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Oncology Section EDGE Task Force on Cancer: Measures of Cancer-Related Fatigue—A Systematic Review

Fisher, Mary Insana, PT, PhD1; Davies, Claire, PT, PhD2; Lacy, Hannah, PT, DPT3; Doherty, Deborah, PT, PhD4

doi: 10.1097/01.REO.0000000000000124
META ANALYSIS & SYSTEMATIC REVIEWS

Background: Cancer-related fatigue (CRF) is one of the most common side effects of cancer and cancer treatment. Being able to accurately screen for and assess CRF will improve access to and prescriptions for interventions. Valid and reliable measures to screen for and assess CRF need to be identified.

Purpose: To identify and recommend reliable, valid, and clinically useful tools to screen for and assess CRF among those treated for cancer.

Methods: A systematic review of the literature was conducted to assess the published psychometric properties and clinical feasibility of each method identified. Task force members independently reviewed each measure using the Cancer EDGE Rating Form.

Results: Review of 136 studies resulted in recommendations for 14 questionnaires. Five unidimensional and 9 multidimensional questionnaires are recommended by the Oncology EDGE Task Force.

Conclusion: The 10-point Numeric Rating Scale for Fatigue is best as a screening tool, whereas the Multidimensional Fatigue Symptom Inventory is a highly recommended multidimensional tool. Ease of screening can promote referral for interventions, whereas thorough assessment drives appropriate interventions.

1Board-Certified Orthopedic Physical Therapist; Certified Lymphedema Therapist; and Associate Professor, Department of Physical Therapy, University of Dayton, Dayton, OH

2Certified Lymphedema Therapist—LANA; and Physical Therapist, Rehabilitation Services, Baptist Health, Lexington, KY

3Physical Therapist, Good Samaritan Hospital, Dayton, OH

4Associate Professor, Human Movement Science Department, Oakland University, Rochester, MI

Correspondence: Mary Insana Fisher, PT, PhD, Department of Physical Therapy, University of Dayton, 300 College Park, Dayton, OH 45469 (mary.fisher@udayton.edu).

Grant support: Funding for conference travel was provided to M. I. Fisher by the Oncology Section.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.rehabonc.com).

The authors acknowledge no conflicts of interest.

Cancer-related fatigue (CRF) is one of the most common side effects of cancer treatment and is not specific to any cancer diagnosis but rather impacts up to 96% of survivors at any point along the survivorship continuum.1 Cancer-related fatigue is defined as a distressing, persistent, subjective sense of physical, emotional, and/or cognitive tiredness or exhaustion related to cancer or its treatment that is not proportional to recent activity and interferes with usual functioning.2 One of the most important considerations, and one often used to assist in diagnosis, is the criterion that CRF is not relieved by rest.2 This sense of fatigue is perceived not only physically but also cognitively and emotionally.3 Fatigue is reported most consistently in those undergoing chemotherapy, whether in isolation or in conjunction with radiation therapy, but may persist after treatment.4 , 5 Research indicates that for at least a subset of patients, CRF may be a significant issue long into survivorship, with a negative effect on quality of life (QOL).6 , 7

Diagnosing CRF is complicated by the multidimensional nature of the fatigue, such as whether it is centrally or peripherally mediated,8 and that this fatigue may be secondary to other side effects of treatment, such as anemia. Along with anemia, cancer treatments themselves, cancer recurrence, pain, medications, sleep disturbances, psychosocial issues including depression and anxiety, malnutrition, decreased functioning, increased proinflammatory cytokines, and immobility are all contributing factors.9 , 10 Other pathophysiological considerations for fatigue include abnormality in growth factors, circadian rhythm modulation, hypothalamic-pituitary-adrenal axis disruption, serotonin dysregulation, vagal afferent activation, abnormalities of the generation of and/or use of adenosine triphosphate, and mitochondrial biogenesis.9 , 11 , 12 Despite this multifactorial causality for CRF, health care providers must be able to screen for CRF and make appropriate referrals, including to physical therapists. Physical therapists, in turn, must be able to accurately and comprehensively assess CRF to appropriately treat this debilitating condition.

Accurate screening and assessment are dependent upon tools that demonstrate strong psychometric properties. Ideal screening tools are simple and efficient to administer, whereas assessment tools should provide a deeper understanding of the problem. The tools must be valid, reliable, and, if used as an outcome measure, sensitive to change. Following the ongoing work of the Evidence Database to Guide Effectiveness (EDGE) Task Force of the Oncology Section of APTA, a review of tools purported to screen for and assess CRF was conducted for the strength of their psychometric properties. The purpose of this systematic review is to identify a core set of both screening and assessment measures that are reliable, valid, responsive, and clinically feasible to assess CRF.

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METHODS

Search Strategy

The task force conducted a systematic review of methods and tools used to screen for and assess CRF in order to identify reliable, valid, and clinically feasible methods that are responsive to change that measure CRF in persons diagnosed with cancer. The primary literature search took place from May 2016 through September 2016 using 5 electronic databases: Google Scholar, PubMed/MEDLINE, CINAHL, EMBASE, and PEDro. Primary search terms used included “cancer,” “CRF,” “reliability,” and “validity.” Search terms included “cancer related fatigue,” “cancer-related fatigue,” “fatigue AND cancer,” AND measures, measurements, questionnaires, AND psychometrics. Additional search terms for the specific clinical measuring tools are given in the Appendix (see Supplemental Digital Content 1, http://links.lww.com/REHABONC/A6). A secondary search was completed in August 2017 to update any new evidence.

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Article Selection

To be included in this review, studies (1) had to have been published in English; (2) described tools used to screen for or assess CRF; (3) reported psychometric properties of the tools used to screen or assess CRF; (4) presented clinically feasible methods for the screening and assessment of CRF; (5) included the adult population (≥18 years); and (6) were published between January 1, 1997, and August 2017. Excluded articles demonstrated a lack of evidence, included the pediatric population, or were not considered to be a fatigue screening or assessment tool. This final exclusion criterion included any scale that evaluated the effect of fatigue or CRF on health-related QOL. If a study published prior to 1997 was deemed a key article to either explain the measure or was foundational in establishing the psychometrics of a test, it was then included. After retrieving all articles, the duplicates were removed. All studies were initially screened on the basis of title and abstract and then on the basis of full text.

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Data Extraction and Analysis

Each article was classified as either unidimensional or multidimensional according to the Breast Cancer EDGE Task Force Outcomes: Evidence-Based Cancer-Related Fatigue Measurement Tools.13 Unidimensional tools are commonly considered a fatigue-specific tool, with one or a few questions to identify the presence and severity of CRF, whereas multidimensional measures often examine the effect of CRF across several domains of patient function that may include behavioral, cognitive, somatic, and affective. For the purposes of this review, the authors consider unidimensional tools to be those that often serve to screen for the presence of the condition or assess only a single factor of fatigue whereas the multidimensional tool provides a more thorough assessment of the fatigue.

Each article was reviewed by 2 teams of 2 reviewers who independently performed data extraction using the Cancer EDGE Task Force Rating Form (see Supplemental Digital Content 2, Figure 1, http://links.lww.com/REHABONC/A5). Psychometric properties included in the Cancer EDGE Task Force Rating Form consist of reliability, validity, ceiling/floor effects, sensitivity to change, and clinical utility. Because CRF tools are self-report questionnaires, the types of reliability evaluated included test-retest reliability and internal consistency. Internal consistency examines whether the items on different questionnaires reliably measure the same thing. The following criteria were applied to describe the strength of the psychometric properties: excellent reliability, 0.90 or more; good reliability, 0.76 to 0.89; moderate reliability, 0.50 to 0.75; and poor reliability, less than 0.50.14 Criterion and construct validity including concurrent, divergent, discriminative, and predictive validity values is reported when available, as well as measures assessing responsiveness to change such as minimal detectable change and minimal clinically important difference. Each reviewer then rated the measure using the updated Cancer EDGE Rating Scale (Figure 2).15 Any discrepancies in ratings were discussed with all 4 reviewers until consensus was obtained.

Fig. 2

Fig. 2

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RESULTS

The literature search initially found 626 articles that included CRF measures. After duplicate studies were removed and the inclusion criteria were applied, 136 articles were reviewed. See Figure 3 for the flowchart.

Fig. 3

Fig. 3

Five unidimensional measures and 9 multidimensional tools are recommended for use. Among the unidimensional CRF questionnaires, 3 are highly recommended (4 rating): Modified Brief Fatigue Inventory (mBFI); Cancer-Related Fatigue Distress Scale; and a 10-point Rating Scale for Fatigue. Two unidimensional tools are recommended (3 rating): MD Anderson Symptom Inventory and Wu Cancer Fatigue Scale. Tables 1 and 2 summarize the features and ratings for the recommended measures. Seven scales received ratings of 1 (not recommended) or 2 (reasonable to use) and are not reviewed in detail. Table 3 lists measures that are reasonable to use or not recommended, with summary rationale. Table 4 provides a summary of the clinical usefulness of the recommended measures.

TABLE 1

TABLE 1

TABLE 2

TABLE 2

TABLE 3

TABLE 3

TABLE 4

TABLE 4

Only one multidimensional tool is highly recommended by the Cancer EDGE Task Force and that is the Multidimensional Fatigue Symptom Inventory. Eight CRF measurement tools received a recommended rating of 3: Bidimensional Fatigue Scale, Cancer Fatigue Scale, Fatigue Symptoms Inventory, Multidimensional Fatigue Inventory, Piper/Quick Piper, Profile of Mood States, Patient Reported Outcome Measure Information System (PROMIS) Cancer Fatigue Short Form, and Schwartz Cancer Fatigue Scale. See Tables 5 (reliability and sensitivity to change) and Table 6 (validity) for details on the psychometric properties of all recommended (rated 3 and 4) tools.

TABLE 5

TABLE 5

TABLE 6

TABLE 6

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DISCUSSION

Accurate diagnosis of CRF is important to guide treatment. Researchers propose that 4 criteria be considered to establish the diagnosis of CRF, including (1) a period of 2 weeks or longer within the preceding month during which significant CRF or diminished energy was experienced each day or almost every day along with additional CRF-related symptoms; (2) the experience of CRF resulting in significant distress or impairment of function; (3) the presence of clinical evidence suggesting that CRF is a consequence of cancer or cancer therapy; and (4) fatigue is not primarily a consequence of a concurrent psychiatric condition, such as major depression.12 Before the diagnosis of CRF is made, it is important that the results of a full medical workup rule out other causes of fatigue such as anemia, endocrine dysfunction, or fatigue directly related to prescription medication. The standardization and comprehensive fatigue assessment guidelines and criteria for clinical practice developed by National Comprehensive Cancer Network (NCCN) were prepared to improve assessment and management of CRF. This review provides evidence to consider when determining the most valid and reliable tools to screen for and assess CRF.

This systematic review resulted in 3 highly recommended unidimensional tools and a single multidimensional tool to screen for or measure CRF. These tools have strong psychometric properties in the population of interest and can be easily used by clinicians. Several other tools are recommended; these have good psychometric properties in the population of interest and are clinically feasible.

Among the unidimensional tools that are either rated 3 or 4 by this task force, the use of a 10-point Rating Scale of Fatigue stands out as the most efficient method to screen for the presence of CRF. An understanding of Numeric Rating Scales (NRSs) and Visual Analog Scales (VASs) is warranted when considering this tool. Numeric Rating Scales, where 0 (absence of a construct) and 10 (worst imaginable experience of a construct) are commonly used clinically to assess the severity of symptoms and most commonly used for pain assessment. The VAS, too, is a frequently employed tool to measure severity of symptoms and consists of a 100-mm line, with markings from 0 to 100 every 10 mm along the line. In evaluating the literature, the authors found a total of 11 studies that used either the NRS or the VAS in examining psychometric qualities of instruments evaluating fatigue. Further analysis of these research studies reveals that the term “NRS” is often used to mean VAS (a written expression of severity); in one case, the VAS was converted to an NRS for telephone interviewing yet was not identified as an NRS in study methodology. While this overlap of terms and rating techniques results in inconsistencies in administration, the overall intent of both methods is based on the premise of rating severity as low to high on a 10-point scale. In the literature search completed by this task force, these 10-point scales had multiple names: NRS for Fatigue, VAS for Fatigue, the One-Item Fatigue Scale, the Single-Item Screening Tool, and the Fatigue Numerical Scale.

The simplicity of a 10-point Numeric Rating Scale for Fatigue makes it an ideal screening tool. The question, “How would you rate your fatigue on a scale of 0 to 10, with 0 being no fatigue and 10 being the worst possible fatigue?” whether verbally or along a 100-mm line, is quick and focused. This simple question captures the presence and intensity of fatigue and can be easily used to drive a referral for greater assessment.2 The simplistic nature of the question belies the strength of the psychometric properties, which demonstrate good test-retest reliability (r = 0.88) and convergent validity with the Fatigue Symptom Index, the Functional Assessment of Chronic Illness Therapy–Fatigue (FACIT-F), and the Multidimensional Fatigue Inventory (general fatigue).31–33 This tool also demonstrates moderate to good sensitivity (0.70-0.85) and specificity (0.61-0.71).31 , 34 The NCCN Guidelines for CRF recommend a referral with a score of 4 or greater.2 While the NCCN Guidelines are most frequently followed, an empirical cutoff score of 5 was derived by taking into consideration an analysis of specificity and sensitivity and based on the area under the curve (0.71).34 Given that the ease and level of efficiency in administration is high, a 10-point Rating Scale for Fatigue receives a highly recommended score by the task force and is an ideal screening tool.

Both the mBFI and the Cancer-Related Fatigue Distress Scale, while unidimensional, are more time-intensive, which may discourage their use to screen for fatigue. The mBFI examines the severity and effect of fatigue on daily functioning in the previous 24 hours through a 9-item questionnaire that can be administered via self-report, interview, or interactive voice recording. Each item is rated 0 to 10, and a global score of fatigue is the average of all items. The mBFI has good to excellent test-retest reliability (0.89-0.95)81 and demonstrates both construct validity with the Multidimensional Fatigue Inventory (Short Form) (r = 0.814)81 and concurrent validity with the FACIT-F scale (r = −0.838 to 0.903).82 The Cancer-Related Fatigue Distress Scale assesses the dimension of distress related to fatigue and examines this in terms of physical, social, psychological, cognitive, and spiritual areas. This 20-item self-report scale evaluates statements on a 0 to 10 scale; higher numbers indicate greater distress.28 The Cancer-Related Fatigue Distress Scale demonstrates excellent item consistency (α = 0.98), good convergent validity with the Wu Cancer Fatigue Scale (r = 0.84), as well as good predictive validity (r = 0.83).83 Understanding the effect of fatigue and the distress experienced can guide clinicians in treatment decisions.

The MD Anderson Symptom Inventory and the Wu Cancer Fatigue Scale, while recommended by the task force, do not possess the strengths of psychometric properties or ease of use that the highly recommended measures possess. The MD Anderson Symptom Inventory is a 19-item self-report scale that examines severity and interference of CRF; higher scores indicate greater levels of fatigue.35 This scale demonstrates acceptable levels of convergent validity with the Brief Fatigue Inventory (r = 0.84) but lower levels with the European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire 30 (EORTC QLQ-C30) (r = −0.60) and lacks sensitivity to change.36 The Wu Cancer Fatigue Scale scores 9 items on a 1- to 5-point Likert scale, with higher values indicating greater fatigue.29 The internal consistency of items is high (α = 0.95),30 but the convergent, concurrent, and predictive validity levels are lower (see Tables 5 and 6). Both are acceptable for use, as they take less than 10 minutes to complete; however, a 10-point Rating Scale for Fatigue remains a better screening tool and the mBFI a stronger unidimensional tool for assessing CRF.

The only highly recommended multidimensional fatigue tool recommended by the Cancer EDGE Task Force, the Multidimensional Fatigue Symptom Inventory (Short Form), examines fatigue in the context of global, somatic, cognitive, and behavioral manifestations across general, physical, emotional, and mental domains.38 , 39 This scale, with 30 self-reported items, takes less than 10 minutes to complete, with each item scored on a 5-point Likert scale; higher numbers indicate greater fatigue. The Multidimensional Fatigue Symptom Inventory provides a comprehensive examination of fatigue across multiple domains, with a high sensitivity to change and an ability to discriminate not only between those with and without fatigue but also among those with differing levels of function due to fatigue,38 and demonstrates moderate to high correlations with other established scales (Fatigue Symptom Inventory, r = 0.82 and SF-36 [36-item Medical Outcomes Questionnaire Short Form], r = −0.82).39

The recommended multidimensional tools outlined in Table 2 are adequate alternatives for the clinicians to comprehensively assess CRF. Each takes less than 10 minutes to complete and demonstrates adequate psychometric properties. The 11-item self-report Bidimensional (Chalder) Fatigue Scale measures the extent and severity of fatigue on a 4-point Likert scale, with a higher global score indicating greater fatigue, or 2 subscale scores (physical and psychological).42 Specifically designed to assess CRF, the Cancer Fatigue Scale is a 15-item self-report scale that takes approximately 2 minutes to complete. It examines fatigue across the physical, affective, and cognitive domains using a 5-point Likert scale, with higher scores indicating greater fatigue.45 The Fatigue Symptom Inventory uses 14 items scored 0 to 10 to assess the severity, frequency, and daily pattern of fatigue, as well as how it interferes with QOL, scored low to high either globally or by subscale.48 The Multidimensional Fatigue Inventory, a 20-item, 5-point Likert questionnaire scored inversely (higher values mean lower fatigue), measures fatigue across general, mental, and physical domains, with consideration for reduced activity and reduced motivation.55 As one of the more well-known fatigue measures, the Piper (22 items)/Quick Piper (15 items) Fatigue Scale assesses fatigue across the temporal, sensory, affective, and intensity/severity domains using a 0- to 10-point VAS, with higher scores indicating greater fatigue.59 The Profile of Mood States-2 assesses fatigue-inertia as one of the 7 mood states, using 35 items scored on a 5-point Likert scale, with higher values indicating greater levels within each mood state.84 The PROMIS assesses fatigue in the past week using a 7-item self-report scale, scored with a 1- to 5-point Likert scale, where higher scores indicate greater fatigue.71 And finally, the Schwartz Cancer Fatigue Scale, developed specifically for CRF, assesses fatigue across 4 domains—physical, emotional, cognitive, and temporal—through a 28-item 5-point Likert self-report, with higher scores indicating greater fatigue.72

Limitations to this review need to be noted as the clinician uses this information to inform practice. As with all reviews, new data may become available after completion of the literature search and are not included here. This review does not assess study quality, and it is possible that psychometric evaluation is based on small sample sizes or studies with methodological flaws. Finally, while this review is intended to evaluate measures to assess CRF, some fatigue instruments lack validation in the cancer population.

Cancer-related fatigue remains one of the most prevalent comorbidities of a cancer diagnosis along the survivorship continuum. As such, knowing the fatigue status of survivors is essential to design appropriate and comprehensive treatment plans and to monitor patient status and the effectiveness of those treatment programs. While this review defines reliable, valid, and clinically useful tools for use in screening for and assessing CRF, clinicians need to consider whether the tool will be used for screening or for assessment. By combining the findings from this investigation with patient needs, appropriate referral and intervention can occur.

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                                                                                                Keywords:

                                                                                                Psychometrics; measurement; surveys or questionnaires

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