- Email: [email protected]
Surgery and Surgical Consult Rates for Early Stage Lung Cancer in Ontario: A Population-Based Study
Surgery and Surgical Consult Rates for Early Stage Lung Cancer in Ontario: A Population-Based Study Anna M. Bendzsak, MD, MHS, Thomas K. Waddell, MD, PhD, David R. Urbach, MD, MS, and Gail E. Darling, MD Department of Surgery, University of Toronto; Division of Thoracic Surgery, University Health Network; and Department of Surgery and Institute of Health Policy Management and Evaluation, Dalla Lana School of Public Health, University of Toronto, and Division of General Surgery, University Health Network, Institute for Clinical Evaluative Science, Toronto, Ontario, Canada
Background. Surgery offers the best chance for survival for early (stage I and II) non-small cell lung cancer (NSCLC), but worldwide resection rates range from 49% to 77%. We investigated factors that may play a role in resection rates. Methods. Using administrative data, new diagnoses of NSCLC from 2010 through 2012 were captured. The rate of surgical consultation and resection overall and by age group were determined, as well as rates of pulmonary function testing and radiation therapy. Results. Of 4,309 persons diagnosed with stage I or II NSCLC between 2010 and 2012, 3,487 (80.9%) received surgical consultations, but only 58.9% (2,539) received surgery. Rates of consultation and surgery decreased with increasing patient age: only 60.3% of patients older than 80 received consultations and 29.9% had resections. Of the 1,770 patients who did not receive surgery, 948 (53.6%)
received a surgical consultation, and in this group, 688 (72.5%) were treated with radiation. Of the 822 patients who did not see a surgeon, only 476 (57.9%) were treated with radiation. Pulmonary function testing was performed in 799 (84.3%) of patients who had surgical consults but in only 569 (69.2%) of those who did not see a surgeon. Conclusions. Resection rates for early lung cancer appear low, which may be partly due to low rates of surgical consultation. Interestingly, patients who are seen by surgeons but who do not receive surgery are more likely to receive radiation than patients who are not referred for surgery. Further research is required to identify factors influencing resection rates.
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patient preferences, as well as surgeon comfort level with high-risk patients also factor into decision making for surgery [7, 8]. Given the reported rates of surgery for potentially curable disease, we wanted to determine whether referral to a surgeon was the determining factor for resection rates, or whether decision making by surgeons plays the larger role. The primary objectives were to determine rates of surgical consultation and resection for patients diagnosed with stage I and II NSCLC in Ontario between 2010 and 2012. Secondary objectives were to explore the reasons why patients do not receive surgery by measuring rates of pulmonary function testing and radiation therapy.
ung cancer remains the third-most common cancer diagnosed for men and the second-most common type of cancer among women in Canada, representing 23,780 people diagnosed in 2015 [1]. Cure for early (stage I and II) non-small cell lung cancer (NSCLC) is best achieved with surgical resection [2]. Other treatment modalities including radiation therapy, stereotactic radiation, and radiofrequency ablation have not yet been shown to offer the same long-term survival advantage as surgery [3]. Although surgery remains the optimal treatment choice for early NSCLC, resection rates for stage I and II range from 49% to 77% [4–6]. Evaluation of surgical risk is critical for selection of patients for surgery and remains a clinical judgment. American College of Chest Physicians guidelines for high-risk patients include pulmonary function tests (PFTs) [6], but other patient comorbidities,
(Ann Thorac Surg 2016;-:-–-) Ó 2016 by The Society of Thoracic Surgeons
Patients and Methods Study Design and Sources of Data
Accepted for publication Sept 7, 2016. Presented at the Poster Session of the Fifty-second Annual Meeting of The Society of Thoracic Surgeons, Phoenix, AZ, Jan 23–27, 2016. Address correspondence to Dr Darling, University of Toronto, Division of Thoracic Surgery, University Health Network, 200 Elizabeth Street, 9N955, Toronto, ON M5G 2C4, Canada; email: [email protected].
Ó 2016 by The Society of Thoracic Surgeons Published by Elsevier
We conducted a retrospective cohort study using provincial health administrative data sources and a cancer registry. The databases used capture all hospital discharge abstracts, physician billings, and diagnoses of new cancers in Ontario. The lung cancer stage variable in the Ontario Cancer Registry is obtained by collaborative 0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2016.09.025
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BENDZSAK ET AL RATES OF CONSULTATION AND SURGERY FOR NSCLC
Ann Thorac Surg 2016;-:-–-
staging methods [9]. The study protocol was approved by the Research Ethics Board of the Sunnybrook Health Sciences Center at the University of Toronto.
Table 1. Distribution of Treatments for Stage I and II NonSmall Cell Lung Cancer
Study Population
Total number of patients Surgical resection Surgical consultation Pulmonary function test Radiation therapya
We studied all adults aged at least 18 years in Ontario who were diagnosed with stage I and II primary NSCLC between January 1, 2010, and December 31, 2012.
Outcomes We examined the rates of surgery, consultation with a surgeon, radiation therapy, and pulmonary function testing. To ensure complete capture of lung resections in our databases, we defined surgery as lobectomy, pneumonectomy, or sublobar resection of the lung occurring within 2 months before or 6 months after a diagnosis of primary lung cancer. We defined assessment by a surgeon as a surgical consult occurring within 2 months before or 6 months after a diagnosis of primary lung cancer. Pulmonary function testing was defined as receiving a PFT within 1 year before or 6 months after a diagnosis of primary lung cancer. We used radiation planning codes to examine rates of radiation therapy, occurring any time after 2 months before diagnosis. Receipt of chemotherapy was not measured because of database limitations.
Analyses We conducted descriptive analyses to examine the rate of interventions, and report unadjusted results. Our primary analyses examined rates of surgical consults and surgery for the entire cohort. In the group of patients who did not have surgery, we examined rates of surgical consultation, PFT, and radiation therapy. Further, we evaluated rates of PFT and radiation therapy among those who did not receive surgical consults, as well as for those who received a consultation with a surgeon but did not receive surgery. To evaluate whether our findings varied by age, we conducted all analyses by age groups.
Results Between January 1, 2010, and December 31, 2012, 17,752 persons were diagnosed with NSCLC, and 3,206 persons (18%) went on to receive surgery. Of the total number diagnosed during this period, 4,309 (24.3%) presented with stage I or II NSCLC. In this group, 3,487 (80.9%) received surgical consults, and 2,539 (58.9%) received surgery. Of all patients diagnosed with stage I and II NSCLC, PFTs were performed in 3,831 (88.9%; Table 1). Of the 1,770 patients who did not receive surgery, 1,164 (65.8%) were treated with radiation and 606 received no treatment. Only 948 (53.6%) of these patients were assessed by a surgeon. Patients who were assessed by a surgeon but not treated with surgery were more likely to receive treatment with radiation (688 of 948, or 72.6%) compared with patients who did not have a surgical consult (476 of 822, or 57.9%). Similarly, patients assessed by a surgeon but who subsequently received no treatment were more likely to have PFTs (799 of 948, or 84.3%)
Patient Characteristics
Total (%) 4,309 2,539 (58.9) 3,487 (80.9) 3,831 (88.9) 1,164 (27.0)
Stage I (%) Stage II (%) 3,469 2,038 2,772 3,075 940
(80.5) (58.7) (79.9) (88.6) (27.1)
840 501 715 756 224
(19.5) (59.6) (85.1) (90.0) (26.7)
a
Includes patients who received only radiation therapy as a treatment; 563 patients received both surgery and radiation therapy as treatment.
compared with patients not assessed by a surgeon (569 of 822, or 69.2%). Of the non-surgical patients overall, PFTs were performed in 1,368 (77.2%)—1,011 (86.9%) of those treated with radiation and 357 (58.9%) of those who received no treatment—versus 2,463 of the 2,539 surgical patients (97%). Patients treated with radiation who had a surgical consult (688) were more likely to have received a PFT (613, or 89.1%). The age distribution at diagnosis reveals that the majority of patients diagnosed with stage I and II NSCLC (66%) are diagnosed between 60 and 79 years of age (2,844 of 4,309 patients; Table 2). Surgery rates are the highest (77.0%) for patients aged less than 60 years, but decreased to 58.7% (908 of 1,546) for those aged 70 to 79 years and to 39.7% (219 of 552) for those aged 80 to 84 years. Surgical consults are also highest (91.7%) for patients aged less than 60 years, and decrease to 81.8% for those aged 70 to 79 years and to 68.7% (379 of 552) for those aged 80 to 84 years. The proportion not treated with either surgery or radiation increased with age. Below the age of 70 years, 205 patients (10.7%) did not receive a surgical consultation and 166 (8.7%) received no surgical or radiation therapy treatment; whereas in the group aged 70 to 79 years, 281 patients (18.2%) did not receive a surgical consult and 195 (12.6%) received no treatment. For the group more than 80 years of age, 336 of the 848 patients (39.6%) did not have a consult, and 245 (28.9%) received neither surgery nor radiation therapy.
Comment Our study of 4,309 stage I and II NSCLC patients in Ontario between 2010 and 2012 found a surgical consultation rate of 80.9% and a resection rate of 58.9%. Table 2. Age Distribution and Receipt of Surgical Consultation and Surgical Resection Patient Age (years)
Total
<60 60–69 70–79 80–84 85
617 1,298 1,546 552 296
Values are n or n (%).
Surgical Consultation 566 1,144 1,265 379 133
(91.7) (88.1) (81.8) (68.7) (44.9)
Surgical Resection 475 905 908 219 35
(77.0) (69.7) (58.7) (39.7) (11.8)
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Although surgery is the standard of care for early stage NSCLC, fewer than half (46.4%) of the patients not treated surgically were assessed by a surgeon. Patients who were assessed by a surgeon even though they did not undergo resection were more likely to receive radiation treatment and to be assessed with PFTs. With increasing age, patients were less likely to receive a surgical consultation and a higher proportion of those over 70 years of age received no treatment. Although a limited number of studies have reported resection rates for early stage lung cancer, our study is the first to investigate potential explanations for resection rates by examining population-level consultation rates and the use of pulmonary function testing and radiation therapy. The administrative databases allowed us to capture all events in Ontario during the study period, thereby minimizing potential selection bias. Our Ontario resection rate for early NSCLC of 58.9% falls within the lower end of the range of reported resection rates worldwide. A study from the Pacific Northwest of the United States found that 70.2% to 71.2% of all patients with stage I and II NSCLC received surgery for their cancer. An examination of the Surveillance, Epidemiology, and End Results (SEER) database from 2001 to 2006 reported resection rates of 77.1% for patients with stage I and II NSCLC [5]. In comparison, an English study reported significantly lower resection rates of 49% to 57% of patients with stage I and II NSCLC between 2004 and 2009 [4]. Overall resection rates for NSCLC in England during this period, however, were reported to be approximately 9% [10], in comparison with resection rates in the United States of 18% to 25% [11–13]; and therefore the reported resection rates for early lung cancer are likely inappropriately low. Our finding of approximately 20% of newly diagnosed early stage NSLC patients in Ontario not receiving referral to a surgeon may explain, in part, somewhat lower than expected resection rates for early stage lung cancer. Although the majority of early stage lung cancer patients were referred to surgeons, a higher consultation rate might have been expected given that early stage NSCLC represents potentially curable disease and surgical resection is the standard of care. Determinants for nonreferral may include patient comorbidity, patient preference, or perception of surgical risk. We were not able to determine comorbidity in our dataset, but did find that consultations among the elderly were considerably lower. Patient comorbidities increase with age, and hence, age is often an important determinant for surgical selection [14, 15]. There is a general consensus, however, that older patients should not be denied surgery based on age alone, as many studies have shown that appropriately selected patients have perioperative outcomes and survival advantages similar to those of standard patient selection [16–18]. In a recent analysis of the SEER database, Ganti and associates [19] found that rates of surgery among patients more than 80 years of age with stage I and II NSCLC have been increasing over time, with an overall resection rate for cases between 1998 and 2007 of 44.4%. In our study,
BENDZSAK ET AL RATES OF CONSULTATION AND SURGERY FOR NSCLC
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the resection rate of patients aged more than 80 years was only 29.9%, significantly lower than that reported in the SEER database study. The differences in resection rates may be due to differences in the use of wedge resection as an excisional biopsy in the elderly for the purpose of diagnosis and definitive management, or may reflect differences in the use of surgical resection for cure in the elderly. Wedge resection as a definitive surgical therapy for elderly patients has been shown to have similar longterm survival as lobectomy [20, 21], and therefore, is an important option when considering management of elderly patients with lung cancer. The use of videoassisted thoracoscopy surgery resections compared with open lung resections reduces the risk of death in the elderly [22], with mortality from video-assisted thoracoscopy surgery resections for elderly patients reported as low as 1.19% [23]; and survival for selected patients more than 80 years of age is similar to that for younger patients [24]. We similarly found that the rate of consultation among patients aged more than 80 years (60.4%) was lower than that for younger age groups (86%). These lower rates of consultation may be explained by the greater comorbidities of these patients that would preclude surgery, or possibly by referring physicians who are not aware of surgical approaches that can yield good results for selected elderly patients. Although other variables may also play a role, ideally patients should have an opportunity for informed decision making. Despite decreasing consultation rates with increasing age, we did not, however, find that age distributions completely accounted for the group of patients who did not receive surgical consultations; although 40.9% of those more than 80 years of age comprised this group, the majority of the patients were less than 80 years of age (34.2% were aged 70 to 79 years and 24.9% were less than 70 years of age). Many younger patients, therefore, also did not receive surgical consultation. Further investigation is required to determine if there is a baseline comorbidity rate that may preclude surgery in younger patients, or whether referral patterns, patient preference, or other variables explain our results. A better understanding of decisions for surgical referral is important, particularly with the increasing adoption of nonsurgical treatments, namely, stereotactic body radiation therapy, for early lung cancer [25]. Pulmonary function testing remains an important tool in preoperative evaluation, and is a critical guide for determining operative risks [26, 27]. Guidelines recommend that all surgical patients receive pulmonary function testing [28], but the use of PFTs for patients not referred for surgery has not been previously reported. Poor pulmonary reserve as reflected by poor results on PFTs may have been used to determine suitability for referral to a surgeon but we found that the use of PFTs was much less in the group who did not receive surgical consideration compared with all patients with early stage lung cancer (69.2% versus 88.9%, respectively). Clearly, other factors influence the decision to refer a patient to a surgeon. Surgeons receive referrals from any number of physicians, including family physicians, respirologists,
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BENDZSAK ET AL RATES OF CONSULTATION AND SURGERY FOR NSCLC
and oncologists, and PFTs may be ordered at any point along the referral process. The decreased use of PFTs for patients who receive no treatment may represent an incomplete assessment for suitability for referral, or may reflect other nonrespiratory comorbidities such as coronary artery disease and heart failure, which is known to increase surgical risk [29]. Our study examines the principal types of curative treatment, and we found that 14% of early stage NSCLC patients received no treatment at all. A better understanding of referral patterns for lung cancer could potentially help to explain our results. Rich and colleagues [30] examined resection rates among National Health Service centers in the United Kingdom and found that whether patients received surgery for lung cancer depended on whether they were initially evaluated in a center with thoracic surgery units. After adjusting for patient variables, patients seen in a thoracic surgery center were 51% more likely to have surgery [30]. Before our study’s time period, thoracic surgery in Ontario was regionalized to 14 centers, all associated with radiation therapy units, and multidisciplinary care for lung cancer patients is the prescribed standard of care [31]. Lung cancer patients seen in multidisciplinary settings are more likely to receive guideline-based treatments [32], and early stage lung cancer patients who do not receive surgery are more likely to receive radiation treatment [33]. In Ontario, because of the regionalization of thoracic surgery, some patients may not have access to thoracic surgery units. Our finding of a low rate of radiation therapy treatment (57.9%) among patients who did not receive surgical consultation suggests that perhaps some patients are being managed outside of thoracic centers affiliated with radiation therapy units. Conversely, the relatively higher rate of radiation therapy among patients who were seen by a surgeon but then did not receive surgery (72.6%) suggests that patients are more likely to receive some form of treatment for their lung cancer if they are seen by a surgeon at some point after their diagnosis. Furthermore, the high rate of PFTs among patients who receive surgery (97%) and patients who receive radiation therapy (86.9%) suggests that patients seen in thoracic units likely receive guidelineconcordant care. Our finding that only 72.8% of early-stage lung cancer patients referred for surgery go on to receive surgery is somewhat surprising. Lung resection is the standard of care for early stage lung cancer, and carries a mortality risk as high as 2% [34], although lower in high-volume centers and higher for high-risk patients [35]. American College of Chest Physician guidelines state that lowerrisk operations such as segmentectomy or wide wedge resection are acceptable for higher-risk patients [6], and several series report success with this approach [36, 37]. It may be that that not all surgeons have an equal surgical appetite for high-risk patients. For example, minimally invasive segmentectomy is a technically more demanding procedure [38], and not all surgeons in the province may be comfortable in performing this procedure. Further investigations with more detailed clinical data would help to understand surgical decision making.
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Limitations of our study include the use of administrative data that lack detailed clinical information on the severity of comorbid conditions. We therefore could not describe all comorbidities of patients not referred for surgery. However, we were able to capture the use of PFTs and therefore assess an important variable in preoperative assessment. Second, the limited data variables permitted only descriptive analyses. In conclusion, surgery rates for early NSCLC surgery in Ontario appear lower than previously published in the literature but are not fully explained by surgical consultation rates alone, as overall consultation rates are high. However, patients assessed by a surgeon and deemed not to be operative candidates are more likely to receive pulmonary function testing and to receive treatment with radiation compared with patients not assessed by a surgeon. Although increasing age appears to influence referral for surgical assessment, awareness among referring physicians of the appropriateness of surgery for elderly patients and the importance of surgeon assessment should be stressed. Similarly, surgery for selected elderly patients by surgeons should be supported. A deeper understanding of other patient factors requires exploration to appreciate which patients do not receive surgical consultation or other treatment, with a view to ensuring that all patients have an opportunity for curative treatment whenever appropriate. This study was conducted with the support of the Ontario Institute for Cancer Research and Cancer Care Ontario (CCO) through funding provided by the Government of Ontario [HSRPPRAP UHN RA #33]. This study was supported through provision of data by the Institute for Clinical Evaluative Sciences (ICES) and CCO, and through funding support to ICES from an annual grant by the Ministry of Health and Long-Term Care (MOHLTC). The opinions, results, and conclusions reported in this paper are those of the authors. No endorsement by ICES, CCO, or the Government of Ontario is intended nor should it be inferred.
References 1. Canadian Cancer Society. Canadian cancer statistics 2015. Available at: http://www.cancer.ca/w/media/cancer.ca/cw/ cancer%20information/cancer%20101/canadian%20cancer% 20statistics/canadian-cancer-statistics-2015-en.pdf2015. Accessed January 17, 2016. 2. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology non small cell lung cancer v. 7.2015. 2015. Available at: https://www.nccn.org/professiona ls/physician_gls/f_guidelines_nojava.asp. Accessed March 15, 2015. 3. Jones GC, Kehrer JD, Kahn J, et al. Primary treatment options for high-risk/medically inoperable early stage NSCLC patients. Clin Lung Cancer 2015;16:413–30. 4. Khakwani A, Rich AL, Powell HA, et al. Lung cancer survival in England: trends in non-small-cell lung cancer survival over the duration of the National Lung Cancer Audit. Br J Cancer 2013;109:2058–65. 5. Zeliadt SB, Sekaran NK, Hu EY, et al. Comparison of demographic characteristics, surgical resection patterns, and survival outcomes for veterans and nonveterans with nonsmall cell lung cancer in the Pacific Northwest. J Thorac Oncol 2011;6:1726–32.
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6. Donington J, Ferguson M, Mazzone P, et al. American College of Chest Physicians and Society of Thoracic Surgeons consensus statement for evaluation and management for high-risk patients with stage I non-small cell lung cancer. Chest 2012;142:1620–35. 7. Brunelli A. Risk assessment for pulmonary resection. Semin Thorac Cardiovasc Surg 2010;22:2–13. 8. Rocco G, Internullo E, Cassivi SD, van Raemdonck D, Ferguson MK. The variability of practice in minimally invasive thoracic surgery for pulmonary resections. Thorac Surg Clin 2008;18:235–47. 9. Cancer Quality Council of Ontario. Reporting of cancer stage at diagnosis. 2016. Available at: http://www.csqi.on.ca/by_ patient_journey/diagnosis/reporting_of_cancer_stage_at_dia gnosis/. Accessed July 22, 2016. 10. Riaz SP, Luchtenborg M, Jack RH, et al. Variation in surgical resection for lung cancer in relation to survival: populationbased study in England 2004–2006. Eur J Cancer 2012;48: 54–60. 11. Fry WA, Menck HR, Winchester DP. The National Cancer Data Base report on lung cancer. Cancer 1996;77:1947–55. 12. Humphrey EW, Smart CR, Winchester DP, et al. National survey of the pattern of care for carcinoma of the lung. J Thorac Cardiovasc Surg 1990;100:837–43. 13. Connolly CK, Johnston I, Milroy R, Jones R. Surgical resection rate in lung cancer. Thorax 1999;54:375. 14. Dell’Amore A, Monteverde M, Martucci N, et al. Lobar and sub-lobar lung resection in octogenarians with early stage non-small cell lung cancer: factors affecting surgical outcomes and long-term results. Gen Thorac Cardiovasc Surg 2015;63:222–30. 15. Janssen-Heijnen ML, Maas HA, Houterman S, Lemmens VE, Rutten HJ, Coebergh JW. Comorbidity in older surgical cancer patients: influence on patient care and outcome. Eur J Cancer 2007;43:2179–93. 16. Dillman RO, Zusman DR, McClure SE. Surgical resection and long-term survival for octogenarians who undergo surgery for non-small-cell lung cancer. Clin Lung Cancer 2009;10:130–4. 17. Hino H, Murakawa T, Ichinose J, et al. Results of lung cancer surgery for octogenarians. Ann Thorac Cardiovasc Surg 2015;21:209–16. 18. Demmy TL, Curtis JJ. Minimally invasive lobectomy directed toward frail and high-risk patients: a case-control study. Ann Thorac Surg 1999;68:194–200. 19. Ganti AK, Shostrom V, Alorabi M, et al. Early stage nonsmall-cell lung cancer in octogenarian and older patients: a SEER database analysis. Clin Lung Cancer 2016;17:285–91. 20. Mery CM, Pappas AN, Bueno R, et al. Similar long-term survival of elderly patients with non-small cell lung cancer treated with lobectomy or wedge resection within the Surveillance, Epidemiology, and End Results database. Chest 2005;128:237–45. 21. Razi SS, John MM, Sainathan S, Stavropoulos C. Sublobar resection is equivalent to lobectomy for T1a non-small cell lung cancer in the elderly: a Surveillance, Epidemiology, and End Results database analysis. J Surg Res 2016;200: 683–9. 22. Bravo Iniguez CE, Armstrong KW, Cooper Z, et al. Thirtyday mortality after lobectomy in elderly patients eligible for lung cancer screening. Ann Thorac Surg 2016;101:541–6.
BENDZSAK ET AL RATES OF CONSULTATION AND SURGERY FOR NSCLC
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23. Armstrong KW, Bravo-Iniguez CE, Jacobson FL, Jaklitsch MT. Recent trends in surgical research of cancer treatment in the elderly, with a primary focus on lung cancer: presentation at the 2015 annual meeting of SIOG. J Geriatric Oncol 2016 July 22 [E-Pub ahead of print]. 24. Owonikoko TK, Ragin CC, Belani CP, et al. Lung cancer in elderly patients: an analysis of the Surveillance, Epidemiology, and End Results database. J Clin Oncol 2007;25: 5570–7. 25. Pan H, Simpson DR, Mell LK, Mundt AJ, Lawson JD. A survey of stereotactic body radiotherapy use in the United States. Cancer 2011;117:4566–72. 26. Mazzone P. Preoperative evaluation of the lung resection candidate. Cleve Clin J Med 2012;79(E-Suppl 1):e17–22. 27. Martin J. Lung resection in the pulmonary-compromised patient. Thorac Surg Clin 2004;14:157–62. 28. Colice GL, Shafazand S, Griffin JP, Keenan R, Bolliger CT. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: ACCP evidencedbased clinical practice guidelines (2nd edition). Chest 2007;132(Suppl):161–77. 29. Eagle KA, Berger PB, Calkins H, et al. ACC/AHA guideline update for perioperative cardiovascular evaluation for noncardiac surgery—executive summary a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (committee to update the 1996 guidelines on perioperative cardiovascular evaluation for noncardiac surgery). Circulation 2002;105:1257–67. 30. Rich AL, Tata LJ, Free CM, et al. Inequalities in outcomes for non-small cell lung cancer: the influence of clinical characteristics and features of the local lung cancer service. Thorax 2011;66:1078–84. 31. Sundaresan S, Langer B, Oliver T, et al. Standards for thoracic surgical oncology in a single-payer healthcare system. Ann Thorac Surg 2007;84:693–701. 32. Kehl KL, Landrum MB, Kahn KL, Gray SW, Chen AB, Keating NL. Tumor board participation among physicians caring for patients with lung or colorectal cancer. J Oncol Pract 2015;11:e267–78. 33. 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;105:113–21. 34. Allen MS, Darling GE, Pechet TT, et al. Morbidity and mortality of major pulmonary resections in patients with early-stage lung cancer: initial results of the randomized, prospective ACOSOG Z0030 trial. Ann Thorac Surg 2006;81: 1013–20. 35. Bach PB, Cramer LD, Schrag D, Downey RJ, Gelfand SE, Begg CB. The influence of hospital volume on survival after resection for lung cancer. N Engl J Med 2001;345:181–8. 36. Sancheti MS, Melvan JN, Medbery RL, et al. Outcomes after surgery in high-risk patients with early stage lung cancer. Ann Thorac Surg 2016;101:1043–51. 37. Martin-Ucar AE, Nakas A, Pilling JE, West KJ, Waller DA. A case-matched study of anatomical segmentectomy versus lobectomy for stage I lung cancer in high-risk patients. Eur J Cardiothorac Surg 2005;27:675–9. 38. Leshnower BG, Miller DL, Fernandez FG, Pickens A, Force SD. Video-assisted thoracoscopic surgery segmentectomy: a safe and effective procedure. Ann Thorac Surg 2010;89:1571–6.
Background. Surgery offers the best chance for survival for early (stage I and II) non-small cell lung cancer (NSCLC), but worldwide resection rates range from 49% to 77%. We investigated factors that may play a role in resection rates. Methods. Using administrative data, new diagnoses of NSCLC from 2010 through 2012 were captured. The rate of surgical consultation and resection overall and by age group were determined, as well as rates of pulmonary function testing and radiation therapy. Results. Of 4,309 persons diagnosed with stage I or II NSCLC between 2010 and 2012, 3,487 (80.9%) received surgical consultations, but only 58.9% (2,539) received surgery. Rates of consultation and surgery decreased with increasing patient age: only 60.3% of patients older than 80 received consultations and 29.9% had resections. Of the 1,770 patients who did not receive surgery, 948 (53.6%)
received a surgical consultation, and in this group, 688 (72.5%) were treated with radiation. Of the 822 patients who did not see a surgeon, only 476 (57.9%) were treated with radiation. Pulmonary function testing was performed in 799 (84.3%) of patients who had surgical consults but in only 569 (69.2%) of those who did not see a surgeon. Conclusions. Resection rates for early lung cancer appear low, which may be partly due to low rates of surgical consultation. Interestingly, patients who are seen by surgeons but who do not receive surgery are more likely to receive radiation than patients who are not referred for surgery. Further research is required to identify factors influencing resection rates.
L
patient preferences, as well as surgeon comfort level with high-risk patients also factor into decision making for surgery [7, 8]. Given the reported rates of surgery for potentially curable disease, we wanted to determine whether referral to a surgeon was the determining factor for resection rates, or whether decision making by surgeons plays the larger role. The primary objectives were to determine rates of surgical consultation and resection for patients diagnosed with stage I and II NSCLC in Ontario between 2010 and 2012. Secondary objectives were to explore the reasons why patients do not receive surgery by measuring rates of pulmonary function testing and radiation therapy.
ung cancer remains the third-most common cancer diagnosed for men and the second-most common type of cancer among women in Canada, representing 23,780 people diagnosed in 2015 [1]. Cure for early (stage I and II) non-small cell lung cancer (NSCLC) is best achieved with surgical resection [2]. Other treatment modalities including radiation therapy, stereotactic radiation, and radiofrequency ablation have not yet been shown to offer the same long-term survival advantage as surgery [3]. Although surgery remains the optimal treatment choice for early NSCLC, resection rates for stage I and II range from 49% to 77% [4–6]. Evaluation of surgical risk is critical for selection of patients for surgery and remains a clinical judgment. American College of Chest Physicians guidelines for high-risk patients include pulmonary function tests (PFTs) [6], but other patient comorbidities,
(Ann Thorac Surg 2016;-:-–-) Ó 2016 by The Society of Thoracic Surgeons
Patients and Methods Study Design and Sources of Data
Accepted for publication Sept 7, 2016. Presented at the Poster Session of the Fifty-second Annual Meeting of The Society of Thoracic Surgeons, Phoenix, AZ, Jan 23–27, 2016. Address correspondence to Dr Darling, University of Toronto, Division of Thoracic Surgery, University Health Network, 200 Elizabeth Street, 9N955, Toronto, ON M5G 2C4, Canada; email: [email protected].
Ó 2016 by The Society of Thoracic Surgeons Published by Elsevier
We conducted a retrospective cohort study using provincial health administrative data sources and a cancer registry. The databases used capture all hospital discharge abstracts, physician billings, and diagnoses of new cancers in Ontario. The lung cancer stage variable in the Ontario Cancer Registry is obtained by collaborative 0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2016.09.025
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Ann Thorac Surg 2016;-:-–-
staging methods [9]. The study protocol was approved by the Research Ethics Board of the Sunnybrook Health Sciences Center at the University of Toronto.
Table 1. Distribution of Treatments for Stage I and II NonSmall Cell Lung Cancer
Study Population
Total number of patients Surgical resection Surgical consultation Pulmonary function test Radiation therapya
We studied all adults aged at least 18 years in Ontario who were diagnosed with stage I and II primary NSCLC between January 1, 2010, and December 31, 2012.
Outcomes We examined the rates of surgery, consultation with a surgeon, radiation therapy, and pulmonary function testing. To ensure complete capture of lung resections in our databases, we defined surgery as lobectomy, pneumonectomy, or sublobar resection of the lung occurring within 2 months before or 6 months after a diagnosis of primary lung cancer. We defined assessment by a surgeon as a surgical consult occurring within 2 months before or 6 months after a diagnosis of primary lung cancer. Pulmonary function testing was defined as receiving a PFT within 1 year before or 6 months after a diagnosis of primary lung cancer. We used radiation planning codes to examine rates of radiation therapy, occurring any time after 2 months before diagnosis. Receipt of chemotherapy was not measured because of database limitations.
Analyses We conducted descriptive analyses to examine the rate of interventions, and report unadjusted results. Our primary analyses examined rates of surgical consults and surgery for the entire cohort. In the group of patients who did not have surgery, we examined rates of surgical consultation, PFT, and radiation therapy. Further, we evaluated rates of PFT and radiation therapy among those who did not receive surgical consults, as well as for those who received a consultation with a surgeon but did not receive surgery. To evaluate whether our findings varied by age, we conducted all analyses by age groups.
Results Between January 1, 2010, and December 31, 2012, 17,752 persons were diagnosed with NSCLC, and 3,206 persons (18%) went on to receive surgery. Of the total number diagnosed during this period, 4,309 (24.3%) presented with stage I or II NSCLC. In this group, 3,487 (80.9%) received surgical consults, and 2,539 (58.9%) received surgery. Of all patients diagnosed with stage I and II NSCLC, PFTs were performed in 3,831 (88.9%; Table 1). Of the 1,770 patients who did not receive surgery, 1,164 (65.8%) were treated with radiation and 606 received no treatment. Only 948 (53.6%) of these patients were assessed by a surgeon. Patients who were assessed by a surgeon but not treated with surgery were more likely to receive treatment with radiation (688 of 948, or 72.6%) compared with patients who did not have a surgical consult (476 of 822, or 57.9%). Similarly, patients assessed by a surgeon but who subsequently received no treatment were more likely to have PFTs (799 of 948, or 84.3%)
Patient Characteristics
Total (%) 4,309 2,539 (58.9) 3,487 (80.9) 3,831 (88.9) 1,164 (27.0)
Stage I (%) Stage II (%) 3,469 2,038 2,772 3,075 940
(80.5) (58.7) (79.9) (88.6) (27.1)
840 501 715 756 224
(19.5) (59.6) (85.1) (90.0) (26.7)
a
Includes patients who received only radiation therapy as a treatment; 563 patients received both surgery and radiation therapy as treatment.
compared with patients not assessed by a surgeon (569 of 822, or 69.2%). Of the non-surgical patients overall, PFTs were performed in 1,368 (77.2%)—1,011 (86.9%) of those treated with radiation and 357 (58.9%) of those who received no treatment—versus 2,463 of the 2,539 surgical patients (97%). Patients treated with radiation who had a surgical consult (688) were more likely to have received a PFT (613, or 89.1%). The age distribution at diagnosis reveals that the majority of patients diagnosed with stage I and II NSCLC (66%) are diagnosed between 60 and 79 years of age (2,844 of 4,309 patients; Table 2). Surgery rates are the highest (77.0%) for patients aged less than 60 years, but decreased to 58.7% (908 of 1,546) for those aged 70 to 79 years and to 39.7% (219 of 552) for those aged 80 to 84 years. Surgical consults are also highest (91.7%) for patients aged less than 60 years, and decrease to 81.8% for those aged 70 to 79 years and to 68.7% (379 of 552) for those aged 80 to 84 years. The proportion not treated with either surgery or radiation increased with age. Below the age of 70 years, 205 patients (10.7%) did not receive a surgical consultation and 166 (8.7%) received no surgical or radiation therapy treatment; whereas in the group aged 70 to 79 years, 281 patients (18.2%) did not receive a surgical consult and 195 (12.6%) received no treatment. For the group more than 80 years of age, 336 of the 848 patients (39.6%) did not have a consult, and 245 (28.9%) received neither surgery nor radiation therapy.
Comment Our study of 4,309 stage I and II NSCLC patients in Ontario between 2010 and 2012 found a surgical consultation rate of 80.9% and a resection rate of 58.9%. Table 2. Age Distribution and Receipt of Surgical Consultation and Surgical Resection Patient Age (years)
Total
<60 60–69 70–79 80–84 85
617 1,298 1,546 552 296
Values are n or n (%).
Surgical Consultation 566 1,144 1,265 379 133
(91.7) (88.1) (81.8) (68.7) (44.9)
Surgical Resection 475 905 908 219 35
(77.0) (69.7) (58.7) (39.7) (11.8)
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Although surgery is the standard of care for early stage NSCLC, fewer than half (46.4%) of the patients not treated surgically were assessed by a surgeon. Patients who were assessed by a surgeon even though they did not undergo resection were more likely to receive radiation treatment and to be assessed with PFTs. With increasing age, patients were less likely to receive a surgical consultation and a higher proportion of those over 70 years of age received no treatment. Although a limited number of studies have reported resection rates for early stage lung cancer, our study is the first to investigate potential explanations for resection rates by examining population-level consultation rates and the use of pulmonary function testing and radiation therapy. The administrative databases allowed us to capture all events in Ontario during the study period, thereby minimizing potential selection bias. Our Ontario resection rate for early NSCLC of 58.9% falls within the lower end of the range of reported resection rates worldwide. A study from the Pacific Northwest of the United States found that 70.2% to 71.2% of all patients with stage I and II NSCLC received surgery for their cancer. An examination of the Surveillance, Epidemiology, and End Results (SEER) database from 2001 to 2006 reported resection rates of 77.1% for patients with stage I and II NSCLC [5]. In comparison, an English study reported significantly lower resection rates of 49% to 57% of patients with stage I and II NSCLC between 2004 and 2009 [4]. Overall resection rates for NSCLC in England during this period, however, were reported to be approximately 9% [10], in comparison with resection rates in the United States of 18% to 25% [11–13]; and therefore the reported resection rates for early lung cancer are likely inappropriately low. Our finding of approximately 20% of newly diagnosed early stage NSLC patients in Ontario not receiving referral to a surgeon may explain, in part, somewhat lower than expected resection rates for early stage lung cancer. Although the majority of early stage lung cancer patients were referred to surgeons, a higher consultation rate might have been expected given that early stage NSCLC represents potentially curable disease and surgical resection is the standard of care. Determinants for nonreferral may include patient comorbidity, patient preference, or perception of surgical risk. We were not able to determine comorbidity in our dataset, but did find that consultations among the elderly were considerably lower. Patient comorbidities increase with age, and hence, age is often an important determinant for surgical selection [14, 15]. There is a general consensus, however, that older patients should not be denied surgery based on age alone, as many studies have shown that appropriately selected patients have perioperative outcomes and survival advantages similar to those of standard patient selection [16–18]. In a recent analysis of the SEER database, Ganti and associates [19] found that rates of surgery among patients more than 80 years of age with stage I and II NSCLC have been increasing over time, with an overall resection rate for cases between 1998 and 2007 of 44.4%. In our study,
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the resection rate of patients aged more than 80 years was only 29.9%, significantly lower than that reported in the SEER database study. The differences in resection rates may be due to differences in the use of wedge resection as an excisional biopsy in the elderly for the purpose of diagnosis and definitive management, or may reflect differences in the use of surgical resection for cure in the elderly. Wedge resection as a definitive surgical therapy for elderly patients has been shown to have similar longterm survival as lobectomy [20, 21], and therefore, is an important option when considering management of elderly patients with lung cancer. The use of videoassisted thoracoscopy surgery resections compared with open lung resections reduces the risk of death in the elderly [22], with mortality from video-assisted thoracoscopy surgery resections for elderly patients reported as low as 1.19% [23]; and survival for selected patients more than 80 years of age is similar to that for younger patients [24]. We similarly found that the rate of consultation among patients aged more than 80 years (60.4%) was lower than that for younger age groups (86%). These lower rates of consultation may be explained by the greater comorbidities of these patients that would preclude surgery, or possibly by referring physicians who are not aware of surgical approaches that can yield good results for selected elderly patients. Although other variables may also play a role, ideally patients should have an opportunity for informed decision making. Despite decreasing consultation rates with increasing age, we did not, however, find that age distributions completely accounted for the group of patients who did not receive surgical consultations; although 40.9% of those more than 80 years of age comprised this group, the majority of the patients were less than 80 years of age (34.2% were aged 70 to 79 years and 24.9% were less than 70 years of age). Many younger patients, therefore, also did not receive surgical consultation. Further investigation is required to determine if there is a baseline comorbidity rate that may preclude surgery in younger patients, or whether referral patterns, patient preference, or other variables explain our results. A better understanding of decisions for surgical referral is important, particularly with the increasing adoption of nonsurgical treatments, namely, stereotactic body radiation therapy, for early lung cancer [25]. Pulmonary function testing remains an important tool in preoperative evaluation, and is a critical guide for determining operative risks [26, 27]. Guidelines recommend that all surgical patients receive pulmonary function testing [28], but the use of PFTs for patients not referred for surgery has not been previously reported. Poor pulmonary reserve as reflected by poor results on PFTs may have been used to determine suitability for referral to a surgeon but we found that the use of PFTs was much less in the group who did not receive surgical consideration compared with all patients with early stage lung cancer (69.2% versus 88.9%, respectively). Clearly, other factors influence the decision to refer a patient to a surgeon. Surgeons receive referrals from any number of physicians, including family physicians, respirologists,
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and oncologists, and PFTs may be ordered at any point along the referral process. The decreased use of PFTs for patients who receive no treatment may represent an incomplete assessment for suitability for referral, or may reflect other nonrespiratory comorbidities such as coronary artery disease and heart failure, which is known to increase surgical risk [29]. Our study examines the principal types of curative treatment, and we found that 14% of early stage NSCLC patients received no treatment at all. A better understanding of referral patterns for lung cancer could potentially help to explain our results. Rich and colleagues [30] examined resection rates among National Health Service centers in the United Kingdom and found that whether patients received surgery for lung cancer depended on whether they were initially evaluated in a center with thoracic surgery units. After adjusting for patient variables, patients seen in a thoracic surgery center were 51% more likely to have surgery [30]. Before our study’s time period, thoracic surgery in Ontario was regionalized to 14 centers, all associated with radiation therapy units, and multidisciplinary care for lung cancer patients is the prescribed standard of care [31]. Lung cancer patients seen in multidisciplinary settings are more likely to receive guideline-based treatments [32], and early stage lung cancer patients who do not receive surgery are more likely to receive radiation treatment [33]. In Ontario, because of the regionalization of thoracic surgery, some patients may not have access to thoracic surgery units. Our finding of a low rate of radiation therapy treatment (57.9%) among patients who did not receive surgical consultation suggests that perhaps some patients are being managed outside of thoracic centers affiliated with radiation therapy units. Conversely, the relatively higher rate of radiation therapy among patients who were seen by a surgeon but then did not receive surgery (72.6%) suggests that patients are more likely to receive some form of treatment for their lung cancer if they are seen by a surgeon at some point after their diagnosis. Furthermore, the high rate of PFTs among patients who receive surgery (97%) and patients who receive radiation therapy (86.9%) suggests that patients seen in thoracic units likely receive guidelineconcordant care. Our finding that only 72.8% of early-stage lung cancer patients referred for surgery go on to receive surgery is somewhat surprising. Lung resection is the standard of care for early stage lung cancer, and carries a mortality risk as high as 2% [34], although lower in high-volume centers and higher for high-risk patients [35]. American College of Chest Physician guidelines state that lowerrisk operations such as segmentectomy or wide wedge resection are acceptable for higher-risk patients [6], and several series report success with this approach [36, 37]. It may be that that not all surgeons have an equal surgical appetite for high-risk patients. For example, minimally invasive segmentectomy is a technically more demanding procedure [38], and not all surgeons in the province may be comfortable in performing this procedure. Further investigations with more detailed clinical data would help to understand surgical decision making.
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Limitations of our study include the use of administrative data that lack detailed clinical information on the severity of comorbid conditions. We therefore could not describe all comorbidities of patients not referred for surgery. However, we were able to capture the use of PFTs and therefore assess an important variable in preoperative assessment. Second, the limited data variables permitted only descriptive analyses. In conclusion, surgery rates for early NSCLC surgery in Ontario appear lower than previously published in the literature but are not fully explained by surgical consultation rates alone, as overall consultation rates are high. However, patients assessed by a surgeon and deemed not to be operative candidates are more likely to receive pulmonary function testing and to receive treatment with radiation compared with patients not assessed by a surgeon. Although increasing age appears to influence referral for surgical assessment, awareness among referring physicians of the appropriateness of surgery for elderly patients and the importance of surgeon assessment should be stressed. Similarly, surgery for selected elderly patients by surgeons should be supported. A deeper understanding of other patient factors requires exploration to appreciate which patients do not receive surgical consultation or other treatment, with a view to ensuring that all patients have an opportunity for curative treatment whenever appropriate. This study was conducted with the support of the Ontario Institute for Cancer Research and Cancer Care Ontario (CCO) through funding provided by the Government of Ontario [HSRPPRAP UHN RA #33]. This study was supported through provision of data by the Institute for Clinical Evaluative Sciences (ICES) and CCO, and through funding support to ICES from an annual grant by the Ministry of Health and Long-Term Care (MOHLTC). The opinions, results, and conclusions reported in this paper are those of the authors. No endorsement by ICES, CCO, or the Government of Ontario is intended nor should it be inferred.
References 1. Canadian Cancer Society. Canadian cancer statistics 2015. Available at: http://www.cancer.ca/w/media/cancer.ca/cw/ cancer%20information/cancer%20101/canadian%20cancer% 20statistics/canadian-cancer-statistics-2015-en.pdf2015. Accessed January 17, 2016. 2. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology non small cell lung cancer v. 7.2015. 2015. Available at: https://www.nccn.org/professiona ls/physician_gls/f_guidelines_nojava.asp. Accessed March 15, 2015. 3. Jones GC, Kehrer JD, Kahn J, et al. Primary treatment options for high-risk/medically inoperable early stage NSCLC patients. Clin Lung Cancer 2015;16:413–30. 4. Khakwani A, Rich AL, Powell HA, et al. Lung cancer survival in England: trends in non-small-cell lung cancer survival over the duration of the National Lung Cancer Audit. Br J Cancer 2013;109:2058–65. 5. Zeliadt SB, Sekaran NK, Hu EY, et al. Comparison of demographic characteristics, surgical resection patterns, and survival outcomes for veterans and nonveterans with nonsmall cell lung cancer in the Pacific Northwest. J Thorac Oncol 2011;6:1726–32.
Ann Thorac Surg 2016;-:-–-
6. Donington J, Ferguson M, Mazzone P, et al. American College of Chest Physicians and Society of Thoracic Surgeons consensus statement for evaluation and management for high-risk patients with stage I non-small cell lung cancer. Chest 2012;142:1620–35. 7. Brunelli A. Risk assessment for pulmonary resection. Semin Thorac Cardiovasc Surg 2010;22:2–13. 8. Rocco G, Internullo E, Cassivi SD, van Raemdonck D, Ferguson MK. The variability of practice in minimally invasive thoracic surgery for pulmonary resections. Thorac Surg Clin 2008;18:235–47. 9. Cancer Quality Council of Ontario. Reporting of cancer stage at diagnosis. 2016. Available at: http://www.csqi.on.ca/by_ patient_journey/diagnosis/reporting_of_cancer_stage_at_dia gnosis/. Accessed July 22, 2016. 10. Riaz SP, Luchtenborg M, Jack RH, et al. Variation in surgical resection for lung cancer in relation to survival: populationbased study in England 2004–2006. Eur J Cancer 2012;48: 54–60. 11. Fry WA, Menck HR, Winchester DP. The National Cancer Data Base report on lung cancer. Cancer 1996;77:1947–55. 12. Humphrey EW, Smart CR, Winchester DP, et al. National survey of the pattern of care for carcinoma of the lung. J Thorac Cardiovasc Surg 1990;100:837–43. 13. Connolly CK, Johnston I, Milroy R, Jones R. Surgical resection rate in lung cancer. Thorax 1999;54:375. 14. Dell’Amore A, Monteverde M, Martucci N, et al. Lobar and sub-lobar lung resection in octogenarians with early stage non-small cell lung cancer: factors affecting surgical outcomes and long-term results. Gen Thorac Cardiovasc Surg 2015;63:222–30. 15. Janssen-Heijnen ML, Maas HA, Houterman S, Lemmens VE, Rutten HJ, Coebergh JW. Comorbidity in older surgical cancer patients: influence on patient care and outcome. Eur J Cancer 2007;43:2179–93. 16. Dillman RO, Zusman DR, McClure SE. Surgical resection and long-term survival for octogenarians who undergo surgery for non-small-cell lung cancer. Clin Lung Cancer 2009;10:130–4. 17. Hino H, Murakawa T, Ichinose J, et al. Results of lung cancer surgery for octogenarians. Ann Thorac Cardiovasc Surg 2015;21:209–16. 18. Demmy TL, Curtis JJ. Minimally invasive lobectomy directed toward frail and high-risk patients: a case-control study. Ann Thorac Surg 1999;68:194–200. 19. Ganti AK, Shostrom V, Alorabi M, et al. Early stage nonsmall-cell lung cancer in octogenarian and older patients: a SEER database analysis. Clin Lung Cancer 2016;17:285–91. 20. Mery CM, Pappas AN, Bueno R, et al. Similar long-term survival of elderly patients with non-small cell lung cancer treated with lobectomy or wedge resection within the Surveillance, Epidemiology, and End Results database. Chest 2005;128:237–45. 21. Razi SS, John MM, Sainathan S, Stavropoulos C. Sublobar resection is equivalent to lobectomy for T1a non-small cell lung cancer in the elderly: a Surveillance, Epidemiology, and End Results database analysis. J Surg Res 2016;200: 683–9. 22. Bravo Iniguez CE, Armstrong KW, Cooper Z, et al. Thirtyday mortality after lobectomy in elderly patients eligible for lung cancer screening. Ann Thorac Surg 2016;101:541–6.
BENDZSAK ET AL RATES OF CONSULTATION AND SURGERY FOR NSCLC
5
23. Armstrong KW, Bravo-Iniguez CE, Jacobson FL, Jaklitsch MT. Recent trends in surgical research of cancer treatment in the elderly, with a primary focus on lung cancer: presentation at the 2015 annual meeting of SIOG. J Geriatric Oncol 2016 July 22 [E-Pub ahead of print]. 24. Owonikoko TK, Ragin CC, Belani CP, et al. Lung cancer in elderly patients: an analysis of the Surveillance, Epidemiology, and End Results database. J Clin Oncol 2007;25: 5570–7. 25. Pan H, Simpson DR, Mell LK, Mundt AJ, Lawson JD. A survey of stereotactic body radiotherapy use in the United States. Cancer 2011;117:4566–72. 26. Mazzone P. Preoperative evaluation of the lung resection candidate. Cleve Clin J Med 2012;79(E-Suppl 1):e17–22. 27. Martin J. Lung resection in the pulmonary-compromised patient. Thorac Surg Clin 2004;14:157–62. 28. Colice GL, Shafazand S, Griffin JP, Keenan R, Bolliger CT. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: ACCP evidencedbased clinical practice guidelines (2nd edition). Chest 2007;132(Suppl):161–77. 29. Eagle KA, Berger PB, Calkins H, et al. ACC/AHA guideline update for perioperative cardiovascular evaluation for noncardiac surgery—executive summary a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (committee to update the 1996 guidelines on perioperative cardiovascular evaluation for noncardiac surgery). Circulation 2002;105:1257–67. 30. Rich AL, Tata LJ, Free CM, et al. Inequalities in outcomes for non-small cell lung cancer: the influence of clinical characteristics and features of the local lung cancer service. Thorax 2011;66:1078–84. 31. Sundaresan S, Langer B, Oliver T, et al. Standards for thoracic surgical oncology in a single-payer healthcare system. Ann Thorac Surg 2007;84:693–701. 32. Kehl KL, Landrum MB, Kahn KL, Gray SW, Chen AB, Keating NL. Tumor board participation among physicians caring for patients with lung or colorectal cancer. J Oncol Pract 2015;11:e267–78. 33. 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;105:113–21. 34. Allen MS, Darling GE, Pechet TT, et al. Morbidity and mortality of major pulmonary resections in patients with early-stage lung cancer: initial results of the randomized, prospective ACOSOG Z0030 trial. Ann Thorac Surg 2006;81: 1013–20. 35. Bach PB, Cramer LD, Schrag D, Downey RJ, Gelfand SE, Begg CB. The influence of hospital volume on survival after resection for lung cancer. N Engl J Med 2001;345:181–8. 36. Sancheti MS, Melvan JN, Medbery RL, et al. Outcomes after surgery in high-risk patients with early stage lung cancer. Ann Thorac Surg 2016;101:1043–51. 37. Martin-Ucar AE, Nakas A, Pilling JE, West KJ, Waller DA. A case-matched study of anatomical segmentectomy versus lobectomy for stage I lung cancer in high-risk patients. Eur J Cardiothorac Surg 2005;27:675–9. 38. Leshnower BG, Miller DL, Fernandez FG, Pickens A, Force SD. Video-assisted thoracoscopic surgery segmentectomy: a safe and effective procedure. Ann Thorac Surg 2010;89:1571–6.