Colorectal cancer (CRC) is the third most commonly diagnosed cancer and the third highest cause of cancer-related deaths in the United States. About 136 830 adults in the United States in 2014 will be diagnosed with CRC.1 More than 90% of cases are diagnosed in patients older than 50 years, and the incidence is 50 times greater in those aged 60 to 79 years than in people younger than 40 years and decreasing muscle strength is common with aging.2 Colorectal cancer is curable, and CRC-related mortality is on the decline because of multiple factors such as early-stage detection from regular screening, timely interventions, and improvement in surgical techniques.3, 4 Survival rates for metastatic CRC have been consistently reported to be about 50% at 5 years and 25% at 10 years posttreatment.3, 4 While the population of older adults in the United States is continually growing, the incidence rates of CRC have been decreasing each year since 1998.2 There are about 1.2 million people with a previous diagnosis of CRC in the United States. Cancer recurrence is not uncommon among colorectal survivors; about 50% of surgically treated patients will experience a recurrence in the first 3 years after surgery.4 Colorectal cancer survivors are also at increased risk of second primary cancers of the colon and rectum, as well as other cancer sites, especially those within the digestive system.5
A colectomy alone can be considered curative for lower stages of CRC, but because around 50% of localized lesions eventually return or become metastatic, postoperative adjunctive chemotherapy treatment is often recommended.2, 4 The combination of cytotoxic chemotherapy and biologic agents is the current standard of metastatic CRC care.5 The use of chemotherapy and radiation therapy is an effective treatment for CRC cancer, but it can cause a multitude of acute and late toxicities that affect many systems in the body. General adverse effects of CRC treatment include pain, weakness, and fatigue, greatly affecting a patient's function and quality of life. Cardiotoxicity and pulmonary damage are potential adverse effects that target a patient's endurance level.
Colorectal cancer survivors are among a large group of cancer survivors who experience peripheral neuropathy as a result of neurotoxic chemotherapy such as oxaliplatin that is frequently used in the treatment of CRC. Peripheral nerves may be damaged, causing peripheral neuropathy altering sensation, reflexes, movement, balance, and decreasing strength.6 The chemotherapy-induced peripheral neuropathy may result in more prolonged or permanent sensory and motor neuropathy, leading to motor changes such as reduced lower extremity (LE) muscle strength and diminished sensation with impaired position sense, all of which contribute to increased risk of falls in persons with peripheral neuropathy.7–9 Other neuromuscular functions that could be impaired by cancer treatments include loss of range of motion (due to scar tissue formation), strength deficits from inflammatory-induced muscle wasting, and balance disruptions.6 Isokinetic testing for muscle strength and endurance has been reported in pilot testing in patients with CRC; however, sample size was small (n = 4) and the clinical utility of isokinetic testing is poor.10–14
Most long-term survivors of CRC report lower physical quality of life, but psychological quality of life is often comparable with that of the general population.15–17 Bowel dysfunction is common, especially among those diagnosed with late-stage cancer. In patients who are physically able, physical activity may accelerate recovery from the acute adverse effects of treatment and prevent late effects and may reduce the risk of recurrence and increase survival rate.15–17 In observational studies among CRC survivors, moderate physical activity has been associated with reduced risk of death from all causes and CRC.18 As the management and advancement of cancer treatment improve, so does the role of rehabilitation in the oncology patient population. Rehabilitation of oncology patients has progressed from supportive and palliative care to more complex programs designed to restore function and integrity of organ systems. In these settings, specific tests and measures used by physical therapists (PTs) may provide relevant information about cancer-related impairments such as muscle weakness, loss of range of motion, peripheral neuropathy, gait pattern abnormalities, reduced balance, and cardiopulmonary impairments limiting strength and endurance.6 Small intervention studies have shown that exercise can improve strength, reduce fatigue, anxiety, depression, improve self-esteem, happiness, and quality of life in cancer survivors.14, 15 Randomized, controlled trials of specific interventions designed to increase strength and improve balance in individuals with CRC affected by chemotherapy-induced peripheral neuropathy using good outcome measures such as measures of strength are needed.
With the greater emphasis placed on the use of evidence-based practice in physical therapy, there has been an increased demand for valid and reliable outcome measures to document effectiveness of rehabilitative interventions.10, 19–22 In the clinical setting, outcome measures are used to document change in status after a patient is admitted, identify patients who are at risk for poor outcomes, improve continuity of care, identify the most cost-effective rehabilitation setting, assess practitioner and organizational performance, and provide evidence to support treatment effectiveness for a particular condition.10, 19–22 In order for an outcome measure to effectively evaluate change, it must be standardized, have detailed instructions for administration, scoring, and interpretation of the results, and meet accepted criteria for psychometric properties.10, 19–22 It should also be clinically accessible in terms of cost, ease of use, and availability. Outcome measures are frequently developed for specific patient populations. Therefore, it is important for PTs to select outcome measures that are suitable for the population they are treating, because using an outcome measure in a different patient population than the one it was designed and validated for will reduce its reliability and validity.10
In 2010, the American Physical Therapy Association's Oncology Section created the Evaluation Database to Guide Effectiveness (EDGE) Task Force to develop recommendations for outcome measures to be used when assessing the status of cancer survivors.23 The Task Force has previously published work on breast cancer and prostate cancer. The purpose of this systematic review was to identify and make recommendations of the best methods to evaluate muscular strength and endurance based on the psychometric properties and clinical utility in a CRC population.
A Boolean search was conducted to systematically retrieve studies published after 1995 with reported psychometric properties for outcome measures that directly assess strength and endurance. The primary search of electronic databases conducted with assistance from a reference librarian included Google Scholar, Ovid, PubMed/MEDLINE, CINAHL, Web of Science, Cochrane Review, PEDro, Scopus, and Clinical Key and was performed between December 13, 2014, and March 4, 2015. The following key search terms were used alone and in combination: colorectal cancer/neoplasm, colon cancer/neoplasm, rectal cancer/neoplasm, colectomy, colorectal neoplasm radiotherapy, colorectal neoplasm biological therapy, and colorectal neoplasm immunotherapy (strength measure/measurement/test/tool, endurance measure/measurement/test/tool, psychometric properties, clinimetrics, power, energy, lower extremity, dynamometry, manual muscle test, grip strength, clinical measure, workload measurement). The following MESH terms were also used with PubMed searches: “Muscle strength dynamometer” or “Muscle Strength” or “Hand Strength.” Inclusion criteria were as follows: studies published in the English language, reported psychometric properties of outcome measures for muscular strength and endurance, present clinically feasible methods, and have adult participants. Studies were excluded if they investigated nonclinical measures of strength and endurance, functional mobility measures (Timed Up and Go, Sit to Stand, walk tests, etc), and if they were published prior to 1995. First priority of the search was given to articles with CRC populations; however, if insufficient literature was yielded, the search was expanded to consider patients with other types of cancer, age-matched individuals (>50 years) with chronic diseases, age-matched individuals, and then the general population.
DATA EXTRACTION AND SYNTHESIS
After the literature search was completed, relevant articles were grouped into 5 categories for strength measurement on the basis of characteristics of each measurement tool described in the available literature. No categorization was needed for muscle endurance measures as few were identified in the literature search. Each outcome measure was graded by 2 reviewers independently using the Cancer EDGE Task Force Rating Form (Figure 1). Outcome measures were then rated on the 1–4 Cancer EDGE Task Force Rating Scale (Table 1) taking into consideration both psychometric properties and clinical utility (Figure 1). Relevant psychometric data included intra-, inter-, and test-retest reliability values, with confidence intervals as available, validity, minimal detectable change (MDC), standard error of measurement (SEM), and minimal clinical important difference (MCID). Reliability and validity were determined by either the Pearson (r) or intraclass correlation coefficient (ICC) or kappa values (κ). Correlation coefficients of greater than 0.75 are considered good to excellent, 0.5–0.74 moderate, and less than 0.5 poor.19 Kappa values greater than 80% demonstrated excellent agreement, 61%–80% substantial agreement, 41%–60% adequate agreement, and less than 40% poor agreement.19 Clinical utility was assessed using the criteria of availability of resources, cost, ease of use including time necessary to complete testing and clinician training, scoring and interpretation, and availability of normative data for comparison. If an outcome measure rating was found to be in disagreement between the 2 independent reviewers, the disagreement was resolved by having a third reviewer evaluate and decide on a final EDGE grade.
The search for muscle strength and endurance outcome measurements generated 4922 articles that matched our inclusion criteria. Each article was independently screened and duplicates were removed. Article abstracts were divided in half for each group of 2 reviewers to further read and identify studies that specifically addressed the purpose of this systematic review. One hundred eight articles were assessed for eligibility. See Figure 2 for the PRISMA Flow Diagram for our detailed literature search process. Five clinical measures of strength were identified: hand grip strength (HGS), hand-held dynamometry (HHD), isometric strength, manual muscle testing (MMT), trunk flexion strength/LE dynamometry, and endurance. By category, the number of articles reviewed for each outcome measure was 3 on MMT, 8 on HHD, 4 on HGS, 3 on isometric strength, 3 on LE/Trunk Flexion dynamometry, and 1 on muscular endurance. Some of the research studies evaluated multiple outcome measures, such that the number of articles for each category is not mutually exclusive. Table 2 demonstrates the clinical usefulness of strength and muscle endurance testing methods.
Based upon the EDGE Task Force Criteria, 2 measures were scored 3 or recommended by the Colorectal Cancer EDGE Task Force members: HHD and HGS. These measures are recommended for clinical use to objectify strength measures. Isometric strength testing, trunk flexion/LE dynamometry, and MMT were rated a 2B (unable to recommend at this time), because of a lack of clinical utility and the measures not being tested in a CRC population. Muscular endurance testing lacks psychometric support and is difficult to perform in a clinical setting, and was rated by the task force as 1 (do not recommend). Table 2 demonstrates the clinical usefulness of strength and muscle endurance testing measures. Table 3 lists Task Force ratings and clinical utility comments. Table 4 details the psychometric properties of the clinical measures of strength.
Findings from this systematic review indicate that the best clinical measures of strength in patients with CRC are HHD and HGS. No recommendations for the clinical measurement of muscular endurance may be made at this time. Patients with CRC often have strength and endurance impairments that impact functional mobility and subsequently quality of life.15–17 Identifying these impairments is essential when formulating a comprehensive plan of care to address the patient's needs and goals. Physical activity may aid in recovery of chemotherapy/radiation treatments, prevent late adverse effects, reduce the risk of cancer recurrence, and increase the overall survival rate.18 Therefore, it is imperative to use reliable, objective measures that are sensitive to change to monitor progress with physical therapy interventions.
Several clinically feasible and commonly used outcome measures of strength were assessed in this systemic review. The most accurate outcome measures that demonstrated the highest reliability, validity, and other psychometric properties were HHD and HGS. Previous evidence has demonstrated in many other patient populations that HHD and HGS are valid and reliable tools for assessing change over time.24–36 Dynamometers are the tools used for both of these outcome measures and are easy to use clinically, relative to training, interpretation, and cost. Both HHD and HGS have well established psychometric properties to support good validity, reliability, MDC, MCID, and sensitivity to change in the literature and provide the clinician with a feasible method to measure strength. In this systematic review, both HHD and HGS were found to have ICC reliability scores of greater than 0.90 and excellent validity when assessing healthy and critically ill patient populations and smaller SEM when comparing scores from healthy individuals with those with cancer diagnosis including CRC survivors. Research shows that the tester gender, body weight, or grip strength influences the force values obtained using HHD.34, 35 As reported in a previous review of prostate cancer and strength measurement, use of a fixation devices, including brackets or straps, will improve reliability by creating a mechanism for consistent resistance.36 Although reliability is reported as good-excellent in most studies,28–30 research supports using some external fixation for the dynamometer to improve the interrater reliability of dynamometry in a clinical setting. In a clinical situation, mobilization belts may be strapped around the dynamometer and fixed in opposition to the force vector to provide a consistent resistance for maximal voluntary contractions.
Measurement of strength is most accurate using dynamometry. Tools that have a small amount of error indicated by a small SEM and MDC are considered accurate. Hand-held dynamometry and HGS use a unit of measure that is an interval scale as compared with MMT, which uses an ordinal scale, so sensitivity to change over time may be accurately described when using dynamometry. The SEM of the HHD examined in this review varies from 2.1 kg (cancer/critically ill) to 6.9 kg (healthy) with an MDC of 1.75 kg (cancer/critically ill) to 7.1 kg (healthy).28–30 The actual amount of change in force output that is clinically meaningful will vary depending on the muscle group tested, the age and gender of the individual, and the functional needs of that person. This clinically meaningful change requires the judgment of the PTs. The SEM of the HGS examined in this review varies from 0.8 to 3.0 kg.24–27 One small study of people with disabilities and healthy individuals is an exception to these small errors and meaningful change that reported test-retest errors of 5.9 kg and 5.7 kg, respectively, with an MDC of 6 kg to detect real change.25 One kilogram is equivalent to 9.8 N. A large study in healthy individuals reported meaningful change as 15.8 N (1.6 kg) and 21.3 N (2.2 kg) for the left and right hands, respectively.26
Physical therapists evaluate a patient's strength compared with normative values. The use of HHD and HGS allows this comparison to be made as normative values are established for human strength measures with numerous studies reporting these values.37–39 These measures are recommended for use in the clinic; although in a CRC patient population these measures are lacking specific evidence with only a few studies, most with small sample sizes. Based on the good psychometric properties (Table 4) found in the 12 articles reviewed on HHD and HGS, the reviewers rated these outcome measures as 3 on the EDGE Task Force Rating Scale (Table 1).
Although widely used by PTs to make muscle strength assessments, MMT showed poor intra- and interrater reliability ranging from 0.29 to 0.83 dependent upon the muscle group being assessed.40–42 Manual muscle testing is not assessed on an interval scale. Each numerical number is equivalent to a level of strength and the requirements differ to be assigned a particular classification, unlike HHD and grip strength, which measure strength based on kilograms of force exerted as measured by a dynamometer. It was the poor psychometric properties and issues with MMT measurement, which lead the reviewers to rate MMT as a 2B on the EDGE Task Force Scale and not recommend the use of the outcome measure at this time.
Isometric testing for muscle strength was found to have strong interrater reliability of 0.84 and greater in individuals with advanced disease and in one study in patients with cancer, but not CRC (ICC = 0.90-0.96). The elbow extension and knee extension force (newtons) were the only 2 muscle groups tested in the cancer study and the SEM (MDC) were 10.6 (29.4) and 19.8 (54.8) N or 1.1 (3.0) and 2.0 (5.6) kg, respectively. Isometric testing could not be recommended for use at this time because of limited muscle groups tested in patients with cancer and no studies in the CRC population and the clinical utility relative to equipment needed.31, 43 Finally, trunk flexion dynamometry and LE dynamometry were found to have strong psychometric properties and trunk flexion was tested in a CRC population, but they are not clinically feasible given the equipment needed, space need for equipment, and cost of equipment make it more expensive to administer; therefore, it was rated a 2B at this time.44
There was limited evidence for the use of muscular endurance in the cancer and CRC populations; likewise, it has not been widely used in the clinical setting. Muscular endurance is assessed by muscle contraction until failure of the muscle group to continue to perform. It currently demonstrates poor reliability and lacked other psychometric properties. Although muscular endurance is essential for quality of life and performance of multiple repetitive tasks, the testing methods may be costly if using an isokinetic dynamometer or time consuming by using a one-repetition maximum testing to determine the submaximal isotonic load to be repetitively lifted, which may not be conducive for CRC populations.11–14, 45 ACSM suggests a clinical method of measuring muscle endurance using 40% to 60% maximum resistance lifted over time.46 There is a preliminary report of measures of muscle endurance using a BIODEX. Lack of psychometric properties, limited clinical utility, and only pilot testing in patients with CRC in one small study (n = 4) led the reviewers to rate muscle endurance as a 1 on the EDGE Task Force Scale and not recommend the use of the outcome measure at this time.
Possible limitations of this systematic review include, but are not limited to, additional relevant publications that were published after our literature review, publications in English language, publications prior to 1995, and objective assessment of appropriate articles by the reviewers.
Further research is needed in outcome measures that focus on the specific needs of the cancer survivor population examining: reliability and validity, responsiveness to change as well as cutoff scores for specific practice settings/stage of recovery such as acute to chronic recovery as the effect of treatment changes with time are needed to determine intervention effectiveness and to assess the severity of impairment and functional limitations. Specifically, outcomes measurement studies in CRC survivors must be clinically feasible and use reliable, valid, and standardized methods to measure strength and muscular endurance. A clinical method of measuring muscle endurance may use the guiding principles of 40% to 60% maximum resistance over a lifted over time that is responsive enough to detect differences between a patient with cancer and a healthy individual as well as have a reliable and quantifiable normative unit of measure.36
Evidence-based clinical outcome measures should be used in all physical therapy settings. Only measures that have clinical utility and measures that are reliable, valid, and responsive need to be used when measuring clinical outcomes in the variety of cancer diagnoses that PTs encounter. Measuring strength and muscular endurance precisely in individuals with CRC allows clinical decision-making to identify impairments in body structures that may impact activity and participation for any CRC patients. Both HGS and HHD are recommended as valid and reliable methods to assess strength in CRC patients. No clinical measures for muscle endurance may be recommended at this time. Further research is necessary to devise a clinically feasible muscular endurance test with sound psychometric properties for use in cancer survivors and more studies measuring strength in CRC survivors to identify severity of impairments in body structures that impact activity, participation including quality of life.
Support was provided through the Wayne State University Research Librarian, Wendy Wu.
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Keywords:©2016 (C) Academy of Oncologic Physical Therapy, APTA
colorectal neoplasms; dynamometry; muscle performance; outcome measures; psychometrics