SPONTANEOUS REMISSION OF PRIMARY HYPERPARATHYROIDISM RELATED TO AN AUTOIMMUNE DISEASE: A CASE REPORT
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1 Case Report SPONTANEOUS REMISSION OF PRIMARY HYPERPARATHYROIDISM RELATED TO AN AUTOIMMUNE DISEASE: A CASE REPORT Barbara C. Silva, MD, PhD; Jessica Fleischer, MD; Zachary Lenane, BS; Wen-Wei Fan, MPH; Donald J. McMahon, MS; John P. Bilezikian, MD ABSTRACT Objective: To report the unusual case of a woman with unequivocal primary hyperparathyroidism (PHPT) for 13 years who experienced spontaneous remission of her disease concomitant with the diagnosis of psoriatic arthritis. Methods: Clinical presentation, clinical course over 23 years of follow-up, and review of the pertinent literature are presented. Results: A 42-year-old woman was referred for evaluation of persistent hypercalcemia 2 months after unsuccessful parathyroid surgery for PHPT, in which a single, hyperplastic parathyroid gland was removed. Further evaluation confirmed persistent PHPT evidenced by hypercalcemia (12.1 mg/dl), elevated parathyroid hormone (PTH) level (118 pg/ml), normal calcium urinary excretion, and increased bone turnover markers. Persistent hypercalcemia and serum levels of PTH above normal were observed for 11 years after the parathyroid surgery. Thereafter, the patient experienced a downward trend and ultimate normalization of her serum calcium and PTH, which was associated, remarkably, with the development of psoriatic arthritis. Since return to normal of the serum calcium and PTH levels, the PHPT remission has persisted for 10 years without any signs of recurrent disease. Submitted for publication July 30, 2014 Accepted for publication December 23, 2014 From the Metabolic Bone Diseases Unit, Division of Endocrinology, Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, New York. Address correspondence to Dr. John P. Bilezikian, College of Physicians and Surgeons, 630 West 168th Street, New York, NY jpb2@columbia.edu. DOI: /EP14353.CR To purchase reprints of this article, please visit: Copyright 2015 AACE. Conclusion: Spontaneous remission of PHPT is exceedingly rare, and when it occurs, it is usually related to parathyroid hemorrhage or infarction. The patient s clinical course was not characteristic of parathyroid hemorrhage or infarction, and the concomitant appearance of psoriatic arthritis, an autoimmune disease, raises the possibility of an immune-mediated process explaining this outcome. (AACE Clinical Case Rep. 2015;1:e255-e259) Abbreviations: BMD = bone mineral density; CaSR = calcium-sensing receptor; NALP5 = NACHT leucine-rich-repeat protein 5; NSAIDS = nonsteroidal anti-inflammatory drugs; PHPT = primary hyperparathyroidism; PTH = parathyroid hormone INTRODUCTION Primary abnormalities of the parathyroid glands, associated with hypersecretion of parathyroid hormone (PTH), define the common endocrine disorder, primary hyperparathyroidism (PHPT). A solitary, benign parathyroid adenoma is found in approximately 80% of patients with PHPT (1). In patients who meet surgical criteria and agree to parathyroid surgery, a single parathyroid adenoma can be readily identified pre-operatively by a variety of imaging modalities, after which, minimally invasive parathyroid surgery with intra-operative PTH monitoring is associated with a >95% success rate (2). In patients who do not have parathyroid surgery, natural history studies have invariably shown that the disease persists and that complications can ensue (3). Spontaneous remissions are rare, but when they occur, they are usually due to infarction or hemorrhage into or around the hyperfunctioning parathyroid tissue (4-7). Another possible explanation for spontaneous remission of the disease AACE CLINICAL CASE REPORTS Vol 1 No. 4 Autumn 2015 e255
2 e256 Spontaneous Remission of PHPT, AACE Clinical Case Rep. 2015;1(No. 4) would be the development of anti-parathyroid antibodies (8). We report a patient who experienced spontaneous remission of PHPT 11 years after unsuccessful surgery in which 1 abnormal parathyroid gland was removed. The gradual, complete resolution of the hypercalcemia and return to normal of the elevated PTH level was associated with the development of psoriatic arthritis, an autoimmune disease, prompting the possibility that an autoimmune process could have been responsible for this permanent, nonsurgical cure of the disease. CASE REPORT A 42-year-old woman was referred for evaluation of persistent hypercalcemia 2 months after unsuccessful parathyroid surgery for PHPT. Her serum calcium and PTH prior to surgery were elevated, at 11.2 mg/dl (normal, 8.6 to 10.2 mg/dl) and 116 pg/ml (normal, 10 to 65 pg/ml), respectively. Serum phosphorus was 3.1 mg/dl (normal, 2.5 to 4.5 mg/dl), and the total alkaline phosphatase activity was normal, at 121 U/L. Bone mineral density (BMD) by dual energy X-ray absorptiometry showed T-scores of 3.0 at the lumbar spine, 2.2 at the femoral neck, and 1.2 at the distal one-third radius. A 0.8-cm lesion consistent with an enlarged parathyroid gland at the posterior right lobe of the thyroid was seen by magnetic resonance imaging. At the time of parathyroidectomy, the right superior parathyroid gland, weighing only 40 mg, was removed. The other 3 parathyroid glands were identified as normal, but they were not biopsied. Extensive exploration of the neck and the mediastinum did not reveal any other parathyroid tissue. Pathology confirmed the identity of a hyperplastic parathyroid gland. Serum calcium remained elevated, at 11.8 mg/dl, 24 hours after the surgery. When she was seen in our Metabolic Bone Diseases unit, noteworthy aspects of her medical review include a total abdominal hysterectomy and bilateral oophorectomy 2 years earlier for uterine leiomyoma and ovarian cancer, which was coincident with the diagnosis of hypercalcemia. Family history was positive for arthritis but negative for any disorders of calcium metabolism. Physical examination was unremarkable. Her medication included conjugated estrogen, 0.3 mg daily. Further evaluation confirmed persistent hypercalcemia (12.1 mg/dl) and an elevated PTH level (118 pg/ml). 25-hydroxyvitamin D level was 37 ng/ml (normal, 30 to 100 ng/ml), and her 1,25-dihydroxyvitamin D level was 83 pg/ml (normal, 15 to 65 pg/ml). Her 24-hour urine calcium excretion was 185 mg. Serum osteocalcin and urinary deoxypiridinoline were elevated, at 17.6 ng/ml (normal, 1.6 to 9.2 ng/ml) and 31.4 pmol/µmol creatinine (normal, 4 to 21 pmol/µmol creatinine), respectively. Serum albumin and hepatic and kidney function tests were normal. Further parathyroid surgery was not pursued, a decision made by the patient. During the first 11 years of her follow-up, she remained hypercalcemic, with serum calcium values ranging between 10.3 and 12.5 mg/dl. Serum PTH levels continued to be above normal, ranging from 63 to 125 pg/ ml (Fig. 1 A, B). During the first 5 years after surgery, the PTH level remained over 100 pg/ml, whereas the serum calcium showed a small decline. In July of 1997, 5 years after the parathyroidectomy, a serum PTH level of 76 pg/ ml was detected. This level was 3 SD below the mean of previous values and, thus, was considered to be statistically different from the previous PTH concentrations (9). From that point forward, PTH levels continued to trend downward. While still elevated, the serum calcium remained stable and the phosphorus followed an upward trend (Fig. 1 C). BMD was low but unchanged. In 1998, conjugated estrogens were replaced by raloxifene. She reported no neck trauma, further neck surgery, general anesthesia, nor any episodes of hypotension. In February of 2003, 11 years after surgery, normal levels of serum calcium and PTH were detected for the first time (Fig. 1 A, B). Concomitantly, serum phosphorus concentration followed an upward trend. During this period, the patient was still taking raloxifene, which was discontinued a few years later. The trend downward and ultimate normalization of the serum calcium and PTH was, remarkably, associated with the development of psoriatic arthritis. Symptoms of arthritis were first noted in 2001, when the patient started irregular use of nonsteroidal anti-inflammatory drugs (NSAIDs). In 2004, the psoriatic arthritis was evident by synovitis in multiple peripheral joints and contractures of the right elbow. The sedimentation rate was high, at 67 mm, and the C-reactive protein was 2.4 mg/l (normal range, <0.8 mg/l). She was treated with the tumor necrosis factor-alpha blocker, etanercept, and NSAIDs. The inflammatory signs improved, and her symptoms have been under control with a low dose of a NSAID. Since the patient was diagnosed with an autoimmune disease, we considered the possibility that the remission was due to the development of antibodies interfering with parathyroid gland function, but measurements of anti calcium-sensing receptor (CaSR) (10,11) and anti NACHT leucine-rich-repeat protein 5 (NALP5) (12) antibodies made, respectively, 5 and 10 years after the normalization of the PHPT, were negative. Since return to normal of the serum calcium and PTH levels, the PHPT remission has persisted for 10 years without any signs of recurrent disease. BMD could not be followed closely because the patient refused regular monitoring with 3-site measurements. During this period of time, the psoriatic arthritis has continued to require treatment for control. DISCUSSION We report the unusual case of a woman with unequivocal PHPT for 13 years who experienced a spontaneous remission
3 Spontaneous Remission of PHPT, AACE Clinical Case Rep. 2015;1(No. 4) e257 Fig. 1. Biochemical features over 23 years of follow-up. The patient s serum parathyroid hormone (A), calcium (B), and phosphorus (C) levels are shown over time, with shaded areas indicating the range of normal values. Traced lines indicate the time points in which parathyroidectomy was performed and the psoriatic arthritis was diagnosed. PTH = parathyroid hormone; PTX = parathyroidectomy.
4 e258 Spontaneous Remission of PHPT, AACE Clinical Case Rep. 2015;1(No. 4) 11 years after unsuccessful parathyroidectomy. Her serum calcium and PTH levels continued to be normal for as long as she has been followed, for another 10 years. The remission of PHPT was associated with the development of psoriatic arthritis, supporting the possibility that the cure of her PHPT was mediated by an autoimmune mechanism. Spontaneous remission of PHPT, which is exceedingly rare, is usually related to parathyroid hemorrhage or infarction. Neck swelling and tenderness often herald the event (4,5,13). In these situations, normalization of the serum calcium concentration is usually abrupt, and sometimes accompanied by symptoms of hypocalcemia (5,7,13). In the majority of cases of autoparathyroidectomy, the hemorrhage or infarction occurs in a parathyroid adenoma that typically is very large (4-7,13). Different from these reports, the patient that we report did not experience cervical pain or swelling, and the normalization of the serum calcium level was not abrupt. The clinical setting, therefore, makes autoparathyroidectomy due to hemorrhage or infarction a very unlikely cause for the spontaneous remission. The treatment with estrogen or raloxifene of postmenopausal women with PHPT can lead to a small decline or no change in serum calcium levels, to a reduction in bone turnover markers, and an improvement in BMD, without affecting PTH levels (14-16). In contrast, studies in animals and in vitro have shown that estrogens may decrease PTH levels, probably due to an upregulation of fibroblast growth factor 23 (17). In the case we report, the normalization of PTH and calcium serum levels did not coincide with the beginning of the estrogen replacement therapy. In fact, calcium and PTH became normal several years after the discontinuation of conjugated estrogens, while the patient was on raloxifene. Moreover, the remission of PHPT persisted even after the raloxifene was discontinued. These findings, along with the lack of evidence that estrogens and raloxifene reduce PTH in patients with PHPT, suggest that remission of PHPT in this case could not be due to estrogen or raloxifene. On the other hand, an autoimmune etiology for the spontaneous remission of PHPT becomes an intriguing possibility. Two cases of a lymphocytic infiltration that was suggestive of an autoimmune process and partial destruction of parathyroid adenomatous tissue have been previously described in patients with PHPT (8). Although these patients underwent parathyroidectomy while hypercalcemic, the authors speculated, based on the histopathologic findings, that cure of the PHPT could have occurred even if they had not had parathyroid surgery. Autoantibodies to parathyroid gland tissue were first reported in the 1960s (18). Autoimmune destruction of normal parathyroid glands is considered to be the second most common form of hypoparathyroidism in adults (19). The pathogenesis of autoimmune hypoparathyroidism comprises 2 basic mechanisms: one involving an autoimmune destructive process of the parathyroid cell caused by both humoral and cell-mediated mechanisms directed against the parathyroid cells, and another mechanism involving the presence of functional anti-parathyroid antibodies that modulate parathyroid function (20). Two parathyroid antigens, in particular, have been identified as targets for anti-parathyroid antibodies: the CaSR (10, 11) and the NALP5 (12). Anti-CaSR antibodies are usually functional and can lead to hypoparathyroidism by activating the CaSR, thereby inhibiting PTH synthesis and secretion (10,11,20). Anti-NALP5 antibodies, on the other hand, may trigger active cell-mediated immune responses, exerting cytotoxic effects on parathyroid cells (12). These mechanisms, however, have never been described in PHPT in the context of spontaneous remission of the disease. In the present case, an autoimmune destructive process of the parathyroid could explain the spontaneous remission of the PHPT. In support of this possibility, normalization of the serum calcium and PTH levels was associated with the development of psoriatic arthritis. However, anti-casr and -NALP5 antibodies could not be detected several years following the remission of the PHPT. CONCLUSION This unusual case of spontaneous remission of PHPT calls attention to a plausible mechanism for nonsurgical cure of this disease. The clinical course was not characteristic of parathyroid infarction or hemorrhage, and the development of psoriatic arthritis raises the possibility of an immune-mediated process explaining this outcome. Although anti-casr and -NALP5 antibodies were previously documented in patients with autoimmune processes involving the parathyroid gland, approximately 50% of these patients are not yet found to harbor anti-parathyroid antibodies. Further research is necessary to identify additional parathyroid antigens able to incite an autoimmune response against the parathyroid gland. ACKNOWLEDGMENT We thank Dr. Edward Brown from the Brigham and Women s Hospital, Harvard Medical School, for the measurement of the anti-casr antibody, and we thank Dr. Olle Kämpe and his coworkers at the Uppsala University, Sweden, for the measurement of the anti- NALP5 antibody. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Bilezikian JP, Brandi ML, Rubin M, Silverberg SJ. Primary hyperparathyroidism: new concepts in clinical,
5 Spontaneous Remission of PHPT, AACE Clinical Case Rep. 2015;1(No. 4) e259 densitometric and biochemical features. J Intern Med. 2005;257: Udelsman R, Lin Z, Donovan P. The superiority of minimally invasive parathyroidectomy based on 1650 consecutive patients with primary hyperparathyroidism. Ann Surg. 2011;253: Rubin MR, Bilezikian JP, McMahon DJ, et al. The natural history of primary hyperparathyroidism with or without parathyroid surgery after 15 years. J Clin Endocrinol Metab. 2008;93: Efremidou EI, Papageorgiou MS, Pavlidou E, Manolas KJ, Liratzopoulos N. Parathyroid apoplexy, the explanation of spontaneous remission of primary hyperparathyroidism: a case report. Cases J. 2009;2: Kataoka K, Taguchi M, Takeshita A, Miyakawa M, Takeuchi Y. Recurrence of primary hyperparathyroidism following spontaneous remission with intracapsular hemorrhage of a parathyroid adenoma. J Bone Miner Metab. 2008;26: Schinner S, Fritzen R, Schott M, Willenberg HS, Scherbaum WA. Spontaneous remission of primary hyperparathyroidism. Exp Clin Endocrinol Diabetes. 2007;115: Wootten CT, Orzeck EA. Spontaneous remission of primary hyperparathyroidism: a case report and meta-analysis of the literature. Head Neck. 2006;28: Veress B, Nordenström J. Lymphocytic infiltration and destruction of parathyroid adenomas: a possible tumourspecific autoimmune reaction in two cases of primary hyperparathyroidism. Histopathology. 1994;25: Nelson LS. The Shewhart control chart tests for special causes. J Qual Technol. 1984;16: Kemp EH, Gavalas NG, Krohn KJ, Brown EM, Watson PF, Weetman AP. Activating autoantibodies against the calcium-sensing receptor detected in two patients with autoimmune polyendocrine syndrome type 1. J Clin Endocrinol Metab. 2009;94: Kifor O, McElduff A, LeBoff MS, et al. Activating antibodies to the calcium-sensing receptor in two patients with autoimmune hypoparathyroidism. J Clin Endocrinol Metab. 2004;89: Alimohammadi M, Björklund P, Hallgren A, et al. Autoimmune polyendocrine syndrome type 1 and NALP5, a parathyroid autoantigen. N Engl J Med. 2008;358: Nylen E, Shah A, Hall J. Spontaneous remission of primary hyperparathyroidism from parathyroid apoplexy. J Clin Endocrinol Metab. 1996;81: Marcocci C, Bollerslev J, Khan AA, Shoback DM. Medical management of primary hyperparathyroidism: proceedings of the fourth International Workshop on the Management of Asymptomatic Primary Hyperparathyroidism. J Clin Endocrinol Metab. 2014;99: Selby PL, Peacock M. Ethinyl estradiol and norethindrone in the treatment of primary hyperparathyroidism in postmenopausal women. N Engl J Med. 1986;314: Rubin MR, Lee KH, McMahon DJ, Silverberg SJ. Raloxifene lowers serum calcium and markers of bone turnover in postmenopausal women with primary hyperparathyroidism. J Clin Endocrinol Metab. 2003;88: Carrillo-López N, Román-García P, Rodríguez-Rebollar A, Fernández-Martín JL, Naves-Díaz M, Cannata-Andía JB. Indirect regulation of PTH by estrogens may require FGF23. J Am Soc Nephrol. 2009;20: Blizzard RM, Chee D, Davis W. The incidence of parathyroid and other antibodies in the sera of patients with idiopathic hypoparathyroidism. Clin Exp Immunol. 1966;1: Bilezikian JP, Khan A, Potts JT Jr, et al. Hypoparathyroidism in the adult: epidemiology, diagnosis, pathophysiology, target-organ involvement, treatment, and challenges for future research. J Bone Miner Res. 2011;26: Husebye ES. Functional autoantibodies cause hypoparathyroidism. J Clin Endocrinol Metab. 2009;94:
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