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JCO study_Wang_Nov 2011
1.
Published Ahead of
Print on November 7, 2011 as 10.1200/JCO.2010.33.8020 The latest version is at http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2010.33.8020 JOURNAL OF CLINICAL ONCOLOGY O R I G I N A L R E P O R T Nomogram for Predicting the Benefit of Adjuvant Chemoradiotherapy for Resected Gallbladder Cancer Samuel J. Wang, Andrew Lemieux, Jayashree Kalpathy-Cramer, Celine B. Ord, Gary V. Walker, C. David Fuller, Jong-Sung Kim, and Charles R. Thomas Jr See accompanying editorial doi: 10.1200/JCO.2011.37.8604 Samuel J. Wang, Andrew Lemieux, Jayashree Kalpathy-Cramer, Celine B. A B S T R A C T Ord, and Charles R. Thomas Jr, Oregon Health & Science University; Jong-Sung Purpose Kim, Portland State University, Portland, Although adjuvant chemoradiotherapy for resected gallbladder cancer may improve survival for some OR; Gary V. Walker, Baylor College of patients, identifying which patients will benefit remains challenging because of the rarity of this Medicine, Houston; and C. David disease. The specific aim of this study was to create a decision aid to help make individualized Fuller, University of Texas Health estimates of the potential survival benefit of adjuvant chemoradiotherapy for patients with resected Science Center at San Antonio, San gallbladder cancer. Antonio, TX. Submitted November 23, 2010; Methods accepted July 18, 2011; published Patients with resected gallbladder cancer were selected from the Surveillance, Epidemiology, and online ahead of print at www.jco.org on End Results (SEER) –Medicare database who were diagnosed between 1995 and 2005. Covari- November 7, 2011. ates included age, race, sex, stage, and receipt of adjuvant chemotherapy or chemoradiotherapy Supported in part by the Oregon Clini- (CRT). Propensity score weighting was used to balance covariates between treated and untreated cal and Translational Research Institute groups. Several types of multivariate survival regression models were constructed and compared, Career Development Pilot Project grant including Cox proportional hazards, Weibull, exponential, log-logistic, and lognormal models. program and American Society of Clini- Model performance was compared using the Akaike information criterion. The primary end point cal Oncology Young Investigator Award was overall survival with or without adjuvant chemotherapy or CRT. program (S.J.W.); and in part by National Library of Medicine Grant No. Results 5K99 LM009889 (J.K.-C.). A total of 1,137 patients met the inclusion criteria for the study. The lognormal survival model Presented in part at the Annual Sympo- showed the best performance. A Web browser– based nomogram was built from this model to sium of the American Medical Informat- make individualized estimates of survival. The model predicts that certain subsets of patients with ics Association, November 13-17, 2010, at least T2 or N1 disease will gain a survival benefit from adjuvant CRT, and the magnitude of Washington, DC. benefit for an individual patient can vary. Authors’ disclosures of potential con- flicts of interest and author contribu- Conclusion tions are found at the end of this A nomogram built from a parametric survival model from the SEER-Medicare database can be article. used as a decision aid to predict which gallbladder patients may benefit from adjuvant CRT. Corresponding author: Samuel J. Wang, MD, PhD, Department of Radiation J Clin Oncol 29. © 2011 by American Society of Clinical Oncology Medicine, KPV4, Oregon Health & Science University, 3181 SW Sam Jack- cal trials.12 As a result, clinicians have little evidence son Park Rd, Portland, OR 97239-3098; INTRODUCTION e-mail: wangsa@ohsu.edu. to rely on when attempting to determine whether © 2011 by American Society of Clinical Gallbladder cancer is the most common biliary tract adjuvant therapy will be beneficial for a patient. It is Oncology neoplasm, with an annual incidence of almost 10,000 likely that only certain subsets of high-risk patients 0732-183X/11/2999-1/$20.00 and annual mortality of 3,300.1-3 Surgery remains the gain benefit from adjuvant therapy, but determining DOI: 10.1200/JCO.2010.33.8020 only definitively curative therapy.4 However, even after which patients will benefit remains a challenge. In complete resection, locoregional recurrence rates are this setting, prediction models may provide insight high. Consequently, there is considerable interest in into these important clinical questions. exploring the potential benefit of adjuvant chemo- The overall goals of this project were to con- therapy or chemoradiotherapy (CRT).5 Because of struct a decision aid that can be used to predict the rarity of this disease, most published gallbladder which patients will obtain a survival benefit from studies are small, single-institution series, some of adjuvant chemotherapy or CRT and estimate the which seem to indicate potential benefit from adju- magnitude of the benefit. The purpose was to pro- vant chemotherapy or CRT.6-11 Given the low inci- vide additional information to clinicians and patients dence of biliary tract carcinomas, few attempts have to aid in the decision-making process regarding adju- been made to conduct large-scale prospective clini- vant therapy. © 2011 by American Society of Clinical Oncology 1 Information downloaded from jco.ascopubs.org and provided by at Oregon Health Sciences Univ on November 7, 2011 from Copyright © 2011 American Society of Clinical Oncology. All rights reserved. 137.53.32.65 Copyright 2011 by American Society of Clinical Oncology
2.
Wang et al
We previously published a survival model13 built from the Sur- We used a propensity score weighting method to balance observed veillance, Epidemiology, and End Results (SEER) database14 that covariates between treatment and observation groups.17 Propensity scores makes individualized predictions of the benefit of adjuvant radiother- reflect the probability that a patient will receive therapy based on observed covariates.17 By assigning propensity score weights to each patient and apy for patients with gallbladder cancer. We undertook the current incorporating these weights into model construction, we can reduce treat- study to enhance this model by adding the effects of adjuvant chemo- ment bias inherent in retrospective nonrandomized regression analyses. therapy using the SEER-Medicare linked database15 and construct an Propensity scores were calculated using the twang R library (http://cran improved nomogram that utilizes alternative survival modeling tech- .r-project.org/web/packages/twang/index.html), with adjuvant CRT as the niques to predict the survival benefit of adjuvant chemotherapy outcome of interest. and CRT. The primary end point in this study was overall survival. Multivariate regression survival analysis was performed using several survival modeling methods and results were compared. Details of our comparison of different survival modeling methods have been described previously.18,19 We built METHODS semiparametric models (Cox proportional hazards [CPH]) and accelerated failure time parametric models (Weibull, exponential, log logistic, and lognor- mal [LN]). All survival models were constructed using the rms R library by Study Population Harrell16 (http://cran.r-project.org/web/packages/rms). Model performance The SEER database of the National Cancer Institute is the largest was compared using the Akaike information criterion (AIC), a measure of population-based cancer registry in the United States, covering approxi- goodness of fit for statistical models, and the model with the best (lowest) AIC mately 26% of the US population.14 The SEER-Medicare linked database15 was selected.20 To determine if the functional form of the chosen model had an is augmented with Medicare claims data, which can be used to obtain appropriate fit for this data set, we plotted the quantile function (inverse of additional clinical information not contained in SEER, such as chemother- cumulative distribution function) of the selected model and evaluated the apy information. straight-line fit. Survival models were also internally validated (using boot- The study cohort was created from the most recent 10 years of strapping to correct for optimistic bias) by measuring both discrimination and available data in the SEER-Medicare 2008 release,15 which includes claims calibration. Discrimination was evaluated using the concordance index (C- from 1995 to 2007 linked to patients with cancer diagnosed from 1995 to index). The C-index measures the probability that given a pair of randomly 2005. Initial patients were selected using Site Recode 31 for gallbladder selected patients, the model correctly predicts which patient will experience cancer (4,459 patients). Patients were included in this study if they had failure first. Calibration, which compares predicted with actual survival, was nonmetastatic invasive disease and had undergone complete surgical re- evaluated with a calibration curve.16 section of the primary site, with or without regional lymph node dissection The best-performing survival prediction model was then implemented (2,443 patients). The analysis was limited to patients older than 65 years of into an online nomogram, into which a user can enter parameters for a specific age with complete data records who had equal and continuous Medicare patient and obtain an estimate of the expected survival benefit from adjuvant Parts A and B coverage during the first 6 months after diagnosis (1,487 chemotherapy or CRT. The browser-based software tool was programmed patients). To account for postoperative mortality, 266 patients who sur- in JavaScript. vived fewer than 2 months after surgery were excluded. Eighty-four pa- tients who received adjuvant radiotherapy alone were also excluded. Using the SEER Extent of Disease 10 fields for extent (e10ex1) and nodes RESULTS (e10nd1), we grouped patients according to American Joint Committee on Cancer TNM staging (seventh edition). Patients who received adjuvant external beam radiotherapy within the A total of 1,137 patients were included in the study. Of these, 126 first 6 months of diagnosis (Patient Entitlement and Diagnosis Summary File patients (11%) received adjuvant chemotherapy, and an additional rad1 codes 1, 4, 5, or 6) were coded as having received adjuvant radiotherapy. 126 patients (11%) received adjuvant CRT. Table 1 shows a compar- To determine which patients had received chemotherapy, linked Medicare Carrier Claims (National Claims History) and Outpatient (Outpatient Stan- dard Analytical File) files were used. Patients who had Healthcare Common Table 1. Patient Demographics and Clinical Characteristics Before and Procedure Coding System claims codes 96,400 to 96,599, Q0083-Q0085, or After PS Weighting Applied to Balance Covariates Between Untreated J8500-J9999 within 6 months of diagnosis were coded as having received and Treated Groups (N 1,137) adjuvant chemotherapy. Patients were considered to have received adjuvant Original PS Weighted chemoradiotherapy if they had received both radiotherapy and chemotherapy within 6 months after diagnosis. Characteristic No CRT CRT P No CRT CRT P Mean age, years 78 73 .001 73 73 .866 Statistical Analysis Female sex, % 73 71 .674 71 71 .877 All statistical analyses were performed using the R software package Race, % .149 .944 (http://www.r-project.org). Covariates were selected based on our prior gall- White 82 87 88 87 bladder nomogram work,13 known clinically prognostic factors, and availabil- African American 8 9 8 9 ity in the SEER-Medicare database. Included covariates were age, sex, race, Asian/Pacific Islander 10 5 4 5 American Joint Committee on Cancer seventh edition TNM stage, and receipt T stage, % .001 .972 of adjuvant chemotherapy or CRT. All covariates were treated as discrete and T1 30 13 12 13 converted to binary variables, except for age, which was modeled as a T2 29 32 33 32 continuous variable and fitted to a smoothed restricted cubic spline func- T3 35 48 49 48 tion as per Harrell.16 As per SEER-Medicare data use guidelines, stage T4 6 7 6 7 groupings with fewer than 11 patients were grouped with the closest N stage, % .001 .989 neighboring group. Interaction terms between treatment variables and N0 63 50 50 50 stage were investigated to assess their influence on the benefit of adjuvant N 17 41 41 41 chemotherapy and CRT. We used a model-building approach promoted by Harrell,16 in which all covariates are included in the final model, with no Abbreviations: CRT, chemoradiotherapy; PS, propensity score. stepwise variable selection performed. 2 © 2011 by American Society of Clinical Oncology JOURNAL OF CLINICAL ONCOLOGY Information downloaded from jco.ascopubs.org and provided by at Oregon Health Sciences Univ on November 7, 2011 from Copyright © 2011 American Society of Clinical Oncology. All rights reserved. 137.53.32.65
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Gallbladder Cancer Adjuvant
Chemoradiotherapy Prediction Model 1.0 Table 2. Gamel Boag Lognormal Multivariate Regression Model Parameters T1 T2 Covariate Beta Coefficient P Overall Survival (proportion) T3 Intercept 1.6462 .177 0.8 T4 Age† 0.0323 .065 Age 0.1829 .001 0.6 Age 0.4952 .004 Male sex 0.1490 .013 Race 0.4 African American 0.3721 .001 Asian/Pacific Islander 0.3503 .001 T stage 0.2 T2 0.3442 .001 T3 1.1097 .001 T4 1.8108 .001 N stage 0 3 6 9 13 17 21 25 29 33 37 N1 0.5814 .001 Time (months) NA 0.2965 .002 Chemotherapy 0.5341 .036 Fig 1. Kaplan-Meier overall survival plot for all patients with gallbladder disease Chemoradiotherapy 0.5522 .001 grouped by T stage. T2 chemotherapy 0.2600 .421 T3 chemotherapy 0.4973 .089 T4 chemotherapy 0.7656 .069 T2 chemoradiotherapy 0.7886 .001 ison of baseline characteristics between the treated and untreated T3 chemoradiotherapy 0.8919 .001 groups. Treated patients tended to be younger and have higher T- and T4 chemoradiotherapy 1.2876 .001 N-stages. After propensity score weighting, all covariates were bal- N1 chemotherapy 0.4993 .034 anced and no longer had statistically significant differences. NA chemotherapy 0.0269 .926 N1 chemoradiotherapy 0.8060 .001 A Kaplan-Meier overall survival plot for all patients by T-stage is NA chemoradiotherapy 0.4845 .002 shown in Figure 1. Unadjusted median overall survival for all patients Log(sigma) 0.1157 .001 was 16 months. In comparing the performance of survival models, the Abbreviation: NA, not available. LN model had the lowest AIC of 9,263, indicating a better overall fit †Age modeled using restricted cubic spline function with four knots, than the other models (CPH, 19,986; Weibull, 9,540; exponential, requiring three independent coefficients: age, age , and age . 9,538; log logistic, 9,304). For an LN model, the appropriate quantile ˆ function plot is 1[1 S(t)] versus ln(t), where 1 is the inverse of ˆ the standard normal cumulative distribution function, S(t) is the Kaplan-Meier estimate of the survival function, and ln(t) is the natural alone to 21% with adjuvant chemotherapy and 42% with adjuvant logarithm of time. A plot of this quantile function approximated a CRT (Fig 3). straight line, indicating a reasonable fit for these data. The LN model had good discrimination, with a C-index of 0.67. The calibration curve also showed good agreement between predicted and observed out- DISCUSSION comes for the LN model. The beta coefficients for the LN model are listed in Table 2. Clinical prediction calculators and nomograms are becoming increas- Interaction terms indicate how the influence of adjuvant chemo- ingly popular decision aids for use in predicting cancer risk, preven- therapy or CRT varies by T and N stages. The LN model was tion, and therapeutic outcomes.21 There are a number of important implemented as an online survival prediction nomogram (Fig 2) cancer risk prediction models being used today for prostate,22-26 that calculates the expected survival benefit from adjuvant chem- breast,27-31 pancreatic,32 and other cancers.33 Clinical prediction tools otherapy and adjuvant CRT. This browser-based software tool is are useful for individualizing therapeutic recommendations for a spe- available at http://skynet.ohsu.edu/nomograms. cific patient. Although prediction models can never substitute for Table 3 summarizes the key findings from the nomogram. For evidence from prospective randomized clinical trials, these tools are patients with T1 disease, the model estimates no survival benefit from useful adjuncts to clinical decision making in situations in which the addition of adjuvant therapy, regardless of nodal status and other clinical trial data are not available, and optimal therapeutic manage- factors. For patients with T2 or greater disease, the model predicts that ment remains controversial. most patients will derive at least a small benefit from adjuvant CRT, In keeping with our findings, recent series have also suggested a regardless of nodal status. For example, a white man age 75 years with survival benefit from adjuvant chemoradiotherapy, with encouraging T2N0 disease would be predicted to see an improvement in 3-year 5-year survival rates over 30%,8-11 compared with historical reports of survival from 42% to 51% with adjuvant CRT. For patients with 10% to 30% after resection alone.34-36 Duke University reported its node-positive disease, the model predicts a small survival benefit from experience in 22 patients with resected gallbladder carcinoma treated adjuvant chemotherapy and a larger benefit from CRT. For example, with adjuvant therapy.8 Despite the locally advanced nature of pa- for a white woman age 65 years with T3N1 disease, the model predicts tients’ disease (86% of patients were T3/4 and/or node positive), that 3-year overall survival would increase from 11% with surgery 5-year survival was 37%. Median survival was 22.8 months, compared www.jco.org © 2011 by American Society of Clinical Oncology 3 Information downloaded from jco.ascopubs.org and provided by at Oregon Health Sciences Univ on November 7, 2011 from Copyright © 2011 American Society of Clinical Oncology. All rights reserved. 137.53.32.65
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Gallbladder Cancer Survival Prediction Model http://skynet.ohsu.edu/nomograms/ Gallbladder Cancer Adjuvant Therapy Instructions: Enter details below for a patient who has had surgery for gallbladder cancer, and the calculator will estimate benefit from post-operative chemotherapy or chemoradiotherapy. Fig 2. Online prediction calculator esti- mating benefit of adjuvant chemotherapy Female or chemoradiotherapy for individual patient; Age: 70 Sex: Male Race: White Web-based tool available at http://skynet T1: localized (lamina propria or muscular layer) .ohsu.edu/nomograms. CBD, common bile T2: perimuscular connective tissue duct; EHBD, extrahepatic bile duct; HA, he- T Stage (AJCC 7th): T3: serosa, liver, or 1 of (EHBD, duodenum, pancreas, stomach, colon) T4: >1 of (EHBD, duodenum, pancreas, stomach, colon) or PV or HA patic artery; LN, lymph node; PV, portal vein; RT, radiotherapy; SMA, superior mesenteric N0: no positive lymph nodes N1: cystic duct, CBD, hepatic artery, or portal vein LNs artery. N Stage (AJCC 7th): N2: para-aortic, pericaval, SMA, or celiac artery LNs unknown Predicted Median Survival: Surgery Alone: 9 months Surgery + Chemo: 14 months Surgery + ChemoRT: 28 months Predicted 3-year Overall Survival: Surgery Alone: 11% Surgery + Chemo: 21% Surgery + ChemoRT: 42% with 16 months in our study, which may be explained by the higher chemotherapy or CRT regimen for all patients, except those with proportion of patients undergoing radical resection and lymphade- T1b or N0 disease. nectomy in that series. Baeza et al9 reported their experience of treating When using observational data to model treatment effects, there 49 patients with resected gallbladder cancer with chemoradiotherapy. will always be inherent selection bias between treated and untreated In this series, all patients underwent lymphadenectomy in addition to groups, because patient selection for treatment can be influenced by cholecystectomy, with a resultant 5-year overall survival of 52%. The patient or tumor characteristics. Propensity score methods can be Mayo Clinic10 published its experience of R0 resected gallbladder used to reduce the impact of this treatment selection bias.17,38-41 The carcinomas treated with adjuvant chemoradiotherapy. As in our propensity score is defined as the probability of receiving treatment study, adjuvant chemoradiotherapy in this series significantly im- conditional on the patient’s observed baseline covariates.38,39 There proved overall survival (hazard ratio for death, 0.30; 95% CI, 0.113 to are several methods in which propensity scores have been incorpo- 0.69; P .004). Also, in a recently published Korean study11 of a series rated into statistical modeling, including stratification, matching, co- of 100 patients, those with node-positive T2 or T3 disease experienced variate adjustment, and inverse probability of treatment weighting. a survival benefit from adjuvant chemoradiotherapy. Austin17 compared these four methods and found that matching and In comparing adjuvant chemotherapy alone versus adjuvant inverse treatment weighting performed better than the other two CRT, our model found that CRT outperformed chemotherapy alone methods. We chose to implement the inverse treatment weighting for virtually all patient subsets. This finding is consistent with what approach, because this method yields a final survival model, the pa- others have found for hepatobiliary cancers from SEER-Medicare. In rameters of which can be readily incorporated into an interactive fact, Davila et al37 found that SEER-Medicare patients with pancreatic Web tool. cancer who received adjuvant chemotherapy had worse outcomes than those who received surgery alone. However, it is important to note that the majority of patients in these SEER-Medicare studies received fluorouracil alone in an era before gemcitabine was widely 1.0 used. The outcomes predicted by our survival model are consistent KM, surgery alone KM, surgery + CRT Overall Survival (proportion) with current National Comprehensive Cancer Network 2011 LN, surgery alone 0.8 guidelines (http://www.nccn.org) for gallbladder cancer, which LN, surgery + CRT state that one should consider a fluoropyrimidine-based adjuvant 0.6 Table 3. Summary of Nomogram Predictions 0.4 Stage Adjuvant Chemotherapy Adjuvant CRT T1N0 0 0 0.2 T2N0 0 T3N0 0 T4N0 T1N 0 14 28 42 T2N T3N Time (months) T4N Fig 3. Example survival plot: comparison of Kaplan-Meier (KM) survival curve Abbreviations: 0, no benefit; , small benefit; , large benefit; versus predicted lognormal (LN) survival for white woman age 65 years with CRT, chemoradiotherapy. stage T3N1 gallbladder cancer after surgery alone (S) or surgery plus chemora- diotherapy (CRT). 4 © 2011 by American Society of Clinical Oncology JOURNAL OF CLINICAL ONCOLOGY Information downloaded from jco.ascopubs.org and provided by at Oregon Health Sciences Univ on November 7, 2011 from Copyright © 2011 American Society of Clinical Oncology. All rights reserved. 137.53.32.65
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Gallbladder Cancer Adjuvant
Chemoradiotherapy Prediction Model We used the AIC to compare the relative performance of the lymphadenectomy.50-54 In fact, some series have demonstrated models. The AIC is a measure of the goodness of fit of regression that patients who incidentally discover T2 gallbladder cancer after models that is based on the concept of entropy.20 It can be viewed as simple cholecystectomy have better outcomes if they undergo re- the amount of information lost when a model is used to describe a set resection with radical surgery and lymphadenectomy.55 Unfortu- of observations. The AIC includes a penalty for number of model nately, the number of SEER-Medicare patients coded as having parameters and thus represents the tradeoff between bias and vari- undergone these extended procedures is low (6% to 7%), which ance. Lower AIC values indicate a better model fit, and in our analysis, precluded our ability to incorporate these variables in our final the LN model had the lowest AIC. nomogram. However, our preliminary analysis indicated that The LN survival is an accelerated failure time parametric survival these patients generally had better survival outcomes compared model that has a long history of usage in cancer survival.42 Although with those who did not, even after adjuvant CRT, suggesting that not as popular as the semiparametric CPH model, in many settings in patients with gallbladder disease should have these extended pro- which the proportionality assumption does not hold, the LN model cedures performed whenever possible. Interestingly, our prelimi- has been shown to be a more appropriate survival model in, for nary analysis suggests that patients who underwent extended example, breast42-45 and lung cancers.46 Gamel et al47 developed an lymphadenectomy did not derive as large a benefit from adjuvant extension to the original Boag model that allows prognostic covariates chemotherapy or CRT. In the future, when more of these patient to be incorporated into the LN model. In this LN survival model, the cases have accumulated in SEER-Medicare, we plan to incorporate log of survival time has a normal distribution and is a linear function of radical resection and lymphadenectomy as additional covariates in covariates. In this setting, the hazard function is not constant over time the next version of our nomogram. but instead rises quickly to a peak and then declines over time. We In some cases, the model predicted only a small-percentage im- have previously demonstrated that this LN model performs well in provement from the addition of adjuvant therapy, such as in certain modeling extrahepatic cholangiocarcinoma,48 and the current study cases of node-negative disease. We did not specify a specific threshold indicates that an LN model also demonstrates a good fit for gallblad- at which adjuvant therapy should be recommended. We believe that der cancer. the final decision of whether adjuvant therapy should be administered Our current findings are consistent with the overall conclusions is a decision that should be made after thoughtful discussion between from our original SEER-based gallbladder nomogram13 (ie, most pa- clinician and patient, taking into account multiple factors, many of tients with T2 or N gallbladder cancer or greater would be predicted which cannot be accounted for in a prediction model. Quality of life to benefit from adjuvant therapy). Chemotherapy was not included in and specific patient preferences are also important considerations in the original model, because this information is not available in SEER, treatment decision making. but our current SEER-Medicare analysis confirms that the majority of Recently, there has been a movement toward personalized these patients also received chemotherapy. Differences between the medicine, in which specific information about an individual pa- two nomograms in the actual predicted survival estimates are mainly tient is used to optimize the patient’s care. We believe that these the result of the incorporation of more recent data and use of im- types of predictive models will become increasingly important in proved survival modeling methods. the future, as we attempt to improve outcomes by individualizing There are several limitations to this study. This study was per- therapeutic recommendations. formed using SEER-Medicare data and was limited to predictive fac- In summary, we have built an interactive survival prediction tors available in this database. SEER does not include information on model that can make an individualized estimate of the net survival margins or performance status, so these prognostic factors could not benefit of adjuvant therapy for patients with gallbladder cancer. This be included. Patients who received both radiotherapy and chemother- tool can assist clinicians and patients in quantifying the potential apy within a 6-month time window were assumed to have received benefit of adjuvant chemotherapy or CRT after surgical resection of concurrent adjuvant CRT. We also examined a shorter 4-month time gallbladder cancer. window and found similar results. Because SEER does not capture cancer recurrence, this approach may have also inadvertently cap- tured patients who received therapy for an early recurrence within 6 AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS months and those who received sequential and not concurrent ther- OF INTEREST apy, and it would have missed adjuvant therapy administered after 6 months. The author(s) indicated no potential conflicts of interest. Perioperative mortality can bias the apparent effect of adjuvant therapy in nonrandomized observational studies. To partially com- pensate for this bias, we excluded all patients who died within 2 AUTHOR CONTRIBUTIONS months of surgery. However, it is important to note that this type of exclusion may have subjected the results to a different type of bias Conception and design: Samuel J. Wang, Jayashree Kalpathy-Cramer, C. resulting from conditional survival,49 in which all patients’ prognoses David Fuller, Charles R. Thomas Jr improve when they are presumed to have already survived a period of Administrative support: Charles R. Thomas Jr time since treatment. Collection and assembly of data: Samuel J. Wang, Andrew Lemieux, Gary V. Walker To capture the largest relevant data set, we included all pa- Data analysis and interpretation: Samuel J. Wang, Jayashree tients who underwent at least a total cholecystectomy. In looking at Kalpathy-Cramer, Celine B. Ord, C. David Fuller, Jong-Sung Kim extent of resection, several studies have established that gallbladder Manuscript writing: All authors cancer survival outcomes are improved with radical resection and Final approval of manuscript: All authors www.jco.org © 2011 by American Society of Clinical Oncology 5 Information downloaded from jco.ascopubs.org and provided by at Oregon Health Sciences Univ on November 7, 2011 from Copyright © 2011 American Society of Clinical Oncology. All rights reserved. 137.53.32.65
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Harada K, Ochiai T, Inoue K, et al: Optimal covariates between treated and untreated subjects Gallbladder carcinoma: Role of radiation therapy. surgical treatment for patients with pT2 gallbladder in observational studies. Med Decis Making 29:661- Br J Surg 76:448-450, 1989 cancer. Hepatogastroenterology 58:14-19, 2011 677, 2009 36. Arnaud JP, Casa C, Georgeac C, et al: Primary 55. Fuks D, Regimbeau JM, Le Treut YP, et al: 18. Kalpathy-Cramer J, Hersh W, Kim JS, et al: carcinoma of the gallbladder: Review of 143 cases. Incidental gallbladder cancer by the AFC-GBC-2009 Survival prediction models for estimating the benefit Hepatogastroenterology 42:811-815, 1995 study group. World J Surg 35:1887-1897, 2011 ■ ■ ■ 6 © 2011 by American Society of Clinical Oncology JOURNAL OF CLINICAL ONCOLOGY Information downloaded from jco.ascopubs.org and provided by at Oregon Health Sciences Univ on November 7, 2011 from Copyright © 2011 American Society of Clinical Oncology. 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