Health Care Delivery

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Geriatric Oncology for the 21st Century: A Call for Action By Beverly Moy, MD, MPH, Thomas W. Flaig, MD, Hyman B. Muss, MD, Ben Clark, William Tse, MD, and T. Christopher Windham, MD Massachusetts General Hospital Cancer Center, Boston, MA; University of Colorado, Aurora, CO; University of North Carolina/ Lineberger Comprehensive Cancer Center, Chapel Hill, NC; American Society of Clinical Oncology, Alexandria, VA; West Virginia University, Morgantown, WV; and Florida Hospital Memorial Medical Center, Daytona Beach, FL

Thanks to the global improvement of health care, the aging of our population has necessitated an emphasis on geriatric medicine. By the year 2030, the US Census Bureau projects that the number of adults age 65 years and older will double, contributing to a 45% increase in the number of people developing cancer.1 Adults older than age 65 have an 11-fold increase in cancer incidence and a 16-fold increase in cancer mortality compared with younger adults.2 These factors underscore the need for oncologists to be better prepared to care for older patients with cancer. The recently released Institute of Medicine report further emphasizes the need for the oncology community to optimize care of older patients with cancer.3,4 Given that older patients with cancer are under-represented in clinical trials, oncologists lack evidence-based data for treatment decisions.5 The medical literature frequently fails to establish the optimal selection of cancer treatment in older patients and provides little information related to the short- and long-term complications of treatment.6 In his 1988 American Society of Clinical Oncology (ASCO) Presidential address, President B. J. Kennedy called for the study of aging and cancer, stating that care of the older person needs to be integrated into oncology education and geriatric oncology research should be prioritized.7 Since that time, there has been modest progress. Cancerspecific mortality has been found to be higher in older patients compared with younger patients8 and significant benefits from adjuvant treatment have been demonstrated in older patients with early-stage cancer.9 There are also conflicting data suggesting that older patients with cancer do not benefit from adjuvant therapy, thereby increasing confusion about whether age cutoffs should be used for treatment decision making.10 Physician reluctance has emerged as the major barrier to enrollment of older patients with cancer into clinical trials11 and a patient’s age has been found to be the strongest determinant of whether he or she receives adjuvant chemotherapy.12 Brief geriatric assessments that assist in treatment selection have been developed to evaluate older patients with cancer,13-15 but their use has not been established as part of routine oncologic care. Despite a general acknowledgment of these issues, there remains no consensus about how best to address cancer care in older individuals. A necessary step for moving forward is to determine the priorities within geriatric oncology including physician education, patient care, and research. As part of the Copyright © 2014 by American Society of Clinical Oncology

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ASCO leadership development program, we were asked by the ASCO Board of Directors to define future priorities within geriatric oncology. We conducted structured interviews with twelve geriatric oncology thought leaders and a web-based survey of oncologists with a special interest in geriatrics globally. Several themes emerged from these interviews that informed our survey development. There was uniform consensus that increasing the number of geriatric oncologists was not a sufficient approach to address research and care demands in geriatric oncology; rather, better education of oncology providers in the care of older cancer patients should be the focus. The experts identified a lack of clinically useful and readily available resources that are specific for older cancer patients as a critical issue. We used information from these interviews to create a survey that was distributed to members of the International Society of Geriatric Oncology, ASCO members with geriatric oncology designated as a clinical or research interest, and the ASCO Board of Directors. The total sample size for the survey was 673, and we received 117 responses (17.4%), representing a diverse geographic area (Fig 1). Our survey response rate was comparable with most published external surveys.16 Given that surveys with response rates of 5% to 20% can yield accurate measurements, we feel that our survey reveals meaningful perspectives.17,18 The survey focused on three major areas in geriatric oncology: education, research, and patient care. Regarding education, the mandatory integration of the key principles of geriatric care into oncology training was the top priority (Fig 2A). Respondents felt that improved evidence regarding the efficacy

USA/Canada (n = 44) EU/Europe (n = 32) Australia/NZ (n = 9) South America (n = 7) Asia (n = 4) Other (n = 9)

Figure 1. Location of survey respondents, grouped by continent.



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Percentage of Respondents

A

Low

Middle

Table 1. Recommendations for Improving Geriatric Oncology in the 21st Century

High

100 90 80

Area of Focus

Recommendation

70

Education

Incorporate basic principles of geriatric care into oncology training programs

60 50 40

Include geriatric oncology question in board certification and fellowship in-training examinations

30

Develop geriatric oncology modules for board maintenance of certification

20 10

Integrate geriatric oncology content into disease-specific educational tracks at major oncology symposia

0 Knowledge integration

Percentage of Respondents

B

Increase interest Low

Middle

Increase awareness

Research

High

100

Increase funding for clinical and basic science research aimed toward better understanding treatment toxicity in older adults with cancer CARG and others should focus on optimal research approaches (ie, trials restricted to older adults v expanding cohorts in large cooperative group studies)

90 80 70 Patient care

60 50 40

Improve clinically useful geriatric assessment tools and incorporate them into routine oncology practice Incorporate geriatric oncology into diseasespecific clinical practice guidelines

30 20

Abbreviation: CARG, Cancer and Aging Research Group.

10 0 Improve toxicity understanding

Percentage of Respondents

C

Low

Basic science Middle

Barriers to clinical research High

100 90 80 70 60 50 40 30 20 10 0 Integration of functional status

Workforce shortage

Improve access

Figure 2. The survey respondents rated the importance of three geriatric oncology issues in the areas of (A) education, (B) research, and (C) patient care. In each area, the respective issues were rated as high, medium, or low priority.

and toxicity of commonly used cancer therapies and defining who is fit for therapy was the highest priority in geriatric cancer research (Fig 2B). For the optimization of patient care, the integration of comorbidities and functional status into treatment decisions was identified as the highest priority (Fig 2C). In considering these priorities, our group developed several recommendations to address these initiatives (Table 1). Regarding education, first, training in the basic principles of geriatric care should be incorporated into oncology training programs. A specific approach would be to include geriatric oncology questions in fellowship training in-service and board certification examinations. Second, the inclusion of geriatric oncology-specific modules could be made part of the maintenance of 242

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certification program for all oncology specialties. For example, a specific geriatric package, including a predesigned self-improvement module and a medical knowledge module, could be developed for the practicing oncologist. Third, geriatric oncology educational sessions should be seamlessly integrated into each disease site track at oncology meetings, such as the annual meetings of ASCO, the European Society of Medical Oncology, and the American Association of Cancer Research. Integration, as opposed to specialty geriatric sessions, could provide greater general oncology exposure to these issues. These societies should prioritize the highest scoring geriatric oncology research abstracts for more prominent presentations within their disease-specific tracks and symposia, thereby reaching a wider audience. The goals of these efforts are to make caring for older patients with cancer part of lifelong learning and to increase prominence within the broader field of oncology. Regarding research, we make the several recommendations. We suggest increased funding of basic science and clinical research in understanding treatment toxicity in older patients with cancer. Some funding efforts are already in progress. The Cancer and Aging Research Group (CARG), a group of geriatric oncology researchers received funding from a U13 conference grant, bringing together multidisciplinary investigator groups to identify the areas of highest research priorities in cancer and aging. CARG is a collaboration between the National Institute of Aging, the National Cancer Institute, and the Cancer and Leukemia Group B (CALGB).19 This group has implemented research studies enrolling only older patients with cancer. Ongoing studies include an analysis of clinical and biologic predictors of chemotherapy toxicity and the determination of the use of an assessment tool for older patients with cancer. Issues that CARG and others should focus on are

V O L . 10, I S S U E 4

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Geriatric Oncology

whether the optimal research approach should be to conduct clinical trials restricted to older adults with cancer or to expand cohorts of older adults within current cooperative group trials. Although the initial work of CARG holds significant promise, continued efforts and increased funding will need to be made to leverage this collaboration and to generate enthusiasm about their important work. Finally, to optimize patient care, we also have several recommendations. We suggest improving clinically useful tools for oncologists and incorporating them into routine oncology practice. Geriatric assessment tools should offer a practical evaluation of independent predictors of morbidity and mortality in older patients. Tools that predict the risk of toxicity, such as the CRASH (Chemotherapy Risk Assessment Scale for High-Age Patients) and CARG geriatric assessment scales, are increasingly included in clinical trials but have not been routinely incorporated into practice.14,15,20 Several barriers prevent widespread use of these assessment scales, including lack of general awareness and their absence in an easily accessible location such as a popular oncology Web site. The next generation of studies should aim to simplify these tools without sacrificing their predictive value and to identify interventions that can decrease the risk of toxicity for older patients with cancer. In addition, many organizations are issuing practice guidelines on a variety of topics including some specifically for geriatric oncology. Integration of geriatric oncology concepts will likely reach a wider audience if included in all disease site guidelines rather than solely existing as a standalone document. As we move forward, a multipronged approach is required to accomplish the most pressing priorities identified by global geriatric experts. Prioritization of geriatric oncology among key

stakeholders such as oncology providers, researchers, patient advocates, industry representatives, and lawmakers are needed to bridge many of the gaps in our knowledge. Ultimately, our goal should be to provide the best evidence-based care to improve the lives of older patients with cancer. Acknowledgment All authors contributed equally. We thank the 12 geriatric oncology experts who lent us valuable insight. Many thanks to Lodovicco Balducci, MD, Harvey Cohen, MD, William Dale, MD, Jane Driver, MD, Martine Extermann, MD, Arti Hurria, MD, Richard Hodes, MD, Nina Karlin, MD, Heidi Klepin, MD, Stuart Lichtman, MD, Supriya Mohile, MD, and Arash Naeim, MD. Authors’ Disclosures of Potential Conflicts of Interest The authors indicated no potential conflicts of interest. Author Contributions Conception and design: Beverly Moy, Thomas W. Flaig, Hyman B. Muss, William Tse, T. Christopher Windham Administrative support: Beverly Moy, Hyman B. Muss, Ben Clark, William Tse, T. Christopher Windham Collection and assembly of data: Beverly Moy, Thomas W. Flaig, Ben Clark, William Tse, T. Christopher Windham Data analysis and interpretation: All authors Manuscript writing: All authors Final approval of manuscript: All authors Corresponding author: Beverly Moy, MD, MPH, Massachusetts General Hospital Cancer Center, 55 Fruit St, Yawkey 9A, Boston, MA 02114; e-mail: [email protected].

DOI: 10.1200/JOP.2013.001333; published online ahead of print at jop.ascopubs.org on April 29, 2014.

References 1. US Department of Commerce Census Bureau: Population projections. http:// www.census.gov/population/projections/files/summary/NP2012-T2.xls 2. Edwards BK, Howe HL, Ries LA, et al: Annual report to the nation on the status of cancer, 1973-1999, featuring implications of age and aging on U.S. cancer burden. Cancer 94:2766-92, 2002 3. Institute of Medicine: Delivering High-Quality Cancer Care: Charting a New Course for a System in Crisis. Washington, DC, National Academies Press, 2013. http://www.iom. edu/Reports/2013/Delivering-High-Quality-Cancer-Care-Charting-a-New-Course-for-aSystem-in-Crisis.aspx 4. Hurria A, Naylor M, Cohen HJ: Improving the quality of cancer care in an aging population: Recommendations from an IOM report. JAMA 310:1795-1796, 2013 5. Lichtman SM, Balducci L, Aapro M: Geriatric oncology: A field coming of age. J Clin Oncol 25:1821-1823, 2007 6. Muss HB, Woolf S, Berry D, et al: Adjuvant chemotherapy in older and younger women with lymph node-positive breast cancer. JAMA 293:1073-1081, 2005 7. Kennedy BJ: Aging and cancer. J Clin Oncol 6:1903-1911, 1988 8. Smith BD, Jiang J, McLaughlin SS, et al: Improvement in breast cancer outcomes over time: Are older women missing out? J Clin Oncol 29:4647-4653, 2011 9. Sargent DJ, Goldberg RM, Jacobson SD, et al: A pooled analysis of adjuvant chemotherapy for resected colon cancer in elderly patients. N Engl J Med 345: 1091-1097, 2001 10. McCleary NJ, Meyerhardt JA, Green E, et al: Impact of age on the efficacy of newer adjuvant therapies in patients with stage II/III colon cancer: Findings from the ACCENT database. J Clin Oncol 31:2600-2606, 2013

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11. Kemeny MM, Peterson BL, Kornblith AB, et al: Barriers to clinical trial participation by older women with breast cancer. J Clin Oncol 21:2268-2275, 2003 12. Schrag D, Cramer LD, Bach PB, et al: Age and adjuvant chemotherapy use after surgery for stage III colon cancer. J Natl Cancer Inst 93:850-857, 2001 13. Cohen HJ, Feussner JR, Weinberger M, et al: A controlled trial of inpatient and outpatient geriatric evaluation and management. N Engl J Med 346:905-912, 2002 14. Extermann M, Boler I, Reich RR, et al: Predicting the risk of chemotherapy toxicity in older patients: The Chemotherapy Risk Assessment Scale for High-Age Patients (CRASH) score. Cancer 118:3377-3386, 2012 15. Hurria A, Togawa K, Mohile SG, et al: Predicting chemotherapy toxicity in older adults with cancer: A prospective multicenter study. J Clin Oncol 29:34573465, 2011 16. SurveyGizmo: Survey response rates. http://www.surveygizmo.com/surveyblog/survey-response-rates/ 17. Visser PS, Krosnick JA, Marquette J, et al: Mail surveys for election forecasting? An evaluation of the Colombia Dispatch Poll. Public Opinion Quarterly 60: 181-227, 1996 18. Keeter S, Kennedy C, Dimock M, et al: Gauging the Impact of Growing Nonresponse on Estimates from a National RDD Telephone Survey. Public Opinion Quarterly 70:759-779, 2006 19. Hurria A, Mohile SG, Dale W: Research priorities in geriatric oncology: Addressing the needs of an aging population. J Natl Compr Canc Netw 10:286-288, 2012 20. Hurria A, Cirrincione CT, Muss HB, et al: Implementing a geriatric assessment in cooperative group clinical cancer trials: CALGB 360401. J Clin Oncol 29:1290-1296, 2011



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