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Impact of Hospital Procedure Volume on Surgical Operation and Long-Term Outcomes in High-Risk Curatively Resected Rectal Cancer: Findings From the Intergroup 0114 Study

From the Department of Medical Oncology, Dana-Farber Cancer Institute; Division of General Medicine, Department of Medicine, Brigham and Women's Hospital; Department of Health Care Policy and Channing Laboratory, Harvard Medical School; Department of Radiation Oncology, Massachusetts General Hospital, Boston, MA; Department of Radiation Oncology, University of North Carolina School of Medicine, Chapel Hill; Cancer and Leukemia Group B Statistical Center, Durham, NC; Departments of Epidemiology and Biostatistics, Department of Medicine, Health Outcomes Research Group, Memorial Sloan-Kettering Cancer Center; St. Vincent's Clinical Cancer Center, New York, NY; Allegheny Cancer Center, Allegheny General Hospital, Pittsburgh, PA; and Division of Hematology-Oncology, Northwestern University, Chicago, IL.

Address reprint requests to Jeffrey A. Meyerhardt, MD, Dana-Farber Cancer Institute, 44 Binney St, Boston, MA 02115; e-mail: jmeyerhardt{at}partners.org.

	ABSTRACT

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PURPOSE: Prior studies have demonstrated superior outcomes after a curative surgical resection of rectal cancer at hospitals where the volume of such surgeries is high. However, because these studies often lack detailed information on tumor and treatment characteristics as well as cancer recurrence, the true nature of this relation remains uncertain.

PATIENTS AND METHODS: We studied a nested cohort of 1,330 patients with stage II and stage III rectal cancer participating in a multicenter, adjuvant chemoradiotherapy trial. We analyzed differences in rates of sphincter-preserving operations, overall survival, and cancer recurrence by hospital surgical volume.

RESULTS: We observed a significant difference in the rates of abdominoperineal resections across tertiles of hospital procedure volume (46.3% for patients resected at low-volume, 41.3% at medium-volume, and 31.8% at high-volume hospitals; P < .0001), even after adjustment for tumor distance from the anal verge. However, this higher rate of sphincter-sparing operations at high-volume centers was not accompanied by any increase in recurrence rates. Hospital surgical volume did not predict overall, disease-free, recurrence-free, or local recurrence-free survival. However, among patients who did not complete the planned adjuvant chemoradiotherapy (270 patients), those who underwent surgery at low-volume hospitals had a significant increase in cancer recurrence (adjusted hazard ratio, 1.94; 95% CI, 1.01 to 3.72; P = .04 for the trend) and a nonsignificant trend toward increased overall mortality (P = .08) and local recurrence (P = .10). In contrast, no significant volume-outcome relation was noted among patients who did complete postoperative therapy.

CONCLUSION: Using prospectively recorded data, we found that hospital surgical volume had no significant effect on rectal cancer recurrence or survival when patients completed standard adjuvant therapy. Sphincter-preserving surgery was more commonly performed at high-volume centers.

	INTRODUCTION

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An extensive body of literature suggests that hospital procedure volume is predictive of short-term and long-term outcomes in patients undergoing complex medical and surgical procedures [1-17]. Because the majority of these studies have relied on administrative claims-based and registry sources, most of these studies lack detailed information about patient, tumor, and treatment characteristics. Without these important variables, confounding by selection bias of patients at high-volume centers and by postoperative care (including differential use of adjuvant therapy by hospital volume) cannot be excluded as an explanation for these volume-outcome differences. Moreover, because data on cancer relapse are often not available, it remains unclear whether the influence of lower hospital procedure volume on survival is directly related to a higher rate of cancer recurrence. In addition, these studies provide limited information on the processes that underlie these volume-outcome relationships.

In rectal cancer, several studies have suggested a direct relationship between institutional caseload and rates of permanent colostomy [18-20]. These studies could not delineate whether this association was related to institutional surgical experience or differences in patient and tumor characteristics, including distance from the anal verge, bowel obstruction, and extent of invasion through the bowel wall. More importantly, they could not determine whether the price of more sphincter-sparing procedures was higher rates of cancer recurrence. Furthermore, higher hospital surgical volume for rectal cancer has been associated with decreased short-term [19] and long-term mortality in some studies [18,20], but not others [21-23]. Whether these survival differences by institutional volume are related to cancer recurrence or noncancer-related mortality remains unclear.

We used data from a large randomized trial of patients with stage II and III rectal cancer to examine the influence of hospital procedure volume on sphincter-preserving surgery and long-term outcome. Because all patients received standard postoperative adjuvant therapy and follow-up, we were able to isolate the influence of hospital surgical volume from these potential confounding variables.

	PATIENTS AND METHODS

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Patients for this analysis were drawn from a randomized trial of adjuvant chemotherapy and radiation trial for stage II and III rectal cancer with accrual between August 1990 and November 1992 (National Cancer Institute–sponsored Intergroup 0114 [INT-0114]) [24,25]. The study had an enrollment of 1,792 patients, with participation by institutions affiliated with one of the following cooperative groups: Cancer and Leukemia Group B (the coordinating group), North Central Cancer Treatment Group, Eastern Cooperative Oncology Group, National Cancer Institute Canada Clinical Trials Group, Radiation Therapy Oncology Group, and Southwest Oncology Group. Approval by each individual institution's internal review board was required before patient enrollment at that center. As previously described [24,25], 97 patients were deemed ineligible for this trial and were excluded from analysis. Other details of study eligibility, study details, and treatment trial results have been reported elsewhere [24,25].

For this analysis, study staff, who were blinded to patient outcome, reviewed the operative reports of all eligible patients to identify the hospital where primary rectal cancer surgery was performed. We excluded patients who were missing sufficient information to identify the hospital of surgery (n = 5). In addition, because hospital procedure volume rankings were derived from US Medicare claims, we excluded patients who underwent surgery at a Veterans Affairs Research Service or military hospital (n = 106) or non-US hospital (n = 254). After these exclusions, 1,330 patients were eligible for the analysis.

Medicare Hospital Procedure Volume
Using the Medicare claims database, hospitals were ranked by volume according to the number of primary rectal cancer surgeries performed on all Medicare-enrolled patients between 1988 and 1993, the enrollment period inclusive of the clinical trial. Primary rectal cancer surgeries were defined using an International Classification of Disease (ICD) code of 154.x (rectal cancer) and an ICD procedure code of 48.4x, 48.5x, or 48.7x (rectal surgeries) for a particular hospitalization. Our results did not change when we used hospital volume rankings inclusive of both ICD diagnoses and procedure codes of colon and rectal cancer; the two rankings were highly correlated (r = 0.94).

Validation of Medicare Procedure Volume
In previous studies, Medicare case volume was highly correlated with total hospital procedural volume [2]. However, because our patient population included Medicare and non-Medicare patients, we wanted to validate our relative ranking of hospitals for rectal cancer surgery. We used the Nationwide Inpatient Sample (NIS) database from 1988 to 1992, which consists of a random sample of 750 to 900 hospitals per year from 11 states, approximating a 20% sample of US community hospitals. Using the NIS database, we identified the total number of rectal cancer surgeries performed using the same ICD diagnostic and procedural codes as described above, and created a parallel annual volume ranking for all hospitals that were represented in our cohort. Among hospitals that were jointly represented in our cohort study and the NIS database (345 hospitals), the Spearman rank correlation for annual rectal cancer surgery volume as measured by the Medicare claims database and the NIS database was 0.87 (P < .0001). This high correlation supports the use of procedure volume for rectal surgery as calculated from the Medicare claims database as a valid measure of relative overall hospital procedure volume.

Statistical Analysis
We defined tertiles of hospital procedural volume (low [0 to 8.3 Medicare cases/yr], medium [8.4 to 16.7 Medicare cases/yr], and high [17 to 92 Medicare cases/yr]) on the basis of the Medicare procedure volume of the hospital where study participants had surgery. The distribution of baseline characteristics across hospital procedure volume tertiles was evaluated using Mantel-Haenszel ² tests for categoric variables and analysis of variance tests for continuous variables. Overall survival (OS), disease-free survival (DFS), recurrence-free survival (RFS; local or distant), and local recurrence-free survival (LRFS) rates were examined using the methods of Kaplan and Meier [26], and differences among tertiles were assessed by the log-rank test. OS was defined as time from study entry to death as a result of any cause. DFS was defined as time from study entry to tumor recurrence or occurrence of a new primary colorectal tumor, or death as a result of any cause. In contrast, RFS was the time from study entry to tumor recurrence (local, distant, or both) or occurrence of a new primary tumor. Patients who died without known tumor recurrence were censored at time of death. Similarly, LRFS was the time from study entry to local tumor recurrence. For LRFS, patients who died without known local recurrence were censored at time of death. The entire cohort was analyzed using Cox proportional hazards regression [27], with a priori inclusion in the model of age, sex, race, bowel obstruction at presentation, performance status, number of positive lymph nodes, and extent of disease through the bowel wall. We used a robust sandwich estimator to adjust parameter SEs for the clustering of patients within hospitals following the method of Lin and Wei [28]. In these models, we evaluated monotonic trends by using the median value of each category and modeling it as a continuous variable. Tests for interaction were performed by entering into the multivariate model the cross-product terms of hospital volume (modeled continuously using the median value for each category) and the other covariate of interest.

The clinical trial was not planned to study the impact of hospital procedure volume on outcome. However, power computations before this analysis indicated that with 1,425 patients accrued over 2.25 years and observed for 7 additional years, hazard ratios (HRs) for OS of 1.35 and greater could be detected with at least 88% power. If these power calculations were planned for 1,330 patients (the number of patients in these analyses), there is 84% power to detect an HR of 1.35.

Operation type was recorded on study eligibility forms by data managers at individual institutions and verified by one of the principal investigators of the study. Operation type was classified as either low anterior resection (LAR) or abdominoperineal resection (APR). Differences in rates of APR by hospital volume tertile were analyzed using logistic regression, with adjustments for age, race, bowel obstruction at presentation, performance status, number of positive lymph nodes, distance from anal verge (on the basis of operative, sigmoidoscopy, or colonoscopy report), and extent of disease through the bowel wall. Generalized estimating equations were used to account for clustering of patients within hospitals.

We used SAS 8.2 software (SAS Institute, Cary, NC) for all statistical analyses. All P values are two-sided.

	RESULTS

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Baseline Characteristics by Hospital Tertiles
Among the 1,330 patients (age range, 22 to 86 years) included in our analysis, primary rectal cancer surgery was performed at 646 United States hospitals. The baseline characteristics of the cohort according to tertiles of hospital volume are listed in Table 1. Patients who underwent surgical resection at low-volume hospitals were significantly more likely to be nonwhite and younger, and had a nonsignificantly increased rate of clinical bowel obstruction. There were modest significant differences in tumor distance to anal verge by hospital volume. However, other important tumor characteristics, baseline Eastern Cooperative Oncology Group performance status at time of initiation of chemotherapy and rates of completion of adjuvant therapy, were not different across hospital volume tertiles.

Increasing hospital procedure volume was inversely associated with performing an APR (46.3% in low-volume hospitals, 41.3% in medium-volume hospitals, and 31.8% in high-volume hospitals; P < .0001; Table 2). Compared with patients treated at high-volume centers, the adjusted odds ratio of an APR was 1.54 (95% CI, 1.16 to 2.04) for patients treated at medium-volume centers and 1.83 (95% CI, 1.40 to 2.39) for those treated at low-volume facilities.

Survival and Cancer Recurrence by Hospital Procedure Volume
All patients enrolled onto this trial were randomly assigned to receive postoperative fluorouracil-based chemotherapy and external-beam radiotherapy. As previously reported, no significant overall survival advantage was observed among any of the four treatment arms [24,25]. Consequently, patients in all four treatment arms were analyzed jointly according to the procedure volume for the hospital where rectal cancer surgery was performed.

With median follow-up for survivors of 10.1 year, we did not observe a significant influence for hospital procedure volume on DFS or OS (Table 3). Moreover, hospital volume did not significantly predict LRFS or overall RFS. Graphic representations of these survival analyses are shown in Fig 1. Using Cox proportional models, we also examined the influence of hospital procedure volume on the risk of overall mortality and cancer recurrence, after adjusting for other predictors of cancer outcome (Table 4). As shown, no differences in mortality or cancer recurrence were observed across categories of hospital caseload.

View larger version (14K): [in this window] [in a new window]   Fig 1. Kaplan-Meier survival curves for entire cohort of eligible patients, by hospital procedure volume: overall survival (A), local and distant recurrence-free survival (B), and local recurrence-free survival (C).

Influence of Adjuvant Therapy
We considered the possibility that the influence of hospital surgical volume on disease outcome was attenuated by the delivery of postoperative chemotherapy and radiotherapy. We therefore repeated our analysis after stratifying patients according to those who completed planned adjuvant therapy (1,060 patients) and those who failed to complete planned therapy (270 patients; Table 5). The only statistically significant baseline characteristic difference between patients completing all planned adjuvant therapy and those not completing therapy was sex (81.4% of males completed treatment compared with 76.0% of females; P = .008). Whereas hospital volume had no effect on mortality or cancer recurrence among patients who completed adjuvant therapy, hospital volume substantially influenced outcome among those who did not complete planned therapy. Among patients who did not complete therapy, patients resected at low-volume facilities experienced a significantly greater risk of cancer recurrence (HR, 1.94; 95% CI, 1.10 to 3.72; P = 0.04 for the trend), compared with patients whose surgery was at high-volume facilities. Furthermore, among patients who did not complete therapy, there was a trend toward decreased local recurrence (P = .10) and improved overall mortality (P = .08) with increasing procedure caseload. Exclusion of patients who died or developed cancer recurrence during therapy or inclusion of tumor distance to anal verge in the multivariate model did not appreciably alter these results (data not shown).

Although inability to complete adjuvant therapy may be reflective of inherently different patient populations, we observed no significant differences in tumor stage (P = .29), presence of bowel obstruction (P = .94), type of operation (P = .16), performance status (P = .09), or grade of differentiation (P = .24) between patients who completed planned therapy and those who did not. Furthermore, there was no statistically significant difference in rates of completion of therapy by hospital volume (P = .08).

We similarly examined whether the volume-outcome relation was significantly altered according to other predictors of overall mortality and cancer recurrence. No significant interactions were detected between hospital surgical volume and age (interaction term P = .39 for overall mortality and P = .53 for cancer recurrence), performance status (P = .96 and P = .75, respectively), race (P = .80 and P = .34, respectively), or tumor distance to anal verge (P = .26 and P = .47, respectively).

	DISCUSSION

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Among all eligible patients enrolled onto this large trial of postoperative chemotherapy and radiotherapy for stage II and III rectal cancer, hospital surgical volume did not significantly influence rates of cancer recurrence or mortality. Nonetheless, patients who underwent surgery at low-volume centers were significantly more likely to require a permanent colostomy by virtue of undergoing an APR.

Because anal sphincter preservation has important implications for patient quality of life, we examined the APR rates according to hospital volume. In previous studies that examined the influence of institutional caseload on permanent colostomy rates, data on tumor distance from the anal verge were not available, and the findings have been conflicting [18-22]. In this study, increased procedure volume did predict lower rates of APR, even after adjusting for tumor location. Although the use of sphincter-sparing surgery for lower rectal lesions may be associated with incontinence and impaired quality of life in some patients (and a small percentage of patients may have an LAR with diverting colostomy, precluding normal bowel function) preservation of normal bowel function with middle and upper rectal lesions is usually feasible and safe [31]. Although our database does not have long-term data on the adequacy of bowel function, we believe that the increased chance of undergoing an APR at low-volume hospitals for middle and upper rectal cancers (> 5.0 cm from the anal verge) is a noteworthy finding.

Prior volume-outcome studies on rectal cancer have shown conflicting results regarding overall mortality [18,20-23]. Most have been limited by the use of administrative databases and an inability to adjust for important patient and tumor characteristics. Moreover, because use of and compliance with postoperative therapy are not adequately captured from such data sources, the investigators could not examine the influence of adjuvant therapy on the volume-outcome relation. The use of clinical trial data offers the advantage of being able to control for these characteristics and have prospectively recorded data on the date and nature of cancer recurrences.

A limitation of our analysis is an inability to study the influence of individual surgeon volume on rectal cancer outcome. An association between surgeon volume and outcomes has been demonstrated in certain studies [16,21,23,32], although there is a complex relationship between number of operations performed by a surgeon and the institution where the resections occur [16,21]. However, because efforts to regionalize certain cancer surgeries have focused on the caseloads of institutions, we believe studies to understand the true nature and potential mechanisms of the hospital procedure volume-outcome relationship are still critical.

Previous clinical trials of patients with stage II and III rectal cancer demonstrated that the use of postoperative fluorouracil-based chemotherapy and external-beam radiotherapy significantly improve overall survival as well as local and distant failure rates [33]. As such, the administration of postoperative chemoradiotherapy to patients in our study may have obscured the influence of hospital surgical volume on long-term patient outcomes. Indeed, among patients who did not complete planned adjuvant therapy in this trial, surgery at a low-volume center was associated with a significant 94% increase risk in cancer recurrence when compared with a resection at a high-volume facility. In contrast, hospital surgical volume had no effect among patients who did complete the prescribed postoperative treatment. These findings should be interpreted with great caution because it is purely speculative whether adjuvant chemoradiotherapy can correct for less optimal surgical technique. However, these findings do suggest that, with appropriate postoperative care, hospital procedure volume does not seem to have a major influence on long-term outcomes in patients with rectal cancer.

Given that patients were identified for this clinical trial 4 to 6 weeks after primary surgical resection, perioperative (short term) morbidity and mortality were not addressed in this study. We specifically sought to focus on the influence of hospital surgical volume on long-term rectal cancer outcomes. Because patients enrolled onto a randomized clinical trial may not be representative of the broader population of rectal cancer patients nationwide, the generalizability of our findings could be questioned. However, rectal cancer surgery was performed before enrollment onto this trial, and we observed considerable variation in hospital procedure volume within our cohort. In addition, because the study population included patients in both community and academic medical centers, we believe that the surgical treatment is reflective of the general US population. Nonetheless, underlying differences between patients participating in a clinical trial and the general rectal cancer population may limit the external validity of these findings. Furthermore, our results apply to patients who initiated adjuvant therapy and do not address potential volume-related differences in the use of adjuvant therapy in this patient population. Finally, patients in this study had surgery in the early 1990s, before increasing use of total mesorectal excision in rectal cancer surgery. Thus, such changes in surgical technique across hospital volumes may influence these results. To our knowledge, rates of total mesorectal excision use by hospital volume are not available, but may be another important variable influencing these outcomes.

Using data from large, prospective clinical trials with more complete information on patient, tumor, and postoperative treatment characteristics as well as cancer recurrence, we were able to better isolate the effect of institutional caseload on long-term outcomes. Our finding that hospital volume predicted cancer recurrence only among patients who failed to complete adjuvant therapy further emphasizes the importance of chemoradiotherapy in stage II and III rectal cancer. We suspect that the increased use of APR in the low-volume centers reflects inexperience by the individual surgeons and perhaps lack of awareness of the latest clinical data on sphincter preservation. However, this is speculation, and additional research is necessary to identify the specific mechanisms that underlie the volume-outcome relation in rectal cancer surgery. By understanding the nature of these associations, one can direct efforts to improve the quality of care at centers with varying caseloads.

	Appendix

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The following institutions participated in the study: CALGB Statistical Office, Durham, NC–Stephen George, PhD; supported by CA33601, Christiana Care Health Services, Inc CCOP, Wilmington, DE–Irving M. Berkowitz, DO; supported by CA45418, Community Hospital–Syracuse CCOP, Syracuse, NY–Jeffrey Kirshner, MD; supported by CA45389, Dana-Farber Cancer Institute, Boston, MA–George P Canellos, MD; supported by CA32291, Dartmouth Medical School–Norris Cotton Cancer Ctr, Lebanon, NH–L. Herbert Maurer, MD; supported by CA04326, Duke University Medical Center, Durham, NC–Jeffrey Crawford, MD; supported by CA47577, Eastern Cooperative Oncology Group, Philadelphia, PA–Robert L. Comis, MD, Chairman, Eastern Maine Medical Center CCOP, Bangor, ME–Philip L. Brooks, MD; supported by CA35406, Kaiser Permanente CCOP, San Diego, CA–Jonathan A. Polikoff, MD; supported by CA45374, Long Island Jewish Medical Center, Lake Success, NY–Marc Citron, MD; supported by CA11028, Massachusetts General Hospital, Boston, MA–Michael L. Grossbard, MD; supported by CA12449, Milwaukee CCOP, Milwaukee, WI–Ronald Hart, MD; supported by CA45400, Mount Sinai Medical Center CCOP - Miami, Miami Beach, FL–Enrique Davila, MD; supported by CA45564, Mount Sinai School of Medicine, New York, NY–James F Holland, MD; supported by CA04457, National Cancer Institute of Canada Clinical Trials Group, Kingston, Ontario–Joseph L. Pater, MD, Director, North Central Cancer Treatment Group, Rochester, MN–Michael J O'Connell, MD, Chairman; supported by CA25224, Radiation Therapy Oncology Group, Philadelphia, PA–Walter J. Curran, MD, Chairman, Rhode Island Hospital, Providence, RI–Louis A. Leone, MD; supported by CA08025, Roswell Park Cancer Institute, Buffalo, NY–Ellis Levine, MD; supported by CA02599, Southeast Cancer Control Consortium Inc. CCOP, Goldsboro, NC–James N. Atkins, MD; supported by CA45808, Southern Nevada Cancer Research Foundation CCOP, Las Vegas, NV–John Ellerton, MD; supported by CA35421, Southwest Oncology Group, San Antonio, TX–Charles Coltman, MD, Chairman, SUNY Health Science Center at Syracuse, Syracuse, NY–Stephen L. Graziano, MD; supported by CA21060, University of Alabama Birmingham, Birmingham, AL–Robert Diasio, MD; supported by CA47545, University of California at San Diego, San Diego, CA–Stephen L Seagren, MD; supported by CA11789, University of Chicago Medical Center, Chicago, IL–Gini Fleming, MD; supported by CA41287, University of Iowa Hospitals, Iowa City, IA–Gerald H. Clamon, MD; supported by CA47642, University of Maryland Cancer Center, Baltimore, MD–David Van Echo, MD; supported by CA31983, University of Massachusetts Medical Center, Worcester, MA–F. Marc Stewart, MD; supported by CA37135, University of Minnesota, Minneapolis, MN–Bruce A Peterson, MD; supported by CA16450, University of Missouri/Ellis Fischel Cancer Center, Columbia, MO–Michael C Perry, MD; supported by CA12046, University of North Carolina at Chapel Hill, Chapel Hill, NC–Thomas C. Shea, MD; supported by CA47559, University of Tennessee Memphis, Memphis, TN–Harvey B. Niell, MD; supported by CA47555, Wake Forest University School of Medicine, Winston-Salem, NC–David D Hurd, MD; supported by CA03927, Walter Reed Army Medical Center, Washington, DC–John C. Byrd, MD; supported by CA26806, Washington University School of Medicine, St. Louis, MO–Nancy L. Bartlett, MD; supported by CA77440, Weill Medical College of Cornell University, New York, NY–Michael Schuster, MD; supported by CA07968.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Acknowledgment

 
The authors thank Denise Brady for her assistance in data collection and Mike Hadad for his help in compiling Medicare volume data.

	NOTES

 
The research for CALGB 9081 was supported, in part, by grants from the National Cancer Institute (CA31946) to the Cancer and Leukemia Group B (Richard L. Schilsky, MD, Chairman). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Cancer Institute. This study supported by NCI grant to J.A.M. (1K07CA97992-01A1) and an American Society of Clinical Oncology Career Development Award to J.A.M.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

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Submitted April 24, 2003; accepted October 27, 2003.

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