Obstetrics & Gynecology:
Trends in Hospital Volume and Patterns of Referral for Women With Gynecologic Cancers
Wright, Jason D. MD; Neugut, Alfred I. MD, PhD; Lewin, Sharyn N. MD; Lu, Yu-Shiang MS; Herzog, Thomas J. MD; Hershman, Dawn L. MD
Departments of Obstetrics and Gynecology and Medicine and the Herbert Irving Comprehensive Cancer Center, Columbia University College of Physicians and Surgeons, and the Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, New York.
Corresponding author: Jason D. Wright, MD, Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Columbia University College of Physicians and Surgeons, 161 Fort Washington Avenue, 8th Floor, New York, NY 10032; e-mail: firstname.lastname@example.org.
Dr. Hershman is the recipient of a grant from the National Cancer Institute (NCI R01CA134964). This study used the linked Surveillance, Epidemiology, and End Results–Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors.
Financial Disclosure The authors did not report any potential conflicts of interest.
The authors appreciate the efforts of the Applied Research Branch, Division of Cancer Prevention and Population Science, National Cancer Institute; the Office of Information Services, and the Office of Strategic Planning, Health Care Financing Administration; Information Management Services, Inc; and the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries in the creation of the SEER–Medicare database.
OBJECTIVE: To estimate trends in hospital volume and referral patterns for women with uterine and ovarian cancer.
METHODS: The Surveillance, Epidemiology, and End Results–Medicare database was used to identify women aged 65 years or older with ovarian and uterine cancer who underwent surgery from 2000 to 2007. “Volume creep,” when a greater number of patients undergo surgery at the same hospitals, and “market concentration,” when a similar overall number of patients undergo a procedure but at a smaller number of hospitals, were analyzed.
RESULTS: Among 4,522 patients with ovarian cancer, mean hospital volume increased from 3.1 cases during 2000–2001 to 3.4 cases during 2006–2007 (P=.62) suggesting minimal volume creep. Similarly, there was little evidence of market concentration. In 2000–2001, 37.8% of women were treated at the top decile by volume hospitals compared with 41.4% in 2006–2007 (P=.14). In 2006–2007, 201 (63.2%) of the hospitals had an ovarian cancer surgery volume of two or fewer cases. Among 9,908 women with uterine cancer, the mean hospital volume increased slightly from 4.5 in 2000–2001 to 5.4 in 2006–2007 (P=.10). The percentage of patients treated at the top decile by volume of hospitals increased from 40.4% in 2000–2001 to 44.7% in 2006–2007 (P<.001). In 2006–2007, 243 (49.3%) of the hospitals had a uterine cancer surgery volume of two or fewer cases.
CONCLUSION: There have been only modest changes in the referral patterns of women with ovarian and uterine cancer. A large number of hospitals have a very low procedural volume.
LEVEL OF EVIDENCE: II
The relationship between surgical volume and outcome is well established; patients operated on by high-volume surgeons and at high-volume hospitals have superior outcomes compared with patients treated by low-volume health care providers.1–4 Although the importance of surgical volume has long been recognized, the concept gained prominence in the early 2000s after a series of studies showing the effect of volume on outcomes were reported.1–4 In one study that included over 2.5 million patients who underwent high-risk cardiovascular or oncologic surgery, outcomes were superior for all of the procedures when performed at high-volume centers.2
The recognition of the volume–outcome paradigm has led to a number of public health initiatives to attempt to improve patient outcomes.5,6 Public reporting of both surgical volume and outcomes has been advocated by many sources. One such group, the Leapfrog consortium, is a public reporting initiative that selects minimum procedural volume standards for high-risk procedures and reports actual hospital volumes. The intent of these initiatives is to drive evidence-based hospital referrals.7 For some high-risk surgical procedures, there is evidence that these initiatives have led to regionalization of care and have been associated with improved outcomes.8–11
Although the association between high surgical volume and improved outcomes has been demonstrated for many procedures, for gynecologic cancer operations, the relationship is less robust.12–17 To date, the effect of volume-centered initiatives on the patterns of care for women with gynecologic cancer has received little attention. We estimated the referral patterns of women with uterine and ovarian cancer undergoing cancer-directed surgery in the United States.
MATERIALS AND METHODS
The Surveillance, Epidemiology, and End Results (SEER)–Medicare database was used.18 The SEER database is a population-based tumor registry maintained by the National Cancer Institute that provides data on tumor characteristics, treatment, and survival as well as demographic and selected census tract-level information. The Medicare database includes information on patients with Medicare part A (inpatient) and part B (outpatient) including diagnoses and billed claims. Medicare provides coverage to women 65 years of age or older. Exemption from the Columbia University Institutional Review Board was obtained. The SEER–Medicare database has been validated and used in a number of outcomes studies.18–20
We selected women older than 65 years of age with primary cancer of the uterus or ovary who underwent surgery between January 1, 2000, and December 31, 2007. We excluded patients who were enrolled in a non–Medicare health maintenance organization, Medicare beneficiaries resulting from end-stage renal disease, patients diagnosed at autopsy or by death certificate, and those with tumors arising from other primary sites. For the purpose of analysis, surgery for ovarian cancer was considered any of the following procedures: oophorectomy, hysterectomy, tumor debulking, exenteration, or omentectomy. For women with uterine cancer, the criterion for surgery was hysterectomy. For each primary tumor type, patients were classified as early (stage I–II) or advanced stage (stage III–IV) based on the recorded SEER variable for stage. Separate analyses were performed for uterine and ovarian cancer.
Age was categorized as 65–69 years, 70–74 years, 74–79 years, and 80 years of age or older, whereas was race was classified as white, black, Hispanic, or other. Year of diagnosis was recorded from 1999 to 2007; marital status coded as married, unmarried, or unknown; and area of residence as metropolitan or nonmetropolitan. Socioeconomic status was generated from a score derived from education, poverty level, and income from the 2000 census tract data and scores ranked on a scale of 1–5 with 1 being the lowest value. To estimate the prevalence of comorbid disease in our cohort, we used the Klabunde adaptation of the Charlson comorbidity index. Tumor grade was recorded as well, moderately, or poorly differentiated or unknown. For women with uterine cancer, histology was classified as endometrioid, serous, carcinosarcoma, clear cell, leiomyosarcoma, and other or unknown. For ovarian cancer, histology was grouped as epithelial, germ cell and sex cord stromal, and other or unknown. The SEER registries were categorized as eastern (Connecticut, New Jersey), midwestern (Detroit, Iowa, Utah, Atlanta, rural Georgia, Kentucky, Louisiana), and western (San Francisco, Hawaii, New Mexico, San Jose, Seattle, Los Angeles, greater California).
The hospital in which each patient's procedure was performed was identified; those patients for whom the hospital identification information was missing were excluded. Patients then were categorized into 2-year blocks (2000–2001, 2002–2003, 2004–2005, 2006–2007) based on the date of surgery. For each 2-year block, the number of procedures performed in each hospital was calculated and hospitals ranked by volume.
Trends in hospital volume over time were analyzed as previously reported.8 “Volume creep” occurs when a greater number of patients undergo the procedure of interest in the hospitals under study. “Market concentration” occurs when the number of patients who undergo a procedure remains relatively constant but the number of hospitals in which the procedures are performed declines.8 The percentage of procedures concentrated in the highest decile and highest quartile by volume hospitals was analyzed as a measure of market concentration.
For each period of analysis, we estimated the mean and median hospital volumes with standard deviations and interquartile ranges, respectively. Mean and median changes in hospital volumes over time were analyzed using analysis of variance and the Kruskal-Wallis test, respectively. Changes in the number of patients treated at the top quartile and decile by volume hospitals over time were analyzed using χ2. A P value of <.05 was considered statistically significant. All analyses were conducted with SAS 9.13. All statistical tests were two-sided.
A total of 9,908 patients with uterine cancer who underwent surgery were identified (Table 1). In 2000–2001, 2,424 patients were treated across 535 hospitals. By the years 2006–2007, 2,640 patients were treated at 493 hospitals (Table 2). The median per-hospital volume remained two procedures for the years 2000–2001, 2002–2003, and 2004–2005 and increased to three cases by the 2006–2007 time period (P=.72). The mean volume increased over time from 4.5 cases in 2000–2001, to 4.5 cases in 2002–2003, to 5.2 surgeries in 2004–2005, and to 5.4 procedures in 2006–2007 (P=.73) (Fig. 1).
For women with uterine cancer, there was evidence of market concentration at the highest volume hospitals (Table 2). For example, the percentage of patients treated at the highest quartile by volume hospitals increased over time from 63.9% in 2000–2001 to 66.1% in 2002–2003, to 71.0% in 2004–2005, and finally to 71.1% in 2006–2007 (P<.001). Similar trends were noted when the analysis was limited to the highest decile by volume hospitals. In 2000–2001, 40.4% (n=979) of patients were treated at 52 hospitals. By 2006–2007, this had increased to 44.7% (n=1,181) of the patients at 50 centers (P<.001). Despite market concentration, the number of women treated at very low-volume centers remained relatively constant; 35.3% of patients in 2000–2001 were treated at centers that only performed one procedure compared with 34.9% in 2006–2007 (P=.98).
Table 1-b Clinical a...Image Tools
For patients with advanced-stage uterine cancer, both mean (1.6–2.5, P<.001) and median (one to two, P<.001) volume increased from 2000–2001 to 2006–2007 (Table 1). The increase in hospital volume for patients with advanced-stage disease was predominantly the result of volume creep; in 2000–2001, 151 hospitals cared for 243 patients with stage III–IV uterine cancer (10.0% of all patients treated during that time period). By 2006–2007, 225 hospitals provided care for 565 similarly staged patients (21.4% of all patients with uterine cancer during 2006–2007). There was no apparent market concentration for advanced-stage uterine cancer.
Overall, 4,522 patients with ovarian cancer were identified (Table 1). In 2000–2001, 1,235 patients were treated at 396 hospitals. By the years 2006–2007, 1,095 patients underwent surgery at 318 facilities (Table 3). The median hospital volume remained constant at two across all 8 years of the study (P=.84). There was a nonstatistically significant increase in the mean hospital procedural volume with time, from 3.1 cases in 2000–2001 to 3.2 cases in 2002–2003, to 3.1 procedures in 2004–2005, and to 3.4 cases in the final years of the study, 2006–2007 (P=.62) (Fig. 2).
For ovarian cancer, there was modest market concentration to the highest volume hospitals over the years of study. The percentage of patients who underwent surgery at the highest quartile by volume hospitals increased from 62.9% in 2000–2001, to 63.8% in 2002–2003, to 64.1% in 2004–2005, and to 69.0% in 2006–2007 (P=.01). The analysis was then limited to the highest decile by volume hospitals. In 2000–2001, 37.8% (n=467) of patients were treated at the 35 highest decile by volume hospitals compared with 41.4% (n=453) of women who underwent surgery at the 33 highest volume centers in 2006–2007 (P=.14).
The percentage of women treated at hospitals that performed one procedure per time period was 47.5% in 2000–2001, 48.0% in 2002–2003, 48.5% in 2004–2005, and 45.3% in 2006–2007 (P=.85). Among women with advanced-stage ovarian cancer, similar trends were noted, mean volume increased from 2.7 to 3.2 (P=.39), whereas median volume increased from one to two cases (P=.40).
Our findings suggest that, for women with ovarian and uterine cancer, public health initiatives to promote volume concentration have had a minimal effect in elderly women. Over the last decade, we noted modest market concentration with a small increase in the number of patients referred to high-volume hospitals. A large number of women with gynecologic cancers are still treated at very low-volume centers.
A number of reports have suggested that several high-risk or technically complex operations, particularly oncologic procedures, have been increasingly regionalized to high-volume centers.8,10,11,21–25 A study of Medicare beneficiaries who underwent cancer resections or cardiovascular surgery noted increases in hospital volume for all four of the oncologic procedures studied (esophagectomy, pancreatectomy, lung resection, and cystectomy). The median hospital volume for cystectomy increased from five procedures in 1999–2000 to 10 procedures in 2007–2008, whereas the median pancreatectomy volume more than tripled from five to 16 cases over the same time period. The underlying cause for the increased hospital volume was accounted for by both volume creep and market concentration. For example, for esophagectomy, the number of patients who underwent the procedure remained relatively constant but the number of hospitals that performed the procedure declined; in contrast, for pancreatectomy, not only did the number of hospitals performing the procedure decline, but the number of patients undergoing the procedure increased by more than 50%.8
Studies examining regionalization of care for gynecologic cancers have been limited.26–28 A report that analyzed referral patterns in Maryland found an increase in treatment at high-volume hospitals and by high-volume surgeons for women with ovarian cancer in 2001–2008 compared with those treated in the 1990s.27 Similar data were noted in a report from Norway.28 Our findings were clearly more modest; we found no change in the median number of ovarian cancer procedures and a small increase in hospital procedural volume for endometrial cancer.
The goal of regionalization of care is to reduce perioperative mortality and several reports have suggested that this is, in fact, feasible for some procedures.8,9,22,29 A study examining trends in operative mortality suggested that increased procedural volume for six cancer operations was associated with a reduction in inpatient mortality ranging from 0.1% to 2.3%.9 The report by Finks and colleagues8 of Medicare recipients described previously found that increased hospital volume was directly associated with a 32% reduction in mortality for esophagectomy, a 37% reduction in the risk of death for cystectomy, and a 67% reduction in death after pancreatectomy. A population-based analysis from Norway that examined centralization of the care of patients with ovarian cancer to a teaching hospital reported improved survival after centralization.29 A priori, the goal of our study was to assess whether changing referral patterns were associated with reductions in mortality for gynecologic cancer; however, the minimal change in hospital volume precluded examination of mortality.
Regionalization of care tends to be most pronounced for those procedures with the strongest correlation between volume and outcome. Compared with other cancer resections, the association between volume and outcome for gynecologic tumors has been weaker.12–17 A report of elderly women with ovarian cancer found that high hospital procedural volume was associated with a small decrease in 2-year mortality but had no effect on overall survival.13 Similarly, an analysis of women undergoing abdominal hysterectomy for endometrial cancer found that, although patients treated by high-volume physicians had decreased perioperative morbidity, hospital volume had no effect on complications; neither hospital nor surgeon volume was associated with perioperative mortality.12 The limited change in hospital referral patterns we noted may stem, at least in part, from the modest effect of volume on outcome for gynecologic cancer surgery.
Although the effect of procedural volume on outcome for gynecologic cancers is relatively small, the specialty of the surgeon appears to have an important influence on survival for both endometrial and ovarian cancer.30–34 A population-based analysis of women with ovarian cancer found higher rates of tumor cytoreduction for advanced-stage disease, a higher rate of receipt of chemotherapy, and improved survival for patients treated by gynecologic oncologists compared with general gynecologists or surgeons.30 Similarly, Chan and coworkers31 found that treatment by a gynecologic oncologist was an independent predictor of improved survival for women with endometrial cancer. Referral based on physician specialty and not hospital volume may, in part, underlie the minimal regionalization that we noted.
Although our study benefits from the inclusion of a large number of hospitals and patients, we recognize a number of important limitations. Foremost, our data represent relative and not absolute changes in volume. Our data set did not include patients younger than 65 years age, non–Medicare recipients, or patients treated outside of the SEER registries studied. Although our data are a proxy for overall hospital volume, prior work has shown a high correlation between volume calculated using SEER–Medicare data and the actual rank order of hospitals based on volume.35 We did not examine how physician volume and physician characteristics influence referral patterns. Given the importance of physician characteristics in the treatment of gynecologic cancer, this clearly warrants further investigation. We only analyzed data from 2000 to 2007 and cannot exclude the possibility that regionalization may have occurred before that time. Finally, within each cohort, patients often underwent ancillary procedures such as lymphadenectomy or extended cytoreductive procedures. To limit this bias, separate analyses were performed for early and advanced-stage patients for both primary tumor sites.
Should regionalization of care for gynecologic malignancies be encouraged? Although regionalization may be attractive, it is often difficult to implement.36–39 Referral to high-volume centers is often met with resistance by both patients and health care providers, leads to disparities in which minorities and the underinsured are less likely to receive referral to a high-volume center, and is problematic in many regions that lack high-volume facilities.36–39 Furthermore, for lower-risk patients undergoing high-risk surgery, the benefits of volume-based referral are questionable; it appears that the greatest benefits are derived in the highest risk patient population undergoing the highest risk surgeries.40 Given these difficulties, some authors have suggested that regionalization should primarily be encouraged for high morbidity procedures with strong volume–outcome relationships like pancreatectomy and esophagectomy.8 Given the modest association between volume and survival for gynecologic cancer, it is difficult to endorse volume-based referral, and our data suggest that, to date, there has been minimal regionalization. For gynecologic cancer, it would appear that initiatives to promote referral to gynecologic oncologists would offer the greatest benefit to patients.
1. Begg CB, Riedel ER, Bach PB, Kattan MW, Schrag D, Warren JL, et al.. Variations in morbidity after radical prostatectomy. N Engl J Med 2002;346:1138–44.
2. Birkmeyer JD, Siewers AE, Finlayson EV, Stukel TA, Lucas FL, Batista I, et al.. Hospital volume and surgical mortality in the United States. N Engl J Med 2002;346:1128–37.
3. Birkmeyer JD, Stukel TA, Siewers AE, Goodney PP, Wennberg DE, Lucas FL. Surgeon volume and operative mortality in the United States. N Engl J Med 2003;349:2117–27.
4. Schrag D, Cramer LD, Bach PB, Cohen AM, Warren JL, Begg CB. Influence of hospital procedure volume on outcomes following surgery for colon cancer. JAMA 2000;284:3028–35.
5. Lindenauer P. Public reporting and pay-for-performance programs in perioperative medicine: are they meeting their goals? Cleve Clin J Med 2009;76:S3–8.
6. Lindenauer PK, Remus D, Roman S, Rothbeerg MB, Benjamin EM, Ma A, et al.. Public reporting and pay for performance in hospital quality improvement. N Engl J Med 2007;356:486–96.
7. Massarweh NN, Flum DR, Symons RG, Varghese TK, Pellegrini CA. A critical evaluation of the impact of Leapfrog's evidence-based hospital referral. J Am Coll Surg 2011;212:150–9.e1.
8. Finks JF, Osborne NH, Birkmeyer JD. Trends in hospital volume and operative mortality for high-risk surgery. N Engl J Med 2011;364:2128–37.
9. Ho V, Heslin MJ, Yun H, Howard L. Trends in hospital and surgeon volume and operative mortality for cancer surgery. Ann Surg Oncol 2006;13:851–8.
10. Hollenbeck BK, Taub DA, Miller DC, Dunn RL, Montie JE, Wei JT. The regionalization of radical cystectomy to specific medical centers. J Urol 2005;174:1385–9.
11. Smaldone MC, Simhan J, Kutikov A, Canter DJ, Starkey R, Zhu F, et al.. Trends in regionalization of radical cystectomy in three large northeastern states from 1996 to 2009. Urol Oncol 2012 Jun 9 [Epub ahead of print].
12. Wright JD, Lewin SN, Deutsch I, Burke WM, Sun X, Herzog TJ. Effect of surgical volume on morbidity and mortality of abdominal hysterectomy for endometrial cancer. Obstet Gynecol 2011;117:1051–9.
13. Schrag D, Earle C, Xu F, Panageas KS, Yabroff KR, Bristlow RE, et al.. Associations between hospital and surgeon procedure volumes and patient outcomes after ovarian cancer resection. J Natl Cancer Inst 2006;98:163–71.
14. Brookfield KF, Cheung MC, Koniaris LG, Sola JE, Fischer AC. A population-based analysis of 1037 malignant ovarian tumors in the pediatric population. J Surg Res 2009;156:45–9.
15. Diaz-Montes TP, Zahurak ML, Giuntoli RL II, Gardner GJ, Bristow RE. Uterine cancer in Maryland: impact of surgeon case volume and other prognostic factors on short-term mortality. Gynecol Oncol 2006;103:1043–7.
16. Bristow RE, Palis BE, Chi DS, Cliby WA. The National Cancer Database report on advanced-stage epithelial ovarian cancer: impact of hospital surgical case volume on overall survival and surgical treatment paradigm. Gynecol Oncol 2010;118:262–7.
17. Elit L, Bondy SJ, Paszat L, Przybysz R, Levine M. Outcomes in surgery for ovarian cancer. Gynecol Oncol 2002;87:260–7.
18. Potosky AL, Riley GF, Lubitz JD, Mentnech RM, Kessler LG. Potential for cancer related health services research using a linked Medicare-tumor registry database. Med Care 1993;31:732–48.
19. Du X, Freeman JL, Warren JL, Nattinger AB, Zhang D, Goodwin JS. Accuracy and completeness of Medicare claims data for surgical treatment of breast cancer. Med Care 2000;38:719–27.
20. Warren JL, Klabunde CN, Schrag D, Bach PB, Riley GF. Overview of the SEER–Medicare data: content, research applications, and generalizability to the United States elderly population. Med Care 2002;40(suppl):IV-3–18.
21. Morris DS, Taub DA, Wei JT, Dunn RL, Wolf JS Jr, Hollenbeck BK. Regionalization of percutaneous nephrolithotomy: evidence for the increasing burden of care on tertiary centers. J Urol 2006;176:242–6; discussion 246.
22. Gasper WJ, Glidden DV, Jin C, Way LW, Patti MG. 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. Ann Surg 2009;250:472–83.
23. McColl RJ, You X, Ghali WA, Kaplan G, Myers R, Dixon E. Recent trends of hepatic resection in Canada: 1995–2004. J Gastrointest Surg 2008;12:1839–46.
24. Riall TS, Eschbach KA, Townsend CM Jr, Nealon WH, Freeman JL, Goodwin JS. Trends and disparities in regionalization of pancreatic resection. J Gastrointest Surg 2007;11:1242–51.
25. Hill JS, McPhee JT, Messina LM, Ciocca RG, Eslami MH. Regionalization of abdominal aortic aneurysm repair: evidence of a shift to high-volume centers in the endovascular era. J Vasc Surg 2008;48:29–36.
26. Bristow RE, Zahurak ML, del Carmen MG, Gordon TA, Fox HE, Trimble EL, et al.. Ovarian cancer surgery in Maryland: volume-based access to care. Gynecol Oncol 2004;93:353–60.
27. Bristow RE, Zahurak ML, Diaz-Montes TP, Giuntoli RL, Armstrong DK. Impact of surgeon and hospital ovarian cancer surgical case volume on in-hospital mortality and related short-term outcomes. Gynecol Oncol 2009;115:334–8.
28. Aune G, Torp SH, Syversen U, Hagen B, Tingulstad S. Ten years' experience with centralized surgery of ovarian cancer in one health region in Norway. Int J Gynecol Cancer 2012;22:226–31.
29. Tingulstad S, Skjeldestad FE, Hagen B. The effect of centralization of primary surgery on survival in ovarian cancer patients. Obstet Gynecol 2003;102:499–505.
30. Earle CC, Schrag D, Neville BA, Yabroff KR, Topor M, Fahey A, et al.. Effect of surgeon specialty on processes of care and outcomes for ovarian cancer patients. J Natl Cancer Inst 2006;98:172–80.
31. Chan JK, Sherman AE, Kapp DS, Zhang R, Osann KE, Maxwell L, et al.. Influence of gynecologic oncologists on the survival of patients with endometrial cancer. J Clin Oncol 2011;29:832–8.
32. Mercado C, Zingmond D, Karlan BY, Sekaris E, Gross J, Maggard-Gibbons M, et al.. Quality of care in advanced ovarian cancer: the importance of provider specialty. Gynecol Oncol 2010;117:18–22.
33. Bilimoria KY, Phillips JD, Rock CE, Hayman A, Prystowsky JB, Bentrem DJ. Effect of surgeon training, specialization, and experience on outcomes for cancer surgery: a systematic review of the literature. Ann Surg Oncol 2009;16:1799–808.
34. Roland PY, Kelly FJ, Kulwicki CY, Blitzer P, Curcio M, Orr JW Jr. The benefits of a gynecologic oncologist: a pattern of care study for endometrial cancer treatment. Gynecol Oncol 2004;93:125–30.
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. Dimick JB, Finlayson SR, Birkmeyer JD. Regional availability of high-volume hospitals for major surgery. Health Aff (Millwood) 2004;Suppl Web Exclusives:VAR45–53.
37. Liu JH, Zingmond DS, McGory ML, Soo-Hoo NF, Ettner SL, Brook RH, et al.. Disparities in the utilization of high-volume hospitals for complex surgery. JAMA 2006;296:1973–80.
38. Finlayson SR. Delivering quality to patients. JAMA 2006;296:2026–7.
39. Finlayson SR, Birkmeyer JD, Tosteson AN, Nease RF Jr. Patient preferences for location of care: implications for regionalization. Med Care 1999;37:204–9.
40. Bilimoria KY, Bentrem DJ, Talamonti MS, Stewart AK, Winchester DP, Ko CY. Risk-based selective referral for cancer surgery: a potential strategy to improve perioperative outcomes. Ann Surg 2010;251:708–16.
Figure. No available...Image Tools
© 2013 The American College of Obstetricians and Gynecologists