprinted with permission from Udelsman (55). Copyright 2002, Lippincott Williams & Wilkins.) Journal of Clinical Densitometry: Assessment of Skeletal Health

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58 the recurrent laryngeal nerve (52,53). Before all parathyroid surgeries, but especially before reoperation, familial forms of PHPT must be ruled out including multiple endocrine neoplasia 1 and other rare hereditary disorders, such as benign familial hypocalciuric hypercalcemia. Moreover, a meticulous preoperative workup including sestamibi scanning, US, 4DCT, and selective use of venous sampling enhances the chances of surgical success and can guide the surgeon to the site of surgical exploration (3,54). In conclusion, parathyroidectomy is the optimal treatment of PHPT and can cure disease in the vast majority of patients. Patients with overt signs and symptoms of PHPT including neurocognitive changes will in almost all cases benefit from parathyroidectomy. With the advent of significant advances in imaging technology and availability of IOPTH assays, MIP has become the procedure of choice for PHPT at specialized high-volume centers. Both MIP and conventional bilateral cervical neck exploration demonstrate exceptionally high cure rates, whereas the advantages of MIP include decreased complication rates, improved cosmetic results secondary to smaller incisions, and overall decreased cost and length of hospital stay. For the surgeon, conversion from MIP to bilateral exploration is always an option. Regardless of the technique used, surgeon experience is paramount in obtainment of excellent results.

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