Association Between Chronologic Age and Geriatric Assessment–Identified Impairments: Findings From the CARE Registry

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  • 1 Institute for Cancer Outcomes and Survivorship,
  • | 2 O’Neal Comprehensive Cancer Center, and
  • | 3 Division of Hematology and Oncology, Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama;
  • | 4 Revital Cancer Rehabilitation, Select Medical, Mechanicsburg, Pennsylvania; and
  • | 5 Department of Occupational Therapy, Colorado State University, Fort Collins, Colorado.

Background: The NCCN Guidelines for Older Adult Oncology recommend that, when possible, older adults with cancer undergo a geriatric assessment (GA) to provide a comprehensive health appraisal to guide interventions and appropriate treatment selection. However, the association of age with GA-identified impairments (GA impairments) remains understudied and the appropriate age cutoff for using the GA remains unknown. Patients and Methods: We designed a cross-sectional study using the Cancer and Aging Resilience Evaluation (CARE) registry of older adults with cancer. We included adults aged ≥60 years diagnosed with gastrointestinal malignancy who underwent a patient-reported GA prior to their initial consultation at the gastrointestinal oncology clinic. We noted the presence of GA impairments and frailty using Rockwood’s deficit accumulation approach. We studied the relation between chronologic age and GA impairments/frailty using Spearman rank correlation and chi-square tests of trend. Results: We identified 455 eligible older adults aged ≥60 years with gastrointestinal malignancies; the median age was 68 years (range, 64–74 years) and colorectal (33%) and pancreatic (24%) cancers were the most common cancer type. The correlation between chronologic age and number of geriatric impairments was weak and did not reach statistical significance (Spearman ρ, 0.07; P=.16). Furthermore, the prevalence of domain-specific impairments or frailty was comparable across the 3 age groups (60–64 years, 65–74 years, ≥75 years) with the exception of comorbidity burden. Notably, 61% of patients aged 60 to 64 years had ≥2 GA impairments and 35% had evidence of frailty, which was comparable to patients aged 65 to 74 years (66% and 36%, respectively) and ≥75 years (70% and 40%, respectively). Conclusions: Using chronologic age alone to identify which patients may benefit from GA is problematic. Future studies should identify screening tools that may identify patients at high risk of frailty and GA impairments.

Background

Up to 60% of all new cancer diagnoses and 70% of all cancer-related deaths occur among adults aged ≥65 years.1 Older adults with cancer are at high risk of treatment-related toxicity and inferior survival, yet neither chronologic age nor clinician-assessed performance status (PS) adequately captures this vulnerability.2 A geriatric assessment (GA) is a multidimensional tool to uncover this vulnerability or frailty and predicts the risk of morbidity and mortality among older adults with cancer.35 A growing body of literature shows that GA can predict chemotherapy-related toxicity,5,6 as well as mortality,4 guide clinical decision-making,7 and improve patient satisfaction8 among older adults with cancer. Specifically among gastrointestinal cancers, a GA has been shown to predict postsurgical complications among older adults with colorectal cancer9 and gastroesophageal10 and hepatocellular carcinoma,11 as well as chemotherapy-related toxicity12 and short- and long-term mortality.1315 Given these substantial benefits, ASCO16 and NCCN guidelines17 currently recommend that all older adults with cancer undergo a GA.

However, the association between chronologic age and GA impairments and frailty remains understudied. Furthermore, ASCO recommends a GA should be performed among all older adults with cancer aged >65 years, yet the rationale for this age cutoff remains unclear. Because patients with cancer are known to undergo accelerated aging through multiple mechanisms,18 extrapolating from the age cutoff used in the general population may be inaccurate. In this study, we examined the association between chronologic age and GA-identified impairments and frailty among adults aged ≥60 years with gastrointestinal malignancies.

Patients and Methods

Study Population

Using participants from the University of Alabama at Birmingham (UAB) Cancer and Aging Resilience Evaluation (CARE) Study, an ongoing prospective registry enrolling older adults (≥60 years old) undergoing cancer care at UAB Hospitals and Clinics,19,20 we identified patients diagnosed with a gastrointestinal malignancy presenting to our medical oncology clinic for an initial consultation. We chose 60 years of age as a criterion for enrollment in this registry given the uncertainty surrounding the “right” age cutoff and to allow for meaningful age-related subanalyses, such as the current study.21 The UAB Institutional Review Board (IRB-300000092) approved this study.

Geriatric Assessment

We conducted patient-reported GAs as previously described (supplemental eTable 1; available with this article at JNCCN.org).19,20 Our GA comprised the following domains: functional status, comorbidity, cognition, mental health status, nutrition, social support, and health-related quality of life, consistent with recommendations from the International Society of Geriatric Oncology (SIOG).3 We assessed functional status using the Older Americans Resources and Services (OARS) instrumental activities of daily living (IADLs),22 OARS activities of daily living (ADLs),22 patient-reported ECOG PS,23 and number of falls within the last 6 months.24 Nutritional status was evaluated using an abridged version of patient-generated subjective global assessment (PG-SGA).25 Comorbidity assessment was performed using number of medications26 and OARS comorbidity assessment.22,27 We assessed social support using Medical Outcomes Study-Social Support Survey,28 mental health status using the Patient-Reported Outcomes Measurement Information System (PROMIS) Anxiety and Depression measures,29,30 and cognition using the PROMIS Cognitive Function measure.31 Lastly, health-related quality of life was examined using the PROMIS 10-item Global Health tool.32 The GA was completed by the patient. However, if the patient had any vision issues, a member of the study personnel or a primary caregiver could ask the patient the GA questions.

GA Impairments

Based on the GA evaluation, patients were classified as having GA impairment if they met ≥2 of the following criteria33: ≥1 falls in the last 6 months, significant limitation in walking 1 block, impairment in ≥2 IADLs, any ADL impairment, significant weight loss (3% in 3 months or 6% within 6 months), presence of ≥4 comorbidities, poor social support for physical activity, significant interference in social activity, presence of anxiety (T-score ≥60) or depression (T-score ≥60), cognitive impairment (T-score ≤60), or polypharmacy (≥9 medications).

Frailty Index

We constructed a frailty index (the CARE Frailty Index) using the principle of deficit accumulation approach originally described by Rockwood and Mitnitski34 and following the standard procedures outlined by Searle et al.35 Similar methods have been used by Guerard et al4 and Cohen et al36 to construct frailty indices that have been shown to be predictive of chemotherapy toxicity36 and all-cause mortality4 among older adults with cancer. We selected 44 GA variables from the CARE questionnaire, each of which captured a health deficit, and recoded responses using the convention that 0 indicated the absence of the deficit and 1 indicated the presence of deficit; for variables that included a single intermediate response (eg, “sometimes” or “maybe”), we used an additional value of 0.5. We then combined these individual scores into an aggregate frailty score reflecting the overall proportion of deficits (range, 0–1), where 0 = no deficit present and 1 = all 44 deficits present. We then categorized patients as robust (<0.2), prefrail (0.2–0.35), and frail (>0.35), as previously described.35 In case of missing response data, we required that responses to at least 30 items be present to construct a valid frailty index. An index constructed with at least 30 variables has been previously shown to be sufficiently accurate for predicting adverse outcomes among older adults.37 Additional details regarding our definition for GA impairment and construction of the CARE Frailty Index are provided in supplemental eAppendices 1 and 2.

Statistical Analysis

We compared baseline characteristics between the 3 age groups (60–64, 65–74, and ≥75 years) using appropriate bivariate statistical tests, namely, analysis of variance/Kruskal Wallis for continuous variables and chi-square test/Fisher exact test for categorical variables depending on their underlying distribution. To measure the correlation between the number of geriatric impairments (a ranked variable) and chronologic age (continuous variable), we used Spearman rank correlation coefficient and tested the alternative hypothesis that the Spearman ρ was significantly different from 0. We compared the difference in proportion of various GA impairments and frailty categories among increasing age groups (60–64, 65–74, and ≥75 years) using chi-square tests of trend. To evaluate the difference between number of GA impairments across the 3 age groups, we used a nonparametric extension of Wilcoxon rank-sum test.38 All statistical tests were 2-sided and the level of significance was 0.05. We used STATA, version 13 (StataCorp LLC) for all statistical analysis.

Results

Of the 523 consecutive adults aged ≥60 years with gastrointestinal malignancy seen for initial consultation at the UAB medical oncology clinic between September 2017 and October 2019, 455 (87%) enrolled in the CARE registry and underwent GA (supplemental eFigure 1). Of these, 367 (81%) had not started any systemic therapy, whereas the remaining (19%) had previously received treatment elsewhere. The median age of the entire cohort at the time of GA was 68 years (interquartile range [IQR], 64–74 years); 55% were male and 72% were non-Hispanic White. Overall, 28% of the 455 patients were aged 60–64 years, 47% were aged 65–74 years, and 25% were aged ≥75 years. Common cancer types included colorectal (33%) and pancreatic (24%); 46% had stage IV disease. The demographic and clinical characteristics were similar across the 3 age groups, with the exception of marital status and cancer stage, as summarized in Table 1. Compared with nonparticipants, patients enrolled in the CARE registry had similar age, sex, and cancer stage, with the exception of a higher proportion of nonresponders among patients with hepatobiliary and pancreatic cancer (supplemental eTable 2).

Table 1.

Distribution of Baseline Demographic and Clinical Characteristics

Table 1.

Relationship Between Chronologic Age and Geriatric Impairments

There was no significant correlation between chronologic age and number of geriatric impairments (Spearman ρ, 0.07; P=.16). Notably, even in the age group of 60–64 years, 61.4% of patients had GA impairments. This was not significantly different compared with patients aged 65–74 years (66.2%) and ≥75 years (70.5%; P=.11). We found similar rates of impairments in IADLs, ADLs, nutritional status, falls, cognitive, anxiety, depression, polypharmacy, and patient-reported ECOG PS across the age groups. However, there was a higher comorbidity burden (≥3) in the older group (39%, 56%, and 56% among ages 60–64 years, 65–74 years, and ≥75 years, respectively; P<.01) (Table 2). The increased comorbidity burden in the older age groups was mainly driven by a higher proportion of patients reporting arthritis, hypertension, and glaucoma (supplemental eTable 3).

Table 2.

Overall and Domain-Specific Geriatric Impairment and Frailty

Table 2.

Relationship Between Chronologic Age and Frailty

Overall, 37% (n=108) of the cohort were frail, whereas 30% (n=128) were prefrail and 33% (n=143) had robust frailty status. Compared with those who were prefrail or robust, patients who were frail were more likely to have an ECOG PS ≥2 (68% vs 26% vs 4%, respectively; P<.001) and a higher cancer stage (52% vs 42% vs 42%, respectively; P=.03), but did not differ significantly by treatment status (22% vs 20% vs 16%, respectively, were already on treatment; P=.44).

We then compared the rates of frailty categories across the different age groups. Notably, 26% and 35% of patients aged 60–64 years had evidence of prefrail and frail status. This was not significantly different compared with the proportion of patients with prefrail and frail status in the 65–74 age group (30% and 36%, respectively) and ≥75 age group (33% and 40%, respectively) (P=.45).

Discussion

In this study comprising an unselected cohort of older adults aged ≥60 years with gastrointestinal malignancies, we found no significant relationship between chronologic age and the presence of geriatric impairments or frailty. Furthermore, we found comparable prevalence of GA impairments and frailty in the 60–64 age group compared with those aged ≥65 years, suggesting that the traditional cutoff of 65 years for conducting comprehensive GA may not be accurate, and even patients aged <65 years could benefit from GA evaluation.

There is no universal agreement on the age at which a person becomes old. In the United States, age ≥65 years is generally considered the chronologic definition of an older adult, similar to what is used for Medicare eligibility. Accordingly, consensus recommendations for GA from ASCO and SIOG use 65 years as the age cutoff.3,16,17 However, emerging evidence suggests that cancer diagnosis and/or treatment can accelerate the human aging process through multiple mechanisms, including DNA damage and induction of aging-related biologic pathways, such as telomerase activity, DNA hypermethylation, and stem cell exhaustion.18 Hence, the age cutoffs assumed for the general population may not apply to patients with cancer. We postulate that this phenomenon may account for the high prevalence of GA impairments in our cohort aged <65 years.

In a prior study, Aleixo et al21 reported the prevalence of GA impairments among patients aged <65 years with early-stage breast cancer. Patients aged 50 to 64 years had a high prevalence of falls in the past 6 months (15%), abnormal timed up-and-go test >14 seconds (12%), and impaired IADLs (17%). However, patients aged 50 to 64 years comprised <10% of the study population and were derived from exercise intervention trials and compared with patients aged ≥65 years derived from a prospective registry, thus raising a possibility of selection bias. In comparison, our entire cohort includes unselected patients from a cancer registry who underwent initial consultation at the gastrointestinal oncology clinic. However, we report similar findings, with comparable rates of GA impairments and frailty among patients in the 60–65 age group.

Limitations of our study include being a single-institution analysis limited to gastrointestinal malignancies, and therefore our findings may not be generalizable to other settings/populations. The reason for limiting our study to gastrointestinal malignancies was to eliminate the possibility of selection bias as mentioned earlier. Nevertheless, we recognize that our cohort is still quite diverse and there may be substantial variation in the proportion of patients with GA impairment and frailty within individual cancer types and cancer stages. Almost half of our patients had stage IV disease, which may explain the high rate of GA impairments in our study. Notably, another study among patients with early-stage breast cancer reported similar findings.21 All patients who underwent GA evaluation did so at the time of initial contact with the UAB health system. Consequently, not all patients who presented for an initial appointment were previously untreated, and approximately 20% had already undergone cancer therapy at another facility. Furthermore, by limiting our sample to patients completing GA at their initial visit, we may have excluded patients with severe illness requiring hospitalization for urgent treatment or hospice care, such as those with more aggressive malignancies, including hepatobiliary and pancreatic cancers. This may have potentially biased our findings. We did not have data on treatment-related toxicity, treatment discontinuation, or healthcare utilization, which need to be explored in future studies.

Conclusions

Our study adds to the growing body of evidence that chronologic age is an imperfect marker of presence of GA impairment and frailty. Furthermore, GA impairments are seen even among adults aged <65 years, and GA may aid in the clinical management of even younger populations than previously considered.

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Submitted July 2, 2020; final revision received September 25, 2020; accepted for publication October 26, 2020. Published online June 11, 2021.

Previous presentation: This study was presented in abstract form at the 2020 ASCO Virtual Scientific Program; May 29–31, 2020. Abstract 12048.

Author contributions: Study concept and design: Giri, Williams. Data acquisition: Giri, Williams. Data analysis and interpretation: Giri, Williams. Statistical analysis: Giri, Williams. Supervision: Williams, Bhatia. Manuscript preparation: All authors. Critical revision: All authors.

Disclosures: Dr. Giri has disclosed receiving grant/research support from Carevive Systems and Pack Health LLC, and honoraria from Carevive Systems. Dr. Williams has disclosed serving as a consultant for Carevive Systems. The remaining authors have disclosed that they have not received any financial consideration from any person or organization to support the preparation, analysis, results, or discussion of this article.

Funding: This work was supported in part by the Walter B. Frommeyer Fellowship in Investigative Medicine at the University of Alabama at Birmingham and the NCI of the NIH (K08CA234225; G.R. Williams).

Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Correspondence: Smith Giri, MD, MHS, Division of Hematology/Oncology, Institute of Cancer Outcomes and Survivorship, University of Alabama at Birmingham, 1600 7th Avenue South, Lowder 500, Birmingham, AL 35233. Email: smithgiri@uabmc.edu

Supplementary Materials

  • 1.

    Smith BD, Smith GL, Hurria A, et al. Future of cancer incidence in the United States: burdens upon an aging, changing nation. J Clin Oncol 2009;27:27582765.

  • 2.

    Soto-Perez-de-Celis E, Li D, Yuan Y, et al. Functional versus chronological age: geriatric assessments to guide decision making in older patients with cancer. Lancet Oncol 2018;19:e305316.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Wildiers H, Heeren P, Puts M, et al. International Society of Geriatric Oncology consensus on geriatric assessment in older patients with cancer. J Clin Oncol 2014;32:25952603.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Guerard EJ, Deal AM, Chang Y, et al. Frailty Index developed from a cancer-specific geriatric assessment and the association with mortality among older adults with cancer. J Natl Compr Canc Netw 2017;15:894902.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Hurria A, Togawa K, Mohile SG, et al. Predicting chemotherapy toxicity in older adults with cancer: a prospective multicenter study. J Clin Oncol 2011;29:34573465.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Lore Decoster LV, Kenis C, Prenen H, et al. Relevance of geriatric assessment in older patients with colorectal cancer. Clin Colorectal Cancer 2017;16:e221229.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Caillet P, Canoui-Poitrine F, Vouriot J, et al. Comprehensive geriatric assessment in the decision-making process in elderly patients with cancer: ELCAPA study. J Clin Oncol 2011;29:36363642.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Mohile SG, Epstein RM, Hurria A, et al. Communication with older patients with cancer using geriatric assessment: a cluster-randomized clinical trial from the National Cancer Institute Community Oncology Research Program. JAMA Oncol 2020;6:196204.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Reisinger KW, van Vugt JL, Tegels JJ, et al. Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg 2015;261:345352.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Tegels JJ, de Maat MF, Hulsewé KW, et al. Value of geriatric frailty and nutritional status assessment in predicting postoperative mortality in gastric cancer surgery. J Gastrointest Surg 2014;18:439446.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Wagner D, Büttner S, Kim Y, et al. Clinical and morphometric parameters of frailty for prediction of mortality following hepatopancreaticobiliary surgery in the elderly. Br J Surg 2016;103:e8392.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Aaldriks AA, van der Geest LG, Giltay EJ, et al. Frailty and malnutrition predictive of mortality risk in older patients with advanced colorectal cancer receiving chemotherapy. J Geriatr Oncol 2013;4:218226.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Rostoft S. Integration of geriatric assessment in the care of patients with gastrointestinal malignancies. Visc Med 2017;33:275280.

  • 14.

    Siri R, Kristjansson AN, Marit S, et al. Comprehensive geriatric assessment can predict complications in elderly patients after elective surgery for colorectal cancer: a prospective observational cohort study. Crit Rev Oncol Hematol 2010;76:208217.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Lee YH, Oh HK, Kim DW, et al. Use of a comprehensive geriatric assessment to predict short-term postoperative outcome in elderly patients with colorectal cancer. Ann Coloproctol 2016;32:161169.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Mohile SG, Dale W, Somerfield MR, et al. Practical assessment and management of vulnerabilities in older patients receiving chemotherapy: ASCO guideline for geriatric oncology. J Clin Oncol 2018;36:23262347.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Dotan E, Walter LC, Baumgartner J, et al. NCCN Clinical Practice Guidelines in Oncology: Older Adult Oncology. Version 1.2020. Accessed March 7, 2020. To view the most recent version, visit NCCN.org

    • Search Google Scholar
    • Export Citation
  • 18.

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