Asia-Pacific Journal of Clinical Oncology 2016; 12: e298–e304
doi: 10.1111/ajco.12192
ORIGINAL ARTICLE
Impact of the lung oncology multidisciplinary team meetings on the management of patients with cancer Kim Ann UNG, Belinda A CAMPBELL, Danny DUPLAN, David BALL and Steven DAVID Department of Radiation Oncology and Cancer Imaging, Peter MacCallum Cancer Centre, East Melbourne, Victoria, Australia
Abstract Aims: Multidisciplinary team (MDT) meetings are increasingly regarded as a component of multidisciplinary cancer care. We aimed to prospectively measure the impact of MDT meetings on clinicians’ management plans for lung oncology patients, and the implementation rate of the meeting recommendations. Methods: Consecutive patient cases presented at the weekly lung oncology MDT meetings were prospectively enrolled. Investigators compared the clinicians’ management plans pre-meeting with the consensus plans post-meeting. The meeting was considered to have an impact on management plans if ≥1 of the following changes were detected: tumor stage, histology, treatment intent or treatment modality, or if additional investigations were recommended. Investigators reviewed hospital patient records at 4 months to determine if the meeting recommendations were implemented. Reasons for non-implementation were also recorded. Results: Of the 55 eligible cases, the MDT meeting changed management plans in 58% (CI 45–71%; P < 0.005). These changes included: additional investigations (59%), or changes in treatment modality (19%), treatment intent (9%), histology (6%) or tumor stage (6%). The meeting recommendations were implemented in 72% of cases. Reasons for non-implementation included deteriorating patient performance status, clinician’s preference, the influence of new clinical information obtained after the meeting or patient decision. Conclusion: MDT meetings significantly impact on the management plans for lung oncology patients. The majority of MDT recommendations (72%) were implemented into patient care. These findings provide further evidence to support the role of MDT meetings as an essential part of the decision-making process for the optimal multidisciplinary management of patients with cancer. Key words: decision-making, lung cancer, management, multidisciplinary meeting, tumor board.
INTRODUCTION The increasing complexity of management of patients with cancer has led to the widespread implementation of multidisciplinary teams (MDTs).1 Multidisciplinary
Correspondence: Dr Kim Ann Ung MBBS (Hons) BMedSc, Department of Radiation Oncology and Cancer Imaging, Peter MacCallum Cancer Centre, 7 St. Andrews Place, East Melbourne, Vic. 3002, Australia. Email: [email protected] Conflict of interest: none Accepted for publication 16 February 2014.
© 2014 Wiley Publishing Asia Pty Ltd
cancer care has shown to improve outcomes2,3 and adherence to evidence-based guidelines4,5 as well as patient satisfaction.6 Retrospective evidence also suggests an improvement in overall survival favoring oncology patients discussed in MDT meetings.7,8 MDT meetings, a common feature of multidisciplinary cancer care, enable patient management plans to be based on a broad range of expert knowledge and all aspects of treatment options can be considered.9 Many studies have demonstrated the benefits of MDT meetings in the management of patients with cancer. Boxer et al. compared patients with newly diagnosed lung cancer who were presented at MDT meetings and those
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who were not within the same time period, and demonstrated that MDT discussion was associated with better treatment receipt and more referrals to palliative care.10 Health care professionals concur that MDT meetings provide a decision-making forum for clinicians to develop peer-reviewed management plans, help improve communication between specialties, and provide a good educational resource.9,11 We were interested to determine whether MDT meetings had an impact on the clinicians’ management plans. To measure the efficacy of MDT meetings, previous studies have looked into the implementation rate of the meeting recommendations of various tumor streams.12–14 Other studies compared whether there were any changes in the tumor findings or the proposed management plans by the referring clinicians with that by the MDT meeting.15,16 In our study, we aimed to assess the impact of the Peter MacCallum Cancer Centre (Peter Mac) lung oncology service MDT meetings on clinicians’ management plans by prospectively comparing the proposed management plans pre- and post-MDT meeting. The primary end point was to determine the proportion of cases in which the MDT meeting resulted in a change to the clinicians’ pre-meeting management plans. The secondary end point was to determine the implementation rate of the MDT recommendations.
METHODS Approval for this study was obtained from the local ethics committee at Peter Mac. The lung oncology service at Peter Mac meets weekly to discuss patient management plans. Key members of the team include medical oncologists, radiation oncologists, thoracic surgeons, respiratory physicians, a radiologist, a nuclear medicine physician, a cancer nurse coordinator and allied health professionals. Pathology review is available upon request. The patient cases for MDT presentation were selected at the discretion of lung oncology clinicians as needing multidisciplinary input. Clinical history, medical imaging and pathology were reviewed and discussed, and a final consensus is documented. This decision is then discussed with the patient in clinic before a final management plan is agreed upon. Consecutive patient cases presented at the weekly lung oncology MDT meetings were anonymously enrolled in the study. Clinicians submitted cases for presentation in electronic form with relevant clinical information and their proposed management plans; that is, clinicians were
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prospectively asked, “what would your management plans be if the MDT meetings did not exist?” Prior to the MDT meeting, clinical information and the clinicians’ proposed management plans were extracted. For uniformity, one investigator performed this task. If the required information was unavailable, the referring clinicians were contacted to provide further information. Patient demographic data, reasons for referral, Eastern Cooperative Oncology Group performance status, smoking status, tumor histology, tumor stage, proposed investigations, treatment intent and proposed treatment modality were collected. The number of times each case was presented at the meeting was also recorded. Cases were excluded if the clinicians’ proposed management plans were not provided pre-meeting or if there was clinical information unavailable to the clinician prior to the meeting that would affect decision-making (e.g. staging investigation or biopsy results). During the MDT meeting, a second investigator collected the MDT recommendations. To limit bias, this investigator was blinded to the initial pre-meeting plans. For each patient, any changes to the tumor stage or histology, treatment intent, treatment modality and recommendation for further investigations were documented. On completion of the MDT meetings, the investigators compared the pre- and post-MDT meeting management plans recorded. The MDT meeting was considered to have an impact on management plans if the following changes were detected: tumor stage, histology, treatment intent or treatment modality, or additional investigations recommended. If there was more than one change recorded for a patient, the most clinically significant one was chosen at the discretion of one study investigator with experience in thoracic cancer management. The MDT meeting did not have an impact if there was no change to the clinicians’ pre-meeting plans or if the MDT was unable to make recommendations at the meeting. To assess the rate of implementation, investigators reviewed the hospital patient records 4 months after the meeting. For an MDT recommendation to be considered implemented, all aspects of the recommendation (e.g. treatment, additional investigations, referral to specialist units and trial accrual) for each patient case must be fulfilled. Reasons for non-implementation were also recorded.
Statistical analysis For analysis of the primary end point, the Peter Mac lung oncology MDT meeting was not considered worthwhile
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with respect to patient management if the rate of change to the clinician’s proposed management plans was less than 15%. This figure was prospectively determined. It was estimated from the MDT attendees that the true rate of change of management plans was at least 30% in this population. With power of 80% and type 1 error of 5%, a sample size of 51 patients was required. To allow for potential ineligibilities, data were collected from the first 68 consecutive patients. To summarize clinical data, descriptive statistics were reported in the form of means, standard deviations and ranges for quantitative variables. Categorical variables were reported as counts and percentages with 95% confidence intervals. One sample binomial test was used to test whether the rate of change to the clinician’s proposed management plans was greater than 15%.
RESULTS Between March and May 2011, a total of 68 consecutive patients were accrued over 11 weeks. Patient characteristics are listed in Table 1. Fifty-seven percent of cases were non-small cell lung cancers (NSCLCs), 18% were malignant histologies of non-lung origin, 9% were small cell lung cancers and 7% were benign. At the time of case submission, 46 (68%) patients were recommended a treatment with curative intent and 22 (32%) were palliative cases. In terms of frequency of case presentation, 64 cases (94%) were presented once at the MDT meeting. Of the four cases (6%) that were presented more than once, two cases had to be resubmitted because there was insufficient information available at the first case presentation to enable MDT decision-making. The summary of referral patterns is provided in Table 2. Most of the cases were submitted for presentation by radiation oncologists (69%). Reasons for referral were to discuss newly diagnosed lung cancer cases (51%) or to discuss previously diagnosed patients with new management dilemmas (47%). One case (2%) was submitted for general interest. Out of the 68 cases submitted for discussion at the MDT meeting, 13 patients were excluded. Reasons for exclusion were: lack of pre-meeting management plan (eight patients), investigation results unavailable to the referring clinician prior to the meeting (three patients), alteration to the proposed pre-meeting management plan following discovery of biopsy results before the meeting (one patient), and a general interest case without any management dilemmas (one patient). Of the remaining 55 patients available for analysis, 40 patients had
© 2014 Wiley Publishing Asia Pty Ltd
KA Ung et al.
Table 1 Patient and tumor characteristics (n† = 68)‡
Gender Male Female ECOG performance status 0 1 2 3 4 Unknown Ever been a smoker Yes No Tumor type Adenocarcinoma Squamous cell carcinoma Large cell carcinoma Small cell lung cancer Malignant but not lung cancer§ Benign Unknown/indeterminable Tumor staging Non-small cell lung cancer Stage I Stage II Stage III Stage IV Small cell lung cancer Limited stage Extensive stage Unknown/not lung cancer
N
%
43 25
63 37
8 37 13 7 1 2
12 54 19 10 1 3
58 10
85 15
22 15 2 6 12 5 6
32 22 3 9 18 7 9
5 4 19 10
7 6 28 15
4 2 24
6 3 35
†
n, number. ‡Characteristics are at time of case submission. §Head and neck cancers, n = 3; sarcoma, n = 3; cutaneous malignancies, n = 2; thymoma, n = 2; carcinoid tumor, n = 1; chordoma, n = 1. ECOG, Eastern Cooperative Oncology Group.
curative-intent management plans and 15 patients were recommended management plans with palliative intent at the time of case submission.
Impact of MDT meeting The MDT meeting resulted in a change in management plans in 32 cases (58%) (CI 45–71%; P < 0.005). Of these, 18 cases were lung cancers, nine cases were malignant but not of lung origin, and five cases were benign or of unknown histology. The primary reason for a change in the management plan was due to the MDT recommendation for additional investigations (59%). The other reasons were due to change in treatment modality (19%), treatment intent (9%), tumor histology (6%) or
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Table 2
Referral patterns (n† = 68)
Referring doctor Radiation oncologist Medical oncologist Surgeon Respiratory physician Reasons for referral New diagnosis of lung cancer Preexisting patient with new management issues Other †
N
%
47 7 9 5
69 10 13 7
35 32
51 47
1
2
n, number.
Table 3 Impact of MDT meetings on management plans (n† = 55)‡
Change in management plans Radical cases Palliative cases Change due to: Additional investigations Imaging Biopsy Imaging + biopsy Others§ Change in Treatment modality Treatment intent Tumor histology Tumor stage No change in management plans No change due to: No change in management plans Unable to make decision (lack of information)
N
%
32 23 9
58 72 28
19 8 4 3 4
59
6 3 2 2 23
19 9 6 6 42
20 3
87 13
† n, number. ‡13 patients were excluded. §Other investigations include respiratory function test, n = 1; molecular testing, n = 1; tuberculosis testing, n = 1; transthoracic echocardiogram, n = 1. MDT, multidisciplinary team.
tumor stage (6%). Of the 32 cases that sustained a change to the clinicians’ initial management plans, 72% were of radical intent treatment while 28% were palliative cases (Table 3). The MDT meeting did not have impact on management plans in 42% of cases. Of these, the MDT meeting concurred with the clinicians’ original plans in 87%. In the remaining 13%, no formal recommendation was made as insufficient information was available at the time of the meeting.
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Implementation of MDT meeting recommendations Of the original 68 patients, no formal recommendation was made in three cases due to insufficient information available at the time of the MDT meeting, therefore 65 patients remained for evaluation of the clinical implementation of the MDT meeting recommendations. The MDT meeting recommendations were implemented in 47 cases (72%). Reasons for non-implementation included pre-existing poor patient performance status (three cases; 17%), declining performance status due to disease progression (two cases; 11%), clinician preference (five cases; 28%), the availability of new clinical information after the MDT meeting (four cases; 22%), and patient decision (two cases; 11%). In two cases (11%), the reasons for non-implementation were unclear.
DISCUSSION There is increasing evidence that multidisciplinary care has led to the provision of best practice through the adoption of evidence-based guidelines,4,5 improved patient outcomes2,3,7,8 and streamlined treatment pathways.6 Regular team meetings are generally considered an integral component of multidisciplinary care. While team dynamics and individual tumor stream needs may vary,17 the central theme of meetings includes prospective treatment planning.18 The Peter Mac lung oncology service adopts the “tumor board” model, in which the patient’s case is discussed by the MDT, a management recommendation is made and the treating clinician informs the patient of the recommendation, with referrals made as appropriate.18 In our MDT meeting, the cases selected for discussion were not only of new cases, but also of current patients with disease recurrence or new management dilemmas who were referred for tertiary specialist input. There were often no clear evidence or management algorithms to guide the practitioner in these cases. The characteristics of our study group revealed a predominance of male patients, smoking history and adenocarcinoma tumor histology, similar to other lung MDT studies.4,10 The majority of the cases submitted were of good performance status, likely reflecting that most patients were referred from an outpatient setting. Peter Mac provides radiotherapy services for several affiliated hospitals which have their own MDT meetings, which explains the finding that most of the cases (69%) submitted for MDT discussion at our center were by radiation oncologists. It was interesting to observe
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that 18% of malignancies discussed in our lung oncology MDT meetings were of non-lung origin, including head and neck malignancies, cutaneous malignancies and sarcomas (Table 1). Most of these cases were referred to the lung oncology service for advice regarding issues related to metastatic disease to the thorax. We found that in 58% of cases submitted for presentation at the MDT meeting, a change to the clinicians’ initial pre-meeting management plans was recommended. In the majority, this was because additional investigations were recommended during the MDT meeting. These investigations included imaging, biopsies, molecular testing, tuberculosis testing, respiratory function tests and transthoracic echocardiograms (Table 3). The recommendation for additional investigations occurred despite most cases having had prior investigations or MDT discussions at the referring hospital centers. This reflects the complexity of cases discussed and the importance of MDT meetings even in a tertiary specialist setting. A limitation of this study is that the investigations were not graded according to the level of clinical importance such as routine versus non-routine tests, level of invasiveness or degree of clinical risk to patients. For example, some of the imaging tests recommended were considered routine, such as a computed tomography scan of the brain to complete tumor staging. However, there were also investigations that were not widely available or non-routine, such as molecular testing, non-funded indications for positron emission tomography scans, or decisions for repeat biopsies using different techniques. Apart from investigations, the MDT meetings also resulted in changes in tumor stage, histology, treatment modality and treatment intent. A retrospective study by Santoso et al. reported that 6.9% of 459 cases discussed at their gynecologic oncology tumor meeting had changes in tumor site, stage or treatment plans as a result of findings discussed at the meeting.15 Similarly, in patients with breast cancer, Chang et al. compared treatment recommendations made by the referring clinicians with the consensus recommendation made by the MDT (n = 75), and reported that 43% of cases had the initial proposed management adjusted in terms of the type of surgery offered, the need for further investigations and change in diagnosis following pathology review.16 These data demonstrate that MDT reviews help improve the accuracy of tumor diagnosis, staging and the delivery of the most appropriate oncological care. While not all changes result in alterations to the treatment pathways (e.g. non-operable Stage IIIA NSCLC upstaged to Stage IIIB NSCLC can both be treated with concurrent
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KA Ung et al.
chemoradiotherapy with curative intent), these changes may still impact on prognostic information and future management. MDT meetings provide a forum for discussion of management dilemmas in both the curative and noncurative settings. In a large retrospective study, Boxer et al. reported on the benefits of MDT meetings for patients with lung cancer, and found that patients with Stage IV NSCLC who were presented at MDT meetings were significantly more likely to receive radiotherapy, chemotherapy and palliative care referrals.10 The authors of this study also suggested that MDT meetings provide a forum for cross-specialty education, thereby reducing some of these physician biases regarding the management of patients with Stage IV lung cancer. In our study, 28% of cases in which the MDT recommended a change in management plans were of palliative treatment intent. Therefore, our findings suggest that palliative cases are currently underrepresented in our lung oncology MDT meetings; however, these patients may benefit from discussion in this forum as MDT meetings may influence their management. The availability of relevant staging information is important to enable clinical decision-making in an MDT meeting. A survey by the Department of Health, Victoria, Australia, on multidisciplinary meetings reported that only 52% of MDT meetings had patient staging information routinely available and documented during the meeting.1 In our study, the MDT was unable to make decisions in three cases due to lack of information. Two cases did not have the relevant imaging for review as they were performed at external sites, and one was because staging investigations were not yet performed. These reflect some of the barriers to MDT meetings including limited administrative support to enable availability of information in a timely manner.9,18 We hypothesize that the efficiency and effectiveness of the MDT meeting could be optimized by improving the availability of clinical information prior to the MDT meeting, such as overcoming waiting lists for investigations and increasing administrative support to ensure that the results of investigations are more readily available. The multidisciplinary care process includes conveying the MDT recommendations to the patient and subsequent implementation if deemed appropriate and acceptable to the patient. A few studies on various tumor streams have evaluated the concordance between the proposed and the administered treatment plan following MDT meetings. A large retrospective study on 1516 patient cases discussed at the brain tumor multidisciplinary board reported that 91% of meeting recommendations
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were realized within 3 months.13 A smaller Australian study (n = 160) demonstrated that 95% of uro-oncology, upper gastrointestinal and colorectal MDT meeting recommendations were implemented.12 Our implementation rate of MDT recommendations (72%) was not as high as these studies. In our study, one of the main reasons for non-implementation was deteriorating patient performance status (28%). This included 11% in which disease progression had affected performance status, rendering the recommended treatment not deliverable at time of patient contact. This could be attributed to the relatively rapid progression of lung cancers in general.19 The predominance of patients with a smoking history in our cohort also suggests chronic obstructive pulmonary disease as a possible major comorbidity which may limit treatment options. Furthermore, radical management of lung cancers involves thoracic surgery or chemoradiotherapy in which patient performance status and medical fitness are important. In a more similar study on lung oncology patients (n = 344), Leo et al. compared the proposed MDT recommendations with subsequent administered treatment and demonstrated a discordance rate of 4.4% that is much less than in our study (28%).14 This could be explained by the fact that in Leo et al.’s study, treatment decisions were made only after two (32.6%) or more (19.8%) MDT presentations, whereas in our study only 6% of cases were presented more than once. Having more presentations at the meeting would provide opportunities for further information on patient preference and performance status to be gathered each time by the specialist unit, thus enabling MDT recommendations to be more applicable. Another observation in Leo et al.’s study is that the MDT therapeutic decision was grouped into four broad categories of chemotherapy, radiotherapy, chemoradiotherapy and best supportive care. Furthermore, their method of contacting referring physicians to determine implementation of meeting recommendations might be influenced by measurement bias. In our study, for an MDT recommendation to be considered implemented, all aspects of the recommendation (e.g. treatment offered, additional investigations, referrals to specialist units and trial accrual) must be fulfilled. Patient’s medical records were analyzed by a separate investigator to determine implementation. Our stricter implementation criteria and more impartial evaluation of implementation could contribute to the higher discordance rate seen in our patient cohort. It has been previously highlighted that adequate information about the patient’s disease as well as any physical or psychological health issues is required for MDT
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meetings to function effectively.20–22 It is also recommended that information about the patient’s concerns, preferences and social circumstances is presented at the meeting.18 Of the cases in which the MDT recommendations were not implemented, 22% were due to the influence of new information discovered only after the meeting and 11% of patients declined the treatment recommendations. Patient comorbidities and poor performance status as reasons for non-implementation of MDT recommendations seem to be a recurring theme seen in our study as well as others.12,14,21 These reflect two of the limitations of MDT meetings: (i) not all clinicians within the meeting have reviewed the patient personally, thus they are heavily reliant on the adequacy of the information that is presented; and (ii) the onus is on the presenting clinician to provide correct and adequate information regarding patient comorbidities and patient preferences to the MDT meeting to ensure that appropriate recommendations are made.21,22
CONCLUSION Our findings show that the MDT meetings have significant impact on management plans in 58% of patient cases. The majority of MDT recommendations (72%) were implemented into patient care. Our study provides further evidence to support the role of MDT meetings as an essential part of the decision-making process in a tertiary specialist setting. MDT meetings should be audited to assess its performance and effectiveness in providing optimal multidisciplinary management of patients with cancer.
REFERENCES 1 Multidisciplinary Meetings, 2010–2011 – Monitoring Progress Towards Achieving Best Practice Cancer Care: Wellbeing, Integrated Cancer and Ageing, Victorian Government, Department of Health, Melbourne, Victoria. 2011. 2 Palmer G, Martling A, Cedermark B, Holm T. Preoperative tumour staging with multidisciplinary team assessment improves the outcome in locally advanced primary rectal cancer. Colorectal Dis 2011; 13: 1361–9. 3 Stephens M, Lewis WG, Brewster AE et al. Multidisciplinary team management is associated with improved outcomes after surgery for esophageal cancer. Dis Esophagus 2006; 19: 164–71. 4 Conron M, Phuah S, Steinfort D, Dabscheck E, Wright G, Hart D. Analysis of multidisciplinary lung cancer practice. Intern Med J 2007; 37: 18–25. 5 Vinod SK, Sidhom MA, Delaney GP. Do multidisciplinary meetings follow guideline-based care? J Oncol Pract 2010; 6: 276–81.
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6 Gabel M, Hilton NE, Nathanson SD. Multidisciplinary breast cancer clinics. Do they work? Cancer 1997; 79: 2380–4. 7 Bydder S, Nowak A, Marion K, Phillips M, Atun R. The impact of case discussion at a multidisciplinary team meeting on the treatment and survival of patients with inoperable non-small cell lung cancer. Intern Med J 2009; 39: 838–41. 8 Friedland PL, Bozic B, Dewar J, Kuan R, Meyer C, Phillips M. Impact of multidisciplinary team management in head and neck cancer patients. Br J Cancer 2011; 104: 1246–8. 9 Fleissig A, Jenkins V, Catt S, Fallowfield L. Multidisciplinary teams in cancer care: are they effective in the UK? Lancet Oncol 2006; 7: 935–43. 10 Boxer MM, Vinod SK, Shafiq J, Duggan KJ. Do multidisciplinary team meetings make a difference in the management of lung cancer? Cancer 2011; 117: 5112–20. 11 Devitt B, Philip J, McLachlan SA. Team dynamics, decision making, and attitudes toward multidisciplinary cancer meetings: health professionals’ perspectives. J Oncol Pract 2010; 6: e17–20. 12 Au-Yeung GH, Aly A, Bui A, Vermeltfoort CM, Davis ID. Uptake of oncology multidisciplinary meeting recommendations. Med J Aust 2012; 196: 36–7. 13 Lutterbach J, Pagenstecher A, Spreer J et al. The brain tumor board: lessons to be learned from an interdisciplinary conference. Onkologie 2005; 28: 22–6. 14 Leo F, Venissac N, Poudenx M, Otto J, Mouroux J. Multidisciplinary management of lung cancer: how to test its efficacy? J Thorac Oncol 2007; 2: 69–72.
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15 Santoso JT, Schwertner B, Coleman RL, Hannigan EV. Tumor board in gynecologic oncology. Int J Gynecol Cancer 2004; 14: 206–9. 16 Chang JH, Vines E, Bertsch H et al. The impact of a multidisciplinary breast cancer center on recommendations for patient management: the University of Pennsylvania experience. Cancer 2001; 91: 1231–7. 17 Lamb BW, Sevdalis N, Taylor C, Vincent C, Green JS. Multidisciplinary team working across different tumour types: analysis of a national survey. Ann Oncol 2012; 23: 1293–300. 18 National Breast Cancer Centre. Multidisciplinary Meetings for Cancer Care: A Guide for Health Service Providers. National Breast Cancer Centre, Camperdown, NSW 2005. 19 Everitt S, Herschtal A, Callahan J et al. High rates of tumor growth and disease progression detected on serial pretreatment fluorodeoxyglucose-positron emission tomography/ computed tomography scans in radical radiotherapy candidates with nonsmall cell lung cancer. Cancer 2010; 116: 5030–7. 20 Mileshkin L, Zalcberg J. The multidisciplinary management of patients with cancer. Ann Oncol 2006; 17: 1337– 8. 21 Blazeby JM, Wilson L, Metcalfe C, Nicklin J, English R, Donovan JL. Analysis of clinical decision-making in multidisciplinary cancer teams. Ann Oncol 2006; 17: 457–60. 22 Lamb BW, Sevdalis N, Arora S, Pinto A, Vincent C, Green JS. Teamwork and team decision-making at multidisciplinary cancer conferences: barriers, facilitators, and opportunities for improvement. World J Surg 2011; 35: 1970–6.
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doi: 10.1111/ajco.12192
ORIGINAL ARTICLE
Impact of the lung oncology multidisciplinary team meetings on the management of patients with cancer Kim Ann UNG, Belinda A CAMPBELL, Danny DUPLAN, David BALL and Steven DAVID Department of Radiation Oncology and Cancer Imaging, Peter MacCallum Cancer Centre, East Melbourne, Victoria, Australia
Abstract Aims: Multidisciplinary team (MDT) meetings are increasingly regarded as a component of multidisciplinary cancer care. We aimed to prospectively measure the impact of MDT meetings on clinicians’ management plans for lung oncology patients, and the implementation rate of the meeting recommendations. Methods: Consecutive patient cases presented at the weekly lung oncology MDT meetings were prospectively enrolled. Investigators compared the clinicians’ management plans pre-meeting with the consensus plans post-meeting. The meeting was considered to have an impact on management plans if ≥1 of the following changes were detected: tumor stage, histology, treatment intent or treatment modality, or if additional investigations were recommended. Investigators reviewed hospital patient records at 4 months to determine if the meeting recommendations were implemented. Reasons for non-implementation were also recorded. Results: Of the 55 eligible cases, the MDT meeting changed management plans in 58% (CI 45–71%; P < 0.005). These changes included: additional investigations (59%), or changes in treatment modality (19%), treatment intent (9%), histology (6%) or tumor stage (6%). The meeting recommendations were implemented in 72% of cases. Reasons for non-implementation included deteriorating patient performance status, clinician’s preference, the influence of new clinical information obtained after the meeting or patient decision. Conclusion: MDT meetings significantly impact on the management plans for lung oncology patients. The majority of MDT recommendations (72%) were implemented into patient care. These findings provide further evidence to support the role of MDT meetings as an essential part of the decision-making process for the optimal multidisciplinary management of patients with cancer. Key words: decision-making, lung cancer, management, multidisciplinary meeting, tumor board.
INTRODUCTION The increasing complexity of management of patients with cancer has led to the widespread implementation of multidisciplinary teams (MDTs).1 Multidisciplinary
Correspondence: Dr Kim Ann Ung MBBS (Hons) BMedSc, Department of Radiation Oncology and Cancer Imaging, Peter MacCallum Cancer Centre, 7 St. Andrews Place, East Melbourne, Vic. 3002, Australia. Email: [email protected] Conflict of interest: none Accepted for publication 16 February 2014.
© 2014 Wiley Publishing Asia Pty Ltd
cancer care has shown to improve outcomes2,3 and adherence to evidence-based guidelines4,5 as well as patient satisfaction.6 Retrospective evidence also suggests an improvement in overall survival favoring oncology patients discussed in MDT meetings.7,8 MDT meetings, a common feature of multidisciplinary cancer care, enable patient management plans to be based on a broad range of expert knowledge and all aspects of treatment options can be considered.9 Many studies have demonstrated the benefits of MDT meetings in the management of patients with cancer. Boxer et al. compared patients with newly diagnosed lung cancer who were presented at MDT meetings and those
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who were not within the same time period, and demonstrated that MDT discussion was associated with better treatment receipt and more referrals to palliative care.10 Health care professionals concur that MDT meetings provide a decision-making forum for clinicians to develop peer-reviewed management plans, help improve communication between specialties, and provide a good educational resource.9,11 We were interested to determine whether MDT meetings had an impact on the clinicians’ management plans. To measure the efficacy of MDT meetings, previous studies have looked into the implementation rate of the meeting recommendations of various tumor streams.12–14 Other studies compared whether there were any changes in the tumor findings or the proposed management plans by the referring clinicians with that by the MDT meeting.15,16 In our study, we aimed to assess the impact of the Peter MacCallum Cancer Centre (Peter Mac) lung oncology service MDT meetings on clinicians’ management plans by prospectively comparing the proposed management plans pre- and post-MDT meeting. The primary end point was to determine the proportion of cases in which the MDT meeting resulted in a change to the clinicians’ pre-meeting management plans. The secondary end point was to determine the implementation rate of the MDT recommendations.
METHODS Approval for this study was obtained from the local ethics committee at Peter Mac. The lung oncology service at Peter Mac meets weekly to discuss patient management plans. Key members of the team include medical oncologists, radiation oncologists, thoracic surgeons, respiratory physicians, a radiologist, a nuclear medicine physician, a cancer nurse coordinator and allied health professionals. Pathology review is available upon request. The patient cases for MDT presentation were selected at the discretion of lung oncology clinicians as needing multidisciplinary input. Clinical history, medical imaging and pathology were reviewed and discussed, and a final consensus is documented. This decision is then discussed with the patient in clinic before a final management plan is agreed upon. Consecutive patient cases presented at the weekly lung oncology MDT meetings were anonymously enrolled in the study. Clinicians submitted cases for presentation in electronic form with relevant clinical information and their proposed management plans; that is, clinicians were
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prospectively asked, “what would your management plans be if the MDT meetings did not exist?” Prior to the MDT meeting, clinical information and the clinicians’ proposed management plans were extracted. For uniformity, one investigator performed this task. If the required information was unavailable, the referring clinicians were contacted to provide further information. Patient demographic data, reasons for referral, Eastern Cooperative Oncology Group performance status, smoking status, tumor histology, tumor stage, proposed investigations, treatment intent and proposed treatment modality were collected. The number of times each case was presented at the meeting was also recorded. Cases were excluded if the clinicians’ proposed management plans were not provided pre-meeting or if there was clinical information unavailable to the clinician prior to the meeting that would affect decision-making (e.g. staging investigation or biopsy results). During the MDT meeting, a second investigator collected the MDT recommendations. To limit bias, this investigator was blinded to the initial pre-meeting plans. For each patient, any changes to the tumor stage or histology, treatment intent, treatment modality and recommendation for further investigations were documented. On completion of the MDT meetings, the investigators compared the pre- and post-MDT meeting management plans recorded. The MDT meeting was considered to have an impact on management plans if the following changes were detected: tumor stage, histology, treatment intent or treatment modality, or additional investigations recommended. If there was more than one change recorded for a patient, the most clinically significant one was chosen at the discretion of one study investigator with experience in thoracic cancer management. The MDT meeting did not have an impact if there was no change to the clinicians’ pre-meeting plans or if the MDT was unable to make recommendations at the meeting. To assess the rate of implementation, investigators reviewed the hospital patient records 4 months after the meeting. For an MDT recommendation to be considered implemented, all aspects of the recommendation (e.g. treatment, additional investigations, referral to specialist units and trial accrual) for each patient case must be fulfilled. Reasons for non-implementation were also recorded.
Statistical analysis For analysis of the primary end point, the Peter Mac lung oncology MDT meeting was not considered worthwhile
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with respect to patient management if the rate of change to the clinician’s proposed management plans was less than 15%. This figure was prospectively determined. It was estimated from the MDT attendees that the true rate of change of management plans was at least 30% in this population. With power of 80% and type 1 error of 5%, a sample size of 51 patients was required. To allow for potential ineligibilities, data were collected from the first 68 consecutive patients. To summarize clinical data, descriptive statistics were reported in the form of means, standard deviations and ranges for quantitative variables. Categorical variables were reported as counts and percentages with 95% confidence intervals. One sample binomial test was used to test whether the rate of change to the clinician’s proposed management plans was greater than 15%.
RESULTS Between March and May 2011, a total of 68 consecutive patients were accrued over 11 weeks. Patient characteristics are listed in Table 1. Fifty-seven percent of cases were non-small cell lung cancers (NSCLCs), 18% were malignant histologies of non-lung origin, 9% were small cell lung cancers and 7% were benign. At the time of case submission, 46 (68%) patients were recommended a treatment with curative intent and 22 (32%) were palliative cases. In terms of frequency of case presentation, 64 cases (94%) were presented once at the MDT meeting. Of the four cases (6%) that were presented more than once, two cases had to be resubmitted because there was insufficient information available at the first case presentation to enable MDT decision-making. The summary of referral patterns is provided in Table 2. Most of the cases were submitted for presentation by radiation oncologists (69%). Reasons for referral were to discuss newly diagnosed lung cancer cases (51%) or to discuss previously diagnosed patients with new management dilemmas (47%). One case (2%) was submitted for general interest. Out of the 68 cases submitted for discussion at the MDT meeting, 13 patients were excluded. Reasons for exclusion were: lack of pre-meeting management plan (eight patients), investigation results unavailable to the referring clinician prior to the meeting (three patients), alteration to the proposed pre-meeting management plan following discovery of biopsy results before the meeting (one patient), and a general interest case without any management dilemmas (one patient). Of the remaining 55 patients available for analysis, 40 patients had
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Table 1 Patient and tumor characteristics (n† = 68)‡
Gender Male Female ECOG performance status 0 1 2 3 4 Unknown Ever been a smoker Yes No Tumor type Adenocarcinoma Squamous cell carcinoma Large cell carcinoma Small cell lung cancer Malignant but not lung cancer§ Benign Unknown/indeterminable Tumor staging Non-small cell lung cancer Stage I Stage II Stage III Stage IV Small cell lung cancer Limited stage Extensive stage Unknown/not lung cancer
N
%
43 25
63 37
8 37 13 7 1 2
12 54 19 10 1 3
58 10
85 15
22 15 2 6 12 5 6
32 22 3 9 18 7 9
5 4 19 10
7 6 28 15
4 2 24
6 3 35
†
n, number. ‡Characteristics are at time of case submission. §Head and neck cancers, n = 3; sarcoma, n = 3; cutaneous malignancies, n = 2; thymoma, n = 2; carcinoid tumor, n = 1; chordoma, n = 1. ECOG, Eastern Cooperative Oncology Group.
curative-intent management plans and 15 patients were recommended management plans with palliative intent at the time of case submission.
Impact of MDT meeting The MDT meeting resulted in a change in management plans in 32 cases (58%) (CI 45–71%; P < 0.005). Of these, 18 cases were lung cancers, nine cases were malignant but not of lung origin, and five cases were benign or of unknown histology. The primary reason for a change in the management plan was due to the MDT recommendation for additional investigations (59%). The other reasons were due to change in treatment modality (19%), treatment intent (9%), tumor histology (6%) or
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Table 2
Referral patterns (n† = 68)
Referring doctor Radiation oncologist Medical oncologist Surgeon Respiratory physician Reasons for referral New diagnosis of lung cancer Preexisting patient with new management issues Other †
N
%
47 7 9 5
69 10 13 7
35 32
51 47
1
2
n, number.
Table 3 Impact of MDT meetings on management plans (n† = 55)‡
Change in management plans Radical cases Palliative cases Change due to: Additional investigations Imaging Biopsy Imaging + biopsy Others§ Change in Treatment modality Treatment intent Tumor histology Tumor stage No change in management plans No change due to: No change in management plans Unable to make decision (lack of information)
N
%
32 23 9
58 72 28
19 8 4 3 4
59
6 3 2 2 23
19 9 6 6 42
20 3
87 13
† n, number. ‡13 patients were excluded. §Other investigations include respiratory function test, n = 1; molecular testing, n = 1; tuberculosis testing, n = 1; transthoracic echocardiogram, n = 1. MDT, multidisciplinary team.
tumor stage (6%). Of the 32 cases that sustained a change to the clinicians’ initial management plans, 72% were of radical intent treatment while 28% were palliative cases (Table 3). The MDT meeting did not have impact on management plans in 42% of cases. Of these, the MDT meeting concurred with the clinicians’ original plans in 87%. In the remaining 13%, no formal recommendation was made as insufficient information was available at the time of the meeting.
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Implementation of MDT meeting recommendations Of the original 68 patients, no formal recommendation was made in three cases due to insufficient information available at the time of the MDT meeting, therefore 65 patients remained for evaluation of the clinical implementation of the MDT meeting recommendations. The MDT meeting recommendations were implemented in 47 cases (72%). Reasons for non-implementation included pre-existing poor patient performance status (three cases; 17%), declining performance status due to disease progression (two cases; 11%), clinician preference (five cases; 28%), the availability of new clinical information after the MDT meeting (four cases; 22%), and patient decision (two cases; 11%). In two cases (11%), the reasons for non-implementation were unclear.
DISCUSSION There is increasing evidence that multidisciplinary care has led to the provision of best practice through the adoption of evidence-based guidelines,4,5 improved patient outcomes2,3,7,8 and streamlined treatment pathways.6 Regular team meetings are generally considered an integral component of multidisciplinary care. While team dynamics and individual tumor stream needs may vary,17 the central theme of meetings includes prospective treatment planning.18 The Peter Mac lung oncology service adopts the “tumor board” model, in which the patient’s case is discussed by the MDT, a management recommendation is made and the treating clinician informs the patient of the recommendation, with referrals made as appropriate.18 In our MDT meeting, the cases selected for discussion were not only of new cases, but also of current patients with disease recurrence or new management dilemmas who were referred for tertiary specialist input. There were often no clear evidence or management algorithms to guide the practitioner in these cases. The characteristics of our study group revealed a predominance of male patients, smoking history and adenocarcinoma tumor histology, similar to other lung MDT studies.4,10 The majority of the cases submitted were of good performance status, likely reflecting that most patients were referred from an outpatient setting. Peter Mac provides radiotherapy services for several affiliated hospitals which have their own MDT meetings, which explains the finding that most of the cases (69%) submitted for MDT discussion at our center were by radiation oncologists. It was interesting to observe
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that 18% of malignancies discussed in our lung oncology MDT meetings were of non-lung origin, including head and neck malignancies, cutaneous malignancies and sarcomas (Table 1). Most of these cases were referred to the lung oncology service for advice regarding issues related to metastatic disease to the thorax. We found that in 58% of cases submitted for presentation at the MDT meeting, a change to the clinicians’ initial pre-meeting management plans was recommended. In the majority, this was because additional investigations were recommended during the MDT meeting. These investigations included imaging, biopsies, molecular testing, tuberculosis testing, respiratory function tests and transthoracic echocardiograms (Table 3). The recommendation for additional investigations occurred despite most cases having had prior investigations or MDT discussions at the referring hospital centers. This reflects the complexity of cases discussed and the importance of MDT meetings even in a tertiary specialist setting. A limitation of this study is that the investigations were not graded according to the level of clinical importance such as routine versus non-routine tests, level of invasiveness or degree of clinical risk to patients. For example, some of the imaging tests recommended were considered routine, such as a computed tomography scan of the brain to complete tumor staging. However, there were also investigations that were not widely available or non-routine, such as molecular testing, non-funded indications for positron emission tomography scans, or decisions for repeat biopsies using different techniques. Apart from investigations, the MDT meetings also resulted in changes in tumor stage, histology, treatment modality and treatment intent. A retrospective study by Santoso et al. reported that 6.9% of 459 cases discussed at their gynecologic oncology tumor meeting had changes in tumor site, stage or treatment plans as a result of findings discussed at the meeting.15 Similarly, in patients with breast cancer, Chang et al. compared treatment recommendations made by the referring clinicians with the consensus recommendation made by the MDT (n = 75), and reported that 43% of cases had the initial proposed management adjusted in terms of the type of surgery offered, the need for further investigations and change in diagnosis following pathology review.16 These data demonstrate that MDT reviews help improve the accuracy of tumor diagnosis, staging and the delivery of the most appropriate oncological care. While not all changes result in alterations to the treatment pathways (e.g. non-operable Stage IIIA NSCLC upstaged to Stage IIIB NSCLC can both be treated with concurrent
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chemoradiotherapy with curative intent), these changes may still impact on prognostic information and future management. MDT meetings provide a forum for discussion of management dilemmas in both the curative and noncurative settings. In a large retrospective study, Boxer et al. reported on the benefits of MDT meetings for patients with lung cancer, and found that patients with Stage IV NSCLC who were presented at MDT meetings were significantly more likely to receive radiotherapy, chemotherapy and palliative care referrals.10 The authors of this study also suggested that MDT meetings provide a forum for cross-specialty education, thereby reducing some of these physician biases regarding the management of patients with Stage IV lung cancer. In our study, 28% of cases in which the MDT recommended a change in management plans were of palliative treatment intent. Therefore, our findings suggest that palliative cases are currently underrepresented in our lung oncology MDT meetings; however, these patients may benefit from discussion in this forum as MDT meetings may influence their management. The availability of relevant staging information is important to enable clinical decision-making in an MDT meeting. A survey by the Department of Health, Victoria, Australia, on multidisciplinary meetings reported that only 52% of MDT meetings had patient staging information routinely available and documented during the meeting.1 In our study, the MDT was unable to make decisions in three cases due to lack of information. Two cases did not have the relevant imaging for review as they were performed at external sites, and one was because staging investigations were not yet performed. These reflect some of the barriers to MDT meetings including limited administrative support to enable availability of information in a timely manner.9,18 We hypothesize that the efficiency and effectiveness of the MDT meeting could be optimized by improving the availability of clinical information prior to the MDT meeting, such as overcoming waiting lists for investigations and increasing administrative support to ensure that the results of investigations are more readily available. The multidisciplinary care process includes conveying the MDT recommendations to the patient and subsequent implementation if deemed appropriate and acceptable to the patient. A few studies on various tumor streams have evaluated the concordance between the proposed and the administered treatment plan following MDT meetings. A large retrospective study on 1516 patient cases discussed at the brain tumor multidisciplinary board reported that 91% of meeting recommendations
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were realized within 3 months.13 A smaller Australian study (n = 160) demonstrated that 95% of uro-oncology, upper gastrointestinal and colorectal MDT meeting recommendations were implemented.12 Our implementation rate of MDT recommendations (72%) was not as high as these studies. In our study, one of the main reasons for non-implementation was deteriorating patient performance status (28%). This included 11% in which disease progression had affected performance status, rendering the recommended treatment not deliverable at time of patient contact. This could be attributed to the relatively rapid progression of lung cancers in general.19 The predominance of patients with a smoking history in our cohort also suggests chronic obstructive pulmonary disease as a possible major comorbidity which may limit treatment options. Furthermore, radical management of lung cancers involves thoracic surgery or chemoradiotherapy in which patient performance status and medical fitness are important. In a more similar study on lung oncology patients (n = 344), Leo et al. compared the proposed MDT recommendations with subsequent administered treatment and demonstrated a discordance rate of 4.4% that is much less than in our study (28%).14 This could be explained by the fact that in Leo et al.’s study, treatment decisions were made only after two (32.6%) or more (19.8%) MDT presentations, whereas in our study only 6% of cases were presented more than once. Having more presentations at the meeting would provide opportunities for further information on patient preference and performance status to be gathered each time by the specialist unit, thus enabling MDT recommendations to be more applicable. Another observation in Leo et al.’s study is that the MDT therapeutic decision was grouped into four broad categories of chemotherapy, radiotherapy, chemoradiotherapy and best supportive care. Furthermore, their method of contacting referring physicians to determine implementation of meeting recommendations might be influenced by measurement bias. In our study, for an MDT recommendation to be considered implemented, all aspects of the recommendation (e.g. treatment offered, additional investigations, referrals to specialist units and trial accrual) must be fulfilled. Patient’s medical records were analyzed by a separate investigator to determine implementation. Our stricter implementation criteria and more impartial evaluation of implementation could contribute to the higher discordance rate seen in our patient cohort. It has been previously highlighted that adequate information about the patient’s disease as well as any physical or psychological health issues is required for MDT
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meetings to function effectively.20–22 It is also recommended that information about the patient’s concerns, preferences and social circumstances is presented at the meeting.18 Of the cases in which the MDT recommendations were not implemented, 22% were due to the influence of new information discovered only after the meeting and 11% of patients declined the treatment recommendations. Patient comorbidities and poor performance status as reasons for non-implementation of MDT recommendations seem to be a recurring theme seen in our study as well as others.12,14,21 These reflect two of the limitations of MDT meetings: (i) not all clinicians within the meeting have reviewed the patient personally, thus they are heavily reliant on the adequacy of the information that is presented; and (ii) the onus is on the presenting clinician to provide correct and adequate information regarding patient comorbidities and patient preferences to the MDT meeting to ensure that appropriate recommendations are made.21,22
CONCLUSION Our findings show that the MDT meetings have significant impact on management plans in 58% of patient cases. The majority of MDT recommendations (72%) were implemented into patient care. Our study provides further evidence to support the role of MDT meetings as an essential part of the decision-making process in a tertiary specialist setting. MDT meetings should be audited to assess its performance and effectiveness in providing optimal multidisciplinary management of patients with cancer.
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6 Gabel M, Hilton NE, Nathanson SD. Multidisciplinary breast cancer clinics. Do they work? Cancer 1997; 79: 2380–4. 7 Bydder S, Nowak A, Marion K, Phillips M, Atun R. The impact of case discussion at a multidisciplinary team meeting on the treatment and survival of patients with inoperable non-small cell lung cancer. Intern Med J 2009; 39: 838–41. 8 Friedland PL, Bozic B, Dewar J, Kuan R, Meyer C, Phillips M. Impact of multidisciplinary team management in head and neck cancer patients. Br J Cancer 2011; 104: 1246–8. 9 Fleissig A, Jenkins V, Catt S, Fallowfield L. Multidisciplinary teams in cancer care: are they effective in the UK? Lancet Oncol 2006; 7: 935–43. 10 Boxer MM, Vinod SK, Shafiq J, Duggan KJ. Do multidisciplinary team meetings make a difference in the management of lung cancer? Cancer 2011; 117: 5112–20. 11 Devitt B, Philip J, McLachlan SA. Team dynamics, decision making, and attitudes toward multidisciplinary cancer meetings: health professionals’ perspectives. J Oncol Pract 2010; 6: e17–20. 12 Au-Yeung GH, Aly A, Bui A, Vermeltfoort CM, Davis ID. Uptake of oncology multidisciplinary meeting recommendations. Med J Aust 2012; 196: 36–7. 13 Lutterbach J, Pagenstecher A, Spreer J et al. The brain tumor board: lessons to be learned from an interdisciplinary conference. Onkologie 2005; 28: 22–6. 14 Leo F, Venissac N, Poudenx M, Otto J, Mouroux J. Multidisciplinary management of lung cancer: how to test its efficacy? J Thorac Oncol 2007; 2: 69–72.
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15 Santoso JT, Schwertner B, Coleman RL, Hannigan EV. Tumor board in gynecologic oncology. Int J Gynecol Cancer 2004; 14: 206–9. 16 Chang JH, Vines E, Bertsch H et al. The impact of a multidisciplinary breast cancer center on recommendations for patient management: the University of Pennsylvania experience. Cancer 2001; 91: 1231–7. 17 Lamb BW, Sevdalis N, Taylor C, Vincent C, Green JS. Multidisciplinary team working across different tumour types: analysis of a national survey. Ann Oncol 2012; 23: 1293–300. 18 National Breast Cancer Centre. Multidisciplinary Meetings for Cancer Care: A Guide for Health Service Providers. National Breast Cancer Centre, Camperdown, NSW 2005. 19 Everitt S, Herschtal A, Callahan J et al. High rates of tumor growth and disease progression detected on serial pretreatment fluorodeoxyglucose-positron emission tomography/ computed tomography scans in radical radiotherapy candidates with nonsmall cell lung cancer. Cancer 2010; 116: 5030–7. 20 Mileshkin L, Zalcberg J. The multidisciplinary management of patients with cancer. Ann Oncol 2006; 17: 1337– 8. 21 Blazeby JM, Wilson L, Metcalfe C, Nicklin J, English R, Donovan JL. Analysis of clinical decision-making in multidisciplinary cancer teams. Ann Oncol 2006; 17: 457–60. 22 Lamb BW, Sevdalis N, Arora S, Pinto A, Vincent C, Green JS. Teamwork and team decision-making at multidisciplinary cancer conferences: barriers, facilitators, and opportunities for improvement. World J Surg 2011; 35: 1970–6.
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