Abstract: In order to identify the impact of decreasing variability in surgical care through a structured multidisciplinary thoracic oncology program (TOP), the researchers observed changes following the implementation of standardized policies in the management of patients with non–small cell lung cancer (NSCLC) at an academic medical center. A retrospective single institution study of patients undergoing thoracic lobectomy for NSCLC from July 2004 to June 2005 (pre-TOP) and July 2008 to June 2009 (post-TOP) was conducted. A total of 166 patients were identified within our institutional database (pre-TOP, n = 67; post-TOP, n = 99). Post-TOP patients were more likely to be clinically staged (70% vs 42%, P < .001), undergo mediastinoscopy (41% vs 15%, P < .001), bronchoscopy (43% vs 25%, P = 0.021), and video-assisted thorascopic surgery resection (57% vs 15%, P < .001). Post-TOP lobectomies were also associated with a greater number of lymph nodes procured (14 vs 8, P < 0.0001). Among patients clinically staged, pathologic staging was equally concordant in both groups, 61% vs 55% (P = .25). At lobectomy for the post-TOP and pre-TOP patients, pathologic upstaging occurred less frequently (16% vs 25%) and understaging occurred more frequently, respectively. The 5-year survival was not significantly different between pre- and post-TOP eras (56% vs 61%, P = .52). Among patients undergoing mediastinoscopy and lobectomy, post-TOP patients had greater 5-year survival (58% vs 18%, P = .012). Post-TOP lobectomy is associated with increased clinical staging, greater utilization of mediastinoscopy and bronchoscopy, performance of minimally invasive resection, greater number of lymph nodes procured, and decreased length of stay. Direct and indirect benefits of a structured multidisciplinary TOP using standardized policies positively affect surgical outcomes and warrant greater study to evaluate specific metrics associated with improved survival.
Multidisciplinary tumor boards (MDTBs) are used to improve patient outcomes by providing consensus recommendations from specialists within a particular discipline. Disease management through MDTBs has improved quality of care, but the achievement of this success is thought to be multifactorial. Reduction in time from diagnosis to treatment; treatment regimens that follow standardized guidelines; increased communication between specialists; and reduction of inequities in patient care across demographics are believed to be some of the metrics best optimized by this format.1 Despite the long-term institution and widespread use of multidisciplinary teams, the scientific literature is limited in the examination of benefits associated with multidisciplinary team care in non–small cell lung cancer (NSCLC). The objective of this study was to identify the impact of decreasing variability in surgical care through a structured multidisciplinary thoracic oncology program (TOP), using standardized policies in the management of patients with NSCLC.
Our institutional database and medical records were queried for patients undergoing lobectomy for NSCLC during two distinct time periods: July 2004 to June 2005 (pre-TOP) and July 2008 to June 2009 (post-TOP). Institutional medical records and the Social Security Death Index were used to assist in determining vital status through June 2016. The Human Investigation Committee (IRB) of Yale University granted approval for this study.
Demographic characteristics, preoperative data, perioperative outcomes, and overall survival were recorded. Preoperative evaluation included the utilization of a bronchoscopy and mediastinoscopy prior to lobectomy, date of first tissue diagnosis, completion of clinical staging prior to lobectomy, use of neoadjuvant chemotherapy, and positron emission tomography (PET) imaging. Perioperative outcomes included length of stay (LOS), complications, mortality, pathological staging, and timing of adjuvant chemotherapy. Pathologic staging was evaluated using the American Joint Committee on Cancer Cancer Staging Manual (6th ed), given the time periods selected for analysis.2 This edition was selected because it spanned both time periods studied in this investigation.
MDTB TOP Structure
The MDTB consisted of clinical specialists from thoracic surgery, medical oncology, radiation oncology, pulmonology, pathology, radiology, and nuclear medicine. Additional personnel included clinicians from collaborative programs such as the smoking cessation group, clinical trials program, associated hospital staff viewing the conference remotely, the hospital cancer registry office, and other ancillary staff members. Tumor board was held on a weekly basis, with a mandated quorum of representatives from each of the key oncological services. During the study period, a quorum was available for all tumor boards. In the post-TOP era, a codified set of standardized policies based upon an amalgamation of national and international guidelines, as well as from comprehensive programmatic evaluations of existing scientific evidence, were adopted and employed as standardized policies in the management of all patients presented in the MDTB.
Selection of preoperative evaluation (bronchoscopy with or without mediastinoscopy) and operative approach (open or thoracoscopic lobectomy) was performed at the discretion of the surgical team in the pre-TOP era. Table 1 shows changes made through opinions generated by the MDTB in the post-TOP era, based upon the standardized policies regarding the surgical management of patients.
Measured values are reported as percentages or means ± standard deviations. Comparison between groups for LOS was analyzed by the Mann-Whitney test. Comparison between groups with respect to demographic characteristics, preoperative data, and perioperative outcomes were analyzed by student’s t test or Fisher’s exact test. Survival was calculated using Kaplan-Meier analysis, and comparisons between groups made using the log-rank method. Standard errors are reported in the Kaplan-Meier analyses. A P value < .05 was considered statistically significant. Analysis were performed using Prism 6 software (GraphPad Software, La Jolla, CA).
We identified 166 patients in our institutional database treated during our study period. Sixty-seven patients were treated pre-TOP (40%), with 99 patients treated post-TOP (60%). The mean age at the time of operation was 67±10 years. Patient demographics were not significant between groups, as shown in Table 2.
Patients in the post-TOP era were more likely to undergo bronchoscopy (43% vs. 23%; P = .02) and mediastinoscopy (41% vs. 15%; P < .001) compared with the pre-TOP group. Clinical staging was also more likely to be performed in the post-TOP group (70% vs 42%; P < .001). No difference was identified with respect to the use of PET imaging (76% vs 82%; P = .43). The use of neoadjuvant therapy was also equivalent between groups (4% vs 12%; P = .11).
The mean time between tissue diagnosis and lobectomy for the pre-TOP group was 20±44 vs 26±38 days for the post-TOP group (P = .37). In the post-TOP group, 51% of patients underwent mediastinoscopy, either before or simultaneous with their lobectomy; only 21% of the pre-TOP group underwent mediastinoscopy (P < .001). Additionally, patients in the post-TOP group were more likely to undergo video-assisted thoracoscopic surgery (VATS) lobectomy (57%) compared with the pre-TOP group (15%; P < .001). Patients who underwent lobectomy during the post-TOP period had an increased mean number of lymph nodes sample (14 vs 8; P < .001). Patients resected during the post-TOP time period also had a shorted median LOS (4 vs 5 days pre-TOP; P = .01), as shown in Table 3.
No differences in adjuvant chemotherapy treatment for patients with an appropriate indication (positive lymph nodes or tumor > 4 cm) was identified between groups (16% pre-MTDB vs 22% post-MTDB, P = .36; 45% vs 59% received; P = .49). Of those receiving adjuvant chemotherapy, 40% of the pre-TOP and 74% of the post-TOP patients were treated within 8 weeks of their lobectomy (P = .08).
In this study cohort, adenocarcinoma was the predominant tumor type, representing 61% of all cases. Other tumor types included squamous cell carcinoma (25%), carcinoid tumors (6%), large cell carcinoma (5%), and adenosquamous carcinoma (3%). No significant differences in the distribution of tumor pathology type were noted between pre- and post-TOP groups. Eighty percent of all patients had pN0 disease, while pN1, pN2, and pN3 disease was identified in 13%, 6%, and 1% of patients, respectively, (P = .70). Summary TNM Classification of Malignant Tumors pathologic staging was equivalent, as shown in Table 4.
Clinical and pathologic staging was compared between groups (Table 5). The clinical staging assigned preoperatively was concordant with final pathologic staging in 61% of the pre-TOP group and 55% of the post-TOP group (P = .25). Clinical stage underappreciated pathologic stage in 25% of the pre-TOP groups and 16% of post-TOP group. Overstaging occurred in 14% of the pre-TOP group and 29% of post-TOP patients.
The median follow-up for all patients was 7 years, and the overall 5-year survival was 59%. As shown in Figure 1, no difference was noted between pre- and post-TOP groups (58% vs 65%; P = .46). However, 5-year overall survival was significantly different between groups when examining patients that underwent both mediastinoscopy and lobectomy (23% pre-TOP vs 55% post-TOP; P = .03), as shown in Figure 2.
This study characterizes the impact of instituting a MDTB within the context of a TOP, including its association with short- and long-term outcomes in NSCLC patients. The fact that improved clinical upstaging was identified in the post-TOP group is reflective of a greater concerted effort to adhere with guidelines recommending this practice. This observation also reflects that standardized institutional lung cancer protocols, combining national guidelines3 with a comprehensive assessment of the existing data, were used to harmonize the staging and workup of lung cancer patients for surgical therapy.
The use of both bronchoscopy and mediastinoscopy in our series was greater than what has been reported in other investigations.4 Most notably, there was an approximately two-fold increase in the use of preoperative bronchoscopy and three-fold increase in cervical mediastinoscopy in the post-TOP group. As a result, assignment of clinical stages prior to definitive surgical resection increased from 42% to 70% between the study periods.
An increase in clinical upstaging secondary to performance of mediastinal staging is a known outcome of instituting a MDTB, described initially by Forrest and colleagues5 and Freeman and colleagues.6 The recording of the clinical stage was a concerted effort in the post-TOP era, both prior to definitive resection.
Another benefit of instituting a MDTB that adheres to standardized policies was that it allowed the examination of accuracy of clinical staging on predicting final pathologic staging. Although superficially the overall findings showed no significant difference in staging accuracy between the two MDTB eras, a deeper dive provides interesting observations. The pre-TOP group had a higher incidence of understaging (25% vs 16%), and the post-TOP group a higher incidence of overstaging (29% vs 14%). Post-hoc analysis revealed no difference in “surprise” N2 disease between groups in patients with pathologic stage III disease. These findings are consistent with other studies that have examined the effects of MDTBs on clinical staging after the institution of a MDTB. Pawlick and colleagues found that a MDTB for pancreatic cancer resulted in 19% of patients being assigned a different clinical stage, and 3% being assigned a different pathologic staging.7 Wheless and colleagues demonstrated that the use of a MDTB for head and neck cancers resulted in 27% of patients having to change in either a diagnosis, staging, or planned treatment following a MDTB conference.8
The post-TOP cohort had a three-fold increase in the performance of VATS lobectomy compared with pre-TOP patients. Increased adoption of minimally invasive resections has been observed in other studies that have investigated the impact of MDTB initiation on performance metrics in lung cancer.9,10 Additionally, compared with open lobectomy, VATS lobectomy was associated with lower rates of morbidity and shorter LOS,10-12 which is similar to other studies that have demonstrated the benefits of minimally invasive resection.
There was no difference in the delivery of neoadjuvant or adjuvant chemotherapy in the pre- or post-TOP study periods. Previous studies have demonstrated the institution of MDTBs resulted in increased use of adjuvant chemotherapy.5,6 The reasons for this deviation in our observation remain unclear. Although the initiation of MDTB was associated with a harmonization of practice patterns among surgeons, continuity with medical oncologists likely existed prior to the study period within our institution. In the post-TOP era, use of neoadjuvant therapy was more regimented in the institutional standardized policy, and also was reliant upon enrollment in a clinical trial. Outside of this indication, definitive chemoradiation therapy was employed was for stage III disease. Similarly, adjuvant therapy beyond the commonly accepted indications was limited to enrollment in a clinical trial. These reasons possibly could explain the lack of a difference in the use of neoadjuvant and adjuvant therapy, rather than clinician preference.
The beneficial effect of MDTB on survival also remains a controversial issue. In a meta-analysis by Coory and collegues,13 only two of eight studies reported improvement in long-term survival associated with the institution of a MDTB. Neither of these two studies discussed the impact of including surgery on long-term survival in the context of a MDTB.5,14 This trend was also observed in a study by Leo and colleagues, which did not show a significant increase in survival with the institution of a MDTB.15 In a study by Keating and colleagues that included 138 Veterans Affairs medical centers, outcomes for lobectomy were compared between facilities that used a MDTB for lung cancer and centers that did not. One-year survival did not differ (41% vs 43%).16
The findings of our study are in keeping with the aforementioned studies. Although speculative, the lack of a benefit associated with the institution of a MDTB may simply reflect different patient selection. This theoretical observation remains to be validated, but is supported by the findings of this study that demonstrated concordance between the preoperative and postoperative stages among the pre-TOP and post-TOP eras. In the post-TOP era, the concordance may have been due to the confluence of greater incidence of invasive preoperative staging coupled with greater lymph nodes being procured. Understaging preoperatively and postoperatively may have rendered the pre-TOP as possessing a concordance rate similar to that of post-TOP, but may not have been a reflection of accurate staging.
The survival benefit among patients undergoing mediastinoscopy followed by lobectomy in the post-TOP era was remarkably significant. In the absence of more pathologic upstaging in the pre-TOP era when mediastinoscopy was used less frequently, the explanation for this observation is mostly likely multifactorial. Prior to the establishment of a structured MDTB at our institution, a codified set of programmatic guidelines based upon national and international guidelines and a systematic review of the existing scientific evidence did not exist. Concomitant with the inception of a structured MDTB was the creation of a TOP with thoracic surgeons who agreed to harmonize individual practice patterns adhering to discrete standardized protocols for care. Performance of lung cancer resections by dedicated general thoracic surgeons has been shown to be associated with improved survival when compared with nondedicated general thoracic surgeons.10,17 This includes more reliable performance of preoperative mediastinal staging and intraoperative mediastinal dissection, resulting in appropriate staging.10,17,18 The procurement of more lymph nodes in the post-TOP era was reflective of the adherence to the standardized protocols. Better mediastinal staging in our series resulted in increased referral of patients for adjuvant chemotherapy, and suggests a possible mechanism to explain the survival advantage associated with treatment in the post-TOP era.
The lack of information regarding concordance with tumor recommendations and actual therapeutic plans rendered remains a substantial limitation of this study. However, since the performance of lobectomy was the common element among all patients in this investigation, the MDTB’s role ostensibly was to ensure a satisfactory preoperative assessment prior to lobectomy rather than to determine appropriateness for a particular type of resection. Consequently, the results of this analysis are reflective of an adherence to the consensus recommendations of the MDTB. Schmidt and colleagues reported in their series of 479 patients presented in their thoracic MDTB that the original plans were modified in 35%.19 Despite these recommended changes, adherence to the tumor boards’ recommendations was 98%, regardless of whether there was agreement with the original plan or if the original plan was changed. This observation supports the reality that consensus decisions of an MDTB carries significant weight. Coupled with our findings, these results also suggest that there is a collective valuation of limiting variability in surgical care through standardizing management policies.
It warrants mentioning that the initial alignment of the stakeholders in the MDTB and the TOP included an institutional effort to enhance the other disciplines that were fundamental pillars to the TOP. This effort included the recruitment of a greater number of medical oncologists, with a specific focus on increasing the number and enrollment in clinical trials; pulmonologists and interventional pulmonologists, with a specific interest in thoracic oncology; and radiation oncologists, who were focused on contributing regularly to the MDTB and the TOP. All MDTB and TOP members were participants in routine programmatic meetings that were used to consistently review and update the standardized policies employed for all disciplines. Finally, it also is worthwhile to mention that the time period in which the post-TOP era was studied also coincided with the opening of our new cancer hospital. The transition to the new facility, which included a state-of-the-art tumor board conference room, served as a symbol for cultural change in the institution.
It ultimately appears that the institution and use of a MDTB in the context of a TOP improves outcomes for patients undergoing lobectomy for NSCLC. Quantifiable benefits of an MDTB include the greater usage of evidence-based and protocol-driven invasive mediastinal staging, increased use of minimally invasive resection, greater number of lymph nodes procured, and decreased LOS. These direct benefits—as well as innumerable indirect benefits—positively affect surgical outcomes and warrant greater study to determine specific ways to improve the efficiency and performance of lung cancer resection.
1. Powell HA, Baldwin DR. Multidisciplinary team management in thoracic oncology: more than just a concept? Eur Respir J. 2014;43(6):1776-1786.
2. Greene FL PD, Fleming ID, Fritz A, Balch CM, Haller DG, Morrow M, eds. American Joint Committee on Cancer: AJCC Cancer Staging Manual. 6th ed. New York, NY: Springer; 2002.
3. Silvestri GA, AV G, Jantz M, et al. Methods of staging for non-Small cell lung cancer: diagnosis and management of lung cancer 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines Chest. 2013;143(5 Suppl):e211S-e250S.
4. Vinod SK, O’Connell DL, Simonella L, et al. Gaps in optimal care for lung cancer. J Thorac Oncol. 2008;3(8):871-879.
5. Forrest LM, McMillan DC, McArdle CS, Dunlop DJ. An evaluation of the impact of a multidisciplinary team, in a single centre, on treatment and survival in patients with inoperable non-small-cell lung cancer. Br J Cancer. 2005;93(9):977-978.
6. Freeman RK, Van Woerkom JM, Vyverberg A, Ascioti AJ. The effect of a multidisciplinary thoracic malignancy conference on the treatment of patients with lung cancer. Eur J Cardiothorac Surg. 2010;38(1):1-5.
7. Pawlik TM, Laheru D, Hruban RH, et al. Evaluating the impact of a single-day multidisciplinary clinic on the management of pancreatic cancer. Ann Surg Oncol. 2008;15(8):2081-2088.
8. Wheless SA, McKinney KA, Zanation AM. A prospective study of the clinical impact of a multidisciplinary head and neck tumor board. Otolaryngol Head Neck Surg. 2010;143(5):650-654.
9. Martin-Ucar AE, Waller DA, Atkins JL, Swinson D, O’Byrne KJ, Peake MD. The beneficial effects of specialist thoracic surgery on the resection rate for non-small-cell lung cancer. Lung Cancer. 2004;46(2):227-232.
10. Farjah F, Flum DR, Varghese TK, Jr, Symons RG, Wood DE. Surgeon specialty and long-term survival after pulmonary resection for lung cancer. Ann Thorac Surg. 2009;87(4):995-1004; discussion 1005-1006.
11. Scott WJ, Allen MS, Darling G, et al. Video-assisted thoracic surgery versus open lobectomy for lung cancer: a secondary analysis of data from the American College of Surgeons Oncology Group Z0030 randomized clinical trial. J Thorac Cardiovasc Surg. 2010;139(4):976-981; discussion 981-973.
12. Paul S, Altorki NK, Sheng S, et al. Thoracoscopic lobectomy is associated with lower morbidity than open lobectomy: a propensity-matched analysis from the STS database. J Thorac Cardiovasc Surg. 2010;139(2):366-378.
13. Coory M, Gkolia P, Yang IA, Bowman RV, Fong KM. Systematic review of multidisciplinary teams in the management of lung cancer. Lung Cancer. 2008;60(1):14-21.
14. Price A, Kerr G, Gregor A, Ironside J, Little F. The impact of multidisciplinary teams and site specialisation on the use of radiotherapy in elderly people with non-small cell lung cancer (NSCLC). Radiother Oncol. 2002;64(Suppl 1):80.
15. Leo F, Venissac N, Poudenx M, Otto J, Mouroux J; Groupe d’Oncologie Thoracique A. Multidisciplinary management of lung cancer: how to test its efficacy? J Thorac Oncol. 2007;2(1):69-72.
16. Keating NL, Landrum MB, Lamont EB, Bozeman SR, Shulman LN, McNeil BJ. Tumor boards and the quality of cancer care. J Natl Cancer Inst. 2013;105(2):113-121.
17. Ellis MC, Diggs BS, Vetto JT, Schipper PH. Intraoperative oncologic staging and outcomes for lung cancer resection vary by surgeon specialty. Ann Thorac Surg. 2011;92(6):1958-1963; discussion 1963-1954.
18. Osarogiagbon RU, Yu X. Mediastinal lymph node examination and survival in resected early-stage non-small-cell lung cancer in the surveillance, epidemiology, and end results database. J Thorac Oncol. 2012;7(12):1798-1806.
19. Schmidt HM, Roberts JM, Bodnar AM, et al. Thoracic multidisciplinary tumor board routinely impacts therapeutic plans in patients with lung and esophageal cancer: a prospective cohort study. Ann Thorac Surg. 2015;99(5):1719-1724.