Characteristics Associated With Functional Changes During Systemic Cancer Treatments: A Systematic Review Focused on Older Adults

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  • 1 Division of Hematology/Oncology, Department of Medicine, James P. Wilmot Cancer Institute, University of Rochester Medical Center, Rochester, New York;
  • | 2 Division of Hematology/Oncology, Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California;
  • | 3 School of Public Health, University of California, Berkeley, Berkeley, California;
  • | 4 Department of Medical Oncology and Therapeutics Research, City of Hope National Medical Center, Duarte, California;
  • | 5 Department of Adult and Family Medicine, Kaiser Permanente, San Francisco, California;
  • | 6 Division of Medical Oncology, Department of Internal Medicine, The Ohio State University Comprehensive Cancer Center, Columbus, Ohio;
  • | 7 Edward G. Miner Library, University of Rochester School of Medicine and Dentistry, Rochester, New York; and
  • | 8 Division of Geriatrics, University of California, San Francisco, and
  • | 9 San Francisco Veterans Affairs Medical Center, San Francisco, California.

Background: Maintaining functional status is important to older adults with cancer, but data are limited on how systemic treatments affect functional status. We systematically reviewed changes in functional status during systemic cancer treatments and identified characteristics associated with functional decline and improvement. Methods: We searched PubMed, Embase, Web of Science, and Cochrane Register of Controlled Trials for articles examining characteristics associated with functional changes in older adults during systemic cancer treatment published in English between database inception and January 11, 2019 (PROSPERO CRD42019123125). Findings were summarized with descriptive statistics. Study characteristics between older adult–specific and non–older adult–specific studies were compared using the Fisher exact test. Results: We screened 15,244 titles/abstracts and 519 full texts. The final analysis included 44 studies, which enrolled >8,400 patients; 39% of studies focused on older adults (1 study enrolled adults aged ≥60 years, 10 enrolled adults aged ≥65 years, and 6 enrolled adults aged ≥70 years). Almost all studies (98%) used patient-reported outcomes to measure functional status; only 20% used physical performance tests. Reporting of functional change was heterogeneous, with 48% reporting change scores. Older adult–specific studies were more likely to analyze functional change dichotomously (29% vs 4%; P=.008). Functional decline ranged widely, from 6% to 90%. The most common patient characteristics associated with functional decline were older age (n=7 studies), worse performance status (n=4), progressive disease status (n=4), pain (n=4), anemia (n=4), and worse nutritional status (n=4). Twelve studies examined functional improvement and identified 11 unique associated characteristics. Conclusions: Functional decline is increasingly recognized as an important outcome in older adults with cancer, but definitions and analyses are heterogeneous, leading to a wide range of prevalence. To identify patients at highest risk of functional decline during systemic cancer treatments, trials need to routinely analyze functional outcomes and measure characteristics associated with decline (eg, nutrition).

Background

Older adults with cancer are at increased risk for treatment toxicity and functional impairment,14 resulting in increased healthcare use and mortality.510 Maintaining functional status (FS) during cancer treatment is critically important to patients. More than 70% of older patients with cancer report that they would not choose a treatment that results in functional impairment, even if it improves survival.11 Despite the importance of functional outcomes to older adults, cancer clinical trials rarely capture the full impact of treatment on FS. Instead, trials focus on narrow definitions of treatment toxicity using provider-reported adverse effects,12 which do not capture FS or changes over time. As a result, limited data are available on how cancer treatments affect FS in older adults, hindering delivery of goal-concordant care.

Understanding how FS may change during systemic cancer treatment (eg, chemotherapy, immunotherapy, targeted therapy) and which patient characteristics are associated with these changes can inform shared decision-making to individualize cancer care. Identifying which patients are at highest risk of functional decline is necessary to weigh the potential benefits and harms of treatment options, to better inform patient and caregiver anticipatory guidance, and to enable early introduction of tailored interventions, such as exercise and rehabilitation programs, to prevent functional impairment.1315

Given the increasing recognition of the importance of FS in older adults with cancer16 and the explosion of new cancer treatments, an increasing number of studies have examined characteristics associated with FS change during treatment. Although a prior systematic review examined the prognostic and predictive value of FS at baseline,10 no review has systematically synthesized the literature on changes in FS during systemic cancer treatment. Therefore, we aimed to examine changes in FS during systemic cancer treatments with a focus on older adults and to identify patient characteristics associated with functional decline and improvement.

Methods

Search Strategy and Selection Criteria

This systematic review was conducted in accordance with the 2009 PRISMA guidelines.17 With a medical librarian (D.A. Castillo), we searched PubMed, Embase, Web of Science, and Cochrane Central Register of Controlled Trials for articles examining changes in FS during systemic cancer treatment among adults aged ≥65 years published in English between database inception and January 11, 2019. Full search terms are shown in supplemental eTable 1 (available with this article at JNCCN.org) and included the following: “neoplasms,” “cancer,” “malignancy,” or “tumor,” AND “chemotherapy,” “immunotherapy,” or “antineoplastic,” AND “functional status,” “functional decline,” “physical function,” “mobility,” “daily living activity,” or “activities of daily living.” This systematic review is registered with PROSPERO (CRD42019123125).

Studies were evaluated using these inclusion criteria: (1) the study included patients aged ≥65 years with any cancer type; (2) participants received systemic cancer therapy; (3) FS was quantitatively measured using physical performance tests, patient-reported outcomes (PROs; eg, instrumental activities of daily living [IADLs]), physical well-being as part of a quality-of-life measure, physical activity (eg, step count), and/or clinician-reported performance status (PS); (4) FS was measured at ≥2 time points (one before or during treatment such that change in FS during treatment could be ascertained); (5) FS was analyzed as an outcome; (6) the study reported an analysis of associations between patient characteristics and change in FS; and (7) the study was published in English. Studies of systemic therapy and other treatment modalities (eg, surgery) were included only if they reported results separately for patients who received systemic therapy. Notably, studies of concurrent chemoradiation were allowed because chemoradiation is the standard of care for some cancer types (eg, head and neck). In addition, studies of FS interventions (eg, exercise) were required to have control arms to allow evaluation of the effect of systemic cancer treatment on FS. Exclusion criteria included the following: (1) studies of hormone therapy, radiation, or surgery alone; (2) articles that did not report original data; and (3) full text was unavailable.

All identified articles were imported into Covidence (Veritas Health Innovation) and duplicates were removed. At each step described, discrepancies were resolved by consensus. Two investigators independently screened each title and abstract for eligibility. This evaluation was then repeated for full-text review. The final list of included full texts was used for data extraction.

Data Extraction and Quality Appraisal

A standardized template for data extraction was pilot tested. Two investigators independently extracted data for each study. Extracted data included first author, publication year, journal, geographic region, study design, intervention and control arms (if applicable), key inclusion criteria, sample size, age distribution, cancer treatment(s), measure(s) of FS, time points assessed, definition of change in FS, key findings, and characteristics associated with functional change.

Two investigators independently performed each appraisal of study quality using the National Heart, Lung, and Blood Institute (NHLBI) Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies, which consists of 14 criteria.18 Example criteria included clearly defined research question, study population, inclusion criteria, and exposure and outcome measures. Participation rate and loss to follow-up were also considered. Meeting each criterion earned 1 point, and a summary score was calculated.

Data Analysis

Descriptive statistics were used to summarize study characteristics, including cancer type, measures of FS used (PROs, clinician-reported PS, physical performance test), assessment time points, and analytic approach. Fisher exact test was used to compare study characteristics between older adult–specific and non–older adult–specific studies. Characteristics associated with functional decline and improvement were summarized. No meta-analysis was planned a priori, given the heterogeneity in measures used to assess FS, cancer populations studied, and analytic methods.

Results

Study Characteristics

We screened 15,244 titles/abstracts and 519 full texts (supplemental eFigure 1). The final analysis included 44 studies,1,2,1960 which were published from 1991 to 2019 (Figure 1) and enrolled >8,400 patients with cancer. Seventeen studies (39%) focused on older adults (supplemental eTable 2), whereas 27 (61%) included adults of all ages (supplemental eTable 3). Among the older adult–specific studies, which increased in number in recent years (Figure 1), one study enrolled only adults aged ≥60 years,19 10 enrolled only adults aged ≥65 years,1,2,2027 and 6 enrolled only adults aged ≥70 years.2833 One-fourth of studies enrolled a heterogeneous population of patients with a solid or hematologic malignancy, and one-fourth enrolled patients with lung cancer. The next most common cancer types were breast cancer (16%) and hematologic malignancies (16%). Most studies (84%) evaluated FS during chemotherapy, with only 532,33,36,59,60 including targeted therapy and 254,59 including immunotherapy.

Figure 1.
Figure 1.

Included studies, by publication year.

Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 2021; 10.6004/jnccn.2020.7684

Quality Assessment

Using the NHLBI Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies, we found that the mean quality assessment score was 9.86 (range, 7–13; supplemental eTables 2 and 3). The most common reasons for lower study quality were lack of participation rate reporting, lack of sample size justification, loss to follow-up ≥20%, and lack of adjustment for confounders. Outcome assessors were often not blinded to the patient’s exposure status (eg, demographics). Only 59% of studies adjusted for key potential confounders in their analyses between patient characteristics and FS change.

Measures of FS

Almost all studies (98%) used PROs to measure FS (Table 1). The most commonly used PRO was the EORTC Quality of Life Questionnaire-Core 30 (QLQ-C30) physical functioning scale61 (34% of studies). Patient-reported activities of daily living (ADLs) (20%) and IADLs (16%) were also commonly used. Physical performance was tested in 20% of studies, with grip strength, chair stands, and walk tests being the most common. Traditional oncology measures of PS (eg, ECOG PS) were uncommon among included studies. There were no statistically significant differences in FS measures used in older adult–specific versus non–older adult–specific studies.

Table 1.

Measures of Functional Status, Assessment Time Points, and Analytic Approach

Table 1.

Assessment Time Points and Analytic Approach to FS

Most studies assessed FS before starting systemic therapy and at 1 (20% of studies), 2 (14%), or ≥3 (50%) follow-up time points, whereas 16% of studies performed the first assessment after therapy had started (Table 1). Analyses of FS change were heterogeneous, with many reporting change scores between 2 assessments (48% of studies). Only 32% of studies used longitudinal methods to examine trajectories of FS over ≥2 time points. The remaining studies analyzed FS change dichotomously by defining cutoff scores for decline and/or improvement (14% of studies), time to deterioration (5%), or association with patient-reported change (2%). Older adult–specific studies were more likely to analyze FS change dichotomously (29% of older adult–specific studies vs 4% of non–older adult–specific studies; P=.008).

Changes in FS and Associated Characteristics

Among studies that reported the percentage of patients who developed functional decline, results ranged widely, from 6%21 to 90%,33 depending on the cancer type, treatment, measure of FS, and timing of assessments (supplemental eTables 2 and 3). Functional improvement occurred in between 9%55 and 57%21 of patients. The most common patient characteristics associated with functional decline during systemic cancer therapy (Table 2) were older age (7 studies1,2,38,39,42,47,51), worse PS (4 studies35,39,52,60), progressive disease status (4 studies2,31,35,60), pain (4 studies24,35,39,45), anemia (4 studies1,20,24,47), and worse nutritional status (4 studies2,3133). Definitions of these characteristics are listed in Table 2.

Table 2.

Common Characteristics Associated With Functional Decline During Systemic Treatmenta

Table 2.

Only 12 studies19,22,27,29,34,4043,46,51,56 examined characteristics associated with functional improvement. Three articles34,51,56 reporting results of a study of acute myeloid leukemia found that younger age was associated with greater improvement in timed chair stands during intensive chemotherapy. Lower symptom burden was associated with greater improvement in FS in 3 studies.22,40,41 Additional characteristics associated with greater functional improvement included female sex,56 married status,22 baseline functional dependence,27 better cognition,19 lack of depression,41 higher hemoglobin,42 cancer type,43,46 and <4 positive nodes (in a breast cancer study).22 In a randomized controlled trial of a cognitive behavioral therapy intervention, worse comorbidity was associated with greater improvement in FS in the intervention arm.41

Discussion

Over almost 3 decades of research from 1991 to 2019, we identified only 44 studies that included older adults and rigorously examined patient characteristics associated with FS change during systemic cancer treatment. Although the increasing number of studies in more recent years is promising, especially the increasing number of older adult–specific studies, the relative lack of studies examining FS as a longitudinal outcome highlights the importance of synthesizing the existing data and the ongoing need to add this patient-centered outcome to cancer clinical trials and observational cohort studies.

This systematic review identified a substantial amount of heterogeneity between studies in how FS is measured, when it is assessed during systemic cancer treatment, and how it is analyzed, limiting direct comparisons between studies. For example, functional decline was identified in 6% of women aged ≥65 years with breast cancer in a trial of adjuvant therapy using patient-reported worsening physical condition.21 In contrast, with use of ADLs, functional decline was identified in 90% of adults aged ≥70 years with advanced non–small cell lung cancer receiving chemotherapy.33 Study populations also differed widely in cancer types and specific treatments evaluated. However, most studies included only chemotherapy, revealing a gap in understanding of the functional impact of immunotherapy and targeted therapy, which are key components of modern cancer care.

FS was most commonly assessed using PROs (98% of studies), such as the EORTC QLQ-C30.61 The widespread use of PRO measures to assess FS among patients with cancer mirrors the broader surge of PROs used to assess symptoms and adverse effects during routine cancer care and in trials.6265 Advantages of PRO FS measures in clinical care include the ability to assess FS outside of busy clinic visits (eg, previsit questionnaire), remotely without an in-person component (which is increasingly important during the COVID-19 pandemic), and with potentially fewer resources than available when conducting a physical performance test. PROs also allow FS to be more easily studied longitudinally in clinical trials or observational cohort studies in which FS is not the primary outcome. Compared with physical performance tests, PROs are more representative of the patient perspective about their FS. Furthermore, patient-reported functional decline in ADLs is a strong predictor of overall survival among older adults with cancer.31

Several challenges existed in the analysis of FS changes during systemic treatment. There were no uniform definitions of clinically meaningful functional decline or improvement. Despite half of the included studies measuring FS at ≥3 follow-up assessments, >60% only analyzed data from 2 time points, effectively ignoring informative patient-centered information. To illustrate, 48% of studies analyzed longitudinal FS as a change score between 2 assessments, and 14% used a threshold definition of a dichotomous functional decline outcome. Although these types of analytic approaches may assist in clinical interpretation (eg, percentage of patients who experience functional decline after one cycle of chemotherapy30), they do not capture FS trajectories that may include both declines and improvements. In contrast, Hurria et al22 combined more nuanced changes in FS over time and clinically applicable results by conducting 4 analyses using dichotomous outcomes to examine functional decline at the end of adjuvant breast cancer chemotherapy, functional decline at 12 months, improvement of FS among those with decline, and resistance to decline. This study exemplifies an alternative analytic approach that examines several time points and several definitions of FS change.

Older age, which was defined differently across studies, was the most common characteristic associated with functional decline. However, because many studies did not adjust for comorbidity, which is more common among older adults66 and associated with functional decline,5,24,29,49 there may have been residual confounding. We also found that worse PS, comorbidity, worse nutrition, presence of pain, and anemia were associated with functional decline, highlighting the importance of assessing and addressing these concerns. Evaluation of these characteristics and other domains important to older adults (eg, cognition) through geriatric assessment67 is necessary to comprehensively risk-stratify patients. Geriatric assessment results can guide recommendations to address modifiable risk factors via supportive care interventions (eg, physical therapy for worse PS) and comanagement with a multidisciplinary team (eg, palliative medicine for pain, dietitian for malnutrition).68

Some older adults with cancer do not experience functional decline during systemic treatment, some experience decline but later improve, and some never improve. “Resilience” refers to the process of adapting well in the face of a stressor69 or simply the ability to recover to baseline.22,70 Understanding characteristics associated with functional improvement can guide conversations regarding cancer treatment, because patients may be more willing to undergo treatment if they are likely to recover. Future studies should evaluate the underlying mechanisms by which these characteristics lead to functional improvement, which can guide development of interventions.

This systematic review had several limitations. First, our review focused on the effects of systemic cancer therapy on FS changes and did not examine surgery or radiation. Second, we included only studies that reported results separately for patients who received systemic therapy. Therefore, studies were excluded that examined FS changes in a heterogeneous sample of patients with cancer receiving a variety of treatments. In addition, we focused on studies examining patient characteristics associated with functional decline and improvement rather than performing a comprehensive review of the prevalence of functional change. Finally, because of heterogeneity of patient populations, FS measures, time points, and analytic approaches, a meta-analysis was not possible.

Future studies of cancer treatments in older adults, particularly beyond chemotherapy, must include serial FS measures and analyze these data to determine which older patients are at highest risk of functional decline and which may be more resilient. Measurement of characteristics associated with functional decline, such as nutritional status, which is absent from many trials, is equally important. This is especially critical given the rapidly evolving treatment landscape and the need to understand how newer therapies impact older adults. Many cancer trials already contain a collection of valuable, unanalyzed FS information as part of broader quality-of-life questionnaires. These data have the potential to greatly expand the knowledge base on FS changes during cancer treatment and to inform shared decision-making with information on this important patient-centered outcome.

Furthermore, the development of risk prediction tools, such as risk scores or nomograms, would make information about characteristics associated with FS change more clinically accessible for patient care and shared decision-making. Examples of successful translations of research data into clinical practice include the Cancer and Aging Research Group chemotherapy toxicity calculator71,72 and the ePrognosis.org collection of prognostic indices (https://eprognosis.ucsf.edu/).73 Studies of FS changes among older adults with the same cancer type are also needed to make results less heterogeneous and more clinically applicable.

Conclusions

There is increasing recognition that change in FS is an important outcome among older patients with cancer receiving systemic treatment. However, definitions and analyses of functional decline and improvement are heterogeneous, leading to a wide range of prevalence. To better understand functional decline and improve outcomes in this vulnerable population, measures of FS outcomes need to be incorporated with traditional oncology outcomes.

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Submitted August 7, 2020; accepted for publication November 3, 2020.

Author contributions: Literature search: Loh, Lam, Castillo, Wong. Study design: Loh, Lam, Webber, Castillo, Walter, Wong. Data analysis and interpretation: Loh, Lam, Webber, Padam, Sedrak, Musinipally, Grogan, Presley, Grandi, Sanapala, DiGiovanni, Mohile, Walter, Wong. Manuscript preparation: Loh, Lam, Wong. Critical revision: All authors.

Disclosures: Dr. Loh has disclosed serving as a consultant for Pfizer and Seattle Genetics. Dr. Sedrak has disclosed receiving grant/research support from Seattle Genetics, Novartis, Eli Lilly, and Pfizer. Dr. Wong has disclosed having an immediate family member who is employed of Genentech with stock ownership. 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: Research reported in this publication was supported by the NCI of the NIH under award numbers K99CA237744 (K.P. Loh) and K12CA001727 (M.S. Sedrak); the National Institute on Aging of the NIH under grants R03AG064377 (M.S. Sedrak), K24AG056589 and R33AG059206 (S.G. Mohile), P30AG044281 (L.C. Walter and M.L. Wong), and K76AG064431 and R03AG056439 (M.L. Wong); a Wilmot Research Fellowship Award (K.P. Loh); and funding from the University of California, San Francisco Helen Diller Family Comprehensive Cancer Center (M.L. Wong).

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

Correspondence: Melisa L. Wong, MD, Divisions of Hematology/Oncology and Geriatrics, Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, 550 16th Street, Box 1770, San Francisco, CA 94143. Email: melisa.wong@ucsf.edu

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    Yourman LC, Lee SJ, Schonberg MA, et al. . Prognostic indices for older adults: a systematic review. JAMA 2012;307:182192.

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