Metastases to the oral region from pleural mesothelioma: Clinicopathologic review

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1 CLINICAL REVIEW David W. Eisele, MD, Section Editor Metastases to the oral region from pleural mesothelioma: Clinicopathologic review Suraya H. Sinon, DClinDent, 1 Alison M. Rich, PhD, 1 * Haizal M. Hussaini, MDentSci, 1 Han-Seung Yoon, FRACP, 2 Norman A. Firth, MDSc, 1 Gregory J. Seymour AM, PhD 1 1 MedLab Dental Oral Pathology Diagnostic Service and the Sir John Walsh Research Institute, Faculty of Dentistry, University of Otago, Dunedin, New Zealand, 2 Department of Pathology, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand. Received 22 May 2011; Revised 2 July 2011; Accepted 3 August 2011 Published online 15 November 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. Malignant mesothelioma is a rare neoplasm that usually develops after exposure to asbestos and particularly involves the pleural cavity. It has a poor prognosis with aggressive local invasion and metastatic spread. Methods. The literature relating to malignant mesothelioma metastatic to the oral region was reviewed. Results. In all, 14 cases of malignant mesothelioma metastatic to the oral cavity were found. All were from pleural mesotheliomas, the tongue was the most common site of metastasis (8/14), and most metastases (9/13) were of the epithelioid type. The newly reported case is only the second report of a mesothelioma metastasizing to the buccal mucosa. It showed strong immunopositivity for keratin markers, vimentin, calretinin, and Wilms tumor product-1. Conclusions. The incidence of mesothelioma is predicted to continue to increase for at least another decade. Clinicians and pathologists should be aware of this lesion and its propensity to metastasize to the oral cavity. VC 2011 Wiley Periodicals, Inc. Head Neck 35: , 2013 KEY WORDS: oral mucosal metastasis, malignant mesothelioma Malignant mesothelioma is a rare neoplasm with an ageadjusted incidence rate of 1 per 100,000 (both sexes, United States, ) by comparison with a rate of per 100,000 for carcinoma of the lung and bronchus in the same population. 1 It is derived from the mesothelial cells of serosal tissue lining the coelomic cavities. Approximately 80% of cases of mesothelioma develop in the pleural cavity, whereas the other 20% arise in the peritoneum; pericardium is affected very rarely. 2 Most mesotheliomas occur as a result of prior exposure to asbestos, particularly occupational exposure, but also related to incidental events such as laundering asbestos-contaminated clothing. 3,4 Males are affected more frequently than females (ratio 5:1) and most people are in their fourth to seventh decade at the time of diagnosis. 3 The association between mesothelioma and contact with asbestos is particularly strong in male patients with the disease, and in those with pleural mesotheliomas. Female patients and those with peritoneal mesotheliomas are less likely to have been exposed to asbestos. 3 Clinical manifestations The usual symptoms of pleural mesothelioma are dyspnea and chest wall pain. Chest radiographs, CT, and positron emission tomography CT usually show pleural thickening, effusion, and pleural masses. 3 In the early stages *Corresponding author: A. M. Rich, MedLab Dental Oral Pathology Diagnostic Service and the Sir John Walsh Research Institute, Faculty of Dentistry, University of Otago, Dunedin, New Zealand. of pleural mesothelioma there are usually multiple tumor nodules on the visceral and parietal serosal surfaces, which later coalesce, with or without invasion into the lung parenchyma. 3 Pathogenesis Asbestos fibers interfere with mitotic division in mesothelial cells and are able to induce multiple chromosomal abnormalities, particularly deletions, and particularly involving chromosome 22. 5,6 The abnormal expression of oncogenes, with subsequent upregulation of production of cytokines and growth factors, and disturbance of tumor suppressor genes is associated with exposure to asbestos fibers. Early reports described alterations in the p53 and Rb pathways, 7 but mutations in these genes have now been found to be rare and mutations of the tumor suppressor genes NF2 and ink4a, both involved in the regulation of apoptosis, appear to be the most significant in the pathogenesis of mesothelioma. 8,9 Asbestos has been shown to induce proliferation of mesothelial cells in culture through production of tumor necrosis factor-a (TNF-a) and subsequent signaling through nuclear factor (NF)-jb. 10 Crocidolite, the most carcinogenic form of asbestos, causes macrophages to accumulate in the pleura. These macrophages release TNF-a upon contact with asbestos fibers, which in turn activates NF-jb. With the activation of NF-jb mesothelial cells, with DNA damage by the fibers may be able to escape apoptosis, divide, and possibly transform into malignant cells. 8 Although there is some evidence that the DNA virus Simian Virus 40 can induce mesothelioma in experimental animals, 11 the cause of mesothelioma in patients HEAD & NECK DOI /HED APRIL

2 SINON ET AL. without exposure to asbestosis is still unknown, although therapeutic radiation has been implicated in a small number of cases. 12 Histopathology Mesotheliomas are classified according to their histological pattern into epithelioid (most common type and shows a tubulopapillary or pseudoglandular pattern with bland cuboidal cells with uniform round nuclei lining papillary structures or acinae-like spaces), sarcomatoid, or biphasic (mixed epithelioid and sarcomatoid type). 13 Immunohistology No single marker is diagnostic for mesothelioma, and panels of antibodies with appropriate negative and positive controls are necessary. Normal mesothelium expresses low-molecular-weight cytokeratins and vimentin; thus, a tumor expressing both types of intermediate filaments is suggestive of a mesothelial origin. 14 All forms of mesothelioma have been shown to express the glucose transporter protein GLUT-1 in contrast to lack of expression in reactive mesothelial proliferations, and this may be used to discriminate between hyperplastic and neoplastic mesothelial nodules. 15 Most mesotheliomas will react positively with keratin markers (AE1/AE3, cytokeratin [CK]5/6, CK7, CK19, CAM 5.3). 2 Of these, CK5/6 is the most useful to define mesothelioma. 16 Mesotheliomas will usually react positively with epithelial membrane antigen (EMA) and with vimentin. 3 Calretinin, a helix loop helix structural domain found in calciumbinding proteins and widely expressed in neural tissue, is expressed in most cases of epithelioid mesothelioma. 17 Both cytoplasmic and nuclear calretinin positivity may be seen, but it is nuclear staining that is necessary to strongly suggest a diagnosis of mesothelioma. 16 Wilms tumor product (WT1) is expressed in normal adult mesothelium and shows nuclear positivity in most cases of epithelioid mesothelioma. 14,16 Human bone marrow endothelial cell (HBME)-1, an antibody that reacts with antigen on microvilli of normal and malignant epithelioid mesothelial cells and mesothelin are also likely to be positive. 18 Negative markers are the oncofetal antigen carcinoembryonic antigen (CEA) and thyroid transcription factor (TTF1). 16 Sarcomatoid mesotheliomas will show positivity for cytokeratins and vimentin, and some show focal calretinin positivity. 3 Histochemistry, to confirm lack of mucin production in a mesothelioma, and electron microscopy may be useful adjuncts to diagnosis. The use of serum biomarkers for mesothelioma screening is being actively investigated, especially for use in people with known exposure to asbestos. 19,20 The biomarkers of particular interest are soluble mesothelin-related protein, osteopontin, and megakaryocyte potentiating factor. 20 These may also be useful as a noninvasive means to assess response to treatment. Progression of disease and treatment Most people die within 18 months of the initial diagnosis of malignant mesothelioma, and the median survival is less than 12 months. 8,21 Because most people (80%) have late-stage disease at presentation, surgical treatment is not a viable treatment option and surgery cannot eradicate residual microscopic disease. 20 The disease is radiotherapy resistant and relatively resistant to conventional chemotherapy 8 ; however, multimodality therapy with combinations of chemotherapy, surgery, radiotherapy with or without the use of novel agents such as histone deacetylases inhibitors (HDACi), which reduce loss of heterozygosity of tumor suppressor genes, leading to promotion of apoptosis, are showing promising results. 22,23 Drugs that target NF-jb signaling have also been used, with some improvement in survival time 24,25 ; because epidermal growth factor receptor (EGFR) and vascular endothelial growth factor (VEGF) receptor are highly overexpressed in mesotheliomas, there is ongoing clinical research into the effects of EGRF tyrosine kinase inhibitors and anti-angiogenic agents that target the VEGF pathway in patients with nonresectable mesotheliomas. 8,26 Metastases from malignant mesothelioma are common, usually to the local lymph nodes and less often to the pleural surface of the contralateral lung, brain, liver, and bone. 27 Metastases to the oral region are uncommon and usually the sign of widespread malignant disease. The jaw bones, particularly the mandibular molar area, are more likely to be the site of metastases than the oral soft tissues in a ratio of 2:1. 28 It is rare for malignant mesothelioma to metastasize to the oral cavity, and only a few isolated case reports or small series are reported in the literature. The purpose of this paper was to present a comprehensive review of cases of malignant mesothelioma metastatic to the oral cavity and to describe a case of a metastasis to the buccal mucosa from a malignant pleural mesothelioma. MATERIALS AND METHODS A comprehensive search for cases of malignant mesothelioma metastatic to the oral region was performed using English-language references in PubMed using combinations of the words mesiothelioma, metastasis, oral cavity, mouth, buccal, and tongue. A manual review of reference lists in relevant publications was also carried out. Tissue was obtained and stored in accord with the International Accreditation New Zealand guidelines, and signed informed consent to use the tissue for research was obtained from the patient. RESULTS The results of the literature search of cases of oral metastases from mesothelioma are summarized in Table There were 14 previously reported cases of malignant mesothelioma metastatic to the oral cavity; case 11 was reported in different contexts on 2 occasions. Eleven patients were men, giving a male-to-female ratio of 3.7:1. The average age at diagnosis was 60 years (range, years). All but 1 patient, case 14, 42 in which the oral lesion was the first evidence of mesothelioma, had a prior diagnosis of pleural mesothelioma. The primary lesions were predominantly epithelioid mesotheliomas (7/11 where primary type was stated). The most common site of occurrence was the tongue (8/14 cases). There were 4 intrabony metastases, 2 of which involved the overlying mucosa. In 600 HEAD & NECK DOI /HED APRIL 2013

3 TABLE 1. Details of reported cases of malignant mesothelioma metastastic to the oral region. Case no. Year of publication/ reference no. Sex Age at diagnosis, y Site of primary mesothelioma Oral site Time between diagnoses of primary and oral metastasis Histopathology of metastasis Immunopathology of metastasis (þve reactivity only) Outcome 1 Case 1, M 73 Pleural-epithelioid type 2 2-cm submucosal mass ventral tongue 2 Case 2, M 45 Pleural-type not stated Mass on mandibular gingiva with associated bone loss lingual 2 y Epithelioid with 1 y Epithelioid with CKþve Died with multiple metastases 2.5 y after CK, vimentin þve Lost to follow-up M 48 Pleural-sarcomatoid type Mandibular alvelous 4. mo Sarcomatoid CK, vimentin þve Died 4.5 mo after M 52 Pleural-epithelioid type Lesion on lateral tongue 2 y Epithelioid CK, vimentin þve Lost to follow-up M 63 Pleural-biphasic type Mandibular gingival mass gingival mass M 64 Pleural-type not stated ulcerated nodule upper lip M 71 Pleural-epithelioid type Ulcerated mass on dorsolateral tongue F 50 Pleural-epithelioid type 0.8-cm mass buccal mucosa M 53 Pleural-sarcomatoid type Periapical radiolucency associated with mandibular third molar M 70 Pleural-biphasic type 2 1-cm lesion on lateral tongue M 69 Pleural-epithelioid type cm submucosal mass in muscle of anterior tongue F 59 Pleural-epithelioid type cm nodule on dorsal tongue M 71 Pleural-type not stated 3-cm submucosal mass in floor of mouth with tongue involvement F 46 None known at time of oral presentation, subsequent diagnosis of pleural mesothelioma, epithelioid type 15 Sinon et al 2011 current case cm nodule on dorsal tongue M 65 Pleural-epithelioid type 0.8-cm submucosal mass in buccal mucosa 11 mo Epithelioid with 9 mo Epithelioid with Vimentin þve Lost to follow-up CK 19, AE1/3, calretinin, HBME1 þ ve 14 mo Epithelioid CK5/6, CK7, EMA, vimentin, calretininþve Alive at time of report with multiple metastases Died 17 mo after 11 mo Not stated CK, EMA, vimentin, Alive with multiple metastases 13 mo after primary diagnosis 1 mo Sarcomatoid AE1/3, vimentin þve Not stated 9 mo Biphasic CK5, AE1/3 þve Not stated 5 mo Epithelioid CK5/6, AE1/3, CD15, calretinin þve 3 y Epithelioid with 1 y Poorly differentiated with squamoid cells N/A Epithelioid with pseudoglandular areas 1 y Epithelioid with pseudoglandular areas CK5/6, AE1/3, EMA, calretinin, HBME-1, mesothelin, TTF-1 þve CK5, EMA, calretinin þve CK5/6, CK7, CK19, AE1/ 3, Cam 5.2, EMA, calretinin, HBME1, WT1 þve CK5/6, CK7, CK19, Cam 5.2, EMA, calretinin, WT1 þve Alive with extension of tongue lesion to floor of mouth, further metastasis to gluteus muscle Died with multiple metastases 4 y after Died with multiple metastases 15 mo after primary diagnosis Alive with further metastasis to tongue and chest wall 8 mo after diagnosis Died 15 mo after Abbreviations: M, male; F, female; CK, cytokeratin; EMA, epithelial membrane antigen; HBME-1, human bone marrow endothelial cell; TTF1, thyroid transcription factor; CEA, carcinoembryonic antigen; WT1, Wilms tumor product; CAM, anti-cytokeratin.

4 SINON ET AL. all, 5 of 9 patients with follow-up had died by the time their cases were reported, and the remaining 4 patients, although alive, had multiple metastases. A comparison of the immune profiles of lesions that should be included in the differential diagnosis of a lesion in the oral cavity, suspected of being a metastatic mesothelioma, are shown in Table 2. CASE REPORT A soft tissue specimen was received at MedLab Dental Oral Pathology Diagnostic Service, University of Otago from a provincial New Zealand Hospital. It was an incisional biopsy from a firm 0.8-cm-diameter submucosal mass in the left buccal mucosa, adjacent to the labial commissure in a 65-year-old man. The swelling, with normal overlying mucosa, had been present for 2 months and was asymptomatic. The patient had been diagnosed approximately 1 year previously with a pleural malignant mesothelioma, but no other medical history was provided. The gross appearance was of an oral mucosal ellipse with underlying connective tissue measuring cm. The specimen had been fixed in 10% neutral buffered formalin and was paraffin-embedded, after which the blocks were used to prepare routine histopathology and immunohistochemistry slides. Sections were deparaffinized and some were stained with hematoxylin and eosin and others prepared for immunohistochemistry. Sections were reacted with the following antibodies: CK5/6, CK7, CK20, Cam 5.2, EMA, CEA, vimentin, calretinin, WT1, TTF1, in accord with the manufacturer s recommendations, either in the MedLab Dental Oral Pathology Laboratory or at Southern Community Laboratory, Dunedin. Histopathology The specimen showed cellular fibrous and myxoid connective tissue diffusely infiltrated by large oval and cuboidal cells with relatively indistinct vesicular nuclei and abundant pale eosinophilic cytoplasm (Figures 1 and 2). These cells were arranged in sheets and cords with some FIGURE 1. Photomicrograph of sheets and islands of malignant mesothelioma cells. A small amount of fibrous connective tissue is present between the neoplastic cells, which can be seen infiltrating between muscle fibers (hematoxylin eosin stain, original magnification 15). tubular and where there were lumina lined by cuboidal cells. The tumor cells were separating muscle fibers and fibrous collagen bundles. There was a moderately intense chronic inflammatory cell infiltrate at the periphery of the specimen. The tumor extended to all margins. Periodic acid-schiff (PAS) staining, with and without diastase, was negative. Immunohistology The specimen revealed strong immunopositivity for CK5/6, CK7, Cam5.2, EMA, vimentin, calretinin (nuclear TABLE 2. Summary of immunohistochemical markers useful to distinguish oral lesions that might be mistaken for malignant mesothelioma. Marker 1 OSCC 2 Malignant melanoma 2 2 Malignant Adenocarcinoma mesothelioma CK5/6 þ þ þ CK20 þ þ Cam 5.2 þ þ EMA þ Variable þ CEA þ Variable þ Vimentin þ þ S-100 þ 6 Calretinin Focally positive þ WT1 þ þ þ HBME-1 þ Mesothelin þ þ TTF1 þ Abbreviations: OSCC, oral squamous cell carcinoma; CK, cytokeratin; CAM, anti-cytokeratin; EMA, epithelial membrane antigen; CEA, carcinoembryonic antigen; WT1, Wilms tumor product; HBME-1, human bone marrow endothelial cell; TTF1, thyroid transcription factor. FIGURE 2. Photomicrograph of malignant mesothelioma demonstrating large round to cuboidal cells with inconspicuous nuclei and abundant pale cytoplasm (hematoxylin eosin stain, original magnification 20). 602 HEAD & NECK DOI /HED APRIL 2013

5 ORAL METASTASES FROM MALIGNANT MESOTHELIOMA FIGURE 3. Photomicrograph showing nuclear (arrow) and cytoplasmic staining against calretinin (original magnification 10). and cytoplasmic, Figure 3), and WT1, but negative results for CK20, CEA, and TTF1. The diagnosis of a metastatic malignant mesothelioma, epithelioid type, was made. The patient died 3 months after the diagnosis of oral metastasis from pleural mesothelioma was made. DISCUSSION The diagnosis of primary malignant mesothelioma is established by a combination of clinical, imaging, and histopathological features. The diagnosis of a secondary mesothelioma in the oral region is made more readily if there is a known history of a primary lesion, as is usually the case, although Murray et al 42 described a patient where a lingual metastasis was the presenting feature of a pleural mesothelioma. Even with the knowledge of a primary lesion, it is necessary to make a definite diagnosis of a putative oral metastasis to allow for appropriate management. Although the clinical picture of a primary oral squamous cell carcinoma (OSCC) is unlikely to be mistaken for a metastatic lesion by an experienced clinician, OSCC is the most likely diagnosis of a persistent mass, without obvious traumatic or infectious origin, in a middle-aged to elderly man. Wide surgical excision, often the treatment of choice for an OSCC, may be inappropriate for a metastatic mesothelioma, although this has happened where there have been uncertainties with the diagnosis. 41 As well as primary oral lesions, other types of metastases to the oral regions, such as metastatic adenocarcinoma or malignant melanoma, need to be excluded. The case presented in this report is only the second report of a mesothelioma metastatic to the buccal mucosa. Although metastases from all sites to the oral region will more likely affect the jaw bones, 28 mesothelioma metastases, although rare, tend to involve the oral soft tissues, especially the tongue. The overexpression of matrix metalloproteinase (MMP)-14, also known as membrane-type matrix metalloproteinase (MT-MMP) by malignant mesothelioma cells, has been shown to be related to spread into the local fibrous stroma. 43,44 As well, mesothelioma cells express podoplanin, a type-1 transmembrane sialomucin-like glycoprotein and a marker of lymphatic endothelium that is associated with interactions between tumor cells and lymphatic vessels and is thought to facilitate lymphatic invasion The reason the distant metastases from malignant melanoma are often to soft tissue sites rather than bone is not fully understood. Cancer cells that metastasize to distant organs show organ-specific behavior, different to cells from the primary tumor 48 and these phenotypic changes might influence the preferred site of metastasis. Cells from tumors that commonly metastasise to bone (eg, prostate cancer) have been shown to interact with chemokine (C X C motif) ligand (CXCL) 12 and its receptor, chemokine receptor (CXCR) They interfere with the CXCL12/CXCR4 signaling pathway and allow the tumor cells to home into an osteoblastic niche in the bone marrow and to establish a micrometastasis. 49,50 Inhibition of CXCR4 signaling in an experimental animal model reduces metastatic disease. 51 In a similar manner, but via different signaling pathways tumors (eg, malignant mesothelioma) may preferentially disseminate to soft tissue, including the oral cavity. The current patient, a 65-year-old man, fits the profile of others presenting with oral metastases from mesothelioma. His primary lesion was an epithelioid mesothelioma, the most common type of mesothelioma, 16 and the histology of the metastasis reflected this pattern. The aggressive nature of the disease was reflected by the poor outcome. This is consistent with previous cases in which 5 of 9 patients with follow-up were dead at the time their cases were reported in the literature and the remaining 4 patients, although alive, had multiple metastases. Immune markers in metastastatic mesotheliomas usually reflect those of the primary tumor. The use of at least 2 positive (eg, calretinin and WT1) and 2 negative mesothelioma markers (eg, CEA and TTF1) and a broad-spectrum CK as an initial screening panel is recommended. 13,16,18 It is reasonable to extend this recommendation to the situation in which the diagnosis of metastatic mesothelioma is being considered. As well, the proportion of cells staining positively, and the localization of the stain, nuclear and/or cytoplasmic, should be taken into consideration. 16 The current case fit the histologic and immunopathologic profile of a metastatic mesothelioma, epithelioid type. It is anticipated that the incidence of malignant mesothelioma will continue to rise over the next decade, with the peak expected in Australia in 2020 and in France in 2030 to 2040, followed by a slow decline. 52,53 The incidence in the United States peaked around 2000 and is now declining. In the United Kingdom it was expected to peak in 2010, but obviously this has yet to be confirmed. Taking into consideration the long latent period, the preventive measures related to exposure to asbestos may finally be taking effect, at least in the United States. 54 Nevertheless, the worldwide incidence is still likely to increase over the coming decades as the use of asbestos without precautions is still widespread in some developing countries. 55 It follows, therefore, that metastases from mesothelioma will follow this trend and, although it will remain rare, it is important to consider this lesion in a differential diagnosis of oral lesions. Although a prior history of mesothelioma is valuable information for the oral pathologist, the HEAD & NECK DOI /HED APRIL

6 SINON ET AL. histopathologic diagnosis should be made on the histologic and immunohistochemical features. An accurate diagnosis is very important to avoid inappropriate futile surgery and help maintain the patients quality of life. Acknowledgements The authors thank Lynda Horne for technical assistance with the laboratory procedures. REFERENCES Brenner J, Sordillo PP, Magill GB, Golbey RB. Malignant mesothelioma of the pleura: review of 123 patients. Cancer 1982;49: Galateau-Salle F. Pathology of malignant melanoma. London: Springer- Verlag; Wagner JC, Sleggs CA, Marchand P. Diffuse pleural mesothelioma and asbestos exposure in the North Western Cape Province. Br J Ind Med 1960;17: Hesterberg TW, Barrett JC. Induction by asbestos fibers of anaphase abnormalities: mechanism for aneuploidy induction and possibly carcinogenesis. Carcinogenesis 1985;6: Cheng JQ, Lee WC, Klein MA, Cheng GZ, Jhanwar SC, Testa JR. 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