Spinal cord compression: an unusual presentation of malignant pleural mesothelioma. A case report and review of the literature

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1 Tu mo ri, 98: e92-e97, 2012 Spinal cord compression: an unusual of malignant pleural mesothelioma. A case report and review of the literature Carolina Mensi 1,2, Lorenzo Termine 3, Anna Garberi 3, Stefano Meroni 4, Daniel Levi 5, Luca Balzarini 6, and Luciano Riboldi 1,2 1 Clinica del Lavoro Luigi Devoto, Department of Preventive Medicine, Fondazione IRCCS Ca Granda, Ospedale Maggiore Policlinico, Milan; 2 Inhaled Dust Biological Effects Center (EBPI), Department of Occupational Health, Università degli Studi di Milano, Milan; 3 Postgraduate School of Occupational Medicine, Department of Occupational Health, Università degli Studi di Milano, Milan; 4 Postgraduate School of Radiodiagnostics, Università degli Studi di Milano, Milan; 5 Department of Neurosurgery, Humanitas Clinical Institute IRCCS, Rozzano, Milan; 6 Department of Radiology, Humanitas Clinical Institute IRCCS, Rozzano, Milan, Italy ABSTRACT Pleural malignant mesothelioma is a locally invasive tumor that tends to progress due to direct extension of the tumor into the pulmonary parenchyma, the chest wall, the mediastinum, or the abdominal cavity via the diaphragm. In the later stages of the disease, distant metastases can occur. Metastases to the nervous system are rare, and clinical signs of nervous system involvement typically appear between 2 months and 6 years after the primary diagnosis. However, the case presented here manifested as neurological impairment without any respiratory symptoms. Introduction Malignant mesothelioma (MM) is an aggressive tumor that develops at serosal surfaces such as the pleura, peritoneum, and tunica vaginalis of the testis. It has a strong etiological relationship to asbestos exposure 1. Although this tumor type was once rare, its incidence is increasing in several countries as a result of widespread exposure to asbestos 2,3. The symptoms of pleural MM usually involve progressive dyspnea and/or pain in the chest wall. These conditions may be accompanied by dry cough, weight loss, fever, fatigue, and night sweats. MM has a propensity to infiltrate underlying and neighboring structures, especially the lung, chest wall, mediastinum, and diaphragm. Accordingly, 50-67% of autopsies performed on patients with MM detect evidence of distant spread 4-6. The Lombardy Mesothelioma Registry (LMR) is a population-based registry that collects data on all MM cases associated with the pleura, peritoneum, pericardium, and tunica vaginalis of the testis reported for residents of the Lombardy Region of northern Italy (population, 9.8 million). Between 2000 and 2010, more than 3,400 cases were collected, and the regional age-standardized incidence rates of MM for this period were 5.2/100,000 (95% CI: ) and 2.0/100,000 (95% CI: ) per year, respectively, for males and females. The clinical records of each case were collected and reviewed, including radiological exams, histology reports, and disease history. Evaluations of asbestos exposure were also reviewed and included responses to a standardized questionnaire administered by trained interviewers to the patient or his/her next of kin: a detailed occupational history was collected that addressed the industrial sector of employment, the details of the patient s job and tasks, the jobs of the patient s coworkers, and a description of the workplace environment. Residential history, lifestyle habits, hobbies, and information regarding the job performed by all subjects that lived with the pa- Key words: mesothelioma, spinal cord compression, asbestos, occupational exposure. Conflict of interest: None of the authors have any conflicts of interest to report. Financial support: No financial support was provided for this work. Authorship: Mensi C, Termine L, Garberi A, Meroni S, Levi D, acquisition and interpretation of data, review of literature; Mensi C, Termine L, Garberi A, Meroni S, drafting the article; Mensi C, Balzarini L, Riboldi L, approval of final version of manuscript. Correspondence to: Carolina Mensi, Clinica del Lavoro Luigi Devoto, Fondazione IRCCS Ca Granda - Ospedale Maggiore Policlinico, Via San Barnaba 8, Milan, Italy. Tel ; fax ; Received May 16, 2011; accepted January 3, 2012.

2 MALIGNT MESOTHELIOMA WITH SPIL CORD COMPRESSION e93 tient were also obtained. This information was then discussed with an industrial hygienist, occupational health physicians, and epidemiologists to evaluate the potential exposure to asbestos in the patient s workplace and non-workplace environment in accordance with the national guidelines of the Italian Mesothelioma Registry 7. As a result of this epidemiological surveillance, it became apparent that the case reported here is unique based on the patient s of neurological symptoms prior to the onset of respiratory symptoms. A C B D Case report History A 69-year-old non-smoking male previously treated for high blood pressure had suffered a myocardial infarction in In 2005, after a few months of recurrent back pain, the patient developed weakness in both legs, which developed further into paralysis of his left leg. Upon admission to a neurosurgery department, the patient s clinical condition rapidly deteriorated, with worsening of his urinary incontinence and inability to maintain an upright posture. The patient did not report any cardiorespiratory symptoms. Imaging studies Computed tomography (CT) imaging of the patient s chest was performed using a 16-slice CT scanner. Tissue in the left paravertebral region at the level of the aortic arch, with 4 cm of craniocaudal extension and 3 cm of anterior-posterior diameter, was characterized by intense and inhomogeneous contrast enhancement. This tissue area exhibited an infiltrative growth pattern that affected the left profile of T5 and the entire left T4-T5 vertebral foramen due to invasion of the medullary canal. Cranially, the affected tissue raised the proximal portion of the thoracic aorta in the absence of a definite cleavage plane, which was consistent with an infiltrative phenotype. Left pleural effusion was the only pathological finding in the thorax. Magnetic resonance (MR) scans (1.5 T system) of the entire cervical-dorsal spine were obtained using noncontrast sequences including T1W and T2W TSE fatsat. An intravenous bolus injection of gadobutrol was used to obtain the TSE multiplanar sequences. MR imaging confirmed the presence of the paraspinal mass detected on CT scans and also provided information regarding the relationship between the tumor and the spine. The mass was associated with a hypointense signal in T1 (Figure 1A) and a heterogeneous hyperintense signal in T2 (Figure 1B). Intense pathological enhancement characteristic of hypervascularized lesions was also observed (Figure 1C and 1D). The anatomic relationship of the solid mass, especially its spread into the vertebral foramen, and the invasion of the Figure 1 - Magnetic resonance scans of the entire cervical-dorsal spine of a 69-year-old non-smoking male. The left paraspinal tumor mass was associated with a hypointense signal in T1 (A) and a heterogeneous hyperintense signal in T2 (B). Intense pathological enhancement characteristic of hypervascularized lesions was also observed (C and D). medullary canal with spinal cord compression were also detected on the MR images. At the level of T4-T5, the spinal cord was displaced rightwards by the mass and was associated with a mildly hyperintense signal in all of the sequences collected using a craniocaudal extension of 2 cm. Histopathological diagnosis The patient underwent a medial dorsal incision from T3 to T5; skeletonization of the paravertebral channels bilaterally; flavectomy of T3, T4 and T4, T5 and laminotomy of T3 and T4; followed by spinectomy of T3, T4 and T5. After decompression, biopsy of the endocanalar mass collected specimens of extradural dorsal tissue, vertebral bone, and ectopic material from the dorsal spinal canal. Histopathological examination showed a malignant neoplasm composed of spindle-cells and fibrosclerosis-rich stroma. Immunohistochemical staining confirmed the presence of sarcomatous mesothelioma. Clinical evolution After surgery, the patient received palliative radiotherapy to the thoracic spine (T3-T5) at a dose of 20 Gy administered in 5 fractions. The patient showed marked atrophy and flaccid paralysis of the lower limbs, a midthoracic sensory level, and sphincter incontinence. He died after 2 months. Occupational history The patient s work history included employment as a flatiron assembly operator from age 14 to 17 (1949-

3 e94 C MENSI, L TERMINE, A GARBERI ET AL Table 1 - Spinal canal involvement of malignant mesothelioma: review of published cases Reference Age, gender Neurological symptoms 8 67, M Acute paraplegia occurred 10 days prior to sudden paralysis in right leg, followed by gradual paralysis in left leg; urine incontinence for 3 days 9 18, M Weakness and numbness of the lower extremities 10 54, M Right-sided Horner syndrome and Brown- Séquard syndrome with right-sided paralysis and left-sided sensory changes below the T1 level 11 57, M Radicular pain; paresthesia and loss of strength in lower limbs (T6-T10) Mechanism of spread Autopsy report: tumor extended along spinal nerve roots and spread over meningeal surfaces within the spinal canal (extradural spinal involvement) Left paraspinal mass with partial destruction of the vertebral body and transverse process of T12. Tumor tissue was also detected inside the spinal canal and encircling and compressing the spinal cord from the left side at T11-T12 Tumor invaded the lower trunk of the brachial plexus and spread along the T1 nerve root beneath the arachnoid onto the spinal cord Tumor on the left side of the spinal cord with paravertebral expansion at the level of T6- T9. Extradural invasion compressed the medulla at the metameric levels T7-T8 Diagnosis of mesothelioma Autopsy report performed 24 days after hospital admission detected alveolar cell lung carcinoma in addition to mesothelioma 2 years prior to neurological 3 years prior to neurological 5 months prior to Histological type Asbestos exposure The patient worked in the dockyards, although possible asbestos exposure could not be confirmed The patient did not recall any asbestos exposure The patient installed asbestos thermal insulation for 18 months The patient worked in a cement-asbestos factory for 28 years 12 Patient 1 56, F Progressive lower Masses present in the back pain radiating left intervertebral to the back of the legs foramina at L2-L3 and L3-L4, with thickening of the left psoas muscle. Tumor growth at the thoracic and cervical levels extending through the foramen magnum into the skull Pleural effusion was present 7 years prior to. Histological diagnosis concomitant with the onset of neurological symptoms (from a psoas muscle biopsy) confirmed the results of the autopsy report asbestos by the husband s working clothes Patient 2 46, M Pain in the lumbar spine radiating to the loin and loss of strength in the right leg Growth of the MM through the intervertebral foramina that extended into the epidural space and resulted in an epidural cuff reaching from T10 to L3. Tumor progression was observed up to the foramen magnum 6 years prior to neurological Patient 3 41, F Problems walking, weakness in both legs, and pin-prick sensory level below C6 Tumor extended from the right upper thorax into the neck and through the lower cervical foramina into the epidural space, causing cervical spinal cord compression 2 years prior to neurological Continued

4 MALIGNT MESOTHELIOMA WITH SPIL CORD COMPRESSION e95 (Continued) Table 1 - Spinal canal involvement of malignant mesothelioma: review of published cases Reference Age, gender Neurological symptoms Mechanism of spread Diagnosis of mesothelioma Histological type Asbestos exposure 12 Patient 4 53, M Severe back pain radiating to the right loin and abdomen A large paravertebral mass invaded multiple thoracic vertebrae and intervertebral foramina at the T10 level. An epidural cuff caused spinal cord compression 4 months prior to 13 55, F Progressive weakness in the left leg Tumor extended into the spinal canal through the neuroforamina of the T9 nerve root with spinal cord compression 18 months prior to 14 58, M Dorsal pain Tumor invaded the spine and spinal canal leading to cord compression 3 months prior to No asbestos exposure 15 62, M Back pain, decreased muscular strength, and incomplete paralysis below the T10 level Tumor masses penetrated through the neuroforamen into the spinal canal and resulted in spinal cord compression 2 weeks prior to Biphasic asbestos while working in a coal mine 16 61, M Horner syndrome, weakness, sensory loss Tumor extended into the spinal canal through the neuroforamina of C7-T1 and T1-T2 2 years prior to neurological asbestos while working in a chemical plant 17 50, M Acute 2-week history of progressive thoracic back pain, received radiation to the right chest. Progressive weakness and hypoesthesia of the right abdomen and right leg were experienced with slight sphincter disturbance Tumor spread across the dura into the spinal cord at T5 through the intervertebral foramen T4-T5 28 months prior to 18 61, M Progressive weakness of bilateral lower extremities, numbness in body and both legs, sensory deficit and paraplegia, dysfunction of bladder and bowel Tumor directly invaded the spinal cord along the T4 posterior nerve root 7 months prior to asbestos present in car brakes and clutches 19 64, M Low back pain at L2- L3 level, left flank pain, ileus Tumor directly invaded the spine at T11 2 months after intermittent discomfort and pain Poorly differentiated neoplastic cells The patient had no known history of asbestos exposure 20 67, M Weakness of the right leg and subsequent paralysis Tumor invaded the right T4 nerve root suggesting intramedullary involvement More than 6 months prior to neurological M, male; F, female;, not available.

5 e ). This job implied the use of asbestos elements to insulate electric resistance. Subsequently, the patient was employed as a barman (from age 17 to 22; ), a boiler conductor (from age 23 to 59; ), and a transformer maintenance man for the production of electric energy. The latter involved the maintenance of asbestos-caulked machinery and systems. Other sources of possible asbestos exposure including military service, hobbies, and residential history were excluded. Discussion Pleural MM is an aggressive neoplasm that initiates in the pleural layer of cells, then tends to invade locally into adjacent regions (lung, chest wall, mediastinum, and diaphragm). Involvement of the central nervous system is rare. However, when it occurs, it is usually mediated through the bloodstream, although there are some reports of direct infiltration of the spinal cord through the intervertebral foramina In Table 1, all published cases of pleural MM causing neurological compression since 1974 are presented. These cases are characterized by direct involvement of the spinal cord. The clinical onset of medullary invasion is usually associated with local pain that radiates to the limbs, progressive weakness, difficult movement up to the point of paralysis, and paresthesias with or without sensory level. Medullary localization was most often associated with a diagnosis of mesothelioma, independent of the time that had passed since the initial diagnosis (2 weeks to 6 years). In only 2 cases 8,19 were neurological symptoms manifest in the early stages, even prior to the diagnosis of a neoplasm. In 1 case, typical respiratory symptoms were exhibited 8. A second case was recently described involving a patient suffering from low back pain and ileus. In this patient, a CT scan showed a left paraspinal neoplasm over the T11 vertebra, which was associated with high levels of the tumor marker CA In addition, histological studies of the neoplasm revealed the presence of poorly differentiated neoplastic cells with punctuate cytoplasmic staining of mucin, suggesting metastasis of a gastrointestinal tract tumor. PET-CT scans further confirmed that a hypermetabolic nodular lesion was present in the left pleura, resulting in the diagnosis of pleural mesothelioma 19. Of the 16 mesotheliomas described in the literature, the histological types identified included 4 epithelial, 4 sarcomatous, and 1 biphasic. Six case reports did not include a histological diagnosis, and 1 case was associated with poorly differentiated neoplastic cells. In 10 cases, exposure to asbestos was investigated and, as a result, 4 subjects were excluded (no asbestos exposure) 8,9,14,19. However, it is not clear whether this investigation took into account the occupational history of the patients, and whether potential non-occupational sources of exposure were considered. In 5 cases, possible asbestos exposure was not addressed. While only a few cases described in the literature have been associated with medullary invasion by contiguity, the present case is further distinguished by its clinical onset where neurological symptoms, in the absence of respiratory symptoms or chest wall pain, were the first signs of the pleural mesothelioma. Furthermore, the presence of a neoplasm was unexpectedly detected by MR imaging that was intended to investigate the neurological symptoms. Therefore, the ability of MM to invade the intervertebral foramina and apply direct compression to the spinal cord indicates that there is the potential for a neurological component of MM to manifest in the early stages of the disease, although this is more of an exception than a primary characterization of MM. However, for all MM cases an appropriate diagnostic procedure is necessary to reach a definitive diagnosis and to exclude other potential primary tumor sites. Furthermore, histological examination of the neoplastic tissue involved needs to be performed. When a diagnosis of MM is confirmed, an investigation of possible asbestos exposure should be initiated, with considerations for the ethical and legal requirements involved. References C MENSI, L TERMINE, A GARBERI ET AL 1. Ismail-Khan R, Robinson LA, Williams CC Jr, Garrett CR, Bepler G, Simon GR: Malignant pleural mesothelioma: a comprehensive review. Cancer Control, 13: , Peto J, Decarli A, La Vecchia C, Levi F, Negri E: The European mesothelioma epidemic. Br J Cancer, 79: , Kazan-Allen L: Asbestos and mesothelioma: worldwide trends. Lung Cancer, 49 (suppl 1): S3-8, Hulks G, Thomas JS, Waclawski E: Malignant pleural mesothelioma in western Glasgow. Thorax, 44: , King JA, Tucker JA, Wong SW: Mesothelioma: a study of 22 cases. South Med J, 90: , Winfree CJ, Mack WJ, Sisti MB: Solitary cerebellar metastasis of malignant pleural mesothelioma: case report. Surg Neurol, 61: , Nesti M, Adamoli S, Ammirabile F, Ascoli V, Barbieri PG, Cacciarini V, Candela S, Cavone D, Cauzillo G, Chellini E, Chiappino G, Convertini L, Crosignani P, Gennaro V, Gioffrè F, Gorini G, Iavicoli S, Magnani C, Mangone L, Marinaccio A, Marras T, Menegozzo M, Mensi C, Merler E, Mirabelli D, Musti M, Montanaro F, Mosciatti P, Nicita C, Pannelli F, Pascucci C, Pezzarossi AM, Romanelli A, Scarselli A, Scondotto S, Silvestri S, Storchi C, Tosi S, Tumino S: National Guidelines of Malignant Mesothelioma Register, Second Edition. ISPESL (Istituto Superiore per la Prevenzione e la Sicurezza del Lavoro), Rome, Available (in Italian) at da.pdf. Accessed 18 January Cooper D: Malignant mesothelioma invading the spinal canal. Postgrad Med J, 50: , Mikhael MA, Paige ML, Thayer C: Computerized tomography of malignant pleural mesothelioma with spinal canal invasion. Comput Radiol, 6: 11-15, 1982.

6 MALIGNT MESOTHELIOMA WITH SPIL CORD COMPRESSION e Steel TR, Allibone J, Revesz T, D Arrigo C, Crockard HA: Intradural neurotropic spread of malignant mesothelioma. Case report and review of the literature. J Neurosurg, 88: , Rojas JL, Alfageme I, De la Cruz I, Reyes N, Munoz J: Radicular involvement and medullary invasion from a malignant mesothelioma. Respiration, 68: , Gijtenbeek JM, Brouwer HI, Boerman RH, Wiggenraad G, Vecht CJ, Sillevis Smitt PAE: Extensive epidural cufflike growth of malignant pleural mesothelioma causing spinal cord compression. J Thorac Cardiovasc Surg, 124: , Lee AW, Nikitins I, Pozza C, Koblar SA: Pleural mesothelioma with extension into the thoracic spinal cord. Intern Med J, 35: , Margery J, Grassin F, Le Moulec S, Ruffié P: Spinal cord compression from a malignant pleural mesothelioma. Rev Pneumol Clin, 61: , Heyer CM, Theile A, Weisser H, Reichert J, Horch C, Mueller KM, Bauer TT: Subarachnoid-pleural fistula as a complication of malignant pleural mesothelioma. Respirology, 11: , Hillard VH, Liu JK, Kwok A, Schmidt MH: Perineural spread of malignant mesothelioma resulting in an intradural spinal cord mass: case report. J Neurooncol, 81: , Payer M, von Briel T: Intradural pleural malignant mesothelioma. Acta Neurochir, 149: , Okura H, Suga Y, Akiyama O, Kudo K, Tsutsumi S, Abe Y, Yasumoto Y, Ito M, Izumi H, Shiomi K: Pleural malignant mesothelioma causing cord infiltration through the nerve root case report. Neurol Med Chir (Tokyo), 49: , Huang YC, Tu DG, Wu JD, Lee MY: Malignant pleural mesothelioma presenting as low back pain: diagnosed by bone scan coordinating with F-18 FDG PET/CT. Spine, 34: E , Chamberlain MC, Eaton KD, Fink JR, Tredway T: Intradural intramedullary spinal cord metastasis due to mesothelioma. J Neurooncol, 97: , 2010.

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