Abstract

INTRODUCTION

As the baby boomer generation in the United States ages, the numbers of older patients with cancer is also rising. A 67% increase in cancer incidence in those 65+ years of age is projected, compared to an 11% increase among younger adults.^1,2 Oder 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 outside of cancer also carry a high risk of developing significant chemotherapy toxicity, functional and cognitive loss, and physical decline while on treatment.^5,6 The under-representation of older adults in clinical trials places them at risk of receiving inappropriate under- or over-treatment 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, while older patients with both cancer and comorbid conditions are too often treated with therapies with high toxicity rates and low likelihoods of benefit.¹⁰

A recent Institute of Medicine (IOM) report acknowledged that our current systems are ill-prepared to care for the most vulnerable patients with cancer—those who are older (especially patients who are age 80+) 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,¹² community oncology practices should be equipped to recognize common age-related concerns. Despite the rapidly increasing numbers of older patients with cancer, most oncologists have received little geriatrics training, so common aging-related conditions that influence outcomes are rarely detected.^13–16

In this study, community oncologists were recruited to take part of two nationwide, geriatric oncology clinical trials in the University of Rochester Cancer Center 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 utilized to assess whether clinical factors influenced their cancer treatment decision making. This study, however, is the first that assesses how common geriatrics factors (i.e., function and cognition) affects decisions related to first-line chemotherapy in older patients with advanced cancer.

METHODS

RESULTS

Of 498 surveys sent to eligible community oncologists in the UR NCORP network, 305 consented to one or both of the studies (61% response rate). The oncologists were associated with 58 individual practice sites.

Vignette Responses

Chemotherapy Choices

Accounting for all vignettes across all scenarios, 161 (52%) said they would offer at least some form of chemotherapy. Of the 161 oncologists who recommended chemotherapy, 64.6% (n=104) would offer single-agent chemotherapy such as gemcitabine or capecitabine; 35.4% (n=57) would offer multi-agent chemotherapy such as FOLFIRINOX or gemcitabine/nab-paclitaxel.

Bivariate Analyses

There was a consistent relationship between vignette-patient characteristics and a 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, the majority of oncologists (97%) randomized to receive vignette 1 (younger age and no functional or cognitive impairment) would recommend chemotherapy, while 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 geriatrics deficits leading to less aggressive therapy choices.

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Figure 1

Percentage of Oncologists who Recommended Chemotherapy by Varied Factors in Vignettes

Table 4

Percentage of Oncologists’ Recommending Chemotherapy for each Vignette Patient^*

Patient Vignette The patient (initials) is a ______year old female with a history of well-controlled hypertension, hyperlipidemia and osteoarthritis, who is referred for evaluation of metastatic pancreatic cancer. She has a 3 cm pancreatic adenocarcinoma with metastatic disease to the liver. Based upon her cancer diagnosis, her estimated life expectancy is six months or less. She currently reports moderate fatigue which is impacting her daily activities (ECOG PS =1) but denies any other symptoms from her cancer. She currently lives alone.
Vignette Number (N=303)#	Varied Factors	Explanation of Varied Factors	% of Oncologists Recommending Chemotherapy^
Vignette 1 (n=34)	AM is a 72 year old female. She independently performs all activities of daily living and instrumental activities of daily living. She denies any memory problems or history of dementia.	-Younger -No functional impairment -No cognitive impairment	97%	Multi-agent: 63% Monotherapy: 38%
Vignette 2 (n=39)	BL is a 72 year old female. She independently performs all activities of daily living but requires assistance with some instrumental activities of daily living including housekeeping and grocery shopping. She has had 3 falls in the past 6 months, and sustained an injury requiring an emergency room visit during one episode. She denies any memory problems or history of dementia.	-Younger -Functional impairment -No cognitive impairment	74%	Multi-agent: 41% Monotherapy: 59%
Vignette 3 (n=31)	CK is a 72 year old female. She independently performs all activities of daily living and most instrumental activities of daily living. She requires assistance with managing household finances due to memory problems. Cognitive testing is performed and her cognition is found to be impaired (MMSE 15)**.	-Younger -No functional impairment -Cognitive impairment	61%	Multi-agent: 39% Monotherapy: 61%
Vignette 4 (n=27)	DJ is a 72 year old female. She independently performs all activities of daily living but requires assistance with some instrumental activities of daily living including housekeeping, grocery shopping, and managing finances. She has had 3 falls in the past 6 months, and sustained an injury requiring an emergency room visit during one episode. Cognitive testing is performed and her cognition is found to be impaired (MMSE 15)**.	-Younger -Functional impairment -Cognitive impairment	56%	Multi-agent: 13% Monotherapy: 87%
Vignette 5 (n=39)	EK is an 84 year old female. She independently performs all activities of daily living and instrumental activities of daily living. She denies any memory problems or history of dementia.	-Older -No functional impairment -No cognitive impairment	85%	Multi-agent: 38% Monotherapy: 62%
Vignette 6 (n=41)	FH is an 84 year old female. She independently performs all activities of daily living, but requires assistance with some instrumental activities of daily living including housekeeping and grocery shopping. She has had 3 falls in the past 6 months, and sustained an injury requiring an emergency room visit during one episode. She denies any memory problems or history of dementia.	-Older -Functional impairment -No cognitive impairment	44%	Multi-agent: 18% Monotherapy: 82%
Vignette 7 (n=43)	GS is an 84 year old female. She independently performs all activities of daily living and most instrumental activities of daily living. She only requires assistance with managing household finances due to memory problems. Cognitive testing is performed and her cognition is found to be impaired (MMSE 15)**.	-Older -No Functional impairment -Cognitive impairment	37%	Multi-agent: 19% Monotherapy: 81%
Vignette 8 (n=49)	HT is an 84 year old female. She independently performs activities of daily living but requires assistance with some instrumental activities of daily living including housekeeping, grocery shopping and managing finances. She has had 3 falls in the past 6 months, and sustained an injury requiring an emergency room visit during one episode. Cognitive testing is performed and her cognition is found to be impaired (MMSE 15)**.	-Older -Functional impairment -Cognitive impairment	14%	Multi-agent: 0% Monotherapy: 100%

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Bolded item are characteristics that were varied systematically between vignettes.

^*Each physician was randomized to one vignette as part of the survey; two physicians did not provide a response

^{^}Doublet vs monotherapy answer may not add to 100% due to missing data

^**A Mini-Mental State Exam Score (MMSE) of 15 is indicative of problems with learning new information, recognizing close relatives, personality changes, and behavior disorders.

For the patients for whom chemotherapy was recommended, doublet chemotherapy was preferred over monotherapy only for the vignette patient who was 72 years old without functional or cognitive impairment (63% vs. 38%). For the rest 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’s<0.01 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<0.01). 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’s<0.01).

There was no association found between physician beliefs about and confidence in caring for older adults with 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

Oncologists’ demographic and practice characteristics were not associated with the decision to treat with chemotherapy (Table 5). Each varied patient characteristics were independently and strongly associated with the decision to give chemotherapy: younger age (adjusted OR: 5.01; 95% CI: 2.73–9.20), no cognitive impairment (5.42; 3.01–9.76), and no functional impairment (3.85; 2.12–7.00). Older age (adjusted OR: 3.22; 1.43–7.25), impaired cognition (3.13; 1.36–7.20), and functional impairment (2.48; 1.12–5.46) were independently associated with prescribing single-agent over multi-agent chemotherapy.

Table 5

Multivariable Models Evaluating the Associations between Physician and Vignette Patient Characteristics with the Decision to Recommend Chemotherapy (Model A) and the Decision to Recommend Single Agent vs Combination Therapy (Model B)

Variables	Adjusted Odds Ratio	95% Confidence Interval
Model A** Decision to Recommend Chemotherapy vs No Chemotherapy
Physician Characteristics
Age (years)	1.00	0.93–1.08
Gender
Female	1 (ref)
Male	0.85	0.43–1.66
Race
Non-white	1 (ref)
White	0.76	0.39–1.46
Number of years in practice	1.01	0.94–1.09
Number of patients seen per day	1.01	0.97–1.06
Number of days per week seeing patient	1.24	0.87–1.76
Vignette Patient Characteristics
Age (years)
72	5.01*	2.73–9.20
84	1 (ref)
Cognitive impairment
No	5.42*	3.01–9.76
Yes	1 (ref)
Functional impairment
No	3.85*	2.12–7.00
Yes	1 (ref)
Model B^ Decision to Recommend Single Agent vs Combination Therapy
Physician Characteristics
Age (years)	1.01	0.92–1.11
Gender
Female	1 (ref)
Male	1.00	0.39–2.60
Race
Non-white	1 (ref)
White	1.28	0.54–3.08
Number of years in practice	1.00	0.91–1.10
Number of patients seen per day	1.01	0.95–1.08
Number of days per week seeing patient	0.75	0.46–1.24
Vignette Patient Characteristics
Age (years)
72	1 (ref)
84	3.22*	1.43–7.25
Cognitive impairment
No	1 (ref)
Yes	3.13*	1.36–7.20
Functional impairment
No	1 (ref)
Yes	2.48*	1.12–5.46

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^*p<0.05

^**Model A, n=279; 26 observations not included due to missing information for response and exploratory variables

^{^}Model B, n=161; model includes only those observations where chemotherapy was recommended

DISCUSSION

In this study, we found that community oncologists incorporate patient age, functional impairment, and cognitive impairment into decision making for cancer treatment for 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, while only a minority of community oncologists feels confident in assessing and intervening on geriatric issues, the majority utilize 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, multi-drug chemotherapy regimens (e.g., FOLFIRINOX, gemcitabine/nab-paclitaxel) have shown survival benefits.^28–30 The phase III trial of FOLFIRINOX vs. gemcitabine alone only included patients with an ECOG score of 0 or 1 and excluded those aged 76 and older²⁸ with age over 65 years being significantly associated with worse survival.²⁹ Although the phase III trial of gemcitabine/nab-paclitaxel vs. gemcitabine alone did not have an upper age limit (42% of patients enrolled were ≥65 years with only 10% of patients aged 75 and older), 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 over 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 for sepsis and 7% died from treatment.³² Hesitancy to provide multi-agent chemotherapy regimens to older patients, even those who are fit, likely stem from oncologists’ concerns about the ability of older adults to tolerate these regimens.³³ Conversely, many oncologists continue to offer single-agent regimens to older patients with cognitive or functional impairments (often unrecognized without formal GA)¹⁵ despite modestbenefit. This study demonstrates that lack of evidence-based data to support cancer treatment plans in older patients leads to significant variability in treatment decision making.^21,34–37

In this study, physician beliefs about or confidence in evaluation of management of age-related health issues did not influence chemotherapy decisions. However, the majority of oncologists believe that geriatric training is essential for the care of older cancer patients and would appreciate additional training in age-related topics. The majority of 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 primary care physicians, there was significant interest in learning more about dementia, urinary incontinence, and functional assessment.¹⁷ A study by Maggiore et al. investigated perceptions towards geriatrics among University of Chicago hematology/oncology fellows.¹⁶ Under-recognition of geriatric syndromes was identified as a gap in knowledge, as well as under-appreciation of the complexity of geriatric oncology cases. The majority perceived a lack of dedicated formal instruction on older patients with cancer during their fellowship. In a study by Moy et al., oncologist members of American Society of Clinical Oncology (ASCO) reported that the mandatory integration of key principles of geriatrics into oncology training was a high priority.¹⁴ 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 (such as cognitive impairment and functional status) known to affect morbidity and mortality in older patients with cancer that often are 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 cancer patients.^5,26,39,40 Consequently, multiple guidelines, including the National Comprehensive Cancer Network (NCCN) guidelines, 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 GA, which may reflect lack of knowledge, training, and systematic barriers.

In this study, GA information (e.g., IADL impairments, falls, low MMSE score indicating significant cognitive impairment) when provided in vignettes was utilized to guide cancer treatment recommendations. Other studies have demonstrated that GA information can influence an oncologist’s treatment decisions in older cancer patients.^46–48 In six of the ten studies in a systematic review by Hamaker et al., the initial cancer treatment plan was modified in 39% of patients after GA evaluation.⁴⁷ Non-oncological interventions based on the GA were recommended for a median of 83% of patients.⁴⁷ Non-oncological interventions included nutritional interventions, further evaluation and management of cognitive status, interventions for mobility and falls, as well as interventions for minimizing polypharmacy.⁴⁷ Oncologists use of geriatric factors in treatment decisions for patients in the vignettes, despite their limited confidence in assessing for functional and cognitive issues in clinical practice, suggest the importance of routine use of GA in clinical practice to guide management decisions for cancer treatment and non-oncological interventions.

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 understand 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. While the response rate for the survey was higher than that of other studies, it was still just over 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 (e.g., 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 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 multi-site 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 those patients who will be helped and not harmed.

Acknowledgments

Footnotes

References