Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
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1 September 2011 Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization Health System Performance Introduction An estimated 4,000 Canadians were diagnosed with pancreatic cancer and 1,700 with esophageal cancer in , i Surgery is the mainstay potentially curative treatment for individuals diagnosed with early-stage disease; however, only 20% to 30% of individuals with these cancers are candidates for potentially curative surgery, because most are diagnosed with late-stage disease. 2, 3 Surgical interventions for pancreatic and esophageal cancer are among the most demanding procedures undertaken by surgeons. Nurses and ancillary service providers also face difficulties caring for these patients, as serious surgical complications occur frequently. The long-term outlook for those diagnosed with pancreatic or esophageal cancer is dire: only 6% of those with pancreatic cancer and 14% of those with esophageal cancer survive for five years after their diagnosis. 4 A strong relationship between the volume of pancreatic and esophageal surgery and outcomes has been well documented in the literature. 5 9 Consequently, recommendations to shift care from low- to high-volume settings have been promulgated, 5, 6, 10, 11 and evidence of the success of concentrating these complex cases in centres of excellence has been published. 6, 12, 13 Improvements in survival and reductions in morbidity have occurred following implementation of these policies and the regionalization of care i. See the appendix and Table A-1 for a description of the epidemiology of pancreatic and esophageal cancer in Canada. Federal Identity Program Production of this report is made possible by financial contributions from Health Canada and provincial and territorial governments. The views expressed herein do not necessarily represent the views of Health Canada or any provincial or territorial government.
2 Although there are no pan-canadian quality indicators regarding these surgical procedures, Cancer Care Ontario (CCO) has implemented a Surgical Oncology Program that includes guidelines for procedural volume. 5, 6, 18, 19 Guidelines for surgical care for patients with esophageal cancer, including those for procedural volume, were developed by CCO s Expert Panel on Thoracic Surgical Oncology. 5 CCO s Surgical Oncology Program developed hospital volume guidelines for pancreatic cancer through its Cancer System Quality Index (CSQI). 6, 19 In addition to considering hospital procedural volume, CCO specifies criteria for surgeons and hospitals, including specific systems (such as multidisciplinary management and quality assurance), physical resources (such as intraoperative imaging, intensive care and nutrition service) and human resources (such as critical care physicians, specialized nursing expertise and supportive care) that are necessary for 5, 19 optimal care. To date, there have been few descriptions from a pan-canadian perspective of the surgical care provided to patients with pancreatic and esophageal cancer. This report examines the extent to which surgery for pancreatic and esophageal cancer has been centralized and carried out in high-volume acute care hospitals. In addition, data is presented on surgical outcomes for patients who undergo these high-risk procedures. Data Sources and Definitions This section describes data sources, how pancreatic and esophageal cancer patients were identified and how related surgical procedures were defined. Data Sources The source of information for hospital surgical care is the Hospital Morbidity Database (HMDB) at the Canadian Institute for Health Information (CIHI). The HMDB is a national data holding that captures administrative, clinical and demographic information on inpatient separations from all acute care hospitals. All provinces and territories (with the exception of Quebec) submit discharge data to CIHI s Discharge Abstract Database (DAD). Quebec s ministère de la Santé et des Services sociaux submits a data file to CIHI at the end of each year. This data file is mapped, processed and finally merged with the DAD acute care data to create the national HMDB. For these analyses, HMDB data from four fiscal years ( , , and ) was used because by all jurisdictions had implemented ICD-10-CA ii and Canadian Classification of Health Interventions (CCI) codes. Statistics Canada s Postal Code Conversion File (PCCF+) was used to describe the geographic distribution of patients and hospitals. Identifying Cancer Patients and Surgical Procedures Individuals with primary pancreatic cancer were defined as those who had ICD-10-CA diagnostic codes C25.0, C25.1, C25.2, C25.3, C25.4, C25.7, C25.8 and C25.9 mentioned anywhere on their hospital discharge abstract. Primary esophageal cancer cases included those coded to ICD-10-CA codes C15.0, C15.1, C15.2, C15.3, C15.4, C15.5, C15.8, C15.9 and C16.0. Partial, total or radical resections of the pancreas or esophagus (mentioned anywhere on the abstract) were identified using CCI codes. iii If more than one procedure was performed on a patient over the study period, only the first procedure was counted. ii. ICD-10-CA is an enhanced version of the International Statistical Classification of Diseases and Related Health Problems, Tenth Revision (ICD-10). ICD-10-CA was developed by CIHI and is the classification that facilities use to record problems, diagnoses, symptoms and other conditions that require contact with health care providers. iii. Pancreatic procedure codes were 1.OJ.87, 1.OJ.89, 1.OK.87, 1.OK.89 and 1.OK.91. Esophageal procedure codes were 1.NA.87 to 1.NA Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
3 Characterizing Hospital Experience For this report, hospital experience was defined in terms of surgical volume: the number of procedures performed on unique patients by hospitals per fiscal year ( to ). Hospital volume was calculated irrespective of whether the pancreatectomy or esophagectomy was performed for a primary cancer diagnosis. iv The assumption is that a hospital s total experience with the procedure can be generalized to cancer patients. A panel of clinicians with expertise in these procedures advised which procedures to count toward hospital volumes. A key issue in conducting analyses of surgical volume and outcomes is how to define high volume. Canadian investigators who have studied the relationship between hospital volume and outcomes for these procedures have applied different volume thresholds to characterize hospitals. 20, 21 For this report, CCO s definitions of hospital procedural volume were used to describe the extent to which surgical procedures have been centralized (Table 1), in part because more than one-third of pancreatectomies and esophagectomies are performed in Ontario hospitals. Table 1: Cancer Care Ontario Volume Thresholds Used to Define Hospital Procedural Volume Pancreatectomy Low: 1 19 High: 20+ Esophagectomy Low: 1 6 Medium (Level 2): 7 19 High (Level 1): 20+ Sources Pancreatectomy: M. Marcaccio et al., Hepatic, Pancreatic, and Biliary Tract (HPB) Surgical Oncology Standards: A Special Project of the Expert Panel on HPB Surgical Oncology (Toronto, Ont.: Cancer Care Ontario, 2006), accessed on March 24, 2010, from < Esophagectomy: S. Sundaresan et al., Standards for Thoracic Surgical Oncology in a Single-Payer Healthcare System, Annals of Thoracic Surgery 84 (2007): pp Results Hospital Experience Surgical care for patients receiving pancreatectomies and esophagectomies has been concentrated in Canada in relatively few hospitals. In , there were 686 acute care hospitals in Canada, with relatively little variation in this number over the four years studied (see Table A-2 in the appendix). Most Canadian acute care hospitals did not perform these procedures in (572 or 83% in the case of pancreatectomy and 567 or 83% in the case of esophagectomy). Pancreatectomy and esophagectomy were not performed in hospitals in the Yukon and Nunavut from to ; residents of these jurisdictions travelled elsewhere for their surgery. Across Canada in , 114 of 686 acute care hospitals performed pancreatectomy; of these, 18 (16%) were high-volume hospitals (Table 2). In , 119 of 686 acute care hospitals in Canada performed esophagectomy; of these, 22 (18%) were high-volume hospitals. The number of high-volume hospitals remained relatively stable over the four-year period (see Table A-2 in the appendix). iv. Esophageal procedures associated with codes 1.NA.87.LP, 1.NA.87.BA and 1.NA.87.QB performed on patients without a cancer diagnosis were excluded from the analysis when the most responsible diagnosis was K.225 diverticulum of oesophagus, acquired. Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization 3
4 Among hospitals performing these procedures in , there were no high-volume hospitals performing pancreatectomy in New Brunswick or Saskatchewan and no high-volume hospitals performing esophagectomy in New Brunswick. Ontario had the greatest number of high-volume hospitals (eight hospitals performing pancreatectomy and eight hospitals performing esophagectomy) for these two surgical procedures (Table 2). Relative to the size of its population and the number of hospitals performing these procedures, Quebec had relatively few high-volume hospitals (three hospitals performing pancreatectomy and four hospitals performing esophagectomy) (Table 2). Table 2: Number of Acute Care Hospitals Performing Pancreatectomy and Esophagectomy (for Cancer and Non-Cancer Indications) and Number of These Hospitals With a High Volume of Procedures, by Province/ Territory, Province/Territory Pancreatectomy Performed Procedure High Volume Esophagectomy Performed Procedure High Volume British Columbia Alberta Saskatchewan Manitoba Ontario Quebec New Brunswick Nova Scotia Prince Edward Island Newfoundland and Labrador Yukon Northwest Territories Nunavut Canada Source Hospital Morbidity Database, Canadian Institute for Health Information. Care Centralization Most cancer patients who underwent pancreatectomy and esophagectomy in Canada from to were cared for in high-volume hospitals (74% and 58%, respectively) (Table 3). By patient s province of residence, the degree of centralization of these procedures in high-volume hospitals ranged from 59% in Newfoundland and Labrador to 100% in Prince Edward Island for pancreatectomy and from 13% in Quebec to 89% in British Columbia for esophagectomy (Table 3). The degree of centralization of patients in high-volume hospitals was greater for cancer patients (shown in Table 3) than for other patients (74% versus 66% for pancreatectomy and 58% versus 48% for esophagectomy). 4 Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
5 Table 3: Number and Percentage of Cancer Patients Undergoing Pancreatectomy and Esophagectomy at High-Volume Acute Care Hospitals, by Patient s Province/Territory of Residence, to Province/Territory Patients No. Cancer-Related Pancreatectomy Care in High- Volume Hospital No. (%) Patients No. Cancer-Related Esophagectomy Care in High- Volume Hospital No. (%) British Columbia (78%) (89%) Alberta (88%) (76%) Saskatchewan 51 * (14%) Manitoba (76%) (84%) Ontario (79%) 1, (63%) Quebec (64%) (13%) New Brunswick 31 * 59 * Nova Scotia (88%) (72%) Prince Edward Island (100%) 9 * Newfoundland and Labrador (59%) (39%) Yukon * * * * Northwest Territories * * * * Nunavut 0 0 * * Canada 2,130 1,582 (74%) 2,449 1,432 (58%) Note * Figures suppressed due to small numbers. Source Hospital Morbidity Database, Canadian Institute for Health Information. Proximity to Care Very few cancer patients had to leave their province or territory to receive surgery (2% for pancreatectomy and 1% for esophagectomy); however, Canadians residing in rural areas v were more likely than urban residents to have to travel outside of their health region vi for surgical care (74% versus 49% in the case of pancreatectomy and 76% versus 43% in the case of esophagectomy). All high-volume hospitals are located in urban areas. Cancer patients residing in Prince Edward Island, the Yukon, the Northwest Territories and Nunavut had to travel outside of their province/territory for care because cancer-related pancreatectomy and esophagectomy were not performed in area hospitals. Surgical Outcomes Short-term surgical outcomes were generally good for Canadian cancer patients undergoing pancreatectomy and esophagectomy. The vast majority of patients (93% for pancreatic cancer and 90% for esophageal cancer) were discharged home following surgery. Of the pancreatic surgery patients who were discharged home, 36% received support services. vii For esophagectomy patients discharged home, 50% received support services. v. Rural areas were defined according to postal codes using Statistics Canada s Statistical Area Classification. Rural is defined as areas that are outside of the commuting zones of larger urban centres with core populations of 10,000 or more. vi. Health regions are administrative bodies that are legislated by the provincial ministries of health. They are defined by geographical areas and are responsible for providing health services to their residents. vii. The receipt of support services, such as supportive housing, home care and attendant care, is noted in the hospital discharge report. Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization 5
6 In-hospital mortality associated with pancreatectomy (5%, or approximately 25 deaths annually across Canada) and esophagectomy (6%, or approximately 39 deaths annually across Canada) was relatively low for Canadian patients. Conclusions Most Canadians who undergo pancreatectomy or esophagectomy are cared for in high-volume acute care hospitals. While there are no pan-canadian quality indicators for these procedures, it is likely that surgeons and cancer care administrators across Canada are familiar with CCO s guidelines. Ontario accounts for 39% of Canada s population and provides a large share of its health care. Ontario hospitals performed 37% of pancreatectomies and 40% of esophagectomies during the four-year study period. It would therefore be expected that practice patterns in Ontario would substantially weight any pan-canadian estimates. Patients with pancreatic and esophageal cancer are centralized in high-volume hospitals more than other patients are. CCO relied on surgical oncology expert panels to develop guidelines for pancreatectomy and esophagectomy, and this trend of centralization could be explained if surgeons whose practice is focused on cancer are more familiar with and adherent to CCO s guidelines than general surgeons are. Surgical oncologists are also likely to operate in hospitals associated with cancer care programs that have adopted CCO s guidelines. There was considerable variation by province in the proportion of hospitals that were high volume performing pancreatectomies and esophagectomies. For example, while 24% (8 of 34) of hospitals in Ontario that performed pancreatectomy were high-volume hospitals, only 8% (3 of 37) of hospitals in Quebec that performed pancreatectomy were high-volume ones. There was also considerable variation by province in the proportion of patients with pancreatic and esophageal cancer cared for in high-volume hospitals. For example, relatively few patients with esophageal cancer living in Quebec and Saskatchewan and undergoing an esophagectomy were discharged from a high-volume hospital (13% and 14%, respectively). The extent of centralization of care for patients with pancreatic and esophageal cancer was more extensive for pancreatectomy than esophagectomy (74% versus 58% of patients cared for in high-volume settings, respectively). The very low rates of high-volume care for cancer-related esophagectomy in Quebec (13%) and Saskatchewan (14%) explain much of this difference. A full analysis of outcomes related to these provincial differences in patient centralization of care in high-volume settings could not be carried out because the uniform data on comorbidity necessary for risk adjustment was not available for all provinces. viii In setting guidelines, policy-makers must balance the benefits of centralization with its potential limitations. 22 There are practical concerns that high-volume hospitals could become overwhelmed with patients and be unable to serve them if all care was centralized. If high-volume hospitals were overburdened, wait times for surgery could increase. However, because these surgical procedures are rare, those who have addressed this concern feel that centralization is unlikely to have untoward logistical or financial consequences for surgeons or hospitals. 23, 24 This appears to be the case in Canada, where each year relatively few an estimated 137 pancreatic and 254 esophageal surgical cancer patients would have to be shifted from low- to high-volume hospitals if all such procedures were centralized.from a patient perspective, the prospect of travelling great distances from family and supports for a procedure that will involve a lengthy hospital stay is undesirable, especially for elderly patients. If discharged home following surgery, patients living far from a highvolume centre may have difficulty receiving follow-up care from their surgeon. Very few Canadians must travel outside of their province for care, but distance to care can be a significant issue for residents of rural areas. viii. The Charlson Index score, a measure of comorbidity, cannot be computed from the morbidity data available in Quebec. 6 Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
7 The vast majority of Canadians who undergo cancer-related pancreatectomy or esophagectomy fared well following surgery. Patients were most often discharged from hospital to home, and relatively few patients died during their hospital stay. The extent to which hospital volume accounts for these favourable outcomes cannot be determined from these analyses. While the evidence for a volume outcome relationship has mounted since 7, 22, it was first widely publicized in the early 1970s, questions remain as to why the relationship exists. Very little research has been published that identifies the processes or structures of care that are at play. Some suggest that the experience of the surgeon is responsible for the relationship (that is, that practice makes perfect). Others posit that selective referral is at play and that healthier patients tend to receive care at high-volume centres. The levels of staffing, technology and systems of care available at high-volume hospitals are likely explanatory, but only recently have these factors been subject to scrutiny. 27 Our data did not allow us to explore these factors. While difficult to interpret, the results of these pan-canadian analyses appear to differ from those reported in the United States. Unlike in Canada, where the majority of cancer-related pancreatectomies and esophagectomies are performed in high-volume hospitals, estimates from the U.S. suggest that relatively fewer patients are seen in such settings in that country. 16, 26, 28, 29 It is, however, difficult to interpret these apparent discrepancies because of underlying differences in study methods and models of health care delivery. 30 Acknowledgements CIHI would like to acknowledge and thank the many individuals who contributed to the development of this report. At CIHI, these include Marilee Allerdings, Kinga David, Maria Hewitt, Jin Huang, Janet Manuel, Anne McFarlane, Kathleen Morris, Bernie Paillé and Brandon Wagar. The expert panel included Oliver Bathe, Jeffrey Barkun, Heather Bryant, Gail Darling, Robin McLeod and Jonathan Irish. Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization 7
8 Appendix: Pancreatic and Esophageal Cancer The Disease Burden in Canada It was estimated that 4,000 Canadians would be diagnosed with pancreatic cancer and 1,700 with esophageal cancer in 2010 (Table A-1). The incidence of pancreatic cancer is relatively stable. However, a rise in the number of new cases of esophageal cancer will likely increase its burden. The incidence of esophageal cancer is rising rapidly in Western countries, in part because of increased use of surveillance endoscopy for patients suspected of having Barrett s esophagus, a precursor condition that can be caused by (increasingly prevalent) gastro-esophageal reflux disease. 31 Obesity, another risk factor for esophageal cancer, is also on the rise in Canada. 32 Pancreatic and esophageal cancers are diseases of the elderly. In the case of pancreatic cancer, few cases occur among individuals younger than 40, and the peak incidence is in the seventh and eighth decades of life. 2 Esophageal cancer is also rare among those younger than 40, but its incidence rises sharply thereafter, with an eight-fold increase between the age ranges 45 to 54 and 65 to Pancreatic cancer strikes men and women to a comparable degree. Men, however, are three times more likely to develop esophageal cancer than women. Table A-1: Epidemiology of Cancers of the Pancreas and Esophagus, Canada Pancreatic Cancer Esophageal Cancer Percentage of All Incident Cancers 2% 1% Percentage of Cancer Deaths 5% 2% Estimated New Cases (2010) Total* 4,000 1,700 Male 1,950 1,250 Female 2, Age-Standardized Incident Rate (per 100,000) Total* 9 4 Male 10 6 Female 8 2 Estimated Deaths (2010) Total* 3,900 1,800 Male 1,850 1,400 Female 2, Age-Standardized Mortality Rate (per 100,000) Total 9 4 Male 9 7 Female Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
9 Table A-1: Epidemiology of Cancers of the Pancreas and Esophagus, Canada (cont d) Five-Year Relative Survival Ratio (%) Pancreatic Cancer Esophageal Cancer Total 6 14 Male 6 14 Female 6 14 Notes * Totals may not sum to gender-specific totals due to rounding. Pancreatic cancer data, 2002 to 2004; esophageal cancer data, 2003 to Quebec was not included. Pancreatic cancer: C25.0 to C25.9 (excluding morphology types M-9050 to M-9055, M-9140 and M-9590 to M-9989). Esophageal cancer: C15.0 to C15.9 (excluding morphology types M-9050 to M-9055, M-9140 and M-9590 to M-9989). Sources Canadian Cancer Society s Steering Committee, Canadian Cancer Statistics 2009 (Toronto, Ont.: Canadian Cancer Society, 2009); Canadian Cancer Society s Steering Committee, Canadian Cancer Statistics 2010 (Toronto, Ont.: Canadian Cancer Society, 2010). Table A-2: Number of Acute Care Hospitals by Surgical Volume,* to , Canada Pancreatectomy Total Acute Care Hospitals Performed Procedure Total Low Volume Medium Volume High Volume Esophagectomy Note * According to CCO thresholds. Source Hospital Morbidity Database, Canadian Institute for Health Information. Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization 9
10 References 1. Canadian Cancer Society s Steering Committee, Canadian Cancer Statistics 2010 (Toronto, Ont.: Canadian Cancer Society, 2010). 2. P. G. Johnston and M. M. Eatock, Chapter 23: Pancreas, in Treatment of Cancer: Fifth Edition, eds. P. Price et al. (London, U.K.: Edward Arnold Ltd., 2008). 3. D. B. Smith and B. J. Haylock, Chapter 21: Oesophageal Cancer, in Treatment of Cancer: Fifth Edition, eds. P. Price et al. (London, U.K.: Edward Arnold Ltd., 2008). 4. L. F. Ellison and K. Wilkins, An Update on Cancer Survival, Health Reports 21, 3 (2010), accessed September 16, 2010, from < 5. S. Sundaresan et al., Standards for Thoracic Surgical Oncology in a Single-Payer Healthcare System, Annals of Thoracic Surgery 84 (2007): pp B. Langer, Role of Volume Outcome Data in Assuring Quality in HPB Surgery, HPB 9 (2007): pp T. J. Babineau, The Evolution of the Link Between Surgical Outcomes and Volume: How We Got to Leapfrog, Current Surgery 61, 1 (2004): pp B. K. Hollenbeck et al., Volume-Based Referral for Cancer Surgery: Informing the Debate, Journal of Clinical Oncology 25 (2007): pp S. D. Killeen et al., Provider Volume and Outcomes for Oncological Procedures, British Journal of Surgery 92 (2005): pp The Leapfrog Group, Evidence-Based Hospital Referral (EBHR): Factsheet (Washington, D.C.: The Leapfrog Group, 2008). 11. Department of Health, Guidance on Commissioning Cancer Services: Improving Outcomes in Upper Gastrointestinal Cancers: NICE Guidance on Upper GI Cancers (London, U.K.: Department of Health, 2001). 12. K. Leeb et al., Thoracic Cancer Surgeries, Healthcare Quarterly 12, 3 (2009): pp A. K. Lwin and D. S. Shepard, Estimating Lives and Dollars Saved From Universal Adoption of the Leapfrog Safety and Quality Standards: 2008 Update (Washington, D.C.: The Leapfrog Group, 2008), accessed on March 25, 2010, from < Lives_Saved_Leapfrog_Report_2008-Final_(2).pdf>. 14. C. H. Sonnenday and J. D. Birkmeyer, A Tale of Two Provinces: Regionalization of Pancreatic Surgery in Ontario and Quebec, Annals of Surgical Oncology (May 25, 2010). 15. M. W. Wouters et al., Centralization of Esophageal Cancer Surgery: Does It Improve Clinical Outcome?, Annals of Surgical Oncology 16, 7 (2009): pp W. J. Gasper et al., Has Recognition of the Relationship Between Mortality Rates and Hospital Volume for Major Cancer Surgery in California Made a Difference? A Follow-Up Analysis of Another Decade, Annals of Surgery 250, 3 (2009): pp Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
11 17. J. T. McPhee et al., Perioperative Mortality for Pancreatectomy: A National Perspective, Annals of Surgery 246, 2 (2007): pp J. Finks et al., Trends in Hospital Volume and Operative Mortality for High-Risk Surgery, New England Journal of Medicine 364, 22 (2011): pp B. Langer and H. Stern, An Integrated System-Wide Strategy for Quality Improvement in Cancer Surgery, British Journal of Surgery 94 (2007): pp M. Marcaccio et al., Hepatic, Pancreatic, and Biliary Tract (HPB) Surgical Oncology Standards: A Special Project of the Expert Panel on HPB Surgical Oncology (Toronto, Ont.: Cancer Care Ontario, 2006), accessed on March 24, 2010, from < 21. M. Simunovic et al., Influence of Hospital Characteristics on Operative Death and Survival of Patients After Major Cancer Surgery in Ontario, Canadian Journal of Surgery 49, 4 (2006): pp D. R. Urbach et al., Differences in Operative Mortality Between High- and Low-Volume Hospitals in Ontario for 5 Major Surgical Procedures: Estimating the Number of Lives Potentially Saved Through Regionalization, CMAJ 168, 11 (2003): pp M. V. Raval et al., Quality Improvement for Pancreatic Cancer Care: Is Regionalization a Feasible and Effective Mechanism?, Surgical Oncology Clinics of North America 19, 2 (2010): pp A. R. Chappel et al., Small Rural Hospitals and High-Risk Operations: How Would Regionalization Affect Surgical Volume and Hospital Revenue?, Journal of the American College of Surgeons 203, 5 (2006): pp M. J. Forshaw et al., Centralization of Oesophagogastric Cancer Services: Can Specialist Units Deliver?, Annals of the Royal College of Surgeons of England 88, 6 (2006): pp H. S. Luft et al., Should Operations Be Regionalized? The Empirical Relation Between Surgical Volume and Mortality, New England Journal of Medicine 301 (1979): pp C. I. Lauder et al., Systematic Review of the Impact of Volume of Oesophagectomy on Patient Outcome, ANZ Journal of Surgery 80, 5 (2010): pp A. C. Chang and J. D. Birkmeyer, The Volume Performance Relationship in Esophagectomy, Thoracic Surgery Clinics 16 (2006): pp B. Joseph et al., Relationship Between Hospital Volume, System Clinical Resources, and Mortality in Pancreatic Resection, Journal of the American College of Surgeons 208, 4 (2009): pp J. B. Dimick et al., National Trends in Outcomes for Esophageal Resection, Annals of Thoracic Surgery 79, 1 (2005): pp S. H. Teh et al., Patient and Hospital Characteristics on the Variance of Perioperative Outcomes for Pancreatic Resection in the United States: A Plea for Outcome-Based and Not Volume-Based Referral Guidelines, Archives of Surgery 144, 8 (2009): pp D. R. Urbach et al., How Are Volume Outcome Associations Related to Models of Health Care Funding and Delivery? A Comparison of the United States and Canada, World Journal of Surgery 29, 10 (2005): pp Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization 11
12 33. S. DeMeester, Centralization of Esophageal Cancer Surgery: The Right Thing to Do Is Seldom Easy, Annals of Surgical Oncology 16 (2009): pp Public Health Agency of Canada, Obesity in Canada Snapshot (Ottawa, Ont.: PHAC, 2009), accessed November 23, 2010, from < 12 Surgery for Pancreatic and Esophageal Cancer in Canada: Hospital Experience and Care Centralization
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