Treatment of malignant pleural mesothelioma Review Article

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1 Cancer Therapy Vol 6, page 73 Cancer Therapy Vol 6, 73-80, 2008 Treatment of malignant pleural mesothelioma Review Article David F. Heigener*, Martin Reck, Ulrich Gatzemeier Department of Thoracic Oncology, Krankenhaus Grosshansdorf, Germany *Correspondence: David F. Heigener, Krankenhaus Großhansdorf, Woehrendamm 80, Großhansdorf, Germany; Tel: ; Fax: ; Key words: Malignant Mesothelioma, Diagnosis, Therapy Abbreviations: endothelial-growth factor-receptor, (EGFR); International mesothelioma interest group, (IMIG); Malignant Pleural Mesothelioma, (MPM); nuclear magnetic resonance imaging, (NMR); overall survival, (OS); positron-emitting tomography, (PET); Serum mesothelin-related protein, (SMRP); simian-virus 40, (SV-40) Received: 13 January; Revised: 30 January Accepted: 4 February; electronically published: February 2008 Summary Malignant Pleural Mesothelioma is an asbestos-related disease with rising incidence. Diagnosis is often late in the course of the disease because of its insidious onset. Treatment is difficult because of the natural resistance of this tumor-entity. The diagnostic work-up as well as therapeutic options are outlined in this review article. I. Introduction Before 1950, Malignant Pleural Mesothelioma (MPM) was a very rare condition. With the rising use of asbestos after World War II it became more frequent. In the early nineteen-sixties the link between asbestosexposure and MPM was first recognized (Wagner and Sleggs, 1960; Thomson 1963). Asbestos exposure is either occupational or environmental. The latter can be due to air pollution by asbestos-processing facilities or natural exposure in the soil (Constantoupolos et al, 1985). Although the use of asbestos was widely abandoned since 1980 in the western countries, the incidence of MPM will continue to rise until approximately 2020 (Peto et al, 1999). This is due to the long latency between asbestos exposure and development of MPM (up to 58 years) (Kroidl et al, 2000). Other risk factors for the development of MPM are the simian-virus 40 (SV-40) and ionizing radiation. SV-40 DNA can be found in approximately 60% of MPM but also in ependymomas, brain and bone tumours (Rizzo et al, 1998). The virus is a potent inhibitor of tumoursuppressor genes and is considered a co-factor in carcinogenesis. Simian virus 40 was a contaminant in polio vaccines administered to million people in the United States, mostly children, between 1955 and 1963 (Stratton et al, 2002). However, the role of the virus in the pathogenesis of MPM is yet unproven (MacLachlan 2002; Price and Ware 2004). The use of the radioactive, alpha-emitting contrast medium 232ThO2 (Thorotrast ) is another risk factor. Up to 7.8% of exposed patients given more than 20ml of Thorotrast developed MPM (Andersson et al, 1995). There is also a higher incidence of MPM in survivors of the Hiroshima and Nagasaki nuclear attacks (White and Abratt 2005). In summary, the most important risk factor for MPM is undoubtedly asbestos which is responsible for approximately 70-90% of cases (Yates et al, 1997). MPM is a devastating disease with a grim prognosis. Median survival ranges from approximately 4 to 18 months depending on the histological subtype (sarcomatous has a worse prognosis compared to epithelial subtype), tumour stage and some patient derived factors (general condition, age, weight loss, pain, platelets, asbestos exposure) (Manegold et al, 2006). In a series of 49 consecutive patients at our institution median progression free survival was 8 months (Figure 1). II. Diagnosis of MPM A. Signs and Symptoms The onset of symptoms in MPM is subtle and nonspecific, so diagnosis is often late in the course of disease. The majority of patients present with dyspnea and/ or chest pain (Lee et al. 2000). Fatigue, fever and night sweats are also common. B. Imaging techniques The first diagnostic step after clinical examination is a chest X-ray. The most frequent finding here is a pleural effusion (Lee et al, 2000). 73

2 Heigener et al: Treatment of malignant pleural mesothelioma Figure 1. Progression free survival of 49 consecutive patients with MPM at our institution in months. In one series the majority of MPM is located on the right side, in five percent of cases there is a bilateral involvement (Antman 1981). However in our patients there were no bilateral manifestations and 65% right-sided locations in a series of 49 consecutive patients (unpublished data). The next diagnostic step when MPM is suspected should be a computed tomography or a nuclear magnetic resonance imaging (NMR) of the chest. The former is more available than the latter and of nearly similar accuracy. NMR provides little more information concerning chest wall and diaphragm invasion (Heelan et al, 1999). The addition of positron-emitting tomography (PET) can help distinguish between benign pleural thickening and foci of malignancy and makes mediastinal lymph-node staging more accurate (Wang et al, 2004). However this method is not readily available in many institutions. MPM is characterized by local spread involving the mediastinal lymph nodes. There are many case reports about distant metastases in MPM, however in general they seldom occur. Therefore we do not perform any routine imaging technique (i.e. bone-scintigraphy or NMR of the brain) beyond thoracical imaging. Staging should be done based on the TNM staging system by the International mesothelioma interest group (IMIG): the T-descriptors are designated as T1 to T4 describing the local extend of the tumour. T1 is localized disease on the pleura (T1a: parietal pleura only; T1b: involvement of visceral pleura), T2 describes diaphragmal or direct lung involvement, T3 describes involvement of the endothoracic fascia or mediastinal fat (locally advanced but technically resectable) and T4 the diffuse invasion of the chest wall, peritoneum, spine, peri- or myocard as well as the contralateral pleura (locally advanced, unresectable). The N-descriptors N1 to N3 are identical as the ones used in the staging of lung cancer: N1 describes ipsilateral pulmonary or hilar nodes, N2 ipsilateral or subcarinal mediastinal nodes and N3 contralateral mediastinal or supraclavicular nodes. M0 denotes the absence and M1 the presence of distant metastases. The corresponding stages are shown in Table 1 (Rusch 1995). B. Achievement of a tissue diagnosis Evidence of MPM in pleural fluid is found in 33-84% of cases (Whitaker 2000). Aspiration-cytology of pleural fluid (if present) is specific but lacks sensitivity. The latter can be improved with the measurement of hyaluronic acid in the pleural fluid which is markedly elevated in MPM compared to other malignant effusions (Welker et al, 2007). Nevertheless, obtaining a histological specimen is often necessary for an exact diagnosis. Image guided, trans -thoracical core-biopsies lack direct visualisation of the tumor and therefore carry a higher risk of false-negative results compared to direct thoracoscopic forceps-biopsy either in local anaesthesia or video-assisted under general anaesthesia (VATS). Immunhistochemistry should be performed for an exact diagnosis. Typical positive markers are calretinin (epithelial subtype), MNF 116 and AE1/ AE3 cytokeratins, vimentin and many more (Mueller 2005). C. Serum markers Two markers deserve special consideration: Serum mesothelin-related protein (SMRP) and serum osteopontin. SMRP has a sensitivity of 83% and a specifity of 95% in detecting MPM in one study. There are also level-changes parallel to the tumour size, suggesting that it might be a good diagnostic tool for monitoring (Robinson, 2005). The addition of the tumour-marker CA125 did not improve sensitivity (Creaney et al, 2007). Serum osteopontin is significantly elevated in patients with asbestos exposure and MPM compared to patients with asbestos exposure alone (Pass, 2005). It seems to have a lower diagnostic accuracy than SMRP due to its Table 1. Stages of MPM (Rusch, 1995) Stage TNM Ia T1aN0M0 Ib T1bN0M0 II T2N0M0 III Any T3M0; any N1M0; any N2M0 IV Any T4, any N3; any M1 74

3 Cancer Therapy Vol 6, page 75 low specifity (Grigoriu, 2007). However, by now -lacking large validation series- both markers are not routinely used in our clinical practise. III. Therapy of MPM A. Role of radiation therapy External beam radiation of the hemithorax as a single treatment of MPM has no effect on survival (Baldini 2004). However some series suggest that it might have its place in a multimodality approach to improve local control, especially when using modern techniques (see below) (Rice et al, 2007; Lee et al, 2002; Rusch et al, 2001). Another questionable indication for radiotherapy in MPM is the irradiation of surgical wounds and drainagesites, fearing that otherwise the tumour will spread to the subcutaneous layer along the surgical tract. There are three small randomized controlled trials and some case series. One of the controlled trials showed a small benefit on local control (Boutin et al,1995) and the other two showed no benefit at all (Bydder et al, 2004; O Rourke et al, 2007). In one case series of 85 consecutive patients treated with different chemotherapy regimens without radiation none developed surgical tract metastasis (Pinto et al, 1995). As a result, the practise is discussed with considerably controversy and we do not recommend this procedure routinely although it is implemented in the guidelines of the British Thoracic Society (British Thoracic Society Standards of Care Committee, 2007). External beam radiation is moderately effective in the reduction of pain due to MPM. In one case series of 189 patients 50% had a benefit in terms of pain control when 36 Gray in 4- Gray fractions were used. However pain recurred in a median of 69 days (de Graaf- Strukowska et al, 1999). In a review on that topic, pain relief is described for 50 to 70% of patients (Baldini 2004). B. Role of surgery There are mainly two surgical approaches to MPM. First there is a quite aggressive option, the extrapleural pleuropneumectomy (EPP) or a solely cytoreductive procedure: decortication and/ or pleurectomy. The latter can sometimes be performed via VATS. A case series describing the trimodality approach of EPP plus consecutive chemoradiation showed a five-year survival rate of 22%. However this was a selected group of patients and a control group was lacking (Sugarbaker and Norberto 1998). In another trial the two surgical procedures were compared, showing a benefit in progression free survival for EPP (319 vs. 197 days, p= 0.019) but only a non significant benefit favouring EPP in overall survival (497 vs. 327 days, p=0.079) (Stewart et al, 2004). In both papers the involvement of mediastinal lymph nodes was a predictor of poor survival. To date a large randomized trial is ongoing to clarify the role of radical surgery in MPM (Treasure et al, 2006). C. Role of medical therapy 1. Older Regimens Numerous trials have been conducted in the 1980 s and 1990 s with various cytotoxic agents in the treatment of MPM. Focussing on remission there were some agents with moderate efficacy: the anthracyclines, platinum compounds, alkylating agents, mitomycin C and antimetabolites. However, these results were only based on small case series. No large randomized controlled trials were available and the impact on survival was not clarified (Ryan et al, 1998). There were also some case series with combination therapies but there was no clear evidence for superiority over monotherapies (Ryan et al, 1998). 2. Vinca-Alkaloids Two modern vinca-alkaloids show promising activity in phase II-trials in MPM: Vinorelbine and vinflunine. Vinorelbine was tested in a weekly infusion regimen in 29 patients. 24% of patients achieved a partial response and 55% had stable disease. There was also some improvement in quality of life (Steele et al, 2000). However the patient number was small and phase III studies are clearly needed. 67 patients were enrolled in a phase- II study with vinflunine. Response rate was 13.8% and median survival was 10.8 months (Talbot et al, 2007). 3. Gemcitabine There are several Phase-II studies of either gemcitabine alone ore in combination with cisplatin (Kindler et al, 2002). Monotherapy failed to show significant activity in two trials (van Meerbeeck et al, 1999; Kindler et al, 2001). The combination achieved up to 47.6% partial responses (Byrne et al, 1999). However, as with vinorelbine, phase-iii data are lacking. 4. Taxanes There is only sparse data on paclitaxel in MPM. One trial showed only 9% remissions with high-dose paclitaxel (Vogelzang et al, 1999). Docetaxel also showed at most mildly efficacy as monotherapy (Vorobiof et al, 2002; Belani et al, 2004). Also in combination with irinotecan, the results are disappointing (Knuutila et al, 2000). 5. Antifolates Alpha folate receptor protein is overexpressed in MPM-Cells in approximately 70% of cases. This might explain the responsiveness to antifolate drugs (Bueno et al, 2001) as shown in a group of 60 patients receiving high dose methotrexate. There were 37% responses with one complete response (Solheim et al, 1992). In the beginning of this century, a new multi-targeted antifolate, pemetrexed, was evaluated for its efficacy in MPM. A phase II -trial including 64 patients showed an overall response rate of 14.1% for monotherapy with the substance. Interestingly, overall survival (OS) was higher in those patients who were supplemented with folic acid and vitamin B12 (13 months OS vs 8 months in the not supplemented group). Moreover, neutropenia was lower in the supplemented group (4 grade! neutropenias in the supplemented group vs. 11 in the non-supplemented group) (Scagliotti et al, 2003). However, because of the small subgroups no definite conclusion could be drawn on the impact of vitamin supplementation. A phase III trial with 456 enrolled patients compared pemetrexed and cisplatin with cisplatin alone (Vogelzang et al, 2003). This 75

4 Heigener et al: Treatment of malignant pleural mesothelioma was the first trial ever in MPM showing a significant survival advantage for a chemotherapy regimen with a median survival of 12.1 months for the cisplatin/ pemetrexed-arm vs 9.3 months for cisplatin alone (p=0.02). Again, toxicities were significantly reduced after adding folic acid and vitamin B12 to the regimen. The combination of cisplatin and pemetrexed can now be considered standard first line therapy in MPM in those patients, who can tolerate this fairly toxic regimen. Because of the considerably toxicity of cisplatin, it is sometimes replaced by carboplatin for patient comfort in this palliative setting (Figure 2). Another combination with an antifolate drug with some efficacy in a phase II trial are oxaliplatin and ralitrexed. 70 patients were enrolled, the overall response rate was 20% and one year survival was 26% (Fizazi et al, 2003). There is one case series suggesting that pemetrexed also has efficacy in second-line treatment after a platinumcontaining doublet (mostly platinum/ vinorelbine). In patients treated with carboplatin + pemetrexed (n=11) there were 18% responses with a median time to progression of 32 weeks. In patients treated with pemetrexed alone the numbers were 21% and 21 weeks respectively. Median survival was 39 weeks and 42 weeks respectively (Sorensen et al,2007). 6. Biologicals Although endothelial-growth factor-receptor (EGFR) is overexpressed in the majority of MPM (Dazzi et al, 1990), the inhibition of the downstream signalling of EGFR by means of erlotinib does not seem to work. In a study with 64 patients with MPM, 75% of tumours showed high expression of EGFR. However treatment with erlotinib did not result in any objective remission (Garland et al, 2007). The reason might be, that simple overexpression of EGFR is not predictive of response to erlotinib in other cancers. Only EGFR-mutations seem to have some predictive value. The antisense-oligonucleotide ranpirnase blocks the 30S-subunit of the ribosome and interferes with protein synthesis. In a phase-ii trial a median survival time of 18.5 months was observed (Mikulski et al, 2002). These results encouraged to perform a phase-iii study comparing doxorubicin and ranpirase with doxorubicin alone. The recruitment was finished recently and the results are pending. D. Multimodality treatment As described above, multimodality treatment approaches seem to be promising in a selected group of MPM patients, those in a good performance status (Sugarbaker and Norberto, 1998). In another case series focussing on prognostic factors in MPM, the data suggest that surgery within a multimodality approach improves survival more than surgery alone (pleurectomy or EPP: 10.3 months median survival; pleurectomy or EPP plus chemotherapy and external beam radiotherapy: 20.1 months median survival). There was no statistical significant difference between pleurectomy and EPP in terms of survival when used as a single-modality (median survival 15.8 vs months) (Flores et al, 2007). In a phase-ii trial the combination of hyperthermia (41.8 Celsius body temperature) with chemotherapy (ifosfamide, carboplatin and etoposide) resulted in a response rate of 20% and a two-year survival of 20% (Bakhshandeh et al, 2003). However to date, no phase-iii data were present to support this approach. E. Palliative Treatment Because of the devastating course of the disease almost all patients need sufficient palliative care. Main symptoms are pain and dyspnoea. Pain can be either neuropathic due to infiltration of intercostal nerves or somatic due to chestwall involvement. Often there is a combination of both. Somatic pain responds to non-steroidal analgesic drugs and opiates. Neuropathic pain should be managed with opiates and co-analgesics like antidepressants (i.e. amitryptiline) or anticonvulsants (i.e. carbamazepine, pregabaline; Doyle et al. 2004). Dyspnoea results from pleural effusion as well as entrapment of the lung by the pleural tumor. Pleurodesis either by VATS or pleuroscopy should be done in the former case. However the latter needs symptomatic treatment with opioids (Lee, YC, 2002). IV. Summary MPM is notoriously resistant to therapy. Moreover the natural course can vary widely from only a few months of survival to several years. Because of the diffuse growth pattern, treatment response is not easy to evaluate and inter-observer differences can be great. 76

5 Cancer Therapy Vol 6, page 77 Figure 2. CT-scans before (left) and after (right) four cycles of carboplatin and pemetrexed. All these factors make good clinical trials difficult to perform and many issues remain unanswered. As a practical approach we recommend to establish the diagnosis via VATS in patients with adequate performance status or via pleuroscopy. With the former, pleurectomy/ decortication can be done. The role of radical surgery (EPP) needs to be clarified. Afterwards chemotherapy with platinum and pemetrexed should be made. Radiotherapy is indicated for palliative reasons (i.e. pain control) but not for tumour reduction. In patients with poor performance status monotherapy with pemetrexed is a reasonable option. However, these recommendations lack clear evidence which will hopefully come with further clinical trials. References Andersson M, Wallin H, Jönsson M, Nielsen LL, Visfeldt J, Vyberg M, Bennett WP, De Benedetti VM, Travis LB, Storm HH (1995) Lung carcinoma and malignant mesothelioma in patients exposed to Thorotrast, incidence, histology and p53 status. Int J Cancer 63, Antman KH (1981) Clinical presentation and natural history of benign and malignant Mesothelioma. Semin Oncol 8, Bakhshandeh A, Bruns I, Traynor A, Robins HI, Eberhardt K, Demedts A, Kaukel E, Koschel G, Gatzemeier U, Kohlmann T, Dalhoff K, Ehlers EM, Gruber Y, Zumschlinge R, Hegewisch-Becker S, Peters SO, Wiedemann GJ (2003) Ifosfamide, carboplatin and etoposide combined with 41.8 degrees C whole body hyperthermia for malignant pleural mesothelioma. Lung Cancer Mar 39, Baldini EH (2004) External beam radiation therapy for the treatment of pleural mesothelioma. Thorac Surg Clin 14, Belani CP, Adak S, Aisner S, Stella PJ, Levitan N, Johnson DH; Eastern Cooperative Oncology Group (2004) Docetaxel for malignant mesothelioma, phase II study of the Eastern Cooperative Oncology Group. Clin Lung Cancer 6, Boutin C, Rey F, Viallat JR (1995) Prevention of malignant seeding after invasive diagnostic procedures in patients with pleural mesothelioma. A randomized trial of local radiotherapy. Chest 108, British Thoracic Society Standards of Care Committee: BTS Statement on malignant mesothelioma in the UK, Thorax, Nov 2007; 62 Suppl 2: ii1-ii19 Bueno R, Appasani K, Mercer H, Lester S, Sugarbaker D (2001) The alpha folate receptor is highly activated in malignant pleural mesothelioma.. Thorac Cardiovasc Surg 121, Bydder S, Phillips M, Joseph DJ, Cameron F, Spry NA, DeMelker Y, Musk AW (2004) A randomised trial of singledose radiotherapy to prevent procedure tract metastasis by malignant mesothelioma. Br J Cancer 91, Byrne MJ, Davidson JA, Musk AW, Dewar J, van Hazel G, Buck M, de Klerk NH, Robinson BW (1999) Cisplatin and gemcitabine treatment for malignant mesothelioma, a phase II study. J Oncol Pract 17, Constantopoulos SH, Goudevenos JA, Saratzis N, Langer AM, Selikoff IJ, Moutsopoulos HM (1985) Metsovo lung, pleural calcification and restrictive lung function in northwestern Greece. Environmental exposure to mineral fiber as etiology. Environ Res 10, Creaney J, van Bruggen I, Hof M, Segal A, Musk AW, de Klerk N, Horick N, Skates SJ, Robinson BW (2007) Combined CA125 and mesothelin levels for the diagnosis of malignant mesothelioma. Chest 132, Dazzi H, Hasleton PS, Thatcher N, Wilkes S, Swindell R, Chatterjee AK (1990) Malignant pleural mesothelioma and epidermal growth factor receptor (EGF-R) de Graaf-Strukowska L, van der Zee J, van Putten W, Senan S (1999) Factors influencing the outcome of radiotherapy in malignant mesothelioma of the pleura. A single institution experience with 189 patients. Int J Radiat Oncol Biol Phys 43, Fizazi K, Doubre H, Le Chevalier T, Riviere A, Viala J, Daniel C, Robert L, Barthélemy P, Fandi A, Ruffié P (2003) Combination of raltitrexed and oxaliplatin is an active regimen in malignant mesothelioma, results of a phase II study. J Oncol Pract 21,

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