As the baby boomer generation in the United States ages, the number of older patients with cancer is increasing. A 67% increase in cancer incidence is projected in those individuals aged ≥65 years, compared with an 11% increase among younger adults.1,2 Older patients with cancer have a higher prevalence of comorbidities, geriatric syndromes, and disabilities than younger patients and older patients without cancer.3,4 Older patients with conditions other than cancer also carry a high risk of developing significant chemotherapy toxicity, functional and cognitive loss, and physical decline while on treatment.5,6 The underrepresentation of older adults in clinical trials places them at risk of receiving inappropriate undertreatment or overtreatment for their cancer, leading to disparities in outcomes.5,7–9 For example, fit older patients are less likely to receive evidence-based standard-of-care cancer treatment than younger patients, whereas older patients with both cancer and comorbid conditions are too often treated with therapies with high toxicity rates and low likelihood of benefit.10
A recent Institute of Medicine report acknowledged that our current systems are ill-prepared to care for the most vulnerable patients with cancer—those who are older (especially those aged ≥80 years) and those who have health conditions other than cancer.11 Because older patients with cancer receiving treatment are often seen by their oncology teams more frequently than by their primary care providers (PCPs),12 community oncology practices should be equipped to recognize common age-related concerns. Despite the rapidly increasing population of older patients with cancer, most oncologists have received little geriatrics training, and therefore common aging-related conditions that influence outcomes are rarely detected.13–16
In this study, community oncologists were recruited to participate in 2 nationwide, geriatric oncology clinical trials in the University of Rochester Cancer Center's NCI Community Oncology Research Program (URCC NCORP). During enrollment, they completed a survey regarding their beliefs about and confidence in providing geriatric care.17 Similar to other studies,18–21 randomized vignettes were used to assess whether clinical factors influenced their cancer treatment decision-making. This study, however, is the first that assesses how common geriatric factors (ie, function and cognition) affect decisions related to first-line chemotherapy in older patients with advanced cancer.
Methods
Participants
Participants were community oncologists recruited for 2 geriatric oncology studies (URCC 13059 [ClinicalTrials.gov identifier: NCT02054741] and/or URCC 13070 [NCT02107443]). Both studies involve a geriatric assessment (GA), which is a battery of validated tools to evaluate health status in multiple domains, including function, physical performance, depression, falls, and cognition,22 and evaluate whether providing a GA summary and targeted recommendations to community oncologists can improve outcomes in older patients with cancer.
Community oncologists were eligible to participate if they practiced at an NCI-funded NCORP affiliate site, their NCORP affiliate had IRB approval for either study, and they were not planning on leaving the practice. Oncologists were provided with a link to a survey via e-mail, using REDCap, a secure Web-based electronic data capture tool. If not completed, a paper survey option was offered. Oncologists were required to complete the baseline survey before participating in procedures of the main study. A waiver of consent was approved by the University of Rochester IRB for enrollment of oncologists.
Survey Design
The “Physician Baseline Survey” had 3 components: (1) oncologist demographics and practice characteristics, (2) oncologist ratings of their beliefs about and confidence with management of common geriatric issues, and (3) 1 of 8 randomly assigned clinical vignettes. The beliefs and confidence questions were developed by Cancer and Aging Research Group investigators (A.M., S.G.M., W.D.) and were modeled on a previously published survey.17 In accordance with prior studies,18,21 a vignette with a shared scenario was created describing an older female patient with metastatic pancreatic cancer presenting to her oncologist for a decision regarding first-line chemotherapy. A vignette of a patient with metastatic disease was selected to assess how geriatric factors may influence the weighing of risks and benefits of chemotherapy for frail older patients with limited life expectancies. The patient was an older woman who lived alone with a history of well-controlled hypertension, hyperlipidemia, and osteoarthritis; moderate fatigue (ECOG performance status [PS], 1); and an estimated life expectancy of ≤6 months, with no other symptoms from her cancer. Using this information as a base, 8 patient vignettes were created with 3 varied factors: age (72 vs 84 years), cognitive status (no impairment vs moderate impairment requiring assistance with finances and low Mini-Mental State Examination [MMSE; score of 15]), and functional status (no impairment vs impairment that included falls and deficits in instrumental activities of daily living [IADLs]). These factors were chosen because they are among the most important predictors of poor outcomes in older patients and are associated with frailty.5,23–27 In order to reduce bias (eg, physician answer for one vignette influences responses to others), a randomization scheme was developed so that each enrolled physician would receive 1 of the 8 vignettes.
Statistical Analysis
Descriptive statistics were used to describe physician demographics. Descriptive statistics were also used for the Likert scale questions regarding beliefs about and confidence with geriatrics, with interquartile range, mean, and median reported for each item. Bivariate associations between patient and physician characteristics and decision to treat with chemotherapy were analyzed with chi-square tests for categorical variables and t-tests for continuous variables. A total summary score was calculated for physician beliefs and physician confidence, and each score was categorized into tertiles due to a skewed distribution.
Logistic regression was performed to determine the independent association of the 3 varied vignette-patient characteristics (age, cognitive status, functional status) with primary outcome: whether oncologists would recommend treatment with first-line chemotherapy (yes/no) (Model A). In cases when chemotherapy was recommended, a second regression was conducted, predicting whether oncologists recommended single-agent chemotherapy or combination chemotherapy (Model B). Both models controlled for physician characteristics. Physician characteristics included sex (male/female), race (white/nonwhite), number of patients seen per day, and years in practice. A P value of <.05 was considered significant for all analyses. Analyses were performed using SAS 9.4 (SAS Institute, Cary NC).
Results
Of 498 surveys sent to eligible community oncologists in the URCC NCORP network, 305 consented to one or both of the studies (61% response rate). The oncologists were associated with 58 individual practice sites.
Oncologist Demographics and Practice Characteristics
Participants (N=305) had a mean age of 49 years, and most were male (71%), white (65%), and non-Hispanic (94%) (Table 1). Most were board certified in oncology (95%) and had a mean of 15 years in practice post–oncology fellowship. On average, oncologists saw 17 patients per day and were clinically active 4 days of the week.
Oncologist Perspectives Regarding Geriatrics Care
Most oncologists agreed that “there should be more clinical trials designed specifically for the elderly” (90%) and “the medical care of older adults
Physician Characteristics (N=305)
Oncologist Ratings of Confidence in Geriatric Care
Most oncologists felt “quite to very confident” when it came to discussing advanced directives (84%), preventing and managing osteoporosis (72%), and
Oncologist Perspectives Regarding Geriatrics Training and Experiencea,b
Vignette Responses
Chemotherapy Choices: Accounting for all vignettes across all scenarios, 161 oncologists (52%) said they would offer at least some form of chemotherapy. Of these, 64.6% (n=104) would offer single-agent chemotherapy, such as gemcitabine or capecitabine, and 35.4% (n=57) would offer multiagent chemotherapy, such as FOLFIRINOX or gemcitabine/nab-paclitaxel.
Bivariate Analyses: A consistent relationship was seen between vignette-patient characteristics and the decision to recommend chemotherapy (Table 4 and Figure 1). The proportion of oncologists who recommended any chemotherapy decreased with older patient age, cognitive impairment, and functional impairment. At the extremes, most oncologists (97%) randomized to vignette 1 (younger age and no functional or cognitive impairment) would recommend chemotherapy, whereas only a minority (14%) randomized to vignette 8 (older age, functional impairment, and cognitive impairment) would recommend chemotherapy. There was a general “dose-response” relationship, with older age and greater geriatric deficits leading to less aggressive therapy choices.
For the patients for whom chemotherapy was recommended, doublet chemotherapy was preferred over monotherapy only for the vignette-patient who was aged 72 years without functional or cognitive impairment (63% vs 38%). For the remainder of the vignette-patients, monotherapy was strongly preferred.
Older age (84 years), impaired function, and cognitive impairment were all associated with the decision to not recommend chemotherapy (P<.01 for all). For vignette-patients for whom chemotherapy was recommended, there was a significant relationship between older age and a higher likelihood of recommending single-agent therapy (P<.01). There was also a significant association between impaired functional and cognitive status of the vignette-patient and the likelihood of recommendation for single-agent therapy (P<.01).
Oncologist Ratings of Confidence in Geriatricsa,b
No association was found between physician beliefs about and confidence in caring for older adults and the decision to treat with chemotherapy. Total summary scores of beliefs (Table 2) and confidence (Table 3) were not associated with chemotherapy decisions (decision to treat with chemotherapy or intensity of treatment in those for whom chemotherapy was recommended).
Multivariable Analyses: Oncologist demographic and practice characteristics were not associated with the decision to treat with chemotherapy (Table 5). Varied patient characteristics were independently and strongly associated with the decision to give chemotherapy: younger age (adjusted odds ratio [aOR], 5.01; 95% CI, 2.73–9.20), no cognitive impairment (aOR, 5.42; 95% CI 3.01–9.76), and no functional impairment (aOR, 3.85; 95% CI, 2.12–7.00). Older age (aOR, 3.22; 95% CI, 1.43–7.25), impaired cognition (aOR, 3.13; 95% CI, 1.36–7.20), and functional impairment (aOR, 2.48; 95% CI, 1.12–5.46) were independently associated with prescribing single-agent over multiagent chemotherapy.
Discussion
In this study, we found that community oncologists incorporate patient age, functional impairment, and cognitive impairment into the decision-making process for cancer treatment in older adults. Despite the high prevalence of cognitive and functional decline in older adults with cancer,4 ≤25% of community oncologists rated themselves as “very confident” in assessment and interventions for function, falls, and dementia. To our knowledge, this is the first study to show that, whereas only a minority of community oncologists feels confident in assessing and intervening on geriatric issues, most use this information in clinical decision-making. However, this study also shows that there is significant variability in how geriatric issues are incorporated into decision-making for older patients who are not clearly fit or frail.
Older age was independently associated with chemotherapy decisions, which may result from limited evidence of the risks and benefits of chemotherapy for older patients. For advanced pancreatic cancer, multidrug chemotherapy regimens (eg, FOLFIRINOX, gemcitabine/nab-paclitaxel) have shown survival benefits.28–30 The phase III trial of FOLFIRINOX versus gemcitabine alone only included patients with an ECOG PS of 0 or 1 and excluded those aged ≥76 years,28 with age >65 years being significantly associated with worse survival.29 Although the phase III trial of gemcitabine/nab-paclitaxel versus gemcitabine alone did not have an upper age limit (42% of patients enrolled were ≥65 years, with only 10% of patients ≥75 years), older age was associated with worse survival.31 In addition, the grade 3/4 toxicity rate for these regimens in the clinical trial population is >50%.28–31 Toxicities are more severe and prevalent in the non–clinical trial population; in one study of 46 patients who received FOLFIRINOX, 54% were hospitalized
Percentage of Oncologists Recommending Chemotherapy for Each Patient Vignettea
Percentage of oncologists who recommended chemotherapy by varied factors in vignettes.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 16, 3; 10.6004/jnccn.2017.7047
In this study, physician beliefs about or confidence in their evaluation and management of age-related health issues did not influence chemotherapy decisions. However, most oncologists believe that geriatric training is essential for the care of older patients with cancer and would appreciate additional training in age-related topics. Most oncologists reported lower levels of confidence in assessing and intervening in certain geriatric syndromes—particularly dementia, functional decline, and risk for falls—precisely the areas that were found in the vignettes to influence treatment choices. These results mirror those from other studies. Among 758 PCPs, there was significant interest in learning more about dementia, urinary incontinence, and functional assessment.17 A study by Maggiore et al16 investigated perceptions toward geriatrics among University of Chicago hematology/oncology fellows. Underrecognition of geriatric syndromes was identified as a gap in knowledge, as well as underappreciation of the complexity of geriatric oncology cases. Most perceived a lack of dedicated formal instruction on older patients with cancer during their fellowship. In a study by Moy et al,14 oncologist members of ASCO reported that the mandatory integration of key principles of geriatrics into oncology training was a high priority. The investigators made recommendations to include geriatric training in the fellowship curriculum and to develop geriatric oncology modules for maintenance of certification training.
Only 23% of community oncologists report using standardized GA tools in clinical practice. GA assists with the capture of age-related factors (ie, cognitive impairment and functional status) known to affect morbidity and mortality in older patients with cancer that are often not recognized in clinical practice.15,22,38 In addition, GA has been shown to predict tolerance to treatment and overall survival, and specific variables captured by GA can predict chemotherapy toxicity in older patients with cancer.5,26,39,40 Consequently, multiple guidelines, including those by NCCN, support the use of a GA in older patients with cancer to identify patients at risk for adverse outcomes.41 Falls and cognitive impairment are associated with chemotherapy toxicity in older patients.5,26 Although GA has demonstrated feasibility in the clinical oncology setting,42–45 oncologists have been slow to adopt it, which may reflect lack of knowledge, training, and systematic barriers.
In this study, GA information (eg, IADL impairments, falls, low MMSE score indicating significant cognitive impairment), when provided in vignettes, was used to guide cancer treatment recommendations. Other studies have demonstrated that GA information can influence an oncologist's treatment decisions in older patients with cancer.46–48 In 6 of the 10 studies in a systematic review by Hamaker et al,47 the initial cancer treatment plan was modified in 39% of patients after GA evaluation. Nononcologic interventions based on the GA were recommended for a median of 83% of patients.47 Nononcologic interventions included nutritional interventions, further evaluation and management of cognitive status, interventions for mobility and falls, and interventions for minimizing polypharmacy.47 Oncologists use of geriatric factors in treatment decisions for patients in the
Multivariable Models
Limitations should be considered when evaluating the results of this study. This was a decision-making study using hypothetical vignettes, not decisions for real patients. Nevertheless, studies have shown that decisions made for vignettes were highly correlated with decisions made during patient encounters.18,49,50 Use of vignettes can help elucidate decision-making processes that may not be easily studied in routine practice due to ethical or practical considerations.18,49,50 Systematic control of variables of interest provides insight into the specific role of these selected patient factors in the decision to initiate chemotherapy, but does limit inferences for actual practice. Although the response rate for the survey was higher than that of other studies, it was still just >60%. Because oncologists completed the baseline survey as part of the recruitment procedures for geriatric oncology trials, oncologists who participated may be more sensitive to geriatric issues than those who did not participate. We did not collect detailed information on practice characteristics (eg, access to geriatricians). Despite limitations, this study has a significant strength in that it involved community oncologists from different practices and regions of the country, which improves generalizability.
Conclusions
With the use of randomized vignettes, we found that chronologic age was associated with treatment decisions. Despite their lack of confidence in certain areas of geriatric assessment and evaluation, the oncologists incorporated geriatric factors into treatment decision-making. Because the current investigation was nested in larger, ongoing multisite geriatric oncology studies, future research will examine community oncologists' decision-making for treatment of “real-world” older patients recruited into the trials. Further work is necessary to evaluate and improve geriatrics education for oncologists. As our population ages, it is increasingly important for oncologists to be able recognize geriatric issues so that appropriate evidence-based treatment is provided to patients who will be helped and not harmed.
Dr. Hurria has disclosed that she has received grant or research support from Celgene and Novartis, and has served as a consultant for Boehringer Ingelheim, Pierian Biosciences, and MJH Healthcare Holdings. The remaining authors have disclosed that they have no financial interests, arrangements, affiliations, or commercial interests with the manufacturers of any products discussed in this article or their competitors.
This work was funded through a PCORI program contract (4634), UG1 CA189961 from the NCI, and R01 CA177592 from the NCI. This work was made possible by the generous donors to the WCI geriatric oncology philanthropy fund. All statements in this report, including its findings and conclusions, are solely those of the authors, do not necessarily represent the official views of the funding agencies, and do not necessarily represent the views of PCORI, its Board of Governors, or Methodology Committee.
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