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Breast Cancer EDGE Task Force Outcomes: Evidence-based Cancer-related Fatigue Measurement Tools

Price, Wendy Farnen, PT, MS, CLT, DPT1; Doherty, Deborah, PT, PhD, CEAS2; Adams, Allegra, PT, DPT2; Bohde, Emilee, SPT2

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Background: Cancer-related fatigue (CRF) is the most common and distressing symptom reported by breast cancer survivors with evidence of significant negative impact on a patient's quality of life. There is no consensus for measurement of CRF in persons diagnosed with breast cancer.

Purpose/Objective: The purpose of this study is to identify valid and reliable evidence-based tools to measure CRF in persons diagnosed with breast cancer as a screening and/or an evaluation tool utilizing the American Physical Therapy Association Oncology Section Cancer Evaluation Database to Guide Effectiveness (EDGE) Taskforce Outcome Measure Rating Form.

Methods: A systematic literature review from 2002-2012 was completed to identify measurement tools for CRF utilized in persons diagnosed with breast cancer. The one-dimensional and multidimensional measurement tools identified were further evaluated for their psychometric properties using the modified EDGE criteria.

Results: Out of 43 measurement tools only 3 met the criteria to be classified as highly recommended. They include one one-dimensional tool, the Brief Fatigue Inventory, and two multidimensional measurement tools, the Functional Assessment of Cancer Therapy-Breast cancer subscale, and the Multidimensional Fatigue Symptom Inventory-Short Form.

Limitations: Some studies lacked psychometric data for measurement tool validation with persons diagnosed with breast cancer or the breast cancer specific data was unable to be separated from other participants in the study.

Conclusions: Further studies are warranted to consider the applicability of one or multidimensional measurement tools for screening versus evaluation of CRF.

1Ella Health Clinical Director of Physical Therapy, Westport, CT

2Oakland University, Rochester, MI

Address correspondence to: Wendy Farnen Price, PT, DPT, MS, CLT, Ella Health Clinical Director of Physical Therapy, Ph: 203-557-8030 (wendy@ellahealth.com)

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INTRODUCTION

Cancer-related fatigue (CRF) is the most disabling symptom reported by breast cancer survivors with a significantly negative impact on quality of life.1-3 The reported prevalence of CRF in persons diagnosed with breast cancer varies widely with estimates ranging from 58% to 94%.4 The variability of the estimates of prevalence depends on many factors including the definition of CRF, utilized assessment tools, type of cancer treatments administered, stage of the disease, and where along the continuum of care the assessment is completed.5-8 Cancer-related fatigue is a subjective experience with a multifactorial etiology that varies in clinical expression (Table 1).9-12 Experienced in all stages of cancer, CRF may often persist many years posttreatment.13-15 Research has suggested that CRF may be subdivided based on physiology to central nervous system and peripheral neuromuscular mechanisms.16,17 Cancer-related fatigue differs from everyday life fatigue in the severity, persistence, and rapid onset, and is not caused primarily by physical activities and not relieved by rest or sleep.18

Table 1

Table 1

There have been attempts to define CRF. The National Comprehensive Cancer Network (NCCN) defines CRF as a “distressing persistent, subjective sense of physical, emotional, and/or cognitive tiredness or exhaustion related to cancer or cancer treatment that is not proportional to recent activity and interferes with usual functioning.”19 The International Classification of Diseases (10th edition) uses a criteria-based definition for CRF.20

The problem with standardizing the definition and classification of CRF in the literature is compounded by the large number of different assessment tools being used in the reviewed studies with no gold standard.5,13,21 Most assessment tools are self-report measures, which include checklists, verbal rating scales, numeric rating scales, visual analog scales, and Likert scales. Cancer-related fatigue has been assessed using both singleitem, one-dimensional measures that gauge fatigue presence or severity and multidimensional scales that measure multiple symptoms of CRF affecting physical, emotional, and cognitive domains of patient functioning.1 Instruments vary by psychometric properties, dimensions, stage of cancer, population validation, method of administration, item length, and time frame assessed.22 Selection of a CRF measurement tool is further challenged by the usage, whether a clinic versus research setting or screening versus evaluation/treatment. These factors are among the many barriers to effective assessment of persons diagnosed with breast cancer for CRF. Existing research suggests cancer survivors underreport the symptom of fatigue and clinicians underestimate the severity.19,23,24 Evidence also suggests health care providers do not routinely assess for CRF or provide effective management.5,19 The NCCN recommends rehabilitation should begin at cancer diagnosis.19 They recommend that screening for CRF become the standard of practice in physical therapy evaluation and treatment of breast cancer survivors.19 The prospective model of rehabilitation for persons diagnosed with breast cancer recommends a proactive approach with regular evaluation to provide ongoing assessment.25 This model depends on the utilization of evidencebased assessments that provide clinical utility.

In 2006, the American Physical Therapy Association (APTA) Research Section formed the Evaluation Database to Guide Effectiveness (EDGE) Task Force to “assist in the identification of a core set of tests/measures for each practice area.”26 Subsequently, the APTA Oncology Section formed a task force to examine and categorize the utility of available clinical tests and measures specifically for breast cancer survivors. Utilizing evaluation criteria created by the EDGE Task Force, the purpose of this study is to identify evidence-based measurement tools for evaluation of CRF in breast cancer survivors. Further, this study will provide the evidence available to verify the validity, reliability, responsiveness, and applicability of these tools.

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METHODS

A systematic literature review of CRF in patients diagnosed with breast cancer was completed to determine the multitude of CRF measurement tools utilized. The following search engines were divided among the 4 authors to identify measurement tools: CINAHL, PEDro, PubMed, Medline, Cochrane, First Search, Science Direct, Google Scholar, Hooked on Evidence, Web of Science, Scopus, and Web of Knowledge. Inclusion criteria were met if studies were published in the English language between the years of 2002 to 2012. Due to changes in treatment that has occurred for patients diagnosed with breast cancer, the 10 years prior to the study would reveal the fatigue measurement tools used most frequently.

Upon completion of this exhaustive literature review, CRF measurement tools identified as used with breast cancer populations were divided between the first and second authors for an independent primary review of psychometric properties (Figure 1). The validity and reliability of these tools to measure CRF in patients diagnosed with breast cancer was then determined through another exhaustive literature search that included research prior to 2002 if update of the psychometric properties was not available. All of the tools were evaluated using the modified EDGE rating forms recommended by the APTA EDGE Task Force (Table 2 and Table 3). Agreement was reached by the reviewers through numerous phone calls and discussions of the data.

Figure 1.

Figure 1.

Table 2

Table 2

Table 3

Table 3

Inclusion criteria were met if studies contained a fatigue measurement tool (one-dimensional or multidimensional) utilized with patients diagnosed with breast cancer. Studies with multiple cancer diagnosis were utilized only if data from persons diagnosed with breast cancer was specifically identified.

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RESULTS

Investigators reviewed 497 articles that met the inclusion criteria (Figure 1). Of these, 43 different CRF measurement tools were identified as utilized with persons diagnosed with breast cancer. With numerous phone calls between the first and second authors, the measurement tools were then subdivided into one-dimensional (Table 4) and multidimensional (Table 5) tools. One-dimensional tools are commonly considered a fatigue-specific tool with one or a few questions to identify the prevalence and severity of CRF while multidimensional measures often examine the effect of CRF across several domains of patient function that may include behavioral, cognitive, somatic, and affective. The authors chose to use one-dimensional tools for the screening tool and the multidimensional tool for an evaluation tools to fulfill NCCN guidelines that state “screen every patient for fatigue as vital sign at regular intervals.”19 If the primary evaluation fatigue score is moderate or severe (4 or higher on a 0-10 numeric scale), then assessment of treatable contributing factors is completed and treatment followed by ongoing evaluation is recommended.19

Table 4

Table 4

Table 5

Table 5

Using the modified Breast Cancer EDGE rating scales recommended by the APTA EDGE Task Force (Table 2 and Table 3), each of the identified measurement tools was evaluated. Those measurement tools that met all the EDGE criteria listed were rated as a “4 - Highly Recommend.” The first and second authors communicated via phone numerous times to come to agreement on the tools.

For the 22 one-dimensional CRF measurement tools identified (Table 4), only the Brief Fatigue Inventory (BFI) demonstrated excellent psychometric properties and was validated in the breast cancer population rating it as a “4 - Highly Recommend.” Further review revealed that 5 other measurement tools, including the Visual Analog Scale (VAS), the Bi-dimensional Fatigue Scale (BFS), the European Organization for Research and Treatment of Cancer-Fatigue (EORTC-F) and the Wu Cancer Fatigue Scale (WCFS), and Functional Assessment for Cancer Therapy-Fatigue (FACT-F) met the EDGE criteria for recommendation as a “3-Recommend.” These tools displayed good psychometric properties and were validated in the breast cancer population. Although there were an additional 16 assessment tools reviewed, the tools were evaluated as a “2-Unable to recommend.” Recommendation of a “2” is further subdivided into 2A and 2B. Seven measurement tools were categorized as 2B and 6 were categorized as a 2A.

Of the 21 multidimensional CRF measurement tools identified (Table 5), two measurement tools met the criteria for a rating of “4” - highly recommend. These included the Functional Assessment of Cancer Therapy-breast cancer subscale (FACT-B) scale and the Multidimensional Fatigue Symptom Inventory-Short Form (MFSI-SF). Five tools were identified as a “3-Recommend.” These include the Diagnostic Interview for Cancer Related Fatigue (DICRF), Fatigue Symptom Inventory (FSI), Medical Outcome Survey 36 item Short Form Health Survey (MOS 36-SF), Piper Fatigue Scale Revised (PFS-R), and Profile of Mood States Fatigue/Vigor/and Fatigue/Inertia Subscales (PMS/FVS/PMSI). Of the remaining 14 multidimensional tools, 9 tools were rated as a “2-Unable to recommend” while 5 tools were rated as a “1-Do not recommend.”

Figure 2.

Figure 2.

Although the 43 tools identified have all been used to evaluate CRF in patients diagnosed with breast cancer, few have been validated specifically for the breast cancer population. By using the strict criteria of the EDGE rating form, the list of tools that can be recommended or highly recommended is very limited. Effectiveness of the treatment of CRF and follow up of the treatment were not assessed as part of this study.

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DISCUSSION

Due to the complexity of the etiology and conceptual framework of CRF, identifying appropriate evidence-based assessment tools has proven difficult. Many challenges exist in evaluating the evidence for CRF measurement tools for persons diagnosed with breast cancer including inconsistency in the definition of fatigue, measurement tools that do not always reflect the definitions, and lack of consistency in research protocol preventing comparisons of studies. There is also considerable debate regarding the usefulness and appropriateness of assessing CRF with a one-dimensional versus a multidimensional measure with advantages and disadvantages to both types of tools. “A brief measure may provide a rapid assessment or serve as screening tool; however, it may not capture all the dimensions of fatigue.”11 One-dimensional CRF measurement tools focus on screening for severity, and general impact/physical activity interference. One-dimensional scales are generally quick, easy to administer, and provide baseline criteria to begin education. However, these tools are limited by self-report style and no consideration of other etiologies potentially contributing to the fatigue. This is in stark contrast to the multidimensional measurement tools that focus assessment to include some or all of physical, emotional, cognitive, mental, behavioral, affective, temporal, sensory, and phenomenology. Multidimensional scales may not always be practical in a clinical setting because of time constraints and burden on the patients and clinicians.

Task forces and experts have collaborated together to address some of these difficult issues. The NCCN guidelines have created an algorithm for all cancer populations in screening, evaluating, and treating CRF.19 However; strict validation to persons diagnosed with breast cancer has not been completed. Butt et al stated, “a positive screening should be followed up with a more comprehensive assessment to fully explore symptom etiology and possible treatment routes. In environments with limited resources, effective screening tools hold the promise for identifying those patients who would most benefit from more thorough evaluation and in the process, identifying those patients who may be less likely to be experiencing significant symptoms.”27

The NCCN guidelines suggests, “ongoing surveillance provides an opportunity to identify long-term or persistent, moderate to severe CRF level (> 4 on scale from 0 to 10), particularly in survivors with lower pre-morbid physical function, indicating the need for a comprehensive primary fatigue evaluation and prompt referral to an appropriate rehabilitation program.”19

Despite the above guidelines and recommendations, no study has attempted to apply a rigorous evidence-based approach to the usefulness of the existing tools to assess CRF in persons diagnosed with breast cancer. Although there were 43 scales identified and assessed in this study, only three meet the criteria to be classified as “4-Highly Recommend” when using the modified EDGE form in the breast cancer population. Of these, one onedimensional CRF scale, the BFI is highly recommended. The BFI is available in 43 different languages and is easy to administer and score. This 9-item survey has shown to be internally stable with good construct (0.81- 0.92), concurrent (r = 0.84 - 0.88, P< 0.001), and discriminate validity (r = 0.34 - 0.38, P < 0.001)). In research that included patients diagnosed with breast cancer, Internal consistency was measured as Cronbach's a = .96.28 The authors were unable to find the MCID for this measurement survey. This tool is highly recommended for use as a screening tool in the clinic and for research purposes with the breast cancer population.

There are two multidimensional tools rated as a “4-Highly Recommend.” Both have been validated and used throughout many studies in the breast cancer population. The FACT-B is a 44-item self-report instrument consisting of the FACT-G (general) plus the Breast Cancer Subscale. This tool demonstrates reliability, validity, and sensitivity to change. The tool is easy to administer and score.29 In one study, the MCID was found to be ≥ 8 in the upper bound and ≥ 7 in the lower bound.30 The MFSI-SF is a 30-item survey with general, physical, emotional, mental, and vigor dimensions. The MFSI-SF was found to have internal consistency for each of the subscales in a study that included 186 patients diagnosed with breast cancer. The alpha coefficients for the 5 empirically derived subscales include 0.96 for general fatigue, 0.92 for emotional fatigue, 0.87 for physical fatigue, 0.91 for mental fatigue, and 0.90 for vigor. Divergent and convergent validity was determined through correlations with other fatigue measurement tools with r ranges = 0.21-0.82. The MFSI-SF has proven to be valid and reliable both in clinical and research setting.31,32 The ease of administration and scoring make the MFSI-SF a desirable tool, which has been tested for construct, concurrent, and convergent validity.22,31 The authors were unable to find any determination of MCID for the MFSI-SF.

Five one-dimensional tools were rated as a “3-Recommend” which merit consideration. The BFS, also known as the Chalder or the Fatigue Questionnaire, is useful as a screening tool, but has a lower specificity and positive predictive value.33 A single-item CRF measure, the VAS is simple and easy to use, and has been recommended as an initial screen for all patients diagnosed with cancer or for frequent CRF measurements. However, the VAS has only been validated in the breast cancer population in a very small study (n = 25) and requires further research.22,34 The WCFS is a 9-item measurement tool that demonstrated the psychometric criteria for a rating of “3-Recommend.” Although the WCFS has been validated in the persons diagnosed with breast cancer, this tool has been used less extensively, but may have potential for greater use.35 The FACT-F has been used with persons diagnosed with cancer but less frequently with breast cancer. The FACT-F has been shown to be a good tool to identify persons diagnosed with breast cancer at higher risk of clinically significant ongoing posttreatment fatigue, good for screening fatigue but not as useful as a diagnostic tool.13,22 The 3-item fatigue subscale has been validated in the EORTC QLQ C30 and is recommended because of its brevity and ease of administration.13 In 2003, Knobel et al stated, “However, it has been noted to have a ceiling effect in advanced cancer patients.”36

Five multidimensional studies met the criteria for a “3-Recommend” rating. “The PFS-R is one of the most developed and widely used CRF multidimensional scales.”24 However, the scale's reference point is “present time” therefore anyone assessed must be experiencing fatigue at time of assessment.36 The PFS-R is also relatively long to use in clinical settings but a recent study by Reeve et al in 2012 validated an item reduction for use in persons diagnosed with breast cancer.37-39 The FSI was validated in the persons diagnosed with breast cancer; however, data is limited with test-retest reliability.13,39-41 The rest of the psychometric properties demonstrate its clinical and -research ability.39 The MOS-36/RAND-36 energy fatigue subscale has been shown to be equivalent to the vitality score for the PFS psychometrically.42 This tool demonstrates high internal consistency, strong convergent and discriminate validity.41,42 Because of its overall multidimensional qualities, the MOS-36/RAND-36 is a comprehensive measurement tool for evaluation. The POMS-SF subscales of fatigue/inertia and vigor/activity are easy to administer and score. Reliability estimates show good internal consistency, test-retest correlations, and construct validity as well as responsiveness to changes in CRF.41-44 The DICRF is considered the most comprehensive assessment tool. However, interviews require specialist training to administer and are time consuming. After an effective screening process is completed, this tool is recommended for patients who rate a moderate to severe range on one-dimensional scales.45 Fatigue measurement tools that were unable to be recommended either did not have psychometric data available or the psychometric and/or clinical utility was poor.

Limitations to this overall study include lack of validation for some outcome measures used for persons diagnosed with breast cancer or the breast cancer specific data was unable to be separated from other participants in the study. Lack of psychometric data and quality of measurement of psychometric data limited the proper evaluation of these tools.

This study provides evidence for measurement tools appropriate to evaluate CRF in persons diagnosed with breast cancer. In choosing an evidence-based fatigue measurement tool, there are additional factors to consider such as the dimension of the fatigue to be assessed, the population that is being assessed, and the time allotted for assessment.39 Whitehead states, “The final choice of measure must represent a compromise between the detail required and the practical issues of completion.”47 The answer to these questions may guide your decision to use a onedimensional or multidimensional tool. The one-dimensional tools may be better for screening or in clinical situations, whereas the multidimensional tools will have greater utility in a research setting or patients whose screening suggests moderate to severe fatigue. Based on this study's findings, an algorithm is proposed to serve as a guide to the decision making process (Figure 1).

Many opportunities exist for future research utilizing both the one-dimensional and multidimensional measurement tools. These include validation of CRF measurement tools with persons diagnosed with breast cancer focusing on different diagnosis of breast cancer, different stages of breast cancer, a variety of time frames along the continuum of care and longitudinal studies for long-term analyses. Tools for clinic use have different requirements than those for research studies and need specific validation. Due to the complexity of the etiology of fatigue, more in depth studies looking at the hematologic and biochemical factors associated with fatigue along with self-report could strengthen the use of the tools. With the progression of technology, the validation of electronic fatigue tools would be very useful for medical records, as an application on phones and computers and thus an easy way to communicate to the health care team.

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CONCLUSION

One one-dimensional (recommended for screening) and two multidimensional (recommended for evaluation/treatment) CRF measurement tools meet the criteria to be rated as a “4-Highly Recommend” for breast cancer survivors throughout the continuum of care. Five one-dimensional tools and 5 multidimensional tools meet the criteria for “3-Recommend” for use with breast cancer patients. The use of validated tools for the assessment of CRF may provide a framework for the design of studies or interventions to improve outcome measures in persons diagnosed with breast cancer.

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ACKNOWLEDGEMENTS

We would like to extend our thanks to Mary Ann Wilmarth, PT, DPT, MS, OCS, MTC, CertMDT, Chief of Physical Therapy, Harvard University, for her assistance.

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Keywords:

one-dimensional; multidimensional; continuum of care

©2014 (C) Academy of Oncologic Physical Therapy, APTA