Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Communication With Older Patients With Cancer Using Geriatric Assessment

Communication With Older Patients With Cancer Using Geriatric Assessment Research JAMA Oncology | Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment A Cluster-Randomized Clinical Trial From the National Cancer Institute Community Oncology Research Program Supriya G. Mohile, MD, MS; Ronald M. Epstein, MD; Arti Hurria, MD; Charles E. Heckler, PhD, MS; Beverly Canin; Eva Culakova, PhD, MS; Paul Duberstein, PhD; Nikesha Gilmore, PhD; Huiwen Xu, MHA; Sandy Plumb, BS; Megan Wells, MPH; Lisa M. Lowenstein, PhD; Marie A. Flannery, PhD; Michelle Janelsins, PhD, MPH; Allison Magnuson, DO; Kah Poh Loh, MB, BCh, BAO; Amber S. Kleckner, PhD; Karen M. Mustian, PhD, MPH; Judith O. Hopkins, MD; Jane Jijun Liu, MD; Jodi Geer; Rita Gorawara-Bhat, PhD; Gary R. Morrow, PhD, MS; William Dale, MD, PhD Invited Commentary IMPORTANCE Older patients with cancer and their caregivers worry about the effects of Supplemental content cancer treatment on aging-related domains (eg, function and cognition). Quality conversations with oncologists about aging-related concerns could improve patient-centered outcomes. A geriatric assessment (GA) can capture evidence-based aging-related conditions associated with poor clinical outcomes (eg, toxic effects) for older patients with cancer. OBJECTIVE To determine whether providing a GA summary and GA-guided recommendations to oncologists can improve communication about aging-related concerns. DESIGN, SETTING, AND PARTICIPANTS This cluster-randomized clinical trial enrolled 541 participants from 31 community oncology practices within the University of Rochester National Cancer Institute Community Oncology Research Program from October 29, 2014, to April 28, 2017. Patients were aged 70 years or older with an advanced solid malignant tumor or lymphoma who had at least 1 impaired GA domain; patients chose 1 caregiver to participate. The primary outcome was assessed on an intent-to-treat basis. INTERVENTIONS Oncology practices were randomized to receive either a tailored GA summary with recommendations for each enrolled patient (intervention) or alerts only for patients meeting criteria for depression or cognitive impairment (usual care). MAIN OUTCOMES AND MEASURES The predetermined primary outcome was patient satisfaction with communication about aging-related concerns (modified Health Care Climate Questionnaire [score range, 0-28; higher scores indicate greater satisfaction]), measured after the first oncology visit after the GA. Secondary outcomes included the number of aging-related concerns discussed during the visit (from content analysis of audiorecordings), quality of life (measured with the Functional Assessment of Cancer Therapy scale for patients and the 12-Item Short Form Health Survey for caregivers), and caregiver satisfaction with communication about aging-related patient concerns. RESULTS A total of 541 eligible patients (264 women, 276 men, and 1 patient did not provide data; mean [SD] age, 76.6 [5.2] years) and 414 caregivers (310 women, 101 men, and 3 caregivers did notprovidedata;meanage,66.5[12.5]years)wereenrolled.Patientsintheinterventiongroupwere moresatisfiedafterthevisitwithcommunicationaboutaging-relatedconcerns(differenceinmean score, 1.09 points; 95% CI, 0.05-2.13 points; P = .04); satisfaction with communication about aging-relatedconcernsremainedhigherintheinterventiongroupover6months(differenceinmean score, 1.10; 95% CI, 0.04-2.16; P = .04). There were more aging-related conversations in the intervention group’s visits (difference, 3.59; 95% CI, 2.22-4.95; P < .001). Caregivers in the intervention group were more satisfied with communication after the visit (difference, 1.05; 95% CI, 0.12-1.98; P = .03). Quality of life outcomes did not differ between groups. Author Affiliations: Author affiliations are listed at the end of this CONCLUSIONS AND RELEVANCE Including GA in oncology clinical visits for older adults with article. advanced cancer improves patient-centered and caregiver-centered communication about Corresponding Author: Supriya G. aging-related concerns. Mohile, MD, MS, Department of Medicine, University of Rochester, TRIAL REGISTRATION ClinicalTrials.gov identifier: NCT02107443 601 Elmwood Ave, PO Box 704, Rochester, NY 14642 JAMA Oncol. doi:10.1001/jamaoncol.2019.4728 (supriya_mohile@urmc. Published online November 7, 2019. rochester.edu). (Reprinted) E1 Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment atient-centered communication promotes high- quality conversations prioritizing patient and care- Key Points P giver concerns so that decisions are aligned with their Question Does providing a summary of geriatric assessment preferences and values. Effective communication is charac- results and geriatric assessment–guided recommendations to terized by (1) informed and participatory patients and care- oncologists improve communication about aging-related givers; (2) informed, receptive, and patient-centered clini- concerns? cians; and (3) a health care system providing well-organized Findings In this nationwide cluster-randomized clinical trial of and responsive services that are tailored to patients’ and care- 31 community oncology practices that enrolled 541 older patients 1,2 givers’ needs. Although studies have demonstrated ben- with advanced cancer, providing a geriatric assessment summary efits for interventions that facilitate oncologist-patient with recommendations to oncologists improved postvisit patient 3-5 satisfaction and caregiver satisfaction and increased the number communication, these interventions were not tailored to ad- of conversations about aging-related concerns. These results were dress aging-related concerns of older adults receiving cancer significantly different between the intervention and usual care treatment and their caregivers. groups. Older adults represent most patients with advanced 6,7 Meaning Integrating geriatric assessment into community cancer seen in community oncology practices. Cancer oncology care improves patient and caregiver satisfaction and treatment choices for older adults with aging-related communication about aging-related concerns. conditions (ie, disability, comorbidity, and geriatric syn- 8,9 dromes) are based on extrapolations of evidence derived from clinical trials that enroll younger patients or fit older adults. Many older adults have unidentified, Methods uncommunicated, and therefore unaddressed aging- related conditions that are associated with morbidity Overview and early mortality. A communication intervention for In this cluster-randomized clinical trial, Improving Commu- oncologists who care primarily for older adults—yet nication in Older Cancer Patients and Their Caregivers lack aging-related expertise—could improve patient (COACH), community oncology practices were randomized to and caregiver satisfaction by bringing attention to often- the intervention or usual care group (CONSORT diagram in 12 13 34 overlooked aging-related conditions. Despite controversy, Figure 1 and trial protocol in Supplement 1). We enrolled par- satisfaction with physician communication is considered ticipants from October 29, 2014, to April 28, 2017. The Uni- a metric for quality of health care and even modest improve- versity of Rochester and all participating sites obtained ap- ments in survey scores are linked to increased reim- proval from their institutional review boards. Participants 14-18 bursement. provided written informed consent. 19(p1) To address a “cancer care delivery system in crisis,” the National Academy of Medicine (formally the Institute of Settings and Participants 20,21 Medicine), the American Society of Clinical Oncology We recruited community oncology practices within the Uni- 22 10,23,24 (ASCO), the Cancer and Aging Research Group, and versity of Rochester National Cancer Institute Community On- the International Society of Geriatric Oncology, have all cology Research Program (NCORP) Research Base network. On- called for improved care delivery that attends to aging- cologists enrolled as participants ; only patients of enrolled related conditions of older adults with cancer. A key compo- oncologists were eligible to participate. Other patient eligibil- nent is geriatric assessment (GA), which uses validated ity criteria included aged 70 years or older, at least 1 GA domain 11,25,35-37 patient-reported and objective measures to capture domains impairment, an advanced solid tumor or lymphoma, important to older adults such as function (ie, ability to cancer treatment with palliative intent, planned oncology vis- remain independent) and cognition. As highlighted in a its for at least 3 months, ability to provide informed consent recent ASCO guideline, older adults and caregivers value independently or via a health care proxy, and an understand- 26,27 these GA domains, and GA domains, when formally ing of English. Eligible patients chose 1 caregiver aged 21 years 11,12,28-30 assessed, influence treatment decision-making. or older. Patients with no eligible caregivers could still enroll However, aging-related concerns are rarely addressed in in the study. oncology care, especially outside specialized academic 12,31,32 settings. Study Groups To our knowledge, this study is the first randomized All patients underwent a GA that evaluated 8 domains— clinical trial evaluating whether GA can meaningfully functional status, physical performance, comorbidity, poly- influence oncology care processes for vulnerable older pharmacy, cognition, nutrition, psychological health, and so- 11,25,35-37 37 adults with advanced cancer. With outcome measure cial support. The GA was mostly patient reported. selection guided by input from older patients and Trained coordinators (J.G.) completed the objective perfor- 23,33 caregivers, we hypothesized that providing GA informa- mance and cognitive measures. At practices that were ran- tion to oncologists would improve patient satisfaction with domized to the intervention group, coordinators entered the communication about aging-related concerns by increasing GA scores into a locked web-based folder (http://www.mycarg. the number and quality of conversations during oncology org) that created a tailored GA summary that was printed out clinic visits. for each patient. The summary included information on GA E2 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research Figure 1. CONSORT Flow Diagram for the COACH (Improving Communication in Older Cancer Patients and Their Caregivers) Trial of Practice Clusters, Oncologists, Patients, and Caregivers 552 NCORP component sites contacted 274 NCORP component sites chose not to participate and did not obtain IRB approval 278 Component sites agreed to participate and obtained IRB approval (preclustered practice sites) 85 Practice site clusters 54 Excluded 35 Active clusters never enrolled participants 17 Clusters inactivated study 2 Clusters no longer affiliated 31 Practice site clusters that enrolled patients and caregivers 610 Patients screenedc 64 Excluded 33 Withdrawals 31 Screening failures 31 Practice site clusters randomized (546 patients, 417 caregivers, 132 physicians) 17 Practice sites allocated to intervention 14 Practice sites allocated to usual care 296 Patients 250 Patients 233 Caregivers 184 Caregivers 64 Physicians 68 Physicians Protocol violation Protocol violation 3 Patients 2 Patients 2 Caregivers 1 Caregivers 1 Physician 293 Patients 248 Patients 231 Caregivers 183 Caregivers 63 Physicians 68 Physicians Withdrew Withdrew 2 Patients 3 Patients 2 Caregivers 2 Caregivers Died 290 Patients 245 Patients 1 Patient 229 Caregivers 181 Caregivers 63 Physicians 68 Physicians d e d e Primary aim Secondary aim 1 Primary aim Secondary aim 1 No audio captured No HCCQ 4 Patients 6 Patients No HCCQ No audio captured Protocol violation Answered 2 HCCQ 19 Patients 1 Patient 2 Patients questions 1 Physician 1 Patient Included in primary analysis Included in secondary analysis Included in primary analysis Included in secondary analysis 271 Patients 284 Patients 238 Patients 244 Patients 211 Caregivers 225 Caregivers 177 Caregivers 180 Caregivers 63 Physicians 62 Physicians 67 Physicians 68 Physicians Follow-up at 4 to 6 weeks included 472 patients, at 3 months included 410 Institute Community Oncology Research Program (NCORP) affiliate or with patients, and at 6 months included 348 patients. Follow-up included 348 the University of Rochester NCORP Research Base. caregivers at 4 to 6 weeks, 306 caregivers at 3 months, and 261 caregivers at c Signed consent and participated in screening process. 6 months. HCCQ indicates Health Care Climate Questionnaire. Satisfaction with communication about aging-related concerns. Clusters that maintained institutional review board (IRB) approval but never Conversations about aging-related conditions during clinic visit. enrolled any participants. Irretrievable, site miscommunication, technical difficulty, or protocol violation. Practices are no longer associated with their respective National Cancer jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E3 Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment domain impairments and GA-guided recommendations based Randomization and Blinding 11 38 36 on literature review, guidelines, and expert consensus. Accrual records from University of Rochester NCORP studies As an example, the summary would include information were used to stratify practice clusters as large or small accru- that a patient recently fell, that falls increase the risk of ing sites to assure balance in randomization. Randomization chemotherapy toxic effects, and a recommendation for physical was done at the practice cluster level and recruitment of all par- therapy to prevent falls. The summary and recommendations ticipants was based on the group to which their practice clus- were provided to oncologists once prior to an audiorecorded ter was assigned. Other than the statisticians, all investiga- clinic visit. At study entry, oncologists received a brief training tors were blinded to group; blinding was preserved among the about GA and were told that they had autonomy for if and how telephone team, transcriptionists, and coders. they wished to use GA for their enrolled patients. For the usual care group, oncologists were alerted only if patients had Sample Size abnormal scores on depression and cognitive tests. Sample size and power considerations were based on the pri- mary aim of the HCCQ-age to address patient satisfaction with communication about aging-related concerns. This design had Data Collection and Outcome Measures In both groups, 1 oncology clinic visit within 4 weeks of GA 80% power at the 0.05 significance level to detect a differ- was audiorecorded and transcribed. Within 7 to 14 days of ence of 1.3 in HCCQ-age scores, with an intraclass correlation 3,32 this visit, trained personnel called the patient to assess satis- coefficient (ICC) of 0.14, corresponding to an effect size of faction with communication. During the telephone call, the 0.62. Assuming a withdrawal rate of 5% (based on observa- patients completed 2 versions of the Health Care Climate tional cohort data ), the targeted accrual was 528 patients. The 39,40 Questionnaire (HCCQ). The first version measures satis- design had 80% power at the 0.05 significance level to detect faction with patient-centered physician communication, a difference of 0.46 in the number of conversations about such as whether the patient feels that the physician under- aging-related concerns, with an ICC of 0.12, corresponding to stands her or his perspective and encourages participation an effect size of 0.59. We originally aimed for participation in decisions (score range, 0-20; higher scores indicate by 16 NCORP practices. Because the recruitment was initially greater satisfaction). Similar to other research, the second slower than anticipated, we allowed more practices to partici- version of the HCCQ modified the language of the questions pate (as specified by the trial protocol in Supplement 1). The in the HCCQ to address satisfaction with communication total patient sample size did not change. regarding aging-related concerns (HCCQ-age; score range, 0-28); this modified version of the HCCQ was designed with Statistical Analysis input from advocates who were not enrolled in the trial Descriptive statistics were used to evaluate demographics, GA and was used for the primary outcome (eAppendix in results, and clinical information, and bivariate analyses were Supplement 2). performed to compare between- group differences in charac- A secondary outcome included the number of aging- teristics of patients and caregivers. For the primary outcome, related concerns discussed at the visit. With experts and 4 cod- to follow the intent-to-treat principle and to assess the effect ers, a content analysis framework outlined how to identify of missing values on the study results, we conducted addi- aging-related conversations, assess their quality (whether a tional analyses including all randomized eligible patients. concern was acknowledged and further explored by the on- Under missing at random assumptions, we evaluated the in- cologist), and determine whether an acknowledged concern fluence of missing data on the study results via multiple motivated recommendations for specific GA-guided imputation. The examination of the reasons for missing 3,11,31,32,36,43 interventions. Team coding of the transcribed au- data did not reveal any reason to suspect a missing not at ran- diorecordings occurred until interrater reliability was 70% dom mechanism. Nevertheless, we also applied sensitivity or greater. Subsequently, for each transcript, coding was per- analysis using pattern mixture models. Similar to prior 50,51 formed independently by 2 trained coders, with 20% of tran- research, we conducted responder analyses evaluating the scripts coded by all 4 coders. Final interrater reliability was 82% proportion of participants who reported satisfaction scores for number of concerns and 92% for both quality and inter- within a half SD of the HCCQ score from the perfect score; ventions. achieving a perfect satisfaction score is commonly advocated 52,53 Other secondary outcomes evaluated patient and care- as a metric for high quality in practice. giver quality of life (QoL) as well as caregiver satisfaction Because of the cluster-randomized study design, a linear with communication. Patients completed the Functional mixed model method was applied. The outcome was the re- Assessment of Cancer Therapy scale at enrollment and 4 to sponse, and the group was the fixed effect. Practices were en- 6 weeks, 3 months, and 6 months later. Caregiver QoL was tered as a random effect independent of residual error. Esti- assessed using the 12-Item Short Form Survey and burden mation was performed using restricted maximum likelihood, was assessed using the Caregiver Reaction Assessment at and the null hypothesis of zero mean difference between the same time points as patients. Caregivers completed groups was tested using an F test. The results are presented HCCQ surveys that assessed their satisfaction with commu- as means (or mean difference) adjusted for the practice effect nication about their concerns related to the patient’s aging- and evaluated as marginal means from the linear mixed model. related conditions and overall care (score range for both Practice differences were assessed graphically using best lin- surveys, 0-20). ear unbiased predictors of the mean response for each. E4 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research Figure 2. Patient and Caregiver Satisfaction A Patient satisfaction with communication B Patient satisfaction with overall care C Caregiver satisfaction with communication 25 18.0 18 17.5 17.0 16.5 16.0 Intervention Usual care 15.5 18 15.0 13 Telephone 4-6 wk 3 mo 6 mo Telephone 4-6 wk 3 mo 6 mo 4-6 wk 3 mo 6 mo Assessment Assessment Assessment A, Patient satisfaction with communication about aging-related concerns. B, Patient satisfaction with overall care. C, Caregiver satisfaction with communication about the patient’s age-related conditions. Scores were derived using modified versions of the Health Care Climate Questionnaire. The telephone assessment was 7 to 14 days after the audio-recorded clinic visit. To assess the effect of the intervention on the outcomes [33.1%] vs 74 of 293 [25.3%]; P = .05) (eFigure in Supple- over time, we used a longitudinal linear mixed model. An un- ment 2). Caregivers (n = 414; mean [SD] age, 66.5 [12.5] years; structured correlation matrix was used for the repeated mea- range, 26-92 years) were most likely to be the patient’s sures from the same participant. The model was adjusted spouse or partner (276 [66.7%]; eTable 2 in Supplement 2) and for practice cluster using a random effect independent of the 310 [74.9%] were women. Baseline data for oncologists, 37,56,57 37,56,57 within-participant random effects, and it was fit via re- patients, and caregivers have been published. stricted maximum likelihood. Every effort was made to facilitate participants’ comple- Patient Satisfaction With Communication tion of questionnaires. However, baseline data from some par- For 509 evaluable patients, the mean (SE) satisfaction score ticipants were missing, and there was participant withdrawal for communication about aging-related concerns was 22.8 (Figure 1); anticipating that some patients would not be able (0.27) (range, 5-28 for HCCQ-age) after the clinic visit. The score to be reached by telephone, the protocol allowed for imputa- in the intervention group was 1.09 points higher than in the tion of the 4- to 6-week HCCQ results to assess the primary aim. usual care group (95% CI, 0.05-2.13; P = .04; ICC = 0.02). Af- Analysis was performed with SAS, version 9.4 (SAS Institute ter the clinic visit, the mean (SE) satisfaction score for com- Inc) and R, version 3.5.2 (R Foundation for Statistical Com- munication about overall care was 17.4 (0.16) (range, 5-20 for puting) software. All P values were from 2-sided tests, and the HCCQ). The proportion of patients within a half SD from a per- results were deemed statistically significant at P < .05. fect score was higher in the intervention group (109 of 271 [40.2%] vs 71 of 238 [29.8%]). Over 6 months, patients in the intervention group were more satisfied with communication about aging-related concerns (difference in mean HCCQ-age Results score, 1.10; 95% CI, 0.04-2.16; P =.04) (Figure 2A) and re- Participant Characteristics ported greater satisfaction with overall care (difference in mean From October 29, 2014, to April 28, 2017, 31 practice clusters HCCQ score, 0.70; 95% CI, 0.06-1.25; P = .03) (Figure 2B). (17 intervention and 14 usual care) enrolled participants, in- cluding 131 oncologists, 541 eligible patients, and 414 eligible Number and Quality of Conversations caregivers (Figure 1). Patients had a mean (SD) age of 76.6 (5.2) About Aging-Related Concerns years (range, 70-96 years), and 264 (48.8%) were women; most For 528 evaluable patients, the adjusted mean (SE) number patients had gastrointestinal and lung cancers (278 [51.4%]) of conversations about aging-related concerns during the and were receiving chemotherapy (369 [68.2%]) (eTable 1 in oncology clinic visit was 6.34 (0.48) (range, 0-18). There was Supplement 2). There were no essential differences in demo- an adjusted mean of 8.02 conversations in the intervention graphics or clinical characteristics by group. Most patients had group compared with 4.43 in usual care (difference, 3.59; 2 or more GA domain impairments (mean [SD], 4.5 [1.5]); the 95% CI, 2.22-4.95; P < .001; ICC = 0.14; Figure 3). The inter- prevalence of GA domain impairments ranged from 93.7% vention group had an adjusted mean of 4.60 high-quality (n = 507) for physical performance to 25.1% (n = 136) for psy- conversations, compared with 2.59 in the usual care group chological status; 180 patients (33.3%) had possible cognitive (difference, 2.01 [adjusted by practice site]; 95% CI, 1.20- impairment. A total of 487 of 541 patients (90.0%) had 3 or 2.77; P < .001; ICC = 0.06). There was an adjusted mean of more GA domain impairments. More patients in the usual care 3.20 conversations about recommendations in the interven- group had impaired physical performance (239 of 248 [96.4%] tion group compared with 1.14 in the usual care group vs 268 of 293 [91.5%]; P = .03) and social support (82 of 248 (difference, 2.06; 95% CI, 0.99-3.12; P < .001; ICC = 0.30). jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E5 Score Score Score Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment patients represent less-fit individuals for whom there is lim- Figure 3. Conversations About Aging-Related Conditions ited evidence for the risks and benefits of cancer treatment, yet these patients are commonly seen in real-world commu- P<.001 9 Intervention Usual care nity practices. Although patients had various cancer types, all were incurable and were treated with palliative intent. Evidence increasingly supports the use of GA for evalua- tion and management of older patients with cancer to P<.001 5 guide shared decision-making between older patients, care- P<.001 11,25 4 givers, and oncologists. As highlighted in the ASCO geri- atric oncology guidelines and supported by systematic 29,60 reviews, GA impairments are associated with chemo- therapy toxic effects, lower treatment completion, func- tional decline, early mortality, and higher health care use. All Age-Related Higher-Quality Conversations Like others, we found that older patients with a high preva- Conversations Age-Related With GA-Driven lence of GA domain impairments still receive treatment for Conversations Recommendations advanced cancer, including chemotherapy. Of particular The patient’s visit with the oncologist within 4 weeks of completing the geriatric concern is the one-third of patients who had positive screen- assessment (GA) was audiorecorded, transcribed, and coded. We used an open coding approach of themes and subthemes to quantify the number of ing results for possible cognitive impairment, given the lim- age-related conversations, the number of aging-related discussions with ited evidence for the safety and efficacy of chemotherapy in high-quality communication, and the number of conversations of GA-driven this group. The higher prevalence of GA domain impair- recommendations communicated to patients by oncologists. ments compared with other trials reflects our expanded eli- gibility criteria and our use of a formal GA to evaluate often eTable 3 in Supplement 2 is a joint display illustrating overlooked aging-related conditions. exemplar quotes with mean conversation numbers by Despite patient and caregiver concerns and preferences for 26,27 domain. maintaining function and cognition, oncologists often do not discuss implications of aging-related conditions or in- form older patients and caregivers of heightened risk of ad- Patients’ and Caregivers’ Health-Related Quality of Life Analyses did not detect any statistically significant differ- verse events from treatment. We found that, when GA in- ences between groups in Functional Assessment of Cancer formation was provided, community oncologists used it in Therapy scale score for patients over 6 months (range, 23- communication during the clinic visit, similar to other non- 108; difference [SE], −0.23 [1.03]; P = .82). In addition, there geriatric studies that have systematically provided symptom 62,63 were no differences for caregiver 12-Item Short Form Survey and QoL information to oncologists. Our results align with total scores or Caregiver Reaction Assessment subscales. this research showing that coordinated care for younger pa- tients that captures patient-reported outcomes improves qual- ity of care and outcomes; for older patients with cancer, per- Caregiver Satisfaction With Communication At 4 to 6 weeks after the clinic visit, caregivers in the inter- sonalized care requires attention to aging-related conditions. vention group were more satisfied with their communication We recruited older patients who had several different can- regarding their concerns about the patients’ aging-related cers and treatments, which may have limited our ability to de- conditions (range, 5-20; difference, 1.05; 95% CI, 0.12-1.98; tect QoL effects. In addition, the intervention provided a GA P = .03). The proportion of caregivers within a half SD of a per- summary during 1 clinic visit only to oncologists; studies fect score was higher in the intervention group (74 of 189 that have reported survival and QoL benefits from structured [39.2%] vs 42 of 158 [26.6%]). Caregivers were more satisfied interventions have incorporated evaluation and manage- with their own communication with oncologists with regard ment of patient-reported outcomes over time or have used 29,64 to overall care (range, 2-20; difference, 1.34; 95% CI, 0.50- geriatrics-trained professionals. A randomized study of 2.18; P = .004). The differences in satisfaction scores were not GA-directed therapy for older patients with advanced lung significant when analyzed over 6 months (Figure 2C). cancer demonstrated reduced toxic effects of treatment and less treatment discontinuation in the GA group owing to im- proved treatment allocation. Several ongoing clinical trials will evaluate if GA can help improve clinical outcomes (QoL, Discussion toxic effects, and survival) of patients through improved The COACH cluster-randomized clinical trial is the first large decision-making and GA-guided interventions. multisite intervention study to demonstrate that providing a A previous study using baseline COACH data reported that an increasing number of patient GA domain impairments is as- GA summary with GA-guided recommendations to commu- nity oncologists facilitates communication about aging- sociated with poor caregiver emotional health and QoL. Simi- related concerns and improves patient and caregiver satisfac- lar to early palliative care models that used specialized nurse tion with communication and care. COACH enrolled vulnerable coaches to assess and provide management for patients and older patients with cancer who had significant aging-related caregivers, GA-based interventions could be adapted for both conditions—90% had 3 or more GA domain impairments. These patients and caregivers. E6 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Conversations, No., Adjusted Mean (95% CI) Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research blinded, and thus may have modified their discussions of ag- Strengths and Limitations Strengths of this study include recruitment of a large sample ing; however, the strength of the findings shows that modify- of vulnerable older patients and their caregivers who have ing oncologist behavior to increase communication about ag- rarely been included in cancer trials. This study also demon- ing-related concerns is possible. strates the ability to conduct multisite trials incorporating GA in the community oncology setting. We attribute our success- ful completion of the trial in large part to our patient and care- Conclusions giver research advocate partners from Scoreboard (Stakehold- ers for Care in Oncology and Research for our Elders) who To our knowledge, the COACH cluster-randomized clinical trial 23,33 provided ongoing input and solutions for barriers. is the first trial to demonstrate that provision of a formal GA Limitations include risk of selection bias, as we enrolled a to community oncologists, per ASCO guidelines, can im- specific population of older patients; however, these are pa- prove satisfaction and communication for vulnerable older pa- tients who are commonly seen in community oncology clin- tients with advanced cancer and their caregivers. COACH dem- ics and are underrepresented in research. Although cluster ran- onstrated that a practical and convenient GA summary with domization is a strength, since we were testing a model of care recommendations for aging-sensitive interventions im- as an intervention, there is a risk of selection bias inherent in proves patient-centered outcomes and thus should be consid- cluster randomization. Oncologists in both groups were not ered as the standard of care for older patients with cancer. ARTICLE INFORMATION Concept and design: Mohile, Hurria, Heckler, Canin, from the University of Rochester during the Duberstein, Plumb, Mustian, Hopkins, Dale. conduct of the study. Dr Kleckner reported Accepted for Publication: August 22, 2019. Acquisition, analysis, or interpretation of data: receiving grants from NCI during the conduct of the Published Online: November 7, 2019. All authors. study. Dr Morrow reported receiving a grant from doi:10.1001/jamaoncol.2019.4728 Drafting of the manuscript: Mohile, Hurria, Heckler, NCI and a contract from PCORI during the conduct Open Access: This is an open access article Canin, Xu, Janelsins, Kleckner, Mustian, Hopkins, of the study; and grants from NCI outside the distributed under the terms of the CC-BY License. Dale. submitted work. No other disclosures were © 2019 Mohile SG et al. JAMA Oncology. Critical revision of the manuscript for important reported. intellectual content: Mohile, Epstein, Heckler, Author Affiliations: Department of Medicine, Funding/Support: This study was partially funded Culakova, Duberstein, Gilmore, Xu, Plumb, Wells, University of Rochester, Rochester, New York by the Patient-Centered Outcomes Research Lowenstein, Flannery, Janelsins, Magnuson, Loh, (Mohile, Xu, Plumb, Wells, Magnuson, Loh); Institute (contract CD-12-11-4634 to Dr Mohile). Kleckner, Mustian, Hopkins, Liu, Geer, University of Rochester Cancer Center National Support also came from the National Institute of Gorawara-Bhat, Morrow, Dale. Cancer Institute Community Oncology Research Aging grant R21/R33AG059206 (Drs Mohile, Hurria, Statistical analysis: Mohile, Hurria, Heckler, Program Research Base, Rochester, New York and Dale), National Cancer Institute grant Culakova, Xu, Wells. (Mohile, Heckler, Canin, Culakova, Gilmore, Xu, UG1CA189961 (Drs Mustian and Morrow), National Obtained funding: Mohile, Hurria, Morrow, Dale. Plumb, Wells, Flannery, Janelsins, Magnuson, Loh, Cancer Institute grant R25CA102618 (Drs Janelsins Administrative, technical, or material support: Kleckner, Mustian, Morrow); Department of Family and Morrow), and National Institute of Aging grant Mohile, Hurria, Gilmore, Xu, Plumb, Wells, Medicine, University of Rochester, Rochester, K24AG056589 (Dr Mohile). Lowenstein, Flannery, Magnuson, Loh, Kleckner, New York (Epstein); Department of Medical Role of the Funder/Sponsor: The funding sources Morrow, Dale. Oncology, City of Hope National Medical Center, had no role in the design and conduct of the study; Supervision: Mohile, Janelsins, Magnuson, Mustian, Duarte, California (Hurria); Department of Surgery, collection, management, analysis, and Morrow, Dale. University of Rochester, Rochester, New York interpretation of the data; preparation, review, or (Heckler, Culakova, Gilmore, Janelsins, Kleckner, Conflict of Interest Disclosures: Dr Mohile approval of the manuscript; and decision to submit Mustian, Morrow); Stakeholders for Care in reported receiving a grant from the National Cancer the manuscript for publication. Oncology and Research for our Elders, Rochester, Institute (NCI) and a contract from the Disclaimer: The information presented in this New York (Canin); Department of Health Behavior, Patient-Centered Outcomes Research Institute manuscript is solely the responsibility of the author Society, and Policy, Rutgers University School of (PCORI) during the conduct of the study; and (s) and does not necessarily represent the views of Public Health, Piscataway, New Jersey receiving grants from Carevive outside the the PCORI, its Board of Governors, or Methodology (Duberstein); Department of Health Services submitted work. Dr Epstein reported receiving Committee. All information and materials published Research, University of Texas MD Anderson Cancer grants from NCI and American Cancer Society in the primary manuscript are original. Center, Houston (Lowenstein); University of during the conduct of the study. Dr Hurria reported Rochester School of Nursing, Rochester, New York receiving a contract from PCORI during the conduct Data Sharing Statement: See Supplement 3. (Flannery); Novant Health Oncology Specialists, of the study; and consulting payments from Additional Contributions: We thank all the Winston-Salem, North Carolina (Hopkins); Celgene, Novartis, GSK, Boehringer Ingelheim, patients and caregivers of SCOREboard: Beverly Southeast Clinical Oncology Research Consortium Carevive, Sanofi, GTx Inc, Pierian Biosciences, and Canin (Chair), Mary Whitehead, Margaret National Cancer Institute Community Oncology MJH Healthcare Holdings LLC outside the Sedenquist, Lorraine Griggs, Lynn Finch, John Research Program, Winston-Salem, North Carolina submitted work. Dr Canin reported receiving Aarne, Valerie Targia, Robert Harrison (deceased), (Hopkins); Heartland Cancer Research National personal fees from the University of Rochester Valerie Aarne, Dorothy Dobson, Jacquelyn Dobson, Cancer Institute Community Oncology Research during the conduct of the study. Dr Culakova Burt Court, Polly Hudson, and Ray Hutchins Program, Decatur, Illinois (Liu); Metro Minnesota reported receiving a grant from NCI and a contract (deceased). Susan Rosenthal, MD, University of Community Oncology Research Program, St Louis from PCORI during the conduct of the study. Rochester Cancer Center National Cancer Institute Park (Geer); Department of Medicine, University of Dr Gilmore reported receiving grants from the Community Oncology Research Program Research Chicago, Chicago, Illinois (Gorawara-Bhat); University of Rochester during the conduct of the Base, provided editing. Joseph J. Guido, MS, and Department of Supportive Care, City of Hope study. Ms Plumb reported receiving grants from the Javier Bautista, MS, MBA, University of Rochester National Medical Center, Duarte, California (Dale). University of Rochester during the conduct of the Cancer Center National Cancer Institute Community study. Dr Lowenstein reported receiving a contract Author Contributions: Dr Mohile had full access to Oncology Research Program Research Base, from PCORI during the conduct of the study. all the data in the study and takes responsibility for assisted with data management. Dr Rosenthal, Mr Dr Flannery reported receiving a contract from the integrity of the data and the accuracy of the Guido, and Mr Bautista were compensated for their PCORI and a grant from NCI during the conduct of data analysis. contributions. the study. Dr Magnuson reported receiving grants jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E7 Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment Additional Information: Dr Hurria is deceased. Full and mortality. Arch Intern Med. 2012;172(5):405-411. 28. Mohile S, Dale W, Hurria A. Geriatric oncology protocol is available through University of doi:10.1001/archinternmed.2011.1662 research to improve clinical care. Nat Rev Clin Oncol. Rochester NCORP: https://urcc-ccop.com/ccop/. 2012;9(10):571-578. doi:10.1038/nrclinonc.2012.125 14. Safran DG, Karp M, Coltin K, et al. Measuring patients’ experiences with individual primary care 29. Hamaker ME, Te Molder M, Thielen N, REFERENCES physicians: results of a statewide demonstration van Munster BC, Schiphorst AH, van Huis LH. 1. Arora NK, Street RL Jr, Epstein RM, Butow PN. project. J Gen Intern Med. 2006;21(1):13-21. doi:10. The effect of a geriatric evaluation on treatment Facilitating patient-centered cancer 1111/j.1525-1497.2005.00311.x decisions and outcome for older cancer patients— communication: a road map. Patient Educ Couns. a systematic review. J Geriatr Oncol. 2018;9(5): 15. Grunfeld E, Fitzpatrick R, Mant D, et al. 2009;77(3):319-321. doi:10.1016/j.pec.2009.11.003 430-440. doi:10.1016/j.jgo.2018.03.014 Comparison of breast cancer patient satisfaction 2. Street RL Jr, Elwyn G, Epstein RM. Patient with follow-up in primary care versus specialist 30. Caillet P, Canoui-Poitrine F, Vouriot J, et al. preferences and healthcare outcomes: an care: results from a randomized controlled trial. Br J Comprehensive geriatric assessment in the ecological perspective. Expert Rev Pharmacoecon Gen Pract. 1999;49(446):705-710. decision-making process in elderly patients with Outcomes Res. 2012;12(2):167-180. doi:10.1586/ cancer: ELCAPA study. J Clin Oncol. 2011;29(27): 16. Hospital value-based purchasing: biggest erp.12.3 3636-3642. doi:10.1200/JCO.2010.31.0664 bonuses and penalties: CMS percentage change in 3. Epstein RM, Duberstein PR, Fenton JJ, et al. reimbursement based on process performance and 31. Ramsdale E, Lemelman T, Loh KP, et al. Geriatric Effect of a patient-centered communication patient satisfaction. Mod Healthc. 2013;43(1):34. assessment-driven polypharmacy discussions intervention on oncologist-patient communication, between oncologists, older patients, and their 17. Mann RK, Siddiqui Z, Kurbanova N, Qayyum R. quality of life, and health care utilization in caregivers. J Geriatr Oncol. 2018;9(5):534-539. Effect of HCAHPS reporting on patient satisfaction advanced cancer: the VOICE randomized clinical doi:10.1016/j.jgo.2018.02.007 with physician communication. JHospMed. 2016;11 trial. JAMA Oncol. 2017;3(1):92-100. (2):105-110. doi:10.1002/jhm.2490 32. Lowenstein LM, Volk RJ, Street R, et al. 4. Bernacki R, Hutchings M, Vick J, et al. Communication about geriatric assessment 18. Mariano C, Hanson LC, Deal AM, et al. Development of the Serious Illness Care Program: domains in advanced cancer settings: “missed Healthcare satisfaction in older and younger a randomised controlled trial of a palliative care opportunities”. J Geriatr Oncol. 2019;10(1):68-73. patients with cancer. J Geriatr Oncol. 2016;7(1): communication intervention. BMJ Open. 2015;5 doi:10.1016/j.jgo.2018.05.014 32-38. doi:10.1016/j.jgo.2015.11.005 (10):e009032. doi:10.1136/bmjopen-2015-009032 33. Mohile S, Dale W, Magnuson A, Kamath N, 19. Institute of Medicine. Delivering High-Quality 5. Paladino J, Bernacki R, Neville BA, et al. Hurria A. Research priorities in geriatric oncology Cancer Care: Charting a New Course for a System in Evaluating an intervention to improve for 2013 and beyond. Cancer Forum. 2013;37(3): Crisis. Washington, DC: National Academies Press; communication between oncology clinicians and 216-221. patients with life-limiting cancer: a cluster 34. Campbell MK, Piaggio G, Elbourne DR, 20. Nekhlyudov L, Levit L, Hurria A, Ganz PA. randomized clinical trial of the Serious Illness Care Altman DG; CONSORT Group. Consort 2010 Patient-centered, evidence-based, and Program. JAMA Oncol. 2019;5(6):801-809. doi:10. statement: extension to cluster randomised trials. cost-conscious cancer care across the continuum: 1001/jamaoncol.2019.0292 BMJ. 2012;345:e5661. doi:10.1136/bmj.e5661 translating the Institute of Medicine report into 6. DeSantis CE, Miller KD, Dale W, et al. Cancer clinical practice. CA Cancer J Clin. 2014;64(6): 35. Hurria A, Gupta S, Zauderer M, et al. statistics for adults aged 85 years and older, 2019 408-421. doi:10.3322/caac.21249 Developing a cancer-specific geriatric assessment: [published online August 7, 2019]. CA Cancer J Clin. a feasibility study. Cancer. 2005;104(9):1998-2005. 21. Hurria A, Naylor M, Cohen HJ. Improving the doi:10.3322/caac.21577 doi:10.1002/cncr.21422 quality of cancer care in an aging population: 7. Smith BD, Smith GL, Hurria A, Hortobagyi GN, recommendations from an IOM report. JAMA. 2013; 36. Mohile SG, Velarde C, Hurria A, et al. Geriatric Buchholz TA. Future of cancer incidence in the 310(17):1795-1796. doi:10.1001/jama.2013.280416 assessment-guided care processes for older adults: United States: burdens upon an aging, changing a Delphi consensus of geriatric oncology experts. 22. Hurria A, Levit LA, Dale W, et al; American nation. J Clin Oncol. 2009;27(17):2758-2765. doi: J Natl Compr Canc Netw. 2015;13(9):1120-1130. Society of Clinical Oncology. Improving the 10.1200/JCO.2008.20.8983 doi:10.6004/jnccn.2015.0137 evidence base for treating older adults with cancer: 8. Mohile SG, Xian Y, Dale W, et al. Association of a American Society of Clinical Oncology statement. 37. Kehoe LA, Xu H, Duberstein P, et al. Quality of cancer diagnosis with vulnerability and frailty in J Clin Oncol. 2015;33(32):3826-3833. doi:10.1200/ life of caregivers of older patients with advanced older Medicare beneficiaries. J Natl Cancer Inst. JCO.2015.63.0319 cancer. J Am Geriatr Soc. 2019;67(5):969-977. 2009;101(17):1206-1215. doi:10.1093/jnci/djp239 doi:10.1111/jgs.15862 23. Mohile SG, Hurria A, Cohen HJ, et al. Improving 9. Mohile SG, Fan L, Reeve E, et al. Association of the quality of survivorship for older adults with 38. Hurria A, Wildes T, Blair SL, et al. Senior adult cancer with geriatric syndromes in older Medicare cancer. Cancer. 2016;122(16):2459-2568. doi:10. oncology, version 2.2014: clinical practice beneficiaries. J Clin Oncol. 2011;29(11):1458-1464. 1002/cncr.30053 guidelines in oncology. J Natl Compr Canc Netw. doi:10.1200/JCO.2010.31.6695 2014;12(1):82-126. doi:10.6004/jnccn.2014.0009 24. Magnuson A, Allore H, Cohen HJ, et al. Geriatric 10. Hurria A, Dale W, Mooney M, et al; Cancer and assessment with management in cancer care: 39. Vallerand RJ, O’Connor BP, Blais MR. Life Aging Research Group. Designing therapeutic current evidence and potential mechanisms for satisfaction of elderly individuals in regular clinical trials for older and frail adults with cancer: future research. J Geriatr Oncol. 2016;7(4):242-248. community housing, in low-cost community U13 conference recommendations. J Clin Oncol. doi:10.1016/j.jgo.2016.02.007 housing, and high and low self-determination 2014;32(24):2587-2594. doi:10.1200/JCO. nursing homes. Int J Aging Hum Dev. 1989;28(4): 25. Wildiers H, Heeren P, Puts M, et al. 2013.55.0418 277-283. doi:10.2190/JQ0K-D0GG-WLQV-QMBN International Society of Geriatric Oncology 11. Mohile SG, Dale W, Somerfield MR, et al. consensus on geriatric assessment in older patients 40. Fiscella K, Franks P, Srinivasan M, Kravitz RL, Practical assessment and management of with cancer. J Clin Oncol. 2014;32(24):2595-2603. Epstein R. Ratings of physician communication by vulnerabilities in older patients receiving doi:10.1200/JCO.2013.54.8347 real and standardized patients. Ann Fam Med. chemotherapy: ASCO guideline for geriatric 2007;5(2):151-158. doi:10.1370/afm.643 26. Fried TR, Bradley EH, Towle VR, Allore H. oncology. J Clin Oncol. 2018;36(22):2326-2347. Understanding the treatment preferences of 41. Shumway D, Griffith KA, Jagsi R, Gabram SG, doi:10.1200/JCO.2018.78.8687 seriously ill patients. N Engl J Med. 2002;346(14): Williams GC, Resnicow K. Psychometric properties 12. Mohile SG, Magnuson A, Pandya C, et al. 1061-1066. doi:10.1056/NEJMsa012528 of a brief measure of autonomy support in breast Community oncologists’ decision-making for cancer patients. BMC Med Inform Decis Mak. 2015; 27. Wildiers H, Mauer M, Pallis A, et al. End points treatment of older patients with cancer. J Natl 15:51. doi:10.1186/s12911-015-0172-4 and trial design in geriatric oncology research: Compr Canc Netw. 2018;16(3):301-309. doi:10. a joint European Organisation for Research and 42. Hsieh HF, Shannon SE. Three approaches to 6004/jnccn.2017.7047 Treatment of Cancer–Alliance for Clinical Trials in qualitative content analysis. Qual Health Res. 2005; 13. Fenton JJ, Jerant AF, Bertakis KD, Franks P. Oncology–International Society Of Geriatric 15(9):1277-1288. doi:10.1177/1049732305276687 The cost of satisfaction: a national study of patient Oncology position article. J Clin Oncol. 2013;31(29): satisfaction, health care utilization, expenditures, 3711-3718. doi:10.1200/JCO.2013.49.6125 E8 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research 43. Epstein RM, Franks P, Fiscella K, et al. quality assessments. Am J Manag Care. 2017;23 61. Karuturi M, Wong ML, Hsu T, et al. Measuring patient-centered communication in (10):618-622. Understanding cognition in older patients with patient-physician consultations: theoretical and cancer. J Geriatr Oncol. 2016;7(4):258-269. doi:10. 52. Tsai TC, Orav EJ, Jha AK. Patient satisfaction practical issues. Soc Sci Med. 2005;61(7):1516-1528. 1016/j.jgo.2016.04.004 and quality of surgical care in US hospitals. Ann Surg. doi:10.1016/j.socscimed.2005.02.001 2015;261(1):2-8. doi:10.1097/SLA. 62. Detmar SB, Muller MJ, Schornagel JH, 44. Cella DF, Tulsky DS, Gray G, et al. 0000000000000765 Wever LD, Aaronson NK. Health-related The Functional Assessment of Cancer Therapy quality-of-life assessments and patient-physician 53. Will KK, Johnson ML, Lamb G. Team-based care scale: development and validation of the general communication: a randomized controlled trial. JAMA. and patient satisfaction in the hospital setting: measure. J Clin Oncol. 1993;11(3):570-579. 2002;288(23):3027-3034. doi:10.1001/jama.288. a systematic review. J Patient Cent Res Rev. 2019;6 doi:10.1200/JCO.1993.11.3.570 23.3027 (2):158-171. doi:10.17294/2330-0698.1695 45. Ware J Jr, Kosinski M, Keller SDA. A 12-Item 63. Clayton JM, Butow PN, Tattersall MH, et al. 54. Brown H, Prescott R. Applied Mixed Models in Short-Form Health Survey: construction of scales Randomized controlled trial of a prompt list to help Medicine. 2nd ed. Edinburgh, UK: John Wiley & and preliminary tests of reliability and validity. Med advanced cancer patients and their caregivers to Sons, Ltd; 2006. Care. 1996;34(3):220-233. doi:10.1097/ ask questions about prognosis and end-of-life care. 55. Kenward MG, Roger JH. Small sample inference 00005650-199603000-00003 J Clin Oncol. 2007;25(6):715-723. doi:10.1200/JCO. for fixed effects from restricted maximum 2006.06.7827 46. Given CW, Given B, Stommel M, Collins C, likelihood. Biometrics. 1997;53(3):983-997. doi:10. King S, Franklin S. The caregiver reaction 64. Basch E, Deal AM, Kris MG, et al. Symptom 2307/2533558 assessment (CRA) for caregivers to persons with monitoring with patient-reported outcomes during 56. Loh KP, Mohile SG, Epstein RM, et al. chronic physical and mental impairments. Res Nurs routine cancer treatment: a randomized controlled Willingness to bear adversity and beliefs about the Health. 1992;15(4):271-283. doi:10.1002/nur. trial. J Clin Oncol. 2016;34(6):557-565. doi:10.1200/ curability of advanced cancer in older adults. Cancer. 4770150406 JCO.2015.63.0830 2019;125(14):2506-2513. doi:10.1002/cncr.32074 47. Hurria A, Mohile S, Gajra A, et al. Validation of a 65. Corre R, Greillier L, Le Caër H, et al. Use of a 57. Loh KP, Mohile SG, Lund JL, et al. Beliefs about prediction tool for chemotherapy toxicity in older comprehensive geriatric assessment for the advanced cancer curability in older patients, their adults with cancer. J Clin Oncol. 2016;34(20): management of elderly patients with advanced caregivers, and oncologists. Oncologist. 2019;24(6): 2366-2371. doi:10.1200/JCO.2015.65.4327 non-small-cell lung cancer: the phase III e292-e302. doi:10.1634/theoncologist.2018-0890 randomized ESOGIA-GFPC-GECP 08-02 study. 48. van Buuren S. Multiple imputation of discrete 58. Guetterman TC, Fetters MD, Creswell JW. J Clin Oncol. 2016;34(13):1476-1483. doi:10.1200/ and continuous data by fully conditional Integrating quantitative and qualitative results in JCO.2015.63.5839 specification. Stat Methods Med Res. 2007;16(3): health science mixed methods research through 219-242. doi:10.1177/0962280206074463 66. Bakitas M, Lyons KD, Hegel MT, et al. Effects of joint displays. Ann Fam Med. 2015;13(6):554-561. a palliative care intervention on clinical outcomes in 49. Curran D, Molenberghs G, Thijs H, Verbeke G. doi:10.1370/afm.1865 patients with advanced cancer: the Project ENABLE Sensitivity analysis for pattern mixture models. 59. Singh H, Beaver JA, Kim G, Pazdur R. II randomized controlled trial. JAMA. 2009;302(7): J Biopharm Stat. 2004;14(1):125-143. doi:10.1081/ Enrollment of older adults on oncology trials: an 741-749. doi:10.1001/jama.2009.1198 BIP-120028510 FDA perspective. J Geriatr Oncol. 2017;8(3):149-150. 67. Hahn S, Puffer S, Torgerson DJ, Watson J. 50. Bleustein C, Rothschild DB, Valen A, Valatis E, doi:10.1016/j.jgo.2016.11.001 Methodological bias in cluster randomised trials. Schweitzer L, Jones R. Wait times, patient 60. Puts MT, Santos B, Hardt J, et al. An update on BMC Med Res Methodol. 2005;5:10. doi:10.1186/ satisfaction scores, and the perception of care. Am J a systematic review of the use of geriatric 1471-2288-5-10 Manag Care. 2014;20(5):393-400. assessment for older adults in oncology. Ann Oncol. 51. Ehlers AP, Khor S, Cizik AM, et al. Use of 2014;25(2):307-315. doi:10.1093/annonc/mdt386 patient-reported outcomes and satisfaction for jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E9 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png JAMA Oncology Pubmed Central

Loading next page...
 
/lp/pubmed-central/communication-with-older-patients-with-cancer-using-geriatric-8avspg0kk0

References (188)

Publisher
Pubmed Central
Copyright
Copyright 2019 Mohile SG et al. JAMA Oncology.
ISSN
2374-2437
eISSN
2374-2445
DOI
10.1001/jamaoncol.2019.4728
Publisher site
See Article on Publisher Site

Abstract

Research JAMA Oncology | Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment A Cluster-Randomized Clinical Trial From the National Cancer Institute Community Oncology Research Program Supriya G. Mohile, MD, MS; Ronald M. Epstein, MD; Arti Hurria, MD; Charles E. Heckler, PhD, MS; Beverly Canin; Eva Culakova, PhD, MS; Paul Duberstein, PhD; Nikesha Gilmore, PhD; Huiwen Xu, MHA; Sandy Plumb, BS; Megan Wells, MPH; Lisa M. Lowenstein, PhD; Marie A. Flannery, PhD; Michelle Janelsins, PhD, MPH; Allison Magnuson, DO; Kah Poh Loh, MB, BCh, BAO; Amber S. Kleckner, PhD; Karen M. Mustian, PhD, MPH; Judith O. Hopkins, MD; Jane Jijun Liu, MD; Jodi Geer; Rita Gorawara-Bhat, PhD; Gary R. Morrow, PhD, MS; William Dale, MD, PhD Invited Commentary IMPORTANCE Older patients with cancer and their caregivers worry about the effects of Supplemental content cancer treatment on aging-related domains (eg, function and cognition). Quality conversations with oncologists about aging-related concerns could improve patient-centered outcomes. A geriatric assessment (GA) can capture evidence-based aging-related conditions associated with poor clinical outcomes (eg, toxic effects) for older patients with cancer. OBJECTIVE To determine whether providing a GA summary and GA-guided recommendations to oncologists can improve communication about aging-related concerns. DESIGN, SETTING, AND PARTICIPANTS This cluster-randomized clinical trial enrolled 541 participants from 31 community oncology practices within the University of Rochester National Cancer Institute Community Oncology Research Program from October 29, 2014, to April 28, 2017. Patients were aged 70 years or older with an advanced solid malignant tumor or lymphoma who had at least 1 impaired GA domain; patients chose 1 caregiver to participate. The primary outcome was assessed on an intent-to-treat basis. INTERVENTIONS Oncology practices were randomized to receive either a tailored GA summary with recommendations for each enrolled patient (intervention) or alerts only for patients meeting criteria for depression or cognitive impairment (usual care). MAIN OUTCOMES AND MEASURES The predetermined primary outcome was patient satisfaction with communication about aging-related concerns (modified Health Care Climate Questionnaire [score range, 0-28; higher scores indicate greater satisfaction]), measured after the first oncology visit after the GA. Secondary outcomes included the number of aging-related concerns discussed during the visit (from content analysis of audiorecordings), quality of life (measured with the Functional Assessment of Cancer Therapy scale for patients and the 12-Item Short Form Health Survey for caregivers), and caregiver satisfaction with communication about aging-related patient concerns. RESULTS A total of 541 eligible patients (264 women, 276 men, and 1 patient did not provide data; mean [SD] age, 76.6 [5.2] years) and 414 caregivers (310 women, 101 men, and 3 caregivers did notprovidedata;meanage,66.5[12.5]years)wereenrolled.Patientsintheinterventiongroupwere moresatisfiedafterthevisitwithcommunicationaboutaging-relatedconcerns(differenceinmean score, 1.09 points; 95% CI, 0.05-2.13 points; P = .04); satisfaction with communication about aging-relatedconcernsremainedhigherintheinterventiongroupover6months(differenceinmean score, 1.10; 95% CI, 0.04-2.16; P = .04). There were more aging-related conversations in the intervention group’s visits (difference, 3.59; 95% CI, 2.22-4.95; P < .001). Caregivers in the intervention group were more satisfied with communication after the visit (difference, 1.05; 95% CI, 0.12-1.98; P = .03). Quality of life outcomes did not differ between groups. Author Affiliations: Author affiliations are listed at the end of this CONCLUSIONS AND RELEVANCE Including GA in oncology clinical visits for older adults with article. advanced cancer improves patient-centered and caregiver-centered communication about Corresponding Author: Supriya G. aging-related concerns. Mohile, MD, MS, Department of Medicine, University of Rochester, TRIAL REGISTRATION ClinicalTrials.gov identifier: NCT02107443 601 Elmwood Ave, PO Box 704, Rochester, NY 14642 JAMA Oncol. doi:10.1001/jamaoncol.2019.4728 (supriya_mohile@urmc. Published online November 7, 2019. rochester.edu). (Reprinted) E1 Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment atient-centered communication promotes high- quality conversations prioritizing patient and care- Key Points P giver concerns so that decisions are aligned with their Question Does providing a summary of geriatric assessment preferences and values. Effective communication is charac- results and geriatric assessment–guided recommendations to terized by (1) informed and participatory patients and care- oncologists improve communication about aging-related givers; (2) informed, receptive, and patient-centered clini- concerns? cians; and (3) a health care system providing well-organized Findings In this nationwide cluster-randomized clinical trial of and responsive services that are tailored to patients’ and care- 31 community oncology practices that enrolled 541 older patients 1,2 givers’ needs. Although studies have demonstrated ben- with advanced cancer, providing a geriatric assessment summary efits for interventions that facilitate oncologist-patient with recommendations to oncologists improved postvisit patient 3-5 satisfaction and caregiver satisfaction and increased the number communication, these interventions were not tailored to ad- of conversations about aging-related concerns. These results were dress aging-related concerns of older adults receiving cancer significantly different between the intervention and usual care treatment and their caregivers. groups. Older adults represent most patients with advanced 6,7 Meaning Integrating geriatric assessment into community cancer seen in community oncology practices. Cancer oncology care improves patient and caregiver satisfaction and treatment choices for older adults with aging-related communication about aging-related concerns. conditions (ie, disability, comorbidity, and geriatric syn- 8,9 dromes) are based on extrapolations of evidence derived from clinical trials that enroll younger patients or fit older adults. Many older adults have unidentified, Methods uncommunicated, and therefore unaddressed aging- related conditions that are associated with morbidity Overview and early mortality. A communication intervention for In this cluster-randomized clinical trial, Improving Commu- oncologists who care primarily for older adults—yet nication in Older Cancer Patients and Their Caregivers lack aging-related expertise—could improve patient (COACH), community oncology practices were randomized to and caregiver satisfaction by bringing attention to often- the intervention or usual care group (CONSORT diagram in 12 13 34 overlooked aging-related conditions. Despite controversy, Figure 1 and trial protocol in Supplement 1). We enrolled par- satisfaction with physician communication is considered ticipants from October 29, 2014, to April 28, 2017. The Uni- a metric for quality of health care and even modest improve- versity of Rochester and all participating sites obtained ap- ments in survey scores are linked to increased reim- proval from their institutional review boards. Participants 14-18 bursement. provided written informed consent. 19(p1) To address a “cancer care delivery system in crisis,” the National Academy of Medicine (formally the Institute of Settings and Participants 20,21 Medicine), the American Society of Clinical Oncology We recruited community oncology practices within the Uni- 22 10,23,24 (ASCO), the Cancer and Aging Research Group, and versity of Rochester National Cancer Institute Community On- the International Society of Geriatric Oncology, have all cology Research Program (NCORP) Research Base network. On- called for improved care delivery that attends to aging- cologists enrolled as participants ; only patients of enrolled related conditions of older adults with cancer. A key compo- oncologists were eligible to participate. Other patient eligibil- nent is geriatric assessment (GA), which uses validated ity criteria included aged 70 years or older, at least 1 GA domain 11,25,35-37 patient-reported and objective measures to capture domains impairment, an advanced solid tumor or lymphoma, important to older adults such as function (ie, ability to cancer treatment with palliative intent, planned oncology vis- remain independent) and cognition. As highlighted in a its for at least 3 months, ability to provide informed consent recent ASCO guideline, older adults and caregivers value independently or via a health care proxy, and an understand- 26,27 these GA domains, and GA domains, when formally ing of English. Eligible patients chose 1 caregiver aged 21 years 11,12,28-30 assessed, influence treatment decision-making. or older. Patients with no eligible caregivers could still enroll However, aging-related concerns are rarely addressed in in the study. oncology care, especially outside specialized academic 12,31,32 settings. Study Groups To our knowledge, this study is the first randomized All patients underwent a GA that evaluated 8 domains— clinical trial evaluating whether GA can meaningfully functional status, physical performance, comorbidity, poly- influence oncology care processes for vulnerable older pharmacy, cognition, nutrition, psychological health, and so- 11,25,35-37 37 adults with advanced cancer. With outcome measure cial support. The GA was mostly patient reported. selection guided by input from older patients and Trained coordinators (J.G.) completed the objective perfor- 23,33 caregivers, we hypothesized that providing GA informa- mance and cognitive measures. At practices that were ran- tion to oncologists would improve patient satisfaction with domized to the intervention group, coordinators entered the communication about aging-related concerns by increasing GA scores into a locked web-based folder (http://www.mycarg. the number and quality of conversations during oncology org) that created a tailored GA summary that was printed out clinic visits. for each patient. The summary included information on GA E2 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research Figure 1. CONSORT Flow Diagram for the COACH (Improving Communication in Older Cancer Patients and Their Caregivers) Trial of Practice Clusters, Oncologists, Patients, and Caregivers 552 NCORP component sites contacted 274 NCORP component sites chose not to participate and did not obtain IRB approval 278 Component sites agreed to participate and obtained IRB approval (preclustered practice sites) 85 Practice site clusters 54 Excluded 35 Active clusters never enrolled participants 17 Clusters inactivated study 2 Clusters no longer affiliated 31 Practice site clusters that enrolled patients and caregivers 610 Patients screenedc 64 Excluded 33 Withdrawals 31 Screening failures 31 Practice site clusters randomized (546 patients, 417 caregivers, 132 physicians) 17 Practice sites allocated to intervention 14 Practice sites allocated to usual care 296 Patients 250 Patients 233 Caregivers 184 Caregivers 64 Physicians 68 Physicians Protocol violation Protocol violation 3 Patients 2 Patients 2 Caregivers 1 Caregivers 1 Physician 293 Patients 248 Patients 231 Caregivers 183 Caregivers 63 Physicians 68 Physicians Withdrew Withdrew 2 Patients 3 Patients 2 Caregivers 2 Caregivers Died 290 Patients 245 Patients 1 Patient 229 Caregivers 181 Caregivers 63 Physicians 68 Physicians d e d e Primary aim Secondary aim 1 Primary aim Secondary aim 1 No audio captured No HCCQ 4 Patients 6 Patients No HCCQ No audio captured Protocol violation Answered 2 HCCQ 19 Patients 1 Patient 2 Patients questions 1 Physician 1 Patient Included in primary analysis Included in secondary analysis Included in primary analysis Included in secondary analysis 271 Patients 284 Patients 238 Patients 244 Patients 211 Caregivers 225 Caregivers 177 Caregivers 180 Caregivers 63 Physicians 62 Physicians 67 Physicians 68 Physicians Follow-up at 4 to 6 weeks included 472 patients, at 3 months included 410 Institute Community Oncology Research Program (NCORP) affiliate or with patients, and at 6 months included 348 patients. Follow-up included 348 the University of Rochester NCORP Research Base. caregivers at 4 to 6 weeks, 306 caregivers at 3 months, and 261 caregivers at c Signed consent and participated in screening process. 6 months. HCCQ indicates Health Care Climate Questionnaire. Satisfaction with communication about aging-related concerns. Clusters that maintained institutional review board (IRB) approval but never Conversations about aging-related conditions during clinic visit. enrolled any participants. Irretrievable, site miscommunication, technical difficulty, or protocol violation. Practices are no longer associated with their respective National Cancer jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E3 Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment domain impairments and GA-guided recommendations based Randomization and Blinding 11 38 36 on literature review, guidelines, and expert consensus. Accrual records from University of Rochester NCORP studies As an example, the summary would include information were used to stratify practice clusters as large or small accru- that a patient recently fell, that falls increase the risk of ing sites to assure balance in randomization. Randomization chemotherapy toxic effects, and a recommendation for physical was done at the practice cluster level and recruitment of all par- therapy to prevent falls. The summary and recommendations ticipants was based on the group to which their practice clus- were provided to oncologists once prior to an audiorecorded ter was assigned. Other than the statisticians, all investiga- clinic visit. At study entry, oncologists received a brief training tors were blinded to group; blinding was preserved among the about GA and were told that they had autonomy for if and how telephone team, transcriptionists, and coders. they wished to use GA for their enrolled patients. For the usual care group, oncologists were alerted only if patients had Sample Size abnormal scores on depression and cognitive tests. Sample size and power considerations were based on the pri- mary aim of the HCCQ-age to address patient satisfaction with communication about aging-related concerns. This design had Data Collection and Outcome Measures In both groups, 1 oncology clinic visit within 4 weeks of GA 80% power at the 0.05 significance level to detect a differ- was audiorecorded and transcribed. Within 7 to 14 days of ence of 1.3 in HCCQ-age scores, with an intraclass correlation 3,32 this visit, trained personnel called the patient to assess satis- coefficient (ICC) of 0.14, corresponding to an effect size of faction with communication. During the telephone call, the 0.62. Assuming a withdrawal rate of 5% (based on observa- patients completed 2 versions of the Health Care Climate tional cohort data ), the targeted accrual was 528 patients. The 39,40 Questionnaire (HCCQ). The first version measures satis- design had 80% power at the 0.05 significance level to detect faction with patient-centered physician communication, a difference of 0.46 in the number of conversations about such as whether the patient feels that the physician under- aging-related concerns, with an ICC of 0.12, corresponding to stands her or his perspective and encourages participation an effect size of 0.59. We originally aimed for participation in decisions (score range, 0-20; higher scores indicate by 16 NCORP practices. Because the recruitment was initially greater satisfaction). Similar to other research, the second slower than anticipated, we allowed more practices to partici- version of the HCCQ modified the language of the questions pate (as specified by the trial protocol in Supplement 1). The in the HCCQ to address satisfaction with communication total patient sample size did not change. regarding aging-related concerns (HCCQ-age; score range, 0-28); this modified version of the HCCQ was designed with Statistical Analysis input from advocates who were not enrolled in the trial Descriptive statistics were used to evaluate demographics, GA and was used for the primary outcome (eAppendix in results, and clinical information, and bivariate analyses were Supplement 2). performed to compare between- group differences in charac- A secondary outcome included the number of aging- teristics of patients and caregivers. For the primary outcome, related concerns discussed at the visit. With experts and 4 cod- to follow the intent-to-treat principle and to assess the effect ers, a content analysis framework outlined how to identify of missing values on the study results, we conducted addi- aging-related conversations, assess their quality (whether a tional analyses including all randomized eligible patients. concern was acknowledged and further explored by the on- Under missing at random assumptions, we evaluated the in- cologist), and determine whether an acknowledged concern fluence of missing data on the study results via multiple motivated recommendations for specific GA-guided imputation. The examination of the reasons for missing 3,11,31,32,36,43 interventions. Team coding of the transcribed au- data did not reveal any reason to suspect a missing not at ran- diorecordings occurred until interrater reliability was 70% dom mechanism. Nevertheless, we also applied sensitivity or greater. Subsequently, for each transcript, coding was per- analysis using pattern mixture models. Similar to prior 50,51 formed independently by 2 trained coders, with 20% of tran- research, we conducted responder analyses evaluating the scripts coded by all 4 coders. Final interrater reliability was 82% proportion of participants who reported satisfaction scores for number of concerns and 92% for both quality and inter- within a half SD of the HCCQ score from the perfect score; ventions. achieving a perfect satisfaction score is commonly advocated 52,53 Other secondary outcomes evaluated patient and care- as a metric for high quality in practice. giver quality of life (QoL) as well as caregiver satisfaction Because of the cluster-randomized study design, a linear with communication. Patients completed the Functional mixed model method was applied. The outcome was the re- Assessment of Cancer Therapy scale at enrollment and 4 to sponse, and the group was the fixed effect. Practices were en- 6 weeks, 3 months, and 6 months later. Caregiver QoL was tered as a random effect independent of residual error. Esti- assessed using the 12-Item Short Form Survey and burden mation was performed using restricted maximum likelihood, was assessed using the Caregiver Reaction Assessment at and the null hypothesis of zero mean difference between the same time points as patients. Caregivers completed groups was tested using an F test. The results are presented HCCQ surveys that assessed their satisfaction with commu- as means (or mean difference) adjusted for the practice effect nication about their concerns related to the patient’s aging- and evaluated as marginal means from the linear mixed model. related conditions and overall care (score range for both Practice differences were assessed graphically using best lin- surveys, 0-20). ear unbiased predictors of the mean response for each. E4 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research Figure 2. Patient and Caregiver Satisfaction A Patient satisfaction with communication B Patient satisfaction with overall care C Caregiver satisfaction with communication 25 18.0 18 17.5 17.0 16.5 16.0 Intervention Usual care 15.5 18 15.0 13 Telephone 4-6 wk 3 mo 6 mo Telephone 4-6 wk 3 mo 6 mo 4-6 wk 3 mo 6 mo Assessment Assessment Assessment A, Patient satisfaction with communication about aging-related concerns. B, Patient satisfaction with overall care. C, Caregiver satisfaction with communication about the patient’s age-related conditions. Scores were derived using modified versions of the Health Care Climate Questionnaire. The telephone assessment was 7 to 14 days after the audio-recorded clinic visit. To assess the effect of the intervention on the outcomes [33.1%] vs 74 of 293 [25.3%]; P = .05) (eFigure in Supple- over time, we used a longitudinal linear mixed model. An un- ment 2). Caregivers (n = 414; mean [SD] age, 66.5 [12.5] years; structured correlation matrix was used for the repeated mea- range, 26-92 years) were most likely to be the patient’s sures from the same participant. The model was adjusted spouse or partner (276 [66.7%]; eTable 2 in Supplement 2) and for practice cluster using a random effect independent of the 310 [74.9%] were women. Baseline data for oncologists, 37,56,57 37,56,57 within-participant random effects, and it was fit via re- patients, and caregivers have been published. stricted maximum likelihood. Every effort was made to facilitate participants’ comple- Patient Satisfaction With Communication tion of questionnaires. However, baseline data from some par- For 509 evaluable patients, the mean (SE) satisfaction score ticipants were missing, and there was participant withdrawal for communication about aging-related concerns was 22.8 (Figure 1); anticipating that some patients would not be able (0.27) (range, 5-28 for HCCQ-age) after the clinic visit. The score to be reached by telephone, the protocol allowed for imputa- in the intervention group was 1.09 points higher than in the tion of the 4- to 6-week HCCQ results to assess the primary aim. usual care group (95% CI, 0.05-2.13; P = .04; ICC = 0.02). Af- Analysis was performed with SAS, version 9.4 (SAS Institute ter the clinic visit, the mean (SE) satisfaction score for com- Inc) and R, version 3.5.2 (R Foundation for Statistical Com- munication about overall care was 17.4 (0.16) (range, 5-20 for puting) software. All P values were from 2-sided tests, and the HCCQ). The proportion of patients within a half SD from a per- results were deemed statistically significant at P < .05. fect score was higher in the intervention group (109 of 271 [40.2%] vs 71 of 238 [29.8%]). Over 6 months, patients in the intervention group were more satisfied with communication about aging-related concerns (difference in mean HCCQ-age Results score, 1.10; 95% CI, 0.04-2.16; P =.04) (Figure 2A) and re- Participant Characteristics ported greater satisfaction with overall care (difference in mean From October 29, 2014, to April 28, 2017, 31 practice clusters HCCQ score, 0.70; 95% CI, 0.06-1.25; P = .03) (Figure 2B). (17 intervention and 14 usual care) enrolled participants, in- cluding 131 oncologists, 541 eligible patients, and 414 eligible Number and Quality of Conversations caregivers (Figure 1). Patients had a mean (SD) age of 76.6 (5.2) About Aging-Related Concerns years (range, 70-96 years), and 264 (48.8%) were women; most For 528 evaluable patients, the adjusted mean (SE) number patients had gastrointestinal and lung cancers (278 [51.4%]) of conversations about aging-related concerns during the and were receiving chemotherapy (369 [68.2%]) (eTable 1 in oncology clinic visit was 6.34 (0.48) (range, 0-18). There was Supplement 2). There were no essential differences in demo- an adjusted mean of 8.02 conversations in the intervention graphics or clinical characteristics by group. Most patients had group compared with 4.43 in usual care (difference, 3.59; 2 or more GA domain impairments (mean [SD], 4.5 [1.5]); the 95% CI, 2.22-4.95; P < .001; ICC = 0.14; Figure 3). The inter- prevalence of GA domain impairments ranged from 93.7% vention group had an adjusted mean of 4.60 high-quality (n = 507) for physical performance to 25.1% (n = 136) for psy- conversations, compared with 2.59 in the usual care group chological status; 180 patients (33.3%) had possible cognitive (difference, 2.01 [adjusted by practice site]; 95% CI, 1.20- impairment. A total of 487 of 541 patients (90.0%) had 3 or 2.77; P < .001; ICC = 0.06). There was an adjusted mean of more GA domain impairments. More patients in the usual care 3.20 conversations about recommendations in the interven- group had impaired physical performance (239 of 248 [96.4%] tion group compared with 1.14 in the usual care group vs 268 of 293 [91.5%]; P = .03) and social support (82 of 248 (difference, 2.06; 95% CI, 0.99-3.12; P < .001; ICC = 0.30). jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E5 Score Score Score Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment patients represent less-fit individuals for whom there is lim- Figure 3. Conversations About Aging-Related Conditions ited evidence for the risks and benefits of cancer treatment, yet these patients are commonly seen in real-world commu- P<.001 9 Intervention Usual care nity practices. Although patients had various cancer types, all were incurable and were treated with palliative intent. Evidence increasingly supports the use of GA for evalua- tion and management of older patients with cancer to P<.001 5 guide shared decision-making between older patients, care- P<.001 11,25 4 givers, and oncologists. As highlighted in the ASCO geri- atric oncology guidelines and supported by systematic 29,60 reviews, GA impairments are associated with chemo- therapy toxic effects, lower treatment completion, func- tional decline, early mortality, and higher health care use. All Age-Related Higher-Quality Conversations Like others, we found that older patients with a high preva- Conversations Age-Related With GA-Driven lence of GA domain impairments still receive treatment for Conversations Recommendations advanced cancer, including chemotherapy. Of particular The patient’s visit with the oncologist within 4 weeks of completing the geriatric concern is the one-third of patients who had positive screen- assessment (GA) was audiorecorded, transcribed, and coded. We used an open coding approach of themes and subthemes to quantify the number of ing results for possible cognitive impairment, given the lim- age-related conversations, the number of aging-related discussions with ited evidence for the safety and efficacy of chemotherapy in high-quality communication, and the number of conversations of GA-driven this group. The higher prevalence of GA domain impair- recommendations communicated to patients by oncologists. ments compared with other trials reflects our expanded eli- gibility criteria and our use of a formal GA to evaluate often eTable 3 in Supplement 2 is a joint display illustrating overlooked aging-related conditions. exemplar quotes with mean conversation numbers by Despite patient and caregiver concerns and preferences for 26,27 domain. maintaining function and cognition, oncologists often do not discuss implications of aging-related conditions or in- form older patients and caregivers of heightened risk of ad- Patients’ and Caregivers’ Health-Related Quality of Life Analyses did not detect any statistically significant differ- verse events from treatment. We found that, when GA in- ences between groups in Functional Assessment of Cancer formation was provided, community oncologists used it in Therapy scale score for patients over 6 months (range, 23- communication during the clinic visit, similar to other non- 108; difference [SE], −0.23 [1.03]; P = .82). In addition, there geriatric studies that have systematically provided symptom 62,63 were no differences for caregiver 12-Item Short Form Survey and QoL information to oncologists. Our results align with total scores or Caregiver Reaction Assessment subscales. this research showing that coordinated care for younger pa- tients that captures patient-reported outcomes improves qual- ity of care and outcomes; for older patients with cancer, per- Caregiver Satisfaction With Communication At 4 to 6 weeks after the clinic visit, caregivers in the inter- sonalized care requires attention to aging-related conditions. vention group were more satisfied with their communication We recruited older patients who had several different can- regarding their concerns about the patients’ aging-related cers and treatments, which may have limited our ability to de- conditions (range, 5-20; difference, 1.05; 95% CI, 0.12-1.98; tect QoL effects. In addition, the intervention provided a GA P = .03). The proportion of caregivers within a half SD of a per- summary during 1 clinic visit only to oncologists; studies fect score was higher in the intervention group (74 of 189 that have reported survival and QoL benefits from structured [39.2%] vs 42 of 158 [26.6%]). Caregivers were more satisfied interventions have incorporated evaluation and manage- with their own communication with oncologists with regard ment of patient-reported outcomes over time or have used 29,64 to overall care (range, 2-20; difference, 1.34; 95% CI, 0.50- geriatrics-trained professionals. A randomized study of 2.18; P = .004). The differences in satisfaction scores were not GA-directed therapy for older patients with advanced lung significant when analyzed over 6 months (Figure 2C). cancer demonstrated reduced toxic effects of treatment and less treatment discontinuation in the GA group owing to im- proved treatment allocation. Several ongoing clinical trials will evaluate if GA can help improve clinical outcomes (QoL, Discussion toxic effects, and survival) of patients through improved The COACH cluster-randomized clinical trial is the first large decision-making and GA-guided interventions. multisite intervention study to demonstrate that providing a A previous study using baseline COACH data reported that an increasing number of patient GA domain impairments is as- GA summary with GA-guided recommendations to commu- nity oncologists facilitates communication about aging- sociated with poor caregiver emotional health and QoL. Simi- related concerns and improves patient and caregiver satisfac- lar to early palliative care models that used specialized nurse tion with communication and care. COACH enrolled vulnerable coaches to assess and provide management for patients and older patients with cancer who had significant aging-related caregivers, GA-based interventions could be adapted for both conditions—90% had 3 or more GA domain impairments. These patients and caregivers. E6 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Conversations, No., Adjusted Mean (95% CI) Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research blinded, and thus may have modified their discussions of ag- Strengths and Limitations Strengths of this study include recruitment of a large sample ing; however, the strength of the findings shows that modify- of vulnerable older patients and their caregivers who have ing oncologist behavior to increase communication about ag- rarely been included in cancer trials. This study also demon- ing-related concerns is possible. strates the ability to conduct multisite trials incorporating GA in the community oncology setting. We attribute our success- ful completion of the trial in large part to our patient and care- Conclusions giver research advocate partners from Scoreboard (Stakehold- ers for Care in Oncology and Research for our Elders) who To our knowledge, the COACH cluster-randomized clinical trial 23,33 provided ongoing input and solutions for barriers. is the first trial to demonstrate that provision of a formal GA Limitations include risk of selection bias, as we enrolled a to community oncologists, per ASCO guidelines, can im- specific population of older patients; however, these are pa- prove satisfaction and communication for vulnerable older pa- tients who are commonly seen in community oncology clin- tients with advanced cancer and their caregivers. COACH dem- ics and are underrepresented in research. Although cluster ran- onstrated that a practical and convenient GA summary with domization is a strength, since we were testing a model of care recommendations for aging-sensitive interventions im- as an intervention, there is a risk of selection bias inherent in proves patient-centered outcomes and thus should be consid- cluster randomization. Oncologists in both groups were not ered as the standard of care for older patients with cancer. ARTICLE INFORMATION Concept and design: Mohile, Hurria, Heckler, Canin, from the University of Rochester during the Duberstein, Plumb, Mustian, Hopkins, Dale. conduct of the study. Dr Kleckner reported Accepted for Publication: August 22, 2019. Acquisition, analysis, or interpretation of data: receiving grants from NCI during the conduct of the Published Online: November 7, 2019. All authors. study. Dr Morrow reported receiving a grant from doi:10.1001/jamaoncol.2019.4728 Drafting of the manuscript: Mohile, Hurria, Heckler, NCI and a contract from PCORI during the conduct Open Access: This is an open access article Canin, Xu, Janelsins, Kleckner, Mustian, Hopkins, of the study; and grants from NCI outside the distributed under the terms of the CC-BY License. Dale. submitted work. No other disclosures were © 2019 Mohile SG et al. JAMA Oncology. Critical revision of the manuscript for important reported. intellectual content: Mohile, Epstein, Heckler, Author Affiliations: Department of Medicine, Funding/Support: This study was partially funded Culakova, Duberstein, Gilmore, Xu, Plumb, Wells, University of Rochester, Rochester, New York by the Patient-Centered Outcomes Research Lowenstein, Flannery, Janelsins, Magnuson, Loh, (Mohile, Xu, Plumb, Wells, Magnuson, Loh); Institute (contract CD-12-11-4634 to Dr Mohile). Kleckner, Mustian, Hopkins, Liu, Geer, University of Rochester Cancer Center National Support also came from the National Institute of Gorawara-Bhat, Morrow, Dale. Cancer Institute Community Oncology Research Aging grant R21/R33AG059206 (Drs Mohile, Hurria, Statistical analysis: Mohile, Hurria, Heckler, Program Research Base, Rochester, New York and Dale), National Cancer Institute grant Culakova, Xu, Wells. (Mohile, Heckler, Canin, Culakova, Gilmore, Xu, UG1CA189961 (Drs Mustian and Morrow), National Obtained funding: Mohile, Hurria, Morrow, Dale. Plumb, Wells, Flannery, Janelsins, Magnuson, Loh, Cancer Institute grant R25CA102618 (Drs Janelsins Administrative, technical, or material support: Kleckner, Mustian, Morrow); Department of Family and Morrow), and National Institute of Aging grant Mohile, Hurria, Gilmore, Xu, Plumb, Wells, Medicine, University of Rochester, Rochester, K24AG056589 (Dr Mohile). Lowenstein, Flannery, Magnuson, Loh, Kleckner, New York (Epstein); Department of Medical Role of the Funder/Sponsor: The funding sources Morrow, Dale. Oncology, City of Hope National Medical Center, had no role in the design and conduct of the study; Supervision: Mohile, Janelsins, Magnuson, Mustian, Duarte, California (Hurria); Department of Surgery, collection, management, analysis, and Morrow, Dale. University of Rochester, Rochester, New York interpretation of the data; preparation, review, or (Heckler, Culakova, Gilmore, Janelsins, Kleckner, Conflict of Interest Disclosures: Dr Mohile approval of the manuscript; and decision to submit Mustian, Morrow); Stakeholders for Care in reported receiving a grant from the National Cancer the manuscript for publication. Oncology and Research for our Elders, Rochester, Institute (NCI) and a contract from the Disclaimer: The information presented in this New York (Canin); Department of Health Behavior, Patient-Centered Outcomes Research Institute manuscript is solely the responsibility of the author Society, and Policy, Rutgers University School of (PCORI) during the conduct of the study; and (s) and does not necessarily represent the views of Public Health, Piscataway, New Jersey receiving grants from Carevive outside the the PCORI, its Board of Governors, or Methodology (Duberstein); Department of Health Services submitted work. Dr Epstein reported receiving Committee. All information and materials published Research, University of Texas MD Anderson Cancer grants from NCI and American Cancer Society in the primary manuscript are original. Center, Houston (Lowenstein); University of during the conduct of the study. Dr Hurria reported Rochester School of Nursing, Rochester, New York receiving a contract from PCORI during the conduct Data Sharing Statement: See Supplement 3. (Flannery); Novant Health Oncology Specialists, of the study; and consulting payments from Additional Contributions: We thank all the Winston-Salem, North Carolina (Hopkins); Celgene, Novartis, GSK, Boehringer Ingelheim, patients and caregivers of SCOREboard: Beverly Southeast Clinical Oncology Research Consortium Carevive, Sanofi, GTx Inc, Pierian Biosciences, and Canin (Chair), Mary Whitehead, Margaret National Cancer Institute Community Oncology MJH Healthcare Holdings LLC outside the Sedenquist, Lorraine Griggs, Lynn Finch, John Research Program, Winston-Salem, North Carolina submitted work. Dr Canin reported receiving Aarne, Valerie Targia, Robert Harrison (deceased), (Hopkins); Heartland Cancer Research National personal fees from the University of Rochester Valerie Aarne, Dorothy Dobson, Jacquelyn Dobson, Cancer Institute Community Oncology Research during the conduct of the study. Dr Culakova Burt Court, Polly Hudson, and Ray Hutchins Program, Decatur, Illinois (Liu); Metro Minnesota reported receiving a grant from NCI and a contract (deceased). Susan Rosenthal, MD, University of Community Oncology Research Program, St Louis from PCORI during the conduct of the study. Rochester Cancer Center National Cancer Institute Park (Geer); Department of Medicine, University of Dr Gilmore reported receiving grants from the Community Oncology Research Program Research Chicago, Chicago, Illinois (Gorawara-Bhat); University of Rochester during the conduct of the Base, provided editing. Joseph J. Guido, MS, and Department of Supportive Care, City of Hope study. Ms Plumb reported receiving grants from the Javier Bautista, MS, MBA, University of Rochester National Medical Center, Duarte, California (Dale). University of Rochester during the conduct of the Cancer Center National Cancer Institute Community study. Dr Lowenstein reported receiving a contract Author Contributions: Dr Mohile had full access to Oncology Research Program Research Base, from PCORI during the conduct of the study. all the data in the study and takes responsibility for assisted with data management. Dr Rosenthal, Mr Dr Flannery reported receiving a contract from the integrity of the data and the accuracy of the Guido, and Mr Bautista were compensated for their PCORI and a grant from NCI during the conduct of data analysis. contributions. the study. Dr Magnuson reported receiving grants jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E7 Research Original Investigation Communication With Older Patients With Cancer Using Geriatric Assessment Additional Information: Dr Hurria is deceased. Full and mortality. Arch Intern Med. 2012;172(5):405-411. 28. Mohile S, Dale W, Hurria A. Geriatric oncology protocol is available through University of doi:10.1001/archinternmed.2011.1662 research to improve clinical care. Nat Rev Clin Oncol. Rochester NCORP: https://urcc-ccop.com/ccop/. 2012;9(10):571-578. doi:10.1038/nrclinonc.2012.125 14. Safran DG, Karp M, Coltin K, et al. Measuring patients’ experiences with individual primary care 29. Hamaker ME, Te Molder M, Thielen N, REFERENCES physicians: results of a statewide demonstration van Munster BC, Schiphorst AH, van Huis LH. 1. Arora NK, Street RL Jr, Epstein RM, Butow PN. project. J Gen Intern Med. 2006;21(1):13-21. doi:10. The effect of a geriatric evaluation on treatment Facilitating patient-centered cancer 1111/j.1525-1497.2005.00311.x decisions and outcome for older cancer patients— communication: a road map. Patient Educ Couns. a systematic review. J Geriatr Oncol. 2018;9(5): 15. Grunfeld E, Fitzpatrick R, Mant D, et al. 2009;77(3):319-321. doi:10.1016/j.pec.2009.11.003 430-440. doi:10.1016/j.jgo.2018.03.014 Comparison of breast cancer patient satisfaction 2. Street RL Jr, Elwyn G, Epstein RM. Patient with follow-up in primary care versus specialist 30. Caillet P, Canoui-Poitrine F, Vouriot J, et al. preferences and healthcare outcomes: an care: results from a randomized controlled trial. Br J Comprehensive geriatric assessment in the ecological perspective. Expert Rev Pharmacoecon Gen Pract. 1999;49(446):705-710. decision-making process in elderly patients with Outcomes Res. 2012;12(2):167-180. doi:10.1586/ cancer: ELCAPA study. J Clin Oncol. 2011;29(27): 16. Hospital value-based purchasing: biggest erp.12.3 3636-3642. doi:10.1200/JCO.2010.31.0664 bonuses and penalties: CMS percentage change in 3. Epstein RM, Duberstein PR, Fenton JJ, et al. reimbursement based on process performance and 31. Ramsdale E, Lemelman T, Loh KP, et al. Geriatric Effect of a patient-centered communication patient satisfaction. Mod Healthc. 2013;43(1):34. assessment-driven polypharmacy discussions intervention on oncologist-patient communication, between oncologists, older patients, and their 17. Mann RK, Siddiqui Z, Kurbanova N, Qayyum R. quality of life, and health care utilization in caregivers. J Geriatr Oncol. 2018;9(5):534-539. Effect of HCAHPS reporting on patient satisfaction advanced cancer: the VOICE randomized clinical doi:10.1016/j.jgo.2018.02.007 with physician communication. JHospMed. 2016;11 trial. JAMA Oncol. 2017;3(1):92-100. (2):105-110. doi:10.1002/jhm.2490 32. Lowenstein LM, Volk RJ, Street R, et al. 4. Bernacki R, Hutchings M, Vick J, et al. Communication about geriatric assessment 18. Mariano C, Hanson LC, Deal AM, et al. Development of the Serious Illness Care Program: domains in advanced cancer settings: “missed Healthcare satisfaction in older and younger a randomised controlled trial of a palliative care opportunities”. J Geriatr Oncol. 2019;10(1):68-73. patients with cancer. J Geriatr Oncol. 2016;7(1): communication intervention. BMJ Open. 2015;5 doi:10.1016/j.jgo.2018.05.014 32-38. doi:10.1016/j.jgo.2015.11.005 (10):e009032. doi:10.1136/bmjopen-2015-009032 33. Mohile S, Dale W, Magnuson A, Kamath N, 19. Institute of Medicine. Delivering High-Quality 5. Paladino J, Bernacki R, Neville BA, et al. Hurria A. Research priorities in geriatric oncology Cancer Care: Charting a New Course for a System in Evaluating an intervention to improve for 2013 and beyond. Cancer Forum. 2013;37(3): Crisis. Washington, DC: National Academies Press; communication between oncology clinicians and 216-221. patients with life-limiting cancer: a cluster 34. Campbell MK, Piaggio G, Elbourne DR, 20. Nekhlyudov L, Levit L, Hurria A, Ganz PA. randomized clinical trial of the Serious Illness Care Altman DG; CONSORT Group. Consort 2010 Patient-centered, evidence-based, and Program. JAMA Oncol. 2019;5(6):801-809. doi:10. statement: extension to cluster randomised trials. cost-conscious cancer care across the continuum: 1001/jamaoncol.2019.0292 BMJ. 2012;345:e5661. doi:10.1136/bmj.e5661 translating the Institute of Medicine report into 6. DeSantis CE, Miller KD, Dale W, et al. Cancer clinical practice. CA Cancer J Clin. 2014;64(6): 35. Hurria A, Gupta S, Zauderer M, et al. statistics for adults aged 85 years and older, 2019 408-421. doi:10.3322/caac.21249 Developing a cancer-specific geriatric assessment: [published online August 7, 2019]. CA Cancer J Clin. a feasibility study. Cancer. 2005;104(9):1998-2005. 21. Hurria A, Naylor M, Cohen HJ. Improving the doi:10.3322/caac.21577 doi:10.1002/cncr.21422 quality of cancer care in an aging population: 7. Smith BD, Smith GL, Hurria A, Hortobagyi GN, recommendations from an IOM report. JAMA. 2013; 36. Mohile SG, Velarde C, Hurria A, et al. Geriatric Buchholz TA. Future of cancer incidence in the 310(17):1795-1796. doi:10.1001/jama.2013.280416 assessment-guided care processes for older adults: United States: burdens upon an aging, changing a Delphi consensus of geriatric oncology experts. 22. Hurria A, Levit LA, Dale W, et al; American nation. J Clin Oncol. 2009;27(17):2758-2765. doi: J Natl Compr Canc Netw. 2015;13(9):1120-1130. Society of Clinical Oncology. Improving the 10.1200/JCO.2008.20.8983 doi:10.6004/jnccn.2015.0137 evidence base for treating older adults with cancer: 8. Mohile SG, Xian Y, Dale W, et al. Association of a American Society of Clinical Oncology statement. 37. Kehoe LA, Xu H, Duberstein P, et al. Quality of cancer diagnosis with vulnerability and frailty in J Clin Oncol. 2015;33(32):3826-3833. doi:10.1200/ life of caregivers of older patients with advanced older Medicare beneficiaries. J Natl Cancer Inst. JCO.2015.63.0319 cancer. J Am Geriatr Soc. 2019;67(5):969-977. 2009;101(17):1206-1215. doi:10.1093/jnci/djp239 doi:10.1111/jgs.15862 23. Mohile SG, Hurria A, Cohen HJ, et al. Improving 9. Mohile SG, Fan L, Reeve E, et al. Association of the quality of survivorship for older adults with 38. Hurria A, Wildes T, Blair SL, et al. Senior adult cancer with geriatric syndromes in older Medicare cancer. Cancer. 2016;122(16):2459-2568. doi:10. oncology, version 2.2014: clinical practice beneficiaries. J Clin Oncol. 2011;29(11):1458-1464. 1002/cncr.30053 guidelines in oncology. J Natl Compr Canc Netw. doi:10.1200/JCO.2010.31.6695 2014;12(1):82-126. doi:10.6004/jnccn.2014.0009 24. Magnuson A, Allore H, Cohen HJ, et al. Geriatric 10. Hurria A, Dale W, Mooney M, et al; Cancer and assessment with management in cancer care: 39. Vallerand RJ, O’Connor BP, Blais MR. Life Aging Research Group. Designing therapeutic current evidence and potential mechanisms for satisfaction of elderly individuals in regular clinical trials for older and frail adults with cancer: future research. J Geriatr Oncol. 2016;7(4):242-248. community housing, in low-cost community U13 conference recommendations. J Clin Oncol. doi:10.1016/j.jgo.2016.02.007 housing, and high and low self-determination 2014;32(24):2587-2594. doi:10.1200/JCO. nursing homes. Int J Aging Hum Dev. 1989;28(4): 25. Wildiers H, Heeren P, Puts M, et al. 2013.55.0418 277-283. doi:10.2190/JQ0K-D0GG-WLQV-QMBN International Society of Geriatric Oncology 11. Mohile SG, Dale W, Somerfield MR, et al. consensus on geriatric assessment in older patients 40. Fiscella K, Franks P, Srinivasan M, Kravitz RL, Practical assessment and management of with cancer. J Clin Oncol. 2014;32(24):2595-2603. Epstein R. Ratings of physician communication by vulnerabilities in older patients receiving doi:10.1200/JCO.2013.54.8347 real and standardized patients. Ann Fam Med. chemotherapy: ASCO guideline for geriatric 2007;5(2):151-158. doi:10.1370/afm.643 26. Fried TR, Bradley EH, Towle VR, Allore H. oncology. J Clin Oncol. 2018;36(22):2326-2347. Understanding the treatment preferences of 41. Shumway D, Griffith KA, Jagsi R, Gabram SG, doi:10.1200/JCO.2018.78.8687 seriously ill patients. N Engl J Med. 2002;346(14): Williams GC, Resnicow K. Psychometric properties 12. Mohile SG, Magnuson A, Pandya C, et al. 1061-1066. doi:10.1056/NEJMsa012528 of a brief measure of autonomy support in breast Community oncologists’ decision-making for cancer patients. BMC Med Inform Decis Mak. 2015; 27. Wildiers H, Mauer M, Pallis A, et al. End points treatment of older patients with cancer. J Natl 15:51. doi:10.1186/s12911-015-0172-4 and trial design in geriatric oncology research: Compr Canc Netw. 2018;16(3):301-309. doi:10. a joint European Organisation for Research and 42. Hsieh HF, Shannon SE. Three approaches to 6004/jnccn.2017.7047 Treatment of Cancer–Alliance for Clinical Trials in qualitative content analysis. Qual Health Res. 2005; 13. Fenton JJ, Jerant AF, Bertakis KD, Franks P. Oncology–International Society Of Geriatric 15(9):1277-1288. doi:10.1177/1049732305276687 The cost of satisfaction: a national study of patient Oncology position article. J Clin Oncol. 2013;31(29): satisfaction, health care utilization, expenditures, 3711-3718. doi:10.1200/JCO.2013.49.6125 E8 JAMA Oncology Published online November 7, 2019 (Reprinted) jamaoncology.com Communication With Older Patients With Cancer Using Geriatric Assessment Original Investigation Research 43. Epstein RM, Franks P, Fiscella K, et al. quality assessments. Am J Manag Care. 2017;23 61. Karuturi M, Wong ML, Hsu T, et al. Measuring patient-centered communication in (10):618-622. Understanding cognition in older patients with patient-physician consultations: theoretical and cancer. J Geriatr Oncol. 2016;7(4):258-269. doi:10. 52. Tsai TC, Orav EJ, Jha AK. Patient satisfaction practical issues. Soc Sci Med. 2005;61(7):1516-1528. 1016/j.jgo.2016.04.004 and quality of surgical care in US hospitals. Ann Surg. doi:10.1016/j.socscimed.2005.02.001 2015;261(1):2-8. doi:10.1097/SLA. 62. Detmar SB, Muller MJ, Schornagel JH, 44. Cella DF, Tulsky DS, Gray G, et al. 0000000000000765 Wever LD, Aaronson NK. Health-related The Functional Assessment of Cancer Therapy quality-of-life assessments and patient-physician 53. Will KK, Johnson ML, Lamb G. Team-based care scale: development and validation of the general communication: a randomized controlled trial. JAMA. and patient satisfaction in the hospital setting: measure. J Clin Oncol. 1993;11(3):570-579. 2002;288(23):3027-3034. doi:10.1001/jama.288. a systematic review. J Patient Cent Res Rev. 2019;6 doi:10.1200/JCO.1993.11.3.570 23.3027 (2):158-171. doi:10.17294/2330-0698.1695 45. Ware J Jr, Kosinski M, Keller SDA. A 12-Item 63. Clayton JM, Butow PN, Tattersall MH, et al. 54. Brown H, Prescott R. Applied Mixed Models in Short-Form Health Survey: construction of scales Randomized controlled trial of a prompt list to help Medicine. 2nd ed. Edinburgh, UK: John Wiley & and preliminary tests of reliability and validity. Med advanced cancer patients and their caregivers to Sons, Ltd; 2006. Care. 1996;34(3):220-233. doi:10.1097/ ask questions about prognosis and end-of-life care. 55. Kenward MG, Roger JH. Small sample inference 00005650-199603000-00003 J Clin Oncol. 2007;25(6):715-723. doi:10.1200/JCO. for fixed effects from restricted maximum 2006.06.7827 46. Given CW, Given B, Stommel M, Collins C, likelihood. Biometrics. 1997;53(3):983-997. doi:10. King S, Franklin S. The caregiver reaction 64. Basch E, Deal AM, Kris MG, et al. Symptom 2307/2533558 assessment (CRA) for caregivers to persons with monitoring with patient-reported outcomes during 56. Loh KP, Mohile SG, Epstein RM, et al. chronic physical and mental impairments. Res Nurs routine cancer treatment: a randomized controlled Willingness to bear adversity and beliefs about the Health. 1992;15(4):271-283. doi:10.1002/nur. trial. J Clin Oncol. 2016;34(6):557-565. doi:10.1200/ curability of advanced cancer in older adults. Cancer. 4770150406 JCO.2015.63.0830 2019;125(14):2506-2513. doi:10.1002/cncr.32074 47. Hurria A, Mohile S, Gajra A, et al. Validation of a 65. Corre R, Greillier L, Le Caër H, et al. Use of a 57. Loh KP, Mohile SG, Lund JL, et al. Beliefs about prediction tool for chemotherapy toxicity in older comprehensive geriatric assessment for the advanced cancer curability in older patients, their adults with cancer. J Clin Oncol. 2016;34(20): management of elderly patients with advanced caregivers, and oncologists. Oncologist. 2019;24(6): 2366-2371. doi:10.1200/JCO.2015.65.4327 non-small-cell lung cancer: the phase III e292-e302. doi:10.1634/theoncologist.2018-0890 randomized ESOGIA-GFPC-GECP 08-02 study. 48. van Buuren S. Multiple imputation of discrete 58. Guetterman TC, Fetters MD, Creswell JW. J Clin Oncol. 2016;34(13):1476-1483. doi:10.1200/ and continuous data by fully conditional Integrating quantitative and qualitative results in JCO.2015.63.5839 specification. Stat Methods Med Res. 2007;16(3): health science mixed methods research through 219-242. doi:10.1177/0962280206074463 66. Bakitas M, Lyons KD, Hegel MT, et al. Effects of joint displays. Ann Fam Med. 2015;13(6):554-561. a palliative care intervention on clinical outcomes in 49. Curran D, Molenberghs G, Thijs H, Verbeke G. doi:10.1370/afm.1865 patients with advanced cancer: the Project ENABLE Sensitivity analysis for pattern mixture models. 59. Singh H, Beaver JA, Kim G, Pazdur R. II randomized controlled trial. JAMA. 2009;302(7): J Biopharm Stat. 2004;14(1):125-143. doi:10.1081/ Enrollment of older adults on oncology trials: an 741-749. doi:10.1001/jama.2009.1198 BIP-120028510 FDA perspective. J Geriatr Oncol. 2017;8(3):149-150. 67. Hahn S, Puffer S, Torgerson DJ, Watson J. 50. Bleustein C, Rothschild DB, Valen A, Valatis E, doi:10.1016/j.jgo.2016.11.001 Methodological bias in cluster randomised trials. Schweitzer L, Jones R. Wait times, patient 60. Puts MT, Santos B, Hardt J, et al. An update on BMC Med Res Methodol. 2005;5:10. doi:10.1186/ satisfaction scores, and the perception of care. Am J a systematic review of the use of geriatric 1471-2288-5-10 Manag Care. 2014;20(5):393-400. assessment for older adults in oncology. Ann Oncol. 51. Ehlers AP, Khor S, Cizik AM, et al. Use of 2014;25(2):307-315. doi:10.1093/annonc/mdt386 patient-reported outcomes and satisfaction for jamaoncology.com (Reprinted) JAMA Oncology Published online November 7, 2019 E9

Journal

JAMA OncologyPubmed Central

Published: Nov 7, 2019

There are no references for this article.