Persistent Hypercalcemia Despite Multiple Exploratory Neck Surgeries
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1 Persistent Hypercalcemia Despite Multiple Exploratory Neck Surgeries Gregory Cheeney 1 * and Dina N. Greene 1 CASE DESCRIPTION A 46-year-old woman with a complex history of primary hyperparathyroidism presented to the endocrinology clinic for persistent hypercalcemia despite 3 prior neck surgeries with removal of at least 2 parathyroid glands. She was originally diagnosed with primary hyperparathyroidism 27 years earlier at the age of 19 when she developed kidney stones. Since then, she has required intermittent laser lithotripsy with stone removal, eventually requiring a urethral stent placed 2 years before her current presentation. Her first surgery was in 2004 and documentation of this surgery was not available because it was performed at an outside institution. Her second surgery, in 2007, excised the right inferior parathyroid gland and pathologic assessment was consistent with hypercellular parathyroid tissue. In 2012, a 4-gland neck dissection was performed and a left superior parathyroid gland was identified and excised. No parathyroid tissue was identified on the right and no gland was identified in the left inferior aspect. Her intraoperative parathyroid hormone (iopth) 2 decreased from 495 to 258 pg/ml [reference interval (RI) pg/ml] after removal of the left superior parathyroid gland. Despite no residual parathyroid tissue identified at the time of surgery, her hypercalcemia and hyperparathyroidism persisted. Given her persistent increased serum PTH concentrations and her young age at initial presentation, the possibility of a genetic syndrome was evaluated. She denied symptoms of other endocrinopathies such as lactation, gastroesophageal reflux disease, or hypoglycemia, and her laboratory values were not suggestive of them: prolactin 19 ng/ml (RI for adult premenopausal female is <25 ng/ml), gastrin 62 pg/ml (RI 0 99 pg/ml for 8-h fast), and vitamin D (25-hydroxy) total 22.4 ng/ml (RI ng/ml). Genetic testing for MEN1 (menin 1), the most common hereditary cause of primary hyperparathyroidism, was negative (1). At the endocrinology visit, her serum PTH was increased at 148 pg/ml (RI pg/ml) and her calcium was 11.4 mg/dl (RI mg/dl). An ultrasound of the neck (Fig. 1) demonstrated a 1.4-cm soft tissue lesion in the left suprasternal notch with increased vascularity and heterogeneous echotexture. The ultrasound differential included a prominent lymph node and ectopic parathyroid adenoma. A fine needle aspiration (FNA) was performed; the aspirate was sent for cytological assessment, and a saline wash of the FNA needle was sent to the chemistry laboratory for PTH quantification. The FNA PTH wash had an intact PTH concentration of 2550 pg/ml (<100 1 Department of Laboratory Medicine, University of Washington School of Medicine, Seattle, WA. *Address correspondence to this author at: Department of Laboratory Medicine, University of Washington School of Medicine, 1959 NE Pacific St., Box , Seattle, WA Fax ; gcheeney@uw.edu. DOI: /jalm American Association for Clinical Chemistry 2 Nonstandard abbreviations: iopth, intraoperative parathyroid hormone; RI, reference interval; FNA, fine needle aspiration; IHC, immunohistochemical; PPV, positive predictive value. July : JALM 1 Copyright 2017 by American Association for Clinical Chemistry.
2 Persistent Hypercalcemia Despite Multiple Surgeries Fig. 1. Ultrasound image taken from the left suprasternal region demonstrates a 1.4-cm (note markers) soft tissue nodule (red arrow) with variable echotexture. pg/ml suggests non-pth secreting tissue) (2) with concomitant serum PTH of 153 pg/ml (12 88 pg/ml), and immunohistochemical (IHC) staining from the cytology aspirate cell block was consistent with parathyroid tissue (Fig. 2, B and C). Although she had already undergone 3 prior surgeries, she underwent a fourth surgery in 2015 for removal and pathologic assessment of the soft tissue lesion. DISCUSSION The signs and symptoms of hypercalcemia include increased micturition from increased urine calcium, nausea/vomiting, constipation, muscle and bone pain, and neurologic changes. Over time, hypercalcemia can lead to osteoporosis and nephrolithiasis. Primary hyperparathyroidism is the most common cause of hypercalcemia. PTH is produced by chief cells in the parathyroid gland in response to low ionized calcium. In hypercalcemia due to primary hyperparathyroidism, there is unregulated production of PTH leading to increased calcium and PTH concentrations. By contrast, secondary hypercalcemia due to malignancy or other causes will have decreased or low/normal concentrations of serum PTH (3). The quantification of intact serum PTH assists in the differential diagnosis of hypercalcemia. Intact PTH is an 84 amino acid polypeptide (approximately 9.43 kda) that undergoes peripheral proteolysis to several C-terminal fragments present in serum, ranging from 34 to 77 amino acids in length (4). The intact 84 amino acid peptide is the active hormone and has a relatively short half-life of <5 min. Intact PTH and its metabolites are cleared by the liver and kidneys (4, 5). In this case, intact PTH was measured in 3 different settings (serum PTH, iopth, and PTH from an FNA wash). In all measurements, the PTH value was detected using an automated 2-site immunoenzymatic sandwich chemiluminescence assay with detection by monoclonal anti-pth-alkaline phosphatase on a Beckman Coulter DXI instrument. This method is meant for the detection of intact PTH and is mostly specific to intact PTH with minimal cross-reactivity for the smaller PTH proteolytic byproducts. The largest byproduct, PTH 7-84, is the only proteolytic product with known significant and sizable cross-reactivity (4). Beckman Coulter reports a 72% cross-reactivity between PTH 7-84 and intact PTH for the automated intact PTH assay (6). The short half-life of intact PTH enables detection of changes in serum concentration within minutes after removal of a hyperfunctioning parathyroid gland. Using an intraoperative PTH assay allows for close monitoring of serum PTH concentration while the patient is in the operating room with results in <20 min. The main difference between the serum PTH and iopth assays is the shorter assay time in iopth to allow for faster reporting. The 2 assays have identical antibodies, buffers, and detection chemistries, but the iopth assay has decreased wash times, sacrificing lowend precision. This tradeoff is acceptable because the baseline iopth concentrations usually exceed the upper reference limit, and the surgeon expects 2 JALM :01 July 2017
3 Persistent Hypercalcemia Despite Multiple Surgeries CASE REPORT a 50% decrease from baseline to indicate successful parathyroid excision (7). During the patient's third surgery, her baseline PTH was 495 pg/ml, with a drop to 319 pg/ml 10 min after the apparent parathyroid tissue was excised, and then to 258 pg/ml before closing. Her iopth concentration did not decrease to within the normal serum range and only nearly decreased by 50% well into the surgery. There are several iopthmonitoring protocols, including the Miami criterion protocol, which is a 50% decline after 10 min, and the dual criteria protocol, which is a 50% decline after 10 min and a return to normal PTH concentration, with further testing at 20 min if testing fails to meet both criteria. There are other monitoring protocols such as the Mayo protocol, which tests at baseline, 5, and 10 min after excision, with similar criteria to the dual protocol (8). The patient had a negative iopth result during the third surgery, since she did not have a decrease in iopth by 50% at 10 min nor did she return to a PTH concentration within the RI. The third surgery was stopped, however, since an exhaustive bilateral neck dissection did not reveal any additional parathyroid tissue. After the third surgery, during the evaluation of the left suprasternal nodule, an FNA was performed with the aspirate sent for cytological evaluation and a needle wash sent for PTH concentration. Thyroid and parathyroid epithelial cells cannot be distinguished on standard cytology smears. If enough cellular material is present in the aspirate, a cell block and IHC staining for parathyroid hormone and thyroid markers, such as thyroid transcription factor-1 (TTF-1), may be performed. However, there is often insufficient cellular material to perform a cell block; therefore, the PTH concentration from the FNA wash are used as a valuable surrogate. To collect a PTH wash after FNA, a small volume of normal saline is drawn into the needle to wash the needle after the aspirate has been expelled for cytology. In this case, 0.5 ml normal saline was drawn into the needle and then collected into a container. This was performed after each pass of the suprasternal nodule. The wash was refrigerated and immediately transported to the laboratory for intact PTH analysis. Saline washes are a nonstandard fluid; therefore, the individual laboratories must validate this matrix for PTH analysis using the serum mode of their immunochemistry analyzer. Generally, the serum PTH, and not the iopth, assay is used. Performing a parallel serum PTH analysis at the time of the FNA is important to minimize any interference by blood contamination that can conflate interpretation and also to provide a valid sample for comparison concentration. Any procedural related contamination is subsequently diluted; therefore, a PTH concentration in the wash greater than the serum concentration may be interpreted as consistent with sampling parathyroid tissue during the FNA (9, 10). Some institutions use a defined cutoff of >100 pg/ml intact PTH to indicate the presence of parathyroid tissue. This cutoff is based on several reference studies (2, 11, 12). In this case, the FNA PTH wash concentration (2550 pg/ml PTH) was far greater than the serum PTH concentration of 153 pg/ml and the 100 pg/ml cutoff value. In addition, values over 1000 pg/ml have been shown to be consistent with parathyroid tissue sampling (13). Giusti et al. (2) compared the positive predictive value (PPV) and sensitivity of FNA PTH wash to Technetium ( 99m Tc) sestamibi (MIBI) scintigraphy in identifying parathyroid adenomas preoperatively. They found that relative to scintigraphy, which has a PPV of 71% and sensitivity of 69%, FNA wash PTH evaluation had a PPV of 94% and sensitivity of 83%. Given the very high concentration of PTH in the FNA wash, this FNA was interpreted by the clinical team as consistent with parathyroid tissue sampling. This patient had suffered from primary hyperparathyroidism for years despite multiple parathyroidectomy surgeries. In the vast majority of cases, primary hyperparathyroidism is due to a parathyroid adenoma. Persistent increased PTH despite July : JALM 3
4 Persistent Hypercalcemia Despite Multiple Surgeries Fig. 2. Suprasternal nodule aspirate and excision. (A), Hematoxylin and eosin stained cell block from soft tissue nodule aspirate. The aspirated material is variably cellular with bland appearing epithelial cells. (B), Cell block with IHC staining for parathyroid hormone (clone 105G7, Leica Biosystems). The epithelial cells demonstrate positive staining, consistent with parathyroid origin. (C), Cell block with IHC staining for thyroid transcription factor 1 (code M3575, clone 8G7G3/1, Dako UK), a marker of thyroid origin. The epithelial cells are negative. (D), Photomicrograph of the soft tissue nodule demonstrates hypercellular tissue with loss of normal parathyroid gland architecture. IHC (not shown) was consistent with parathyroid tissue. parathyroidectomy is uncommon, with a success rate of over 95% with parathyroidectomy (14). After her third surgery, at which time a decrement of 50% iopth at 10 min was not achieved, a suprasternal nodule was discovered. Based on the ultrasound and FNA results, the immediate clinical concern was for ectopic parathyroid tissue as a cause of the refractory increased PTH. Indeed, in 6% 16% of cases of hyperfunctioning parathyroid gland, the gland is identified in an ectopic location (14). During embryonic development, the parathyroid glands migrate from the third and fourth pharyngeal pouches to a position posterior to the thyroid gland. Ectopic parathyroid glands are due to aberrant migration during this developmental stage. The typical location of ectopic parathyroid glands depends on whether the gland is inferior or superior. In this case, the ectopic parathyroid gland was from the left inferior aspect. The most common location for inferior ectopic glands is in the region of the thymus, consistent with the suprasternal location of this patient's ectopic gland (15). The patient underwent a fourth surgery to remove the suprasternal nodule. Her baseline intraoperative PTH concentration was 311 pg/ml. The operation was closed before results of the 5-min iopth were obtained, since the patient had already undergone an exhaustive bilateral neck dissection during her third surgery. Final pathology on the 4 JALM :01 July 2017
5 Persistent Hypercalcemia Despite Multiple Surgeries CASE REPORT nodule showed parathyroid chief cell hyperplasia consistent with sporadic primary multiglandular parathyroid hyperplasia (Fig. 2D). Approximately 6 months after her fourth surgery, her PTH concentration improved but remained increased at 113 pg/ml (12 88 pg/ml), and her calcium concentration normalized with cinacalcet (Sensipar) treatment to 9.2 mg/dl ( mg/dl). The rate of recurrent primary hyperparathyroidism despite surgical management is about 5% (16). Although still classified as recurrent primary hyperparathyroidism, given her healthy renal function and persistent mildly increased PTH, her calcium concentration was controllable with medication after removal of the ectopic parathyroid tissue. This result underscores the importance of assessing for ectopic parathyroid tissue in patients with a diagnosis of recurrent primary hyperthyroidism and the integral role of laboratory PTH measurements in diagnosis and treatment. TAKEAWAYS The most common cause of primary hyperparathyroidism is a parathyroid adenoma. Presurgical techniques (including ultrasound, FNA, and FNA PTH wash) play an important role in assessing possible parathyroid adenomas. Ectopic parathyroid adenoma is a possible cause of refractory primary parathyroid. Intraoperative PTH and nonstandard uses of PTH assays have clinical utility in standard and complex hyperparathyroidism cases. Proper sample collection and laboratory result interpretation are keys to guiding clinical interpretation. Author Contributions: All authors confirmed they have contributed to the intellectual content of this paper and have met the following 4 requirements: (a) significant contributions to the conception and design, acquisition of data, or analysis and interpretation of data; (b) drafting or revising the article for intellectual content; (c) final approval of the published article; and (d) agreement to be accountable for all aspects of the article thus ensuring that questions related to the accuracy or integrity of any part of the article are appropriately investigated and resolved. Authors Disclosures or Potential Conflicts of Interest: No authors declared any potential conflicts of interest. REFERENCES 1. Cundy T, Grey A, Reid I. Calcium, phosphate and magnesium. In: Marshall W, Lapsley M, Day A, Ayling R, editors. Clinical biochemistry metabolic and clinical aspects, 3rd ed. Churchill Livingstone Elsevier: London; Giusti M, Dolcino M, Vera L, Ghiara C, Massaro F, Fazzuoli L, et al. Institutional experience of PTH evaluation on fine-needle washing after aspiration biopsy to locate hyperfunctioning parathyroid tissue. J Zhejiang Univ Sci B 2009;10: Minisola S, Pepe J, Piemonte S, Cipriani C. The diagnosis and management of hypercalcaemia. BMJ 2015;350:h Nguyen-Yamamoto L, Rousseau L, Brossard JH, Lepage R, Gao P, Cantor Y, D'amour P. Origin of parathyroid hormone (PTH) fragments detected by intact-pth assays. Eur J Endocrinol 2002;147: MacKenzie-Feder J, Sirrs S, Anderson D, Sharif J, Khan A. Primary hyperparathyroidism: an overview. Int J Endocrinol 2011;2011: Access Immunoassay Systems. Intact PTH [package insert]. Fullerton (CA): Beckman Coulter; Chiu B, Sturgeon C, Angelos P. Which intraoperative parathyroid hormone assay criterion best predicts operative success? A study of 352 consecutive patients. Arch Surg 2006;141:483 7; discussion Richards ML, Thompson GB, Farley DR, Grant CS. An optimal algorithm for intraoperative parathyroid hormone monitoring. Arch Surg 2011;146: Erbil Y, Salmaslioğlu A, Kabul E, Is sever H, Tunaci M, Adalet I, et al. Use of preoperative parathyroid fineneedle aspiration and parathormone assay in the July : JALM 5
6 Persistent Hypercalcemia Despite Multiple Surgeries primary hyperparathyroidism with concomitant thyroid nodules. Am J Surg 2007;193: Marcocci C, Mazzeo S, Bruno-Bossio G, Picone A, Vignali E, Ciampi M, et al. Preoperative localization of suspicious parathyroid adenomas by assay of parathyroid hormone in needle aspirates. Eur J Endocrinol 1998;139: Kiblut NK, Cussac JF, Soudan B, Farrell SG, Armstrong JA, Arnalsteen L, et al. Fine needle aspiration and intraparathyroid intact parathyroid hormone measurement for reoperative parathyroid surgery. World J Surg 2004;28: Ketha H, Lasho MA, Algeciras-Schimnich A. Analytical and clinical validation of parathyroid hormone (PTH) measurement in fine-needle aspiration biopsy (FNAB) washings. Clin Biochem 2016;49: Maser C, Donovan P, Santos F, Donabedian R, Rinder C, Scoutt L, Udelsman R. Sonographically guided fine needle aspiration with rapid parathyroid hormone assay. Ann Surg Oncol 2006;13: Roy M, Mazeh H, Chen H, Sippel RS. Incidence and localization of ectopic parathyroid adenomas in previously unexplored patients. World J Surg 2013;37: Noussios G, Anagnostis P, Natsis K. Ectopic parathyroid glands and their anatomical, clinical and surgical implications. Exp Clin Endocrinol Diabetes 2012;120: Hedback G, Oden A. Recurrence of hyperparathyroidism; a long-term follow-up after surgery for primary hyperparathyroidism. Eur J Endocrinol 2003;148: JALM :01 July 2017
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