Malignant Pleural Mesothelioma with Extensive Skeletal Muscle Metastasis

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1 台 灣 癌 症 醫 誌 (J. Cancer Res. Pract.) 1(2), , 2014 DOI: /JCRP Case Report journal homepage:www.cos.org.tw/web/index.asp Malignant Pleural Mesothelioma with Extensive Skeletal Muscle Metastasis Chia-Chun Chiang 1,3, Ming-Shu Hsieh 2, Dwan-Ying Chang 1 * 1 Departments of Oncology, National Taiwan University Hospital, Taipei, Taiwan 2 Departments of Pathology, National Taiwan University Hospital, Taipei, Taiwan 3 Department of Internal Medicine, Penghu General Hospital, Ministry of Health and Welfare, Executive Yuan, Penghu, Taiwan Abstract. We treated a 61-year-old man with malignant pleural mesothelioma complicated by extensive skeletal muscle metastases. The initial presentation included rapidly progressive weakness and stiffness in four extremities. The magnetic resonance image (MRI) and the computed tomography (CT) scan revealed disseminated symmetrical intramuscular nodular lesions. Excisional biopsy was taken and pathology confirmed the presence of a biphasic metastatic mesothelioma by immunohistochemical (IHC) staining. The patient survived for only 3 months from the onset of the symptoms despite of the administration of emergency chemotherapy and optimal supportive care. 病 例 報 告 Keywords : malignant pleural mesothelioma, skeletal muscle metastases, positron emission tomography 惡 性 間 皮 癌 病 患 併 瀰 漫 性 骨 骼 肌 肉 內 轉 移 江 佳 駿 1,3 謝 明 書 2 張 端 瑩 1 * 1 台 灣 大 學 附 設 醫 院 腫 瘤 醫 學 部 2 台 灣 大 學 附 設 醫 院 病 理 部 3 衛 生 福 利 部 澎 湖 醫 院 內 科 部 中 文 摘 要 我 們 報 告 一 位 61 歲 之 惡 性 間 皮 癌 病 人 併 發 瀰 漫 性 的 骨 骼 肌 肉 內 轉 移, 病 人 初 始 症 狀 為 肌 肉 僵 硬 及 無 力 磁 振 造 影 及 電 腦 斷 層 顯 示 為 數 眾 多 大 小 不 一 腫 瘤 分 布 於 全 身 的 骨 骼 肌 肉 內, 病 理 切 片 輔 助 螢 光 免 疫 染 色 法 證 實 為 轉 移 性 惡 性 間 皮 癌 病 人 病 況 迅 速 惡 化, 很 快 就 變 得 不 能 移 動 而 臥 床, 失 去 自 我 照 顧 能 力 且 併 發 肺 炎, 最 後 死 於 呼 吸 衰 竭 儘 管 接 受 了 化 學 治 療, 距 離 症 狀 開 始, 病 人 仍 只 存 活 了 三 個 月 我 們 探 討 此 案 例 骨 骼 肌 肉 內 轉 移 的 臨 床 表 現 及 意 義, 並 回 顧 了 過 往 間 皮 癌 病 人 骨 骼 肌 肉 內 轉 移 的 病 例 報 告 關 鍵 字 : 惡 性 間 質 瘤 骨 骼 肌 轉 移 正 子 攝 影

2 C. C. Chiang et al./jcrp 1(2014) INTRODUCTION Malignant mesothelioma is a neoplasm with very poor prognosis. It arises from mesothelial surfaces of the pleural cavity, peritoneal cavity, tunica vaginalis, or pericardium. Patients with malignant pleural mesothelioma typically present pulmonary symptoms. We are reporting on a 61-year-old man with malignant pleural mesothelioma with disseminated skeletal muscle metastases who initially presented with muscular A symptoms. CASE REPORT A 61-year-old man presented with a one-month history of rapidly progressive weakness and stiffness of the four extremities, and bilateral feet edema. He could not walk because of difficulties in bending his knees, nor could he fully stretch his elbows. He denied having a history of asbestos exposure. The physical findings were unrevealing except for diffuse muscle rigidity and limited range of motion. A soft tissue echo revealed diffuse ill-defined hypodense intramuscular lesions at the bilateral thigh, calf and upper extremities with loss of muscle fiber alignment. Subsequent magnetic resonance image (MRI) demon- B strated disseminated symmetrical intramuscular nodular lesions of mild high SI on T1WI, high SI on T2WI with avidly enhancement distributed diffusely in the visible muscular structures of the pelvis, bilateral thighs and proximal legs (Figure 1A, axial view of thigh, T1WI with gadolinium contrast enhancement; Figure 1B and 1C, coronal view of thigh and calf). Excisional biopsy of a left thigh tumor was taken and pathology confirmed the presence of a biphasic metastatic carcinoma (Figure 2A). By immunohistochemical *Corresponding author: Dwan-Ying Chang M.D. *通訊作者 張端瑩醫師 Tel: ext C Figure 1. (A) Axial view of thigh, T1WI with gado- Fax: linium contrast enhancement; (B,C) coro- nal view of thigh and calf

3 136 C. C. Chiang et al./jcrp 1(2014) A B C D Figure 2. (A) Pathology confirmed the presence of a biphasic metastatic carcinoma; (B) The tumor cells were also positive for a panel of mesothelial markers including calretinin, (C) CK 5/6, (D) D2-40 (IHC) staining, both epithelioid and spindle cells were 3C, neck). The pleural effusion appeared slightly found to be positive for cytokeratin (AE1/AE3) and bloody and cloudy, and there was exudation based on cytokeratin (CK) 7, but negative for thyroid transcrip- the biochemical characteristics. Although the cell tion factor-1, CDX-2, p63, and S100. In addition, the block study failed to make a tissue diagnosis, the fea- tumor cells were also positive for a panel of mesothe- tures of the pleural effusion still strongly suggested a lial markers including calretinin (Figure 2B), CK 5/6 malignant etiology in the absence of infection. (Figure 2C), and D2-40 (Figure 2D). The morpholog- Nonetheless, based on these clinicopathological ical feature and immunophenotype both suggested the findings, the diagnosis was malignant pleural mesothe- diagnosis of a metastatic malignant mesothelioma. A lioma (MPM) with disseminated skeletal muscle me- computed tomography (CT) scan revealed right pleu- tastases (SMM). During work-up, the patient s condi- ral thickening, right pleural effusion, and widespread tion deteriorated rapidly. He became immobile and intramuscular metastases throughout the body, in- bed-ridden, and also started to suffer from trismus. Af- cluding abdominal, paraspinal, neck, and ocular terwards, he received chemotherapy with pemetrexed muscles (Figure 3A, ocular muscle; 3B, paraspinal; plus cisplatin, the standard first-line treatment for meta-

4 C. C. Chiang et al./jcrp 1(2014) static malignant mesothelioma [1]. There was neither objective response nor clinical improvement. Nosocomial pneumonia developed owing to the impaired muscle function and inefficient sputum expectoration. In spite of optimal supportive care, he died of hypercapnic respiratory failure. The patient survived for only 3 months from the onset of the symptoms. A B C Figure 3. A computed tomography (CT) scan revealed right pleural thickening, right pleural effusion, and widespread intramuscular metastases throughout the body, including abdominal, paraspinal, neck, and ocular muscles (A. ocular muscle; B. paraspinal; C. neck) DISCUSSION Malignant mesothelioma is rare, except in large referral centers or epidemiologic hotspots. We treated a 61-year-old man with malignant mesothelioma complicated by extensive skeletal muscle metastases, whose initial presentation included rapidly progressive weakness and stiffness in his four extremities. The patient survived for 3 months from the onset of the symptoms despite administration of emergency chemotherapy and optimal supportive care. The highly aggressive behavior of the tumor, combined with the rare manifestation causing immobility, resulted in fatality in the rather short period. Mesothelioma is a malignant tumor that arises from the mesothelial surfaces, most commonly in the pleural cavity, but occasionally in the peritoneal cavity or elsewhere. Asbestos exposure constitutes the primary cause of pleural and peritoneal mesothelioma in humans. However, our patient claimed not to have a history of asbestos exposure. The public health significance of exposure from asbestos in public and private buildings remains controversial [2]. Malignant mesotheliomas are classified into three major subtypes: epithelioid, sarcomatoid, and biphasic (mixed). The widespread availability and use of immunohistochemistry has greatly improved the accuracy of diagnosis in recent years. There is no single marker that has sufficiently high sensitivity and specificity for malignant mesothelioma. For epithelioid mesothelioma, common positive immunohistochemical markers that can be used to support a diagnosis of malignant mesothelioma include calretinin, CK5/6, the Wilms' tumor-i (WT1) antigen (nuclear staining), and

5 138 C. C. Chiang et al./jcrp 1(2014) D2-40 (podoplanin) [3]. For sarcomatoid or biphasic mesothelioma, D2-40 and calretinin are the most reliable of the affirmative mesothelioma markers [4,5]. MPM is locally aggressive, with frequent invasion of the chest wall, mediastinum and diaphragm. Metastasis to the hilar and mediastinal lymph nodes is present at autopsy in approximately 40%-45% of patients with MPM [6]. While unusual, metastases may occur. The reported metastatic sites include bone, central nervous system, lymph node, liver, lung, and soft tissue [7]. Skeletal muscle metastases are rare. Laurini et al. (1999) reported a case of MPM with the initial manifestation of muscle metastasis. In that case report, the metastatic lesion was a solitary forearm mass [8]. In contrast, our patient presented with widespread skeletal muscle involvement at the time of diagnosis. Different from a readily discernible mass, those numerous tiny nodules of our patient were embedded within muscles and thus were clinically insidious. Though some nodules became palpable over thin muscles, such as platysma and frontalis, they were not perceived until quite late in the treatment. Another observed finding in our patient was pseudo-normality of limb mass, which referred to the lack of obvious wasting despite clinical deterioration. It was probable that the metastatic lesions took the space of atrophied muscle. Grellner et al. (1995) first reported the existence of skeletal muscle metastases in an MPM patient based on autopsy findings. The left temporal muscle and proximal limb skeletal muscles of the right upper arm and both thighs exhibited multiple metastases measuring up to 7 cm in diameter [9]. Aukema et al. (2009) had described a MPM patient with extensive soft tissue metastasis, which was detectable only by the whole-body [18F] fluorodeoxyglucose positron emission tomography with CT (FDG-PET/CT) but not by the conventional CT scan [10]. His general condition also deteriorated rapidly and he died three weeks after FDG-PET/CT. The rarity of skeletal muscle metastases has led to a number of theories, hypotheses and experimental models. Skeletal muscles are characterized by permanent contractions. Direct consequences are high tissue pressure and highly variable blood flow with turbulences in the microcirculation [11,12]. Further negative factors of metastatic growth in muscles include: local heat production due to muscular action, and possible effects of lactic acid metabolism creating a poor milieu for tumors, cellular and humoral immune factors in the local environment of skeletal muscle [13,14]. It is not known how to reconcile the discrepancy between the rarity of clinically apparent SMM and the initial presentation of disseminated SMM in our patient. The seed and soil hypothesis may provide some insight. Paget postulated that the formation of metastases depends on the interaction of specially adapted tumor cells (seeds) and a permissive organ environment (soil) [15]. In more recent formulations of this theory, tumor cells must accumulate specific genetic mutations endowing them with the metastatic phenotype. Once tumor cells acquire the ability to intravasate into the vasculature, they disseminate hematogenously and enter the parenchyma of target organs. Tumor cells then face diverse cellular microenvironments that range from permissive to hostile. Only those cells that are well suited to overcoming obstacles may grow, and only if the cells find themselves in a suitable condition, will they develop into metastases [16]. The complex interactions between tumor cells and distant organs that underly disease-specific patterns of distant failure remain unknown. Haygood et al. (2012) evaluated the epidemiology of skeletal muscle metastases both in the literature and also among cases from M. D. Anderson Cancer Center and studied the prevalence and appearance of SMM among 433 patients undergoing PET/CT scans for non-small-cell lung cancer [17]. The most common source was lung cancer, and the most common site of involvement was the muscles of the trunk. They concluded that SMM are not rare, which may be more apparent in a PET/CT scan than at other staging ex-

6 C. C. Chiang et al./jcrp 1(2014) aminations, particularly a contrast-enhanced CT scan. To our knowledge, we report the first case of MPM with the initial manifestation as disseminated SMM. The dismal outcome could have been attributed to the poor performance status secondary to the disseminated SMM. The advent of more sensitive imaging modalities, particularly multi-slice CT, MRI, and PET/CT, in the past years, may allow more detection of skeletal muscle metastases. REFERENCES 1. Vogelzang NJ, Rusthoven JJ, Symanowski J, et al. Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J Clin Oncology 21: , Antman KH. Natural history and epidemiology of malignant mesothelioma. Chest 103(4 Suppl): 373S-376S, Pathology and Genetics: Tumors of the Lung, Pleura, Thymus, and Heart, IARC, Chu AY, Litzky LA, Pasha TL, et al. Utility of D2-40, a novel mesothelial marker, in the diagnosis of malignant mesothelioma. Mod Pathol 18: 105, Ordóñez NG. The diagnostic utility of immunohistochemistry in distinguishing between mesothelioma and renal cell carcinoma: a comparative study. Hum Pathol 35: 697, Huncharek M, Smith K. Extrathoracic lymph node metastases in malignant pleural mesothelioma. Chest 93: , Janne PA, Baldini EH. Patterns of failure following surgical resection for malignant pleural mesothelioma. Thorac Surg Clin 14: , Laurini JA, Castiglioni T, Elsner B, et al. Soft tissue metastasis as initial manifestation of pleural malignant mesothelioma: a case report. Int J Surg Pathol 7: 39-44, Grellner W, Staak M. Multiple skeletal muscle metastases from malignant pleural mesothelioma. Pathol Res Pract 191(5): ; discussion 461-2, Aukema TS, Teunissen JJ, Burgers SA, et al. Extensive soft-tissue metastases from malignant pleural mesothelioma. J Clin Oncol 27: e24-e25, Sridhar KS, Rao RK, Kunhardt B. Skeletal muscle metastasis from lung carcinoma: MR findings. Cancer 59: , Weiss L. Biomechanical destruction of cancer cells in skeletal muscle: a rate-regulator for hematogenous metastasis. Clin Exp Metastasis 7: , Seely S. Possible reasons for the high resistance of muscle to cancer. Med Hypotheses 6: , Stein-Weiblowski R. Skeletal muscle and tumor metastasis. Experientia 30: , Paget S. The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev 8: , Fidler IJ, Kim SJ, Langley RR. The role of the organ microenvironment in the biology and therapy of cancer metastasis. J Cell Biochem 101: , Haygood TM, Wong J, Lin JC, et al. Skeletal muscle metastases: a three-part study of a not-sorare entity. Skeletal Radiol 41(8): , 2012.

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