TUMOR-INDUCED OSTEOMALACIA DUE TO HITHERTO UNDIAGNOSED SUBCUTANEOUS PHOSPHATURIC MESENCHYMAL TUMOR
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1 Case Report TUMOR-INDUCED OSTEOMALACIA DUE TO HITHERTO UNDIAGNOSED SUBCUTANEOUS PHOSPHATURIC MESENCHYMAL TUMOR Raiz Ahmad Misgar, MBBS, MD, DM 1 ; Danendra Sahu, MBBS, MD 1 ; Ashish Sehgal, MBBS, MD 1 ; Sajad Ahmad Malik, MBBS, MD 1 ; Mir Mohsin, MBBS, MS, MCh 2 ; Arshad Iqbal Wani, MBBS, MD 1 ; Mir Iftikhar Bashir, MBBS, MD 1 ; Shariq Rashid Masoodi, MBBS, MD, DM 1 ABSTRACT Objective: Tumor-induced osteomalacia (TIO) is a rare paraneoplastic syndrome caused by endocrine tumors that secrete fibroblast growth factor 23 (FGF-23), a phosphaturic hormone. Mesenchymal tumors causing TIO are usually deep seated and difficult to localize. We report a case of hitherto undiagnosed TIO because of an easily palpable unsuspecting cystic lesion in the right scapular region. Methods: The clinical, biochemical, and radiologic evaluation of a 50-year-old woman with TIO are presented. Results: A 50-year-old woman presented with a 2-year history of progressive fatigue, musculoskeletal pain, and muscle weakness. Despite multiple consultations, she remained undiagnosed. Our evaluation revealed low serum phosphorus, renal phosphate wasting, and elevated FGF-23 levels, suggesting a diagnosis of TIO. Clinical examination revealed an easily palpable soft and cystic swelling cm in right scapular region. A whole-body scintigraphy with Ga-68 DOTATATE positron emission tomography/ computed tomography revealed a mild tracer-avid heterogeneously enhancing well-defined subcutaneous nodule in right scapular region measuring cm. The histopathologic features of the excised tumor were compatible Submitted for publication October 24, 2017 Accepted for publication October 29, 2017 From the 1 Department of Endocrinology, and 2 Department of Plastic Surgery, Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India. Address correspondence to Dr. Raiz Ahmad Misgar, Department of Endocrinology, Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India. drreyaz07@rediffmail.com. DOI: /ACCR To purchase reprints of this article, please visit: with a phosphaturic mesenchymal tumor. Serum phosphorus normalized on the third postoperative day and resulted in dramatic and remarkable clinical improvement. Conclusion: TIO is a rare paraneoplastic syndrome which should be included in the differential diagnosis in patients with muscle weakness and musculoskeletal pain. Although the most challenging part in the management of these patients is the localization of the causative tumors, very rarely, the tumors can be clinically apparent. Excision of the tumor is curative. (AACE Clinical Case Rep. 2018;4:e240-e244) Abbreviations: 1,25(OH) 2 = 1,25-dihydroxyvitamin ; ALP = alkaline phosphatase; CT = computed tomography; DOTATATE = 1,4,7,10-tetraazacyclododecane 1,4,7,10-tetraacetic acid tyrosine-3-octreotate; FDG = fluorodeoxyglucose; FGF-23 = fibroblast growth factor 23; ipth = intact parathormone; PET = positron emission tomography; TIO = tumor-induced osteomalacia INTRODUCTION Tumor-induced osteomalacia (TIO) is an acquired debilitating osteomalacia characterized by severe hypophosphatemia, renal phosphate wasting, low circulating 1,25-dihydroxyvitamin (1,25[OH] 2 ) concentrations, and elevated serum fibroblast growth factor 23 (FGF-23) concentrations (1). The typical clinical and biochemical phenotype of TIO is similar to that of X-linked hypophosphatemia, the prototypic hypoposphatemic disorder, but the severity of the abnormality is often greater in TIO (2). TIO is usually caused by benign and often difficult to locate mesenchymal tumors, which may occur anywhere in the body (3). More than 80% of these tumors are the classic phosphaturic mesenchymal tumor mixed connec- e240 AACE CLINICAL CASE REPORTS Vol 4 No. 3 May/June 2018
2 Tumor-Induced Osteomalacia, AACE Clinical Case Rep. 2018;4(No. 3) e241 tive tissue (PMTMCT) variants (3). Since the description of the first case by McCance et al seven decades ago, more than 300 cases have been reported in the literature (4,5). We present here case summary of a 50-year-old female who presented with 2-year history of debilitating osteomalacia induced by a subcutaneous phosphaturic mesenchymal tumor. Surgical excision of the tumor led to complete resolution of biochemical abnormalities and a striking clinical improvement. CASE REPORT A previously well 50-year-old female presented to the endocrine center at Sher-i-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India, in August 2016 with a 2-year history of progressive fatigue, generalized severe musculoskeletal pain, and muscle weakness. Due to progressive worsening, she had been unable to walk unassisted and carry on activities of daily living for last 6 months. There was no history of previous malignancy, fractures, or joint stiffness. The relentless progression of her symptoms made her consult three orthopedic surgeons and two primary care physicians, who checked her chemistry panel, which included serum calcium, intact parathormone (ipth), alkaline phosphatase (ALP), 25-hydroxyvitamin D (25-OHD), and renal and liver function tests. Except elevated ALP, all these tests were found to be normal on multiple occasions. The treating orthopedic surgeon also advised 99 Tc methylene diphosphonate whole-body bone scintigraphy, which she underwent twice in view of suspicion of metastatic bone disease. The bone scan revealed multiple foci of increased trace uptake in the bilateral ribs, femora, and lower end of the right tibia. These scans also did not aid in establishing a diagnosis. Serum phosphate was, however, never tested. She was prescribed analgesics, oral and injectable cholecalciferol, multivitamins, and calcitonin nasal spray without any relief. On reporting to us, she could walk only with support. We undertook a detailed history. The onset of symptoms was clearly 2 years previously, and she did not recall any bone disease during her childhood. There was no consanguinity of marriage among her parents and no family history of metabolic bone disease. She had not taken any drugs known to cause osteomalacia or tubulopathy in the preceding 2 years. Clinical examination revealed proximal myopathy, while there was no bone or joint deformity. Dental exam was unremarkable. Her body mass index was kg/m 2. Investigations in our center revealed severe hypophosphatemia (serum phosphate, 0.77 mg/dl and 0.68 mg/ dl; normal range, 2.5 to 4.5 mg/dl) and elevated serum ALP of 202 IU/L (normal range, 30 to 140 IU/L), while serum ph, electrolytes, calcium, creatinine, ipth, and 25-OHD were normal. Further, for investigating hypophosphatemia, we evaluated renal phosphate handling by calculating tubular maximum for phosphate corrected for glomerular filtration rate (TmP/GFR). This was done by testing second morning void urine and a concomitant blood sample and was found to be very low at 0.53 mg/ dl (normal range for age-matched women is 2.72 to 4.39 mg/dl). There was no glycosuria or aminoaciduria. Renal phosphate loss was thus confirmed as a cause of hypophosphatemia, and plasma C-terminal FGF-23 estimation was requested. It was measured by enzyme-linked immunosorbent assay (Immutopics, San Clemente, CA) and found to be elevated more than 2-fold at 347 RU/mL (range, 0.00 to 150 RU/mL). Diagnosis of FGF-23 dependent hypophosphatemia was hence made. Since there was no family history of metabolic disease and age of first presentation of the index patient was 48 years, we narrowed the diagnosis to possible TIO and performed a detailed head-tofoot physical examination. A nontender, soft, and cystic swelling measuring cm was palpable in the right scapular region. On enquiry, the patient had noticed this swelling 15 years back, and for the last 3 years it was increasing in size. Next, functional whole-body imaging was performed with Ga-68 1,4,7,10-tetraazacyclododecane-1,4,7,10- tetraacetic acid tyrosine-3-octreotate (DOTATATE) positron emission tomography (PET)/computed tomography (CT), which revealed a mild tracer-avid, heterogeneously enhancing, well-defined subcutaneous nodule in the right scapular region, measuring cm (Fig. 1 A). It was also remarkable for faint nontracer-avid cortical breaks/ lucencies in multiple bones, representing pseudo-fractures. So, it could now be interpreted that the multiple foci of increased tracer uptake in the bilateral ribs, bilateral femoral bones, and lower end of the right tibia on earlier bone scans were either fractures or underlying extensive osteomalacia. Before attempting surgical excision of this lesion, an anatomic imaging in the form of a CT scan was also performed, which showed a subcutaneous lesion with softtissue attenuation, measuring cm in the same right scapular region (Fig. 1 B). The cystic swelling was easily amenable to surgical excision under local anesthesia. So, fine-needle aspiration was not performed, and it was decided to directly proceed with the excision, following which, there was dramatic clinical improvement. On the third postoperative day, serum phosphate and serum FGF-23 concentrations normalized to 3.6 mg/dl and 52 RU/mL, respectively, and musculoskeletal pain first started to abate. In the next 2 weeks, the patient was able to walk and carry on activities of daily living without support. Microscopy of the excised specimen revealed a tumor comprising proliferation of bland spindle cells with hemangiopericytomatous vessels, ectactic vascular channels, and prominent areas of metaplastic bone formation (Fig. 2 A and B). On followup, she remains well and asymptomatic and is not on any medication.
3 e242 Tumor-Induced Osteomalacia, AACE Clinical Case Rep. 2018;4(No. 3) A B Fig. 1. (A) Gallium-68 1,4,7,10-tetraazacyclododecane 1,4,7,10-tetraacetic acid tyrosine-3-octreotate positron emission tomography/computed tomography showing a mild tracer-avid heterogeneously enhancing, well-defined subcutaneous nodule (arrow) in the right scapular region. (B) Computed tomography showing a subcutaneous lesion (arrow) with soft-tissue attenuation, measuring cm in the right scapular region. A B Fig. 2. Paraffin-embedded section of phosphaturic mesenchymal tumor showing bland spindle cells with hemangiopericytomatous vessels (horizontal arrow), ectactic vascular channels, and prominent metaplastic bone formation (vertical arrow). (A, hematoxylin & eosin, 40 ; B, hematoxylin & eosin 10 ). DISCUSSION The diagnosis of TIO is frequently delayed, and patients remain symptomatic for many years before being correctly diagnosed and treated. Reasons for this delay include rarity of this disease and the nonspecific nature of symptoms. Many reported cases of this disorder have been marked by consultations with numerous health care providers, prolonged morbidity and debility, and a diagnostic delay ranging from 3 to 12 years (6). Our patient also remained undiagnosed for 2 years, when simple serum phosphate estimation could have prompted the diagnosis much earlier. She did not have any bone disease during her childhood. This, however, does not rule out all inborn errors of calcium metabolism. An uncommon autosomal recessive disorder termed hereditary hypophosphatemic rickets with hypercalciuria (HHRH) can have a late onset of clinical and/or biochemical abnormalities (7). In this disorder, there is renal phosphate wasting due to a defect in sodiumdependent phosphate cotransporter 2c, with consequent hypophosphatemia. Suppressed FGF-23 in HHRH, however, distinguishes it from TIO, where it is characteristically elevated and responsible for phosphaturia (7). The biochemical hallmarks of TIO include hypophosphatemia, reduced TmP/GFR, elevated serum ALP, low or inappropriately decreased 1,25(OH) 2, increased serum concentrations of FGF-23, and normal serum levels of calcium and ipth (1,8). In one study, all 13 patients with confirmed phosphaturic tumors had elevated serum FGF-23 concentration (8). Our patient also had more than 2-fold elevation of FGF-23. The actions of this hormone are many. First, it inhibits sodium-phosphate cotransporters 2a and 2c located in the proximal tubules of the kidneys and brings about a strong phosphaturic effect (9). Second, it inhibits renal CYP27B1, which is responsible for synthesis of 1,25(OH) 2, the active form of vitamin D. Finally, it stimulates CYP24A1, an enzyme that mediates degrada-
4 Tumor-Induced Osteomalacia, AACE Clinical Case Rep. 2018;4(No. 3) e243 tion of 1,25(OH) 2. FGF-23 excess is thus associated with the unusual combination of low serum 1,25(OH) 2 and hypophosphatemia. The latter is otherwise a known potent stimulus for inducing renal CYP27B1 and thus expected to elevate serum 1,25(OH) 2 concentrations (1). Hence, an inappropriately low serum 1,25(OH) 2 concentration in the setting of hypophosphatemia and elevated FGF-23 is diagnostic for TIO. The most challenging part in the management of these patients is the localization of the causative tumors, since they are often small in size, slow growing, and can occur anywhere in the body. Rarely, these tumors can be located subcutaneously, palpable on physical examination, and easily amenable to surgical excision (4,10-12). For localization, functional imaging should be done first, followed by anatomic imaging by CT or magnetic resonance imaging to delineate the relationship of the tumor to local anatomic structures before surgical excision is contemplated (13). Functional imaging modalities that have been used include somatostatin receptor scintigraphy and fluorodeoxyglucose (FDG) PET (14,15). FDG PET is sensitive for localizing phosphaturic tumors, but it is nonspecific, as it also identifies areas of increased metabolic activity such as actively healing fracture sites (4). Most of these tumors express somatostatin receptors, and hence, somatostatin receptor scintigraphy has been proposed as a valuable option in imaging of these tumors (16). Octreotide scintigraphy is successfully used to locate tumors in up to 95% of patients with TIO (17). The utility of Ga-68 DOTATATE PET/CT in the diagnosis of TIO has been well established and proposed as a practical first step in functional imaging for this disorder (18). A recent study revealed that Ga-68 DOTATATE PET/CT had greater sensitivity and specificity for TIO localization than either Octreoscan single-photon emission computed tomography (SPECT)/CT or FDG PET/CT (19). In our case, whole-body scintigraphy with Ga-68 DOTATATE PET/CT revealed the culprit tumor. However, in institutions where this facility is not available, confirming the area of uptake documented on Octreoscan SPECT/CT by FDG PET significantly improves the ability to localize phosphaturic tumors and can hence be useful (4). Most tumors causing TIO are mesenchymal in origin. The most common pathologic diagnosis for these tumors has been hemangiopericytoma followed by hemangioma, sarcomas, ossifying fibromas, granulomas, giant cell tumors, and osteoblastomas (3). More than 70 to 80% of mesenchymal tumors causing TIO share a distinct histologic appearance, consistent with that of a PMTMCT variant (3). These tumors are composed of primitive stromal cells, prominent blood vessels, and osteoclast-like giant cells (3). Histopathology of excised tumor in our patient also revealed bland spindle cells with hemangiopericytomatous vessels, ectactic vascular channels, and prominent areas of metaplastic bone formation. The treatment of choice for TIO is resection of the tumor, which results in prompt and complete resolution of long-standing symptoms. It also abates the biochemical abnormalities of TIO, and remineralization of the skeleton follows (1). This prompt and complete reversal of the debilitating symptoms is unmatched in the treatment of metabolic diseases. In our patient, removal of the tumor was associated with rapid clinical and biochemical improvement as early as the third postoperative day. FGF-23 is known to disappear rapidly from the circulation, and serum phosphate returns to normal by day 5 postoperatively (20). Serum phosphate normalized on the third postoperative day in the index patient. Remineralization of bones starts immediately, but, depending on the severity of the disease, it may take up to a year for a significant improvement to be seen. When the tumor cannot be localized or there is relapse after resection, medical treatment with oral phosphate and calcitriol helps to ameliorate the symptoms and biochemical abnormalities (1). Further, an anti FGF-23 antibody is currently in clinical trials for medical management of TIO and may offer a nonsurgical option in the future. Single injection of this antibody has been shown to be safe and effective in another FGF-23 related hypophosphatemic disorder, X-linked hypophosphatemic rickets (21). CONCLUSION In conclusion, TIO should be included in the differential diagnosis in patients presenting with muscle weakness and musculoskeletal pain, and determination of serum phosphorus levels in blood chemistry testing should be done in these patients. Hypophosphatemia should prompt further evaluation in this regard. Utmost attempt should be made to localize and surgically resect the tumors causing TIO, since resection often leads to marked clinical and biochemical improvement. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Drezner MK. Tumor-induced osteomalacia. Rev Endocr Metab Disord. 2001;2: Carpenter TO. New perspectives on the biology and treatment of X-linked hypophosphatemic rickets. Pediatr Clin North Am. 1997;44: Folpe AL, Fanburg-Smith JC, Billings SD, et al. Most osteomalacia-associated mesenchymal tumors are a single histopathologic entity: an analysis of 32 cases and a comprehensive review of the literature. Am J Surg Pathol. 2004;28: Chong WH, Molinolo AA, Chen CC, Collins MT. Tumorinduced osteomalacia. Endocr Relat Cancer. 2011;18:R53-R McCance RA. Osteomalacia with Looser s nodes (Milkman s syndrome) due to a raised resistance to vitamin D acquired about the age of 15 years. Q J Med. 1947;16:33-46.
5 e244 Tumor-Induced Osteomalacia, AACE Clinical Case Rep. 2018;4(No. 3) 6. Clunie GP, Fox PE, Stamp TC. Four cases of acquired hypophosphataemic ( oncogenic ) osteomalacia. Problems of diagnosis, treatment and long-term management. Rheumatology (Oxford). 2000;39: Dhir G, Li D, Hakonarson H, Levine MA. Late-onset hereditary hypophosphatemic rickets with hypercalciuria (HHRH) due to mutation of SLC34A3/NPT2c. Bone. 2017;97: Imel EA, Peacock M, Pitukcheewanont P, et al. Sensitivity of fibroblast growth factor 23 measurements in tumor-induced osteomalacia. J Clin Endocrinol Metab. 2006;91: Ramon I, Kleynen P, Body JJ, Karmali R. Fibroblast growth factor 23 and its role in phosphate homeostasis. Eur J Endocrinol. 2010;162: Oka M, Kamo T, Sasaki E, et al. A case of phosphaturic mesenchymal tumour (mixed connective tissue variant) that developed in the subcutaneous tissue of a patient with oncogenic osteomalacia and produced fibroblast growth factor 23. Br J Dermatol. 2007;157: Ogura E, Kageyama K, Fukumoto S, et al. Development of tumor-induced osteomalacia in a subcutaneous tumor, defined by venous blood sampling of fibroblast growth factor-23. Intern Med (Tokyo). 2008;47: DeWitt CA, Collins MT, Cowen EW. Diffuse pain, hypophosphatemia, and a subcutaneous nodule. J Am Acad Dermatol. 2007;57: Fukumoto S, Takeuchi Y, Nagano A, Fujita T. Diagnostic utility of magnetic resonance imaging skeletal survey in a patient with oncogenic osteomalacia. Bone. 1999;25: Dupond JL, Mahammedi H, Prié D, et al. Oncogenic osteomalacia: diagnostic importance of fibroblast growth factor 23 and F-18 fluorodeoxyglucose PET/CT scan for the diagnosis and follow-up in one case. Bone. 2005;36: Jan de Beur SM, Streeten EA, Civelek AC, et al. Localisation of mesenchymal tumours by somatostatin receptor imaging. Lancet. 2002;359: Duet M, Kerkeni S, Sfar R, Bazille C, Lioté F, Orcel P. Clinical impact of somatostatin receptor scintigraphy in the management of tumor-induced osteomalacia. Clin Nucl Med. 2008;33: Jiang Y, Xia WB, Xing XP, et al. Tumor-induced osteomalacia: an important cause of adult-onset hypophosphatemic osteomalacia in China: report of 39 cases and review of the literature. J Bone Miner Res. 2012;27: Clifton-Bligh RJ, Hofman MS, Duncan E, et al. Improving diagnosis of tumor-induced osteomalacia with Gallium-68 DOTATATE PET/CT. J Clin Endocrinol Metab. 2013;98: El-Maouche D, Sadowski SM, Papadakis GZ, et al. 68Ga-DOTATATE for tumor localization in tumor-induced osteomalacia. J Clin Endocrinol Metab. 2016;101: Khosravi A, Cutler CM, Kelly MH, et al. Determination of the elimination half-life of fibroblast growth factor-23. J Clin Endocrinol Metab. 2007;92: Carpenter TO, Imel EA, Ruppe MD, et al. Randomized trial of the anti-fgf23 antibody KRN23 in X-linked hypophosphatemia. J Clin Invest. 2014;124:
Tarandeep Kaur MD, Eric T Rush MD, FAAP, FACMG, Rajib K Bhattacharya MD FACE. Running head: Phophaturic Mesenchymal Tumor Presenting as TIO
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