A CASE OF TUMOR-INDUCED OSTEOMALACIA ASSOCIATED WITH AN ORGANIZING HEMATOMA
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1 Case Report A CASE OF TUMOR-INDUCED OSTEOMALACIA ASSOCIATED WITH AN ORGANIZING HEMATOMA Seong Hee Ahn, MD, PhD 1 ; Yong-Koo Park, MD, PhD 2 ; In Suh Park, MD, PhD 3 ; Jinseong Kye, MD 4 ; Woo Young Choi, MD 1 ; Da Hea Seo, MD 1 ; So Hun Kim, MD, PhD 1 ; Moon-Suk Nam, MD, PhD 1 ; Seongbin Hong, MD, PhD 1 ABSTRACT Objective: Tumor-induced osteomalacia is a paraneoplastic syndrome characterized by renal phosphate wasting that results in hypophosphatemia and osteomalacia. Tumor-induced osteomalacia is typically associated with benign mesenchymal tumors arising in the bone and soft tissue. Here, we describe a case of tumor-induced osteomalacia associated with an organizing hematoma. Methods: Medical records were reviewed. Results: A 54-year-old, Asian woman presented with progressive pain in the thighs and pelvis for a year that eventually led to a waddling gait. Laboratory examinations showed hypophosphatemia, hyperphosphaturia, normocalcemia, elevated serum alkaline phosphatase levels, and decreased serum calcitriol levels. The patient s bone mineral density was low, and the bone scan showed increased uptake throughout the skeleton. A bone biopsy contained excessive osteoid. We found a palpable mass on her left flank, which had been detected 2 years previously after doing a hula hoop exercise. Computed tomography showed a heterogeneously enhanced, subcutaneous mass Submitted for publication March 13, 2017 Accepted for publication August 3, 2017 From the 1 Division of Endocrinology and Metabolism, Inha University Hospital, Inha University School of Medicine, Incheon, Republic of Korea, 2 Department of Pathology, Kyung Hee University Hospital, Kyung Hee University School of Medicine, Seoul, Republic of Korea, 3 Department of Pathology, Inha University Hospital, Inha University School of Medicine, Incheon, Republic of Korea, and 4 Department of Internal Medicine, Inha University School of Medicine, Incheon, Republic of Korea. Address correspondence to Dr. Seongbin Hong, Division of Endocrinology and Metabolism, Inha University Hospital, Inha University School of Medicine, 27, Inhang-ro, Jung-gu, Incheon 22332, Republic of Korea. sbhongmd@inha.ac.kr. DOI: /EP CR To purchase reprints of this article, please visit: in the left-lateral abdominal wall. We resected the mass and it was identified as a phosphaturic mesenchymal tumor with an organizing hematoma. After surgery, her serum phosphorus level returned to normal, and her thigh and pelvis pain improved. Conclusion: Since a hematoma-associated lesion can be a source of phosphaturic agents, any previous history of injuries should be carefully explored in suspected cases of tumor-induced osteomalacia. (AACE Clinical Case Rep. 2018;4:e157-e161) Abbreviations: PMT = phosphaturic mesenchymal tumor; TIO = tumor-induced osteomalacia INTRODUCTION Tumor-induced osteomalacia (TIO) is a rare, paraneoplastic syndrome characterized by renal phosphate wasting that leads to hypophosphatemia and osteomalacia (1). It is usually associated with benign mesenchymal tumors that secrete phosphaturic hormones (2). Patients affected by TIO present with progressive muscle and bone pain with multiple fractures, and their laboratory findings include hypophosphatemia with hyperphosphaturia, low to normal serum calcitriol (1α,25-dihydroxyvitamin D3) levels, and elevated serum alkaline phosphatase levels. These clinical and biochemical features are often severe since the benign characteristics of the associated tumors delay the diagnosis of TIO (3). However, once a causative tumor is resected, these abnormalities resolve rapidly. Therefore, it is important to make a timely diagnosis of TIO and to localize potential tumors when there is a patient suffering from acquired hypophosphatemic osteomalacia. Here, we reported a rare case of TIO that was easily treated by identifying an organizing hematoma as the disease cause. AACE CLINICAL CASE REPORTS Vol 4 No. 2 March/April 2018 e157
2 e158 TIO and Organizing Hematoma, AACE Clinical Case Rep. 2018;4(No. 2) CASE REPORT A 54-year-old, previously healthy, Asian woman was referred to our outpatient clinic for evaluation of muscle and bone pain with both hypophosphatemia and hyperphosphatasia. She had experienced progressive pain in the thighs and pelvis for a year, and eventually started to limp. She had a history of rib fractures 5 months prior to presentation. She reached menopause at the age of 50 and did not take any medicines that could affect bone metabolism. The patient s height was 149 cm and her weight was 62.3 kg with a body mass index of 28.1 kg/m 2. Laboratory studies showed hypophosphatemia (1.2 mg/ dl, normal range is 2.5 to 4.7 mg/dl), normocalcemia (8.5 mg/dl, normal range is 8.2 to 10.8 mg/dl), and an elevated serum alkaline phosphatase level (1374 IU/L, normal range is 103 to 335 IU/L). Serum levels of both calcitriol (13.2 pg/ml, normal range is 19.6 to 54.3 pg/ml) and calcifediol (25-hydroxyvitamin D3, 15.9 ng/ml, sufficient level is >30.0 ng/ml) levels were low. The parathyroid hormone level was mildly increased (90.4 pg/ml, normal range is 8.0 to 76.0 pg/ml). The patient s 24-h urine phosphorus excretion (641 mg/day, normal levels are >100 mg/day) was indicative of renal phosphate wasting, and the renal tubule phosphate reabsorption rate was decreased (61.7%, normal range is 95.0% under conditions of hypophosphatemia) as was the tubular maximum reabsorption of phosphate per glomerular filtration rate (0.740 mg/dl, normal range for a patient of this age (3) is to mg/dl). Renal and liver function tests were within normal limits. Dual energy X-ray absorptiometry was performed and the T-scores for the lumbar spine, femoral neck, and total hip were -3.1, -4.0, and -3.6, respectively. A bone scan showed multiple areas of increased uptake in the spine, ribs, pelvis, and tibias (Fig. 1 A). We conducted a biopsy of the iliac bone after administering oral tetracyclines twice at 2-week intervals. As expected, excessively demineralized bone tissues were observed (Fig. 1 C), and tetracycline double labels were rarely present. Bone histomorphometry also showed an increase in osteoid (Table 1). Taking the biochemical, imaging, and histologic findings into account, hypophosphatemic osteomalacia due to renal phosphate wasting was diagnosed with TIO strongly suspected. We found a palpable mass on the patient s left flank by performing a detailed physical examination. The mass was soft, movable, and not tender. She remembered that there was a bruise on her left flank after doing a hula hoop exercise 2 years prior. Although she had detected a mass under the bruise, it was not concerning to her since the mass caused no pain and its size did not change. Abdominal computed tomography showed a heterogeneously enhanced, solid mass measuring cm in the subcutaneous layer of the left-lateral abdominal wall (Fig. 2 A). Ultrasonography revealed a well-defined mass with increased vascularity (Fig. 2 B), and the needle biopsy specimen was mostly composed of hemosiderin pigment with extensive infarction, suggesting an organizing hematoma. We decided to surgically remove the mass since no other masses were detected. Finally, a cm solid mass above the external oblique muscle was excised, and it was grossly identified as a hemorrhagic mass surrounded by a capsule (Fig. 3 A). Microscopically the mass included a large portion of organizing hemorrhage with abundant hemosiderin pigment and intrinsic vasculature (Fig. 3 B and C). Interestingly, in the capsular portion of the mass, there were some foci that included spindled to stellate cells with a background of an unusually smudgy, basophilic matrix with calcifications (Fig. 3 B and D). The pathologic diagnosis was a phosphaturic mesenchymal tumor (PMT) (4) with an organizing hematoma. After the tumor was removed, the patient s serum phosphorus levels normalized (3.2 mg/dl) within 3 days. The A B C Fig. 1. Radiologic and histologic features of hypophosphatemic osteomalacia. Bone scans before (A) and 2 months after surgically removing an organizing hematoma (B). Increased uptake throughout the skeleton improved after surgery. Bone biopsy with Goldner s trichrome stain (C). Excessive osteoid or unmineralized bone matrix stains pink, while mineralized bone matrix stains green. The presence of excessive osteoid in this bone biopsy demonstrates severe osteomalacia.
3 TIO and Organizing Hematoma, AACE Clinical Case Rep. 2018;4(No. 2) e159 Table 1 Histomorphometric Assessment of the Patient s Iliac Bone Volume measurements Surface measurements TV (mm 2 ) BS (mm) BV (mm 2 ) OS (mm) Md.V (mm 2 ) 6.73 Ob.S (mm) 0.00 OV (mm 2 ) 6.63 ES (mm) 0.00 BV/TV (%) (23.9 ± 5.3) Oc.S (mm) 0.00 Md.V/BV (%) QS (mm) 6.85 Md.V/TV (%) (23.3 ± 5.4) BS/BV (mm 2 /mm 3 ) (15.9 ± 3.5) OV/BV (%) (2.42 ± 1.22) BS/TV (mm 2 /mm 3 ) 2.52 (3.63 ± 0.50) OV/TV (%) (0.55 ± 0.25) OS/BS (%) (24.9 ± 10.0) Trabecular measurements ES/BS (%) 0.00 (16.6 ± 5.6) Tb.Th (μm) (139 ± 28) QS/BS (%) 5.69 Tb.N (per mm) 1.26 (1.72 ± 0.23) Ob.S/BS (%) 0.00 (7.2 ± 4.1) Tb.Sp (μm) (452 ± 82) Oc.S/BS (%) 0.00 (1.09 ± 0.58) Thickness measurements Number measurements O.Th (μm) (6.4 ± 1.4) N.Ob/OS (per mm OS) 0.00 W.Th (μm) (41.4 ± 5.7) N.Oc/ES (per mm ES) 0.00 Reference values are in parentheses (mean ± SE) (15). Abbreviations: BS = bone surface; BV = bone volume; ES = eroded surface; Md.V = mineralized bone volume; N.Ob = osteoblast number; N.Oc = osteoclast number; O.Th = osteoid thickness; Ob.S = osteoblast surface; Oc.S = osteoclast surface; OS = osteoid surface; OV = osteoid volume; QS = quiescent surface; Tb.N = trabecular number; Tb.Sp = trabecular separation; Tb.Th = trabecular thickness; TV = tissue volume; W.Th = wall thickness. A B Fig. 2. Radiologic features of an organizing hematoma inducing TIO. Abdominal computed tomography showing a heterogeneously enhanced, subcutaneous mass in the left-lateral abdominal wall (A). Abdominal ultrasonography showing a hypervascular, soft-tissue mass in the subcutaneous layer (B).
4 e160 TIO and Organizing Hematoma, AACE Clinical Case Rep. 2018;4(No. 2) 24-h urine phosphorus excretion (276 mg/day) decreased, and the renal phosphate reabsorption rate increased (92.4%) as did the tubular maximum reabsorption of phosphate per glomerular filtration rate (5.013 mg/dl), indicating that the renal phosphate wasting had resolved. Her muscle and bone pain in the thighs and pelvis improved within a week after excision. At her 2-month follow-up, she no longer limped, and her bone scan showed interval improvements (Fig. 1 B). DISCUSSION We report a case of a 54-year-old, Asian woman presenting with acquired hypophosphatemic osteomalacia. By carefully examining the patient s whole body based on the medical history of a new lump, we identified a tumor with the distinguishing characteristics of an organizing hematoma. By verifying the resolution of hypophosphatemia and the improvement of symptoms within a couple of days after surgery, we concluded that the patient had suffered from TIO associated with an organizing hematoma. Hypophosphatemic osteomalacia due to renal phosphate wasting has a widely different range of causes including genetic diseases, excess production of phosphaturic hormones as in TIO, and primary renal transport defects such as in Fanconi syndrome (3). Among these, TIO is a rare, paraneoplastic disorder that presents with excessive urinary excretion of phosphate, diminished synthesis of calcitriol, and subsequent deterioration in bone metabolism. Previous studies have mostly reported the causative tumors to be benign mesenchymal tumors arising in the bone and soft tissues over the whole body (5). These benign tumors ironically delay the diagnosis of TIO since their small and slow-growing characteristics make localization difficult. Nevertheless, since resecting the tumor always brings about a dramatic resolution of the hypophosphatemic osteomalacia, efforts to identify the benign causative tumor are essential (1,3,6). Although many imaging modalities including computed tomography, magnetic Fig. 3. Gross and histologic features of an organizing hematoma inducing TIO. Photography of the excised mass from the abdominal wall (A). Histology of the resected mass includes a large portion of organizing hemorrhage (B, asterisk) with small foci of phosphaturic mesenchymal tumors (4) in the capsule (arrow) (hematoxylin and eosin stain; 40). In the organizing hemorrhagic portion, (C), hemosiderin pigments and abundant vasculature were observed (hematoxylin and eosin stain; 100). In the capsular portion, (D), spindled to stellate cells with smudgy, basophilic matrix were observed (hematoxylin and eosin stain; 100).
5 TIO and Organizing Hematoma, AACE Clinical Case Rep. 2018;4(No. 2) e161 resonance imaging, octreotide scintigraphy, and positron emission tomography have been introduced (7-9), the first and the most important step for locating tumors in TIO is always a detailed physical examination of the patient s whole body with a careful history of new lumps. In the present case, the patient s previous history of a bruise with a palpable mass in the same region allowed for easy identification of the TIO culprit. Fibroblast growth factor-23 is commonly the phosphaturic hormone overexpressed in TIO-inducing tumors (2). Recently, more compounds such as frizzled related protein-4, matrix extracellular phosphoglycoprotein, and fibroblast growth factor-7 have been identified as possible phosphaturic agents (10,11). Although measuring fibroblast growth factor-23 levels in plasma provides crucial information for the diagnosis of TIO, it could not be measured in our patient due to the inaccessibility of a fibroblast growth factor-23 test in Korea. However, the most definite way to confirm TIO is to identify normalization of hypophosphatemia by surgically removing suspected tumors, as described in this case. Interestingly, the tumor identified as the cause of TIO in this case did not show a typical histopathology of a PMT. PMTs are morphologically distinct entities found in about 70 to 80% of tumors associated with TIO. They are characterized by low to moderate proliferation of spindled to stellate cells, producing an unusually smudgy, basophilic matrix. Their matrix calcifies in a grungy or flocculent fashion that can resemble chondroid or osteoid (4,5). However, there have been almost no case reports of a PMT occurring in association with an organizing hematoma like in our patient. There was only one case of a 44-year-old black woman with acquired hypophosphatemia that dramatically resolved after excising an organizing hematoma from the hip (12). For these rare cases, there is a possibility that a PMT may develop from an organizing hematoma. The progress of our patient suggests this since she detected a palpable mass soon after a trauma and became symptomatic a year later. Also, the size of the mass remained unchanged until she became symptomatic. Moreover, a recent in vitro study reported hematomas containing progenitor cells with multilineage mesenchymal capacity (13). This suggests that hematoma-deriven progenitor cells may differentiate into mesenchymal tumors under certain circumstances such as increased inflammatory cytokine levels (13,14). Meanwhile, there is also a possibility that a very small, inactive PMT could become activated by an organizing hematoma that develops after trauma. However, regardless of all possible scenarios, it is notable that a suspicion of an organizing hematoma as the culprit of TIO prevented a delay in diagnosis and protected the patient from further deterioration. CONCLUSION We described a rare case of bone biopsy-confirmed hypophosphatemic osteomalacia that dramatically improved after resecting an organizing hematoma. Since a hematoma-associated lesion can be a source of phosphaturic agents, any history of injuries should be carefully explored in suspected cases of TIO. ACKNOWLEDGMENT This study was supported by a research grant from Inha University. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Jan de Beur SM. Tumor-induced osteomalacia. JAMA. 2005;294: Drezner MK. Tumor-induced osteomalacia. Rev Endocr Metab Disord. 2001;2: Chong WH, Molinolo AA, Chen CC, Collins MT. Tumorinduced osteomalacia. Endocr Relat Cancer. 2011;18:R53-R Goldblum JR, Weiss SW, Folpe AL. Enzinger and Weiss s Soft Tissue Tumors. 6th ed. Philadelphia, PA: Elsevier; 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: Hautmann AH, Hautmann MG, Kolbl O, Herr W, Fleck M. Tumor-induced osteomalacia: an up-to-date review. Curr Rheumatol Rep. 2015;17: Chong WH, Yavuz S, Patel SM, Chen CC, Collins MT. The importance of whole body imaging in tumor-induced osteomalacia. J Clin Endocrinol Metab. 2011;96: Malhotra G, Agrawal A, Jambhekar NA, et al. Interesting image. The search for primary tumor in a patient with oncogenic osteomalacia: F-18 FDG PET resolves the conundrum. Clin Nucl Med. 2010;35: 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: De Beur SM, Finnegan RB, Vassiliadis J, et al. Tumors associated with oncogenic osteomalacia express genes important in bone and mineral metabolism. J Bone Miner Res. 2002;17: White KE, Larsson TE, Econs MJ. The roles of specific genes implicated as circulating factors involved in normal and disordered phosphate homeostasis: frizzled related protein-4, matrix extracellular phosphoglycoprotein, and fibroblast growth factor 23. Endocr Rev. 2006;27: Colt E, Gopan T, Chong HS. Oncogenic osteomalacia cured by removal of an organized hematoma. Endocr Pract. 2005;11: Oe K, Miwa M, Sakai Y, Lee SY, Kuroda R, Kurosaka M. An in vitro study demonstrating that haematomas found at the site of human fractures contain progenitor cells with multilineage capacity. J Bone Joint Surg Br. 2007;89: Angele MK, Knoferi MW, Ayala A, et al. Trauma-hemorrhage delays wound healing potentially by increasing pro-inflammatory cytokines at the wound site. Surgery. 1999;126: Glorieux FH, Travers R, Taylor A, et al. Normative data for iliac bone histomorphometry in growing children. Bone. 2000;26:
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