Good symptom relief with palliative MVP (mitomycin-c, vinblastine and cisplatin) chemotherapy in malignant mesothelioma

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1 Annals of Oncology 9: 9-7, Khmer Academic Publishers. Printed in the Netherlands Original article Good symptom relief with palliative MVP (mitomycin-c, vinblastine and cisplatin) chemotherapy in malignant mesothelioma G. W. Middleton, I. E. Smith, M. E. R. O'Brien, A. Norton, T. Hickish, K. Priest, L. Spencer & S. Ashley Lung Unit, Royal Marsden NHS Trust, Sutton. Surrey. UK Summary Purpose: To evaluate the therapeutic impact of a simple combination chemotherapy regimen on symptoms related to malignant mesothelioma. Materials and methods: Between October 98 and June 997, 9 patients with advanced inoperable malignant mesothelioma were treated with palliative MVP (mitomycin-c 8 mg/ m q. six weeks, vinblastine mg/m q. three weeks and cisplatin 5 mg/m q. three weeks) chemotherapy and assessed for objective response and relief of symptoms. Results: Eight of 9 patients (%) achieved an objective partial response with a median duration of nine months: only five patients had progression of disease during chemotherapy. Twenty-four of 9 (%) had an overall improvement in their symptomology with particularly good responses for pain (79%). These benefits were independent of performance status. Resolution of symptoms was achieved in all responding patients within two treatment cycles. There was no statistically significant difference in duration and incidence of symptom response in those patients achieving radiological PR compared with those with no change and more than % of patients with radiological no change obtained useful symptom control. The treatment was well tolerated with only four patients developing grade leucopenia and three with grade nausea. Conclusions: MVP is a well tolerated regimen and its use in malignant mesothelioma provides useful symptomatic benefit. These results should be the basis for further trials of MVP in the management of mesothelioma with symptom control as a principal endpoint. Key words: chemotherapy, mesothelioma, symptom relief Introduction The incidence of mesothelioma is rising; it is nearly always incurable and its principal symptoms of pain and dyspnoea are difficult to treat. Surgery and radiotherapy are of limited benefit if any. Two recent overviews of chemotherapy were likewise pessimistic about the value of single agent or combination chemotherapy regimens [,]. In the earlier overview the only drugs with acceptable activity in trials meeting standard criteria for phase II studies were detorubicin and doxorubicin. Such activity could not be confirmed in subsequent trials for either drug. A more recent overview collated single agent response rates to trials including more than 5 patients. Only five drugs besides detorubicin showed > % activity. Of these, the anti-folates appear most promising and, a response rate of 7% in evaluable patients treated with high-dose methotrexate and leuocovorin rescue is the highest reported in any phase II study []. Although a Cancer and Leukaemia Group B study of trimetrexate showed only modest response rates, the months median survival duration is the longest seen in any CALGB trial of chemotherapy in malignant mesothelioma [4]. Finally, another folate antagonist, edatrexate, demonstrated 5% activity in assessable patients [5]. Of the remaining drugs with possible activity, the 4% reported response rate for ifosfamide [] has not been confirmed in two large subsequent series [7, 8] and the response rate for mitomycin-c (%) and pirarubicin (%) remains unconfirmed. Both of the overview analyses concluded that combination chemotherapy did not appear to offer any benefit over single agent chemotherapy and that no combination appeared preferable to any other. In the earlier overview only three combinations met the accepted criteria for activity in phase II trials; these were mitomycin-c plus cisplatin, doxorubicin plus cisplatin and high-dose methotrexate plus leucovorin rescue with vincristine. The results for the first two combinations were not subsequently confirmed and, when the data for all trials using the third combination were pooled, the regimen no longer appeared to be particularly active. The lack of a standard regimen has meant that the overwhelming majority of studies are designed solely to detect activity as defined formally in terms of objective response. However, objective response rates do not necessarily reflect symptom relief, an endpoint that is likely to be of more clinical value to the patient. We have recently demonstrated significant palliative chemotherapy benefit in terms of symptom control with low toxicity, in non-small-cell lung cancer using a mito-

2 7 mycin/cisplatin-based regimen (MVP) [9]. Symptom relief was frequently achieved in patients failing to achieve an objective response as denned by standard criteria. A Cancer and Leukaemia Group B randomised comparison of doxorubicin and cisplatin against mitomycin-c and cisplatin shows an improved response rate for the mitomycin/cisplatin combination []. The basis of the inclusion of mitomycin-c and cisplatin in this randomised phase II trial was an earlier pilot study showing a % response rate conducted following the demonstration of synergy between cisplatin and mitomycin-c in a human mesothelioma xenograft model []. In this study we have examined the activity of MVP chemotherapy in patients with advanced malignant mesothelioma and specifically assessed the impact of such treatment on symptom relief. Materials and methods Patient characteristics Thirty-nine patients were entered into the study between October 98 and June 997. Patients had histologically proven malignant mesothelioma, with histology reviewed by pathologists at the Royal Marsden Hospital or the Royal Brompton Hospital, London; adequate renal function (EDTA clearance > ml/min); normal haematological indices; no previous malignancy; no serious medical or psychiatric illness; signed informed consent. All patients underwent pre-treatment physical examination, full blood count, plasma electrolytes, urea and creatinine, serum liver function tests and estimation of renal function using 5 Cr EDTA clearance, or Cockcroft and Gault calculation [], together with chest radiography. Chest CT scan was performed, to stage disease more accurately and to evaluate maximum response and repeat chest X-ray assessment was made prior to each course of chemotherapy. Only two patients were not assessed by CT scanning prior to the commencement of treatment. Thirty-one of 7 evaluable patients were either assessed by CT scan as having advanced inoperable disease (T4, stage IV) as staged according to the International Mesothelioma Investigative Group (IMIG) [], which includes locally advanced tumours which are felt to be technically unresectable, or were referred directly from cardiothoracic surgeons with disease which had been assessed surgically as being inoperable. Of the remaining six patients,fivehad either stage III disease or were considered medically unfit for surgery. Performance status was assessed by WHO criteria [4]. Table Patient characteristics. Number of patients Sex Male Female Age (in years) Median Range WHO PS at start of treatment Previous treatments Tamoxifen 9 7 years patient 5 Datient None of the patients received radiation therapy. Although therapeutic pleural aspiration was performed in a small number of patients, this was either in patients before the start of treatment or upon symptomatic progression of dyspnoea and therefore had no impact on the duration of palliation of this symptom. Assessment of response and toxicity Complete response (CR) was defined as the disappearance of all known disease for at least four weeks Partial response (PR) was defined as a greater than or equal to 5% decrease in the sum of the products of the tumours' longest dimension and its widest perpendicular measurement for at least four weeks, without the appearance of new lesions or progression of any one lesion. Stable disease (SD/NC) was defined as a less than 5% decrease or less than 5% increase in the size of the measurable disease, without the appearance of new lesions or progression of any lesion > 5%, for a minimum of four weeks Progressive disease (PD) was defined as a greater than 5% increase in one or more of the measurable lesions or the appearance of a new lesion(s). Response duration and survival were calculated from the date of first treatment using the standard life-table method of Kaplan and Meier [5]. Symptom response duration for objective responders and objective non-responders were compared using the log-rank test. Tumour-related symptoms were recorded at the start of treatment under the following general headings: malaise, pain, cough, dyspnoea, or 'other' which was then specified. Symptoms were then reassessed independently of the medical team by a research nurse following each course of treatment with patients asked to grade change in symptoms using simple descriptive criteria as follows: a) complete disappearance of symptoms (CR); b) good improvement of symptoms (PR); c) minor or no change of symptoms (NC); d) worse (PD). Toxicity was assessed according to standard WHO criteria []. Treatment regimen All patients received the following regimen; mitomycin-c 8 mg/m i.v. day (given on courses,, 4 and ), vinblastine mg/m (maximum mg) i.v. day, and cisplatin 5 mg/m i.v. day, repeated every days. Standard intravenous pre- and post-treatment hydration was given with cisplatin. This consisted of.5 litres N Saline + 4 mmol KCL + 4 mg Frusemide over two hours pre-cisplatin. followed by litres N Saline + 4 mmol KCL over hours post-cisplatin. which patients received overnight as an inpatient. Renal function was assessed during the earlier part of the study by EDTA clearance and latterly using the Cockcroft and Gault formula. Dose reductions for cisplatin were as follows: EDTA 4- ml/min - cisplatin dose equivalent to creatinine clearance; creatinine clearance <4 ml/min - no cisplatin given. Treatment was continued until the development of progressive disease, unacceptable toxicity or to a maximum of six cycles in patients achieving objective response and/or symptomatic relief. Results Thirty-nine patients entered into this study. Two patients were not assessable for toxicity, because of clinical deterioration at home and lack of formal follow-up assessment. These were included in assessment of efficacy, as showing progressive disease. Demographic details are presented in Table. A median of three cycles of chemotherapy was given (range -). Objective response and survival Eight of the 9 patients (%) achieved an objective partial response; there were no complete responses. All

3 7 responding patients did so within two courses. Only five of 9 patients had progression of disease during chemotherapy, all within two cycles. Median survival for the entire group was six months (range - months). Median duration of objective response was 9+ months with a range of.5-+ months. Table. Toxicity. WHO grade (worst grade over all courses) 4 Grade - (%) Grade -4 (%) Symptomatic response All patients had tumour related symptoms at the start of treatment. Twenty-four of 9 (%) patients had overall improvement in their symptomatology. Although patients were graded as having overall progression of symptoms, eight of these had an improvement in at least one specific symptom. Responses to specific symptoms were as follows: pain 7 of 4 (79%); dyspnoea of 7 (54%); malaise nine of (9%); cough 4 of (7%). Twenty-seven patients had a performance status (PS) of, had a PS of and two had PS. Attainment of symptom relief was not dependent upon performance status or advanced stage with of 7 patients with PS obtaining symptom relief compared with five of with PS and both patients with PS. All patients achieving a symptomatic response did so within one cycle, except for one who did so within two. All eight patients (%) achieving objective PR achieved a symptomatic response, whilst of (%) of patients with no obvious radiological improvement also derived symptomatic benefit. There was a difference in the duration of symptom response between the patients achieving radiological PR and those assessed as NC, with median time to failure in the former group of + months (+-+ months) with five of eight patients achieving > months of symptomatic relief, compared with just over three months in the latter group (range.5-9+ months). However, three patients with no objective response derived greater than eight months of symptom control, with a further four obtaining 4.5 months of useful palliation. Indeed, there was no statistical difference in the duration of symptom control between objective responders and non-responders. Median symptom response duration for the entire group was five months (range.5-+ months). Six of the eight patients with an objective response received six cycles of chemotherapy; three had maximal symptom response after three cycles and the other three had further incremental symptomatic responses beyond this. Conversely, no patient who achieved a symptomatic response but no objective response appeared to derive further symptomatic benefit beyond three cycles of treatment. Toxicity Treatment was well tolerated, with only three patients developing grade nausea and vomiting and two patients developing grade infection. Neutropenic sepsis in the absence of significant symptomatic benefit was the reason for early stoppage in two patients. One further Non-haematological Infection Nausea/vomiting Mucositis Diarrhoea Alopecia Neuropathy Constipation Nephrotoxicity Haematological Anaemia Leucopenia Thrombocytopenia patient wished to stop treatment early due to grade nausea. Toxicity data are presented in Table. Discussion At present there is no standard management for the treatment of malignant mesothelioma. A limited number of patients with small volume disease and good performance status can be considered for extrapleural pneumonectomy [7]. This approach is controversial however. A Lung Cancer Study Group trial demonstrated that only of 8 patients were able to undergo the procedure with a 5% post-operative mortality [8]. Furthermore there was no improvement in overall survival for this group compared with those undergoing less extensive surgery or non-operative management. This group had both experience in treating malignant mesothelioma and access to a large number of patients [9]. There may be a subset of patients who may benefit from extrapleural pneumonectomy in a multimodality approach together with adjuvant chemoradiation []. A 45%fiveyear survival was seen in patients with epithelial histology and negative mediastinal lymph nodes and such an approach in centres with the necessary experience may be justified. Pleurectomy may provide control of effusions and palliation of dyspnoea and pain []. The delivery of radical doses of radiotherapy is limited by the extensive nature of mesothelioma and the consequent risk of lung and adjacent organ damage. Low dose radiotherapy (less than 4 gray) is relatively ineffective in palliation [] but both the Brompton/ Royal Marsden and Joint Centre for Radiation Therapy series suggest that with higher doses some patients will obtain symptomatic relief with control with effusions. In the former study, in which patients were treated using an off-axis rotational technique, complications included nausea and malaise (in 5% of patients), radiation hepatitis and oesophagitis []. 59 8

4 7 The limitations of chemotherapy have already been summarised in the Introduction. The overview by Ong and Vogelzang [] identified only six regimens showing greater than % activity, enrolling more than 5 patients. These included a % response rate for mitomycin-c and cisplatin in the multicentre randomised phase II CALGB trial mentioned above. The response rate for doxorubicin and cisplatin of 4% in this trial was much lower than in a FONICAP study of the same combination but 5% of these patients were Butchart stage I and CT assessment of response was not used in all patients. The other four studies have so far only been presented in abstract form. Our objective response rate of % is thus in line with that from the CALGB study and demonstrates that MVP has modest activity in malignant mesothelioma. Pharmacodynamic considerations suggest that, for both cisplatin and mitomycin-c, considerably greater exposure of tumour to drug can be achieved by intrapleural instillation when compared to systemic delivery []. Pilot studies suggest that such an approach may be worth pursuing especially in those with small volume disease or as adjuvant therapy following decorticating [4]. Reports of cure using any of the treatment modalities described, either alone or in combination, are largely anecdotal and thus emphasis must be placed on the palliative impact of treatment. This study has shown for the first time as far as we are aware that nearly twothirds of patients treated with a simple chemotherapy regimen can obtain useful symptom relief, for a median of five months and sometimes for almost a year. Symptomatic responses were rapidly obtained, independent of stage and crucially occurred in over % of patients who did not achieve an objective response. Toxicity was relatively mild in most patients and only three preferred to stop because of side effects. Patients failing to respond symptomatically could be selected early on during treatment, after one or at the most two courses, thus sparing them the need for protracted ineffective chemotherapy. There was a suggestion that patients obtaining an objective response to treatment derived further incremental benefit when receiving further chemotherapy up to a maximum of six cycles whereas patients not objectively responding did not appear to obtain benefit beyond three to four cycles. The optimal duration of chemotherapy requires further assessment in the context of a randomised study. We believe that these results, with a low toxicity, low cost regimen should be the basis for larger randomised trials of MVP compared with other regimens or with best supportive care in the palliative management of malignant mesothelioma, using symptom relief as a principal endpoint. References. Krarup Hansen A. Hansen HH. Chemotherapy in malignant mesothelioma: A review. Cancer Chemother Pharmacol 99; 8: 9-.. Ong FT, Vogelzang NJ. Chemotherapy in malignant pleural mesothelioma: A review. J Clin Oncol 99: 4: Solheim OP. Saeter G, Finnanger AM et al. High-dose methotrexate in the treatment of malignant mesothelioma of the pleura. A phase II study. Br J Cancer 99; 5: Vogelzang NJ, Weissman LB, Herndon JE et al. Trimetrexate in malignant mesothelioma: A CALGB phase II study. J Clin Oncol 994; : Belani CP, Herndon J, Vogelzang NJ et al. Edatrexate for malignant mesothelioma: A phase II study of the Cancer and Leukaemia Group B, 9. Proc Am Soc Clin Oncol 994; : 9 (Abstr 87).. Alberts AS, Falkson G, Zyl LV. Malignant pleural mesothelioma: Phase II pilot study of Ifosfamide and mesna. J Natl Cancer Inst 988; 8: Zidar BL, Metch B, Balcerzak SP et al. A phase II evaluation of ifosfamide and mesna in unresectable diffuse malignant mesothelioma: A Southwest Oncology Group Study. Cancer 99; 7' Falkson G, Hunt M, Borden EC et al. An extended phase II trial of Ifosfamide plus mesna in malignant mesothelioma. Invest New Drugs 99; : 7^. 9. Ellis PA, Smith IE, Hardy JR et al. Symptom relief with MVP (mitomycin-c, vinblastine and cisplatin) chemotherapy in advanced non-small-cell lung cancer. Br J Cancer 995; 7: -7. Chahinian AP, Antman K. Goutsou M et al. Randomized phase II trial of cisplatin with mitomycin or doxorubicin for malignant mesothelioma by the Cancer and Leukaemia Group B J Clin Oncol 99; :559-5 Chahinian AP, Szrafer L, Malawi S. Comparative activity of three platinum analogues against human malignant mesothelioma xenografts in nude mice. Proc Am Assoc Cancer Res 985; : (Abstr).. Cockcroft DW, Gault MH. Prediction of creatinine clearance from serum creatinine. Nephron 97, : -4.. Rusch VW. A proposed new international TNM staging system for malignant pleural mesothelioma (from the International Mesothelioma Interest Group). Chest 995; 8: Miller AB, Hoogstraten B, Staquet M. Winkler A. Reporting results of cancer treatment. Cancer 98; 47: Kaplan EL, Meier P. Non parametric estimation from incomplete estimation. J Am Stat Assoc 958; 5: World Health Organisation. Handbook for Reporting Results of Cancer Treatment. WHO Offset Publication No. 48. Geneva: WHO Butchart EG. Ashcroft T, Barnsley WC et al. Pleuropneumonectomy in the management of diffuse malignant mesothelioma of the pleura. Experience with 9 patients. Thorax 97; : Rusch VW. Piantadosi S, Holmes EC. The role of extrapleural pneumonectomy in malignant pleural mesothelioma. A Lung Cancer Study Group trial. J Thorac Cardiovasc Surg 99: : Rusch VW. Trials in malignant mesothelioma. LCSG 85 and 88. Chest 994; : Sugarbaker DJ. Strauss GM. Lynch TJ et al. Node status has prognostic significance in the multimodality therapy of diffuse, malignant mesothelioma. J Clin Oncol 99: : Law MR. Gregor A. Hodson ME et al. Malignant mesothelioma of the pleura: a study of 5 treated and 4 untreated patients. Thorax 984: 9: Gordon W. Antman K. Breenberger et al. Radiation therapy in the management of patients with mesothelioma. Int J Radiat Oncol Biol Phys 98: 8: 9.. Rusch V. Niedzwiecki D, Pow Y et al. Intrapleural cisplatin and

5 7 mitomycin for malignant mesothelioma following pleurectomy: Correspondence to: Pharmacokinetic studies. J Clin Oncol 99; : -. Dr.. E. Smith (Head of Lung Unit) 4. Markman M, Cleary S, King M et al. Cisplatin and cytarabine Royal Marsden NHS Trust administered intrapleurally as treatment for malignant pleural Sutton effusions. Med Pediatr Oncol 985; : 9-. Surrey, SM 5PT UK Received 7 October 997; accepted 8 December 997.

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