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Oncology Section EDGE Task Force on Prostate Cancer Outcomes: A Systematic Review of Clinical Measures of Strength and Muscular Endurance

Fisher, Mary Insana, PT, PhD, OCS, CLT1; Davies, Claire C., PT, PhD, CLT2; Colon, Genevieve, SPT3; Geyer, Hannah, SPT4; Pfalzer, Lucinda, PT, PhD, FACSM, FAPTA5

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Background: Strength deficits are a common morbidity following treatment for prostate cancer. Accurate assessment of strength and muscular endurance following prostate cancer treatments is essential to identify deficits and plan rehabilitation.

Purpose: To identify strength and muscular endurance outcome measures that possess strong psychometric properties and are clinically useful for examination of men treated for prostate cancer.

Methods: Multiple electronic databases were searched for articles published after 1995. Studies of tools used to assess strength and muscular endurance were included if they reported psychometric properties, were clinically feasible methods, performed on adults, and published in the English language. Each outcome measure was independently reviewed and rated by two reviewers. A single Cancer EDGE Task Force Outcome Measure Rating Form was completed for each category of strength or endurance assessment, and a recommendation was made using the 4-point Cancer EDGE Task Force Rating Scale.

Results: Of the original 683 articles found, 30 were included in this review. Hand-grip strength and hand-held dynamometry were rated 3, recommended for clinical use. One repetition maximum was rated 2A, unable to recommend at this time but the measure has been used in research on individuals with prostate cancer. Manual muscle testing was rated 2B, unable to recommend at this time due to lack of psychometric support, and muscular endurance testing was not recommended (1).

Conclusions: Utilizing objective dynamometry for hand grip and muscle strength testing provides precise measurement to assess baseline status and monitor change among men treated for prostate cancer.

1Assistant Professor, Department of Physical Therapy, University of Dayton, Dayton, OH

2Physical Therapist, Rehabilitation Services, Baptist Health Lexington, Lexington, KY

3Student Physical Therapist, University of Michigan - Flint, Flint, MI

4Student Physical Therapist, University of Dayton, Dayton, OH

5Professor Emerita, Physical Therapy Department, University of Michigan - Flint, Flint, MI

Address correspondence to: Mary I. Fisher, PT, PhD, OCS, CLT, Department of Physical Therapy, University of Dayton, 300 College Park, Dayton, OH 45469, Ph: (937) 229-5617, Fax: (937) 229-5601 (mary.fisher@udayton.edu).

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INTRODUCTION

Prostate cancer is estimated to be the most common form of cancer in American men. After lung cancer, it is the leading cause of cancer death among males.1 The American Cancer Society estimates that approximately 221,000 new cases of prostate cancer will be diagnosed in the year 2015 alone, and approximately 1 in 7 men will be diagnosed with prostate cancer during their lifetime.1 Incidence rates of prostate cancer have changed dramatically over the past 20 years; rapidly increasing from 1988 to 1992, declining sharply from 1992 to 1995, remaining relatively stable from 1995 to 2000, and again decreasing from 2000 to 2010.1 This unpredictable trend primarily reflects the change in the utilization of prostate-specific antigen (PSA) blood testing by health care providers for the detection of prostate cancer.1 Prostate cancer may be a fatal disease, but most men diagnosed with prostate cancer do not die from it. The relative United States 5-year survival rate for all stages of prostate cancer is nearly 100%, while the 10-year and 15-year survival rates are 99% and 94%, respectively, with more than 2.9 million men still living.1

As the number of men living beyond a prostate cancer diagnosis rises, focus of care has broadened to include quality of life (QOL) issues. Recent research provides evidence that the majority of cancer survivors have significant impairments that often go undetected and/or untreated, and therefore may result in disability.2 Androgen deprivation therapy (ADT) is a common treatment method for the early stages of prostate cancer. During the first year of ADT, survivors of prostate cancer (PCS) often experience a deficiency in sex hormones, insulin resistance, an increased central/visceral adiposity, a decrease in bone density, lean muscle mass, and whole body muscle strength.3 What is significant for PCS is that the impairments can often be seen in the whole body, rather than just the area treated for cancer. Prostate cancer survivors receiving ADT had 40% less upper body strength than a group of non-ADT PCS and 22% less upper and lower body strength than a healthy control group, and 27% reduction in strength compared to a PCS non-ADT group.4 Strength is reduced on isotonic testing such as chest press and leg extension, isokinetic knee extension testing and isometric testing with grip dynamometer.4-7 The long term effects of ADT persist over time with a decrease in lean muscle mass.6 Adverse changes in muscle composition may exacerbate normal sarcopenia, thereby further impacting muscular strength and endurance as well as physical function and independent living. The decrease in muscle mass and subsequent strength is associated with impaired functional mobility as indicated by increased times to complete a 5 repetition sit-to-stand test and 6 meter walk test.6,8

Diminished muscular endurance and fatigue are also increasingly recognized as a troublesome complaint among patients with cancer.7,9 Cancer-related fatigue has been hypothesized to be both a central phenomenon as well as a peripheral occurrence. Centrally mediated fatigue is thought to arise from the loss of voluntary activation of muscles due to processes proximal to the neuromuscular junction, while peripheral fatigue has been attributed to failure of muscular contraction or metabolic changes within the muscle.10 Muscular changes associated with ADT use can influence muscular endurance in PCS and have a significant negative impact on QOL and patients' self-care abilities. Researchers have reported impairments among PCS to be as high as 24% for activities of daily living (ADLs) and 42% for instrumental activities of daily living (IADLS).8 Among such patients, the prevalence of fatigue is generally reported to be greater than 65%.11 Furthermore, complaints of diminished endurance and of fatigue persist beyond the treatment timeframe.7,12,13

Impairments in strength and muscular endurance have been linked to declines in independence, functional mobility, and subsequent QOL. Activities of daily living deficits, the use of an assistive device, and abnormal functional screen findings are associated with an increased risk of falling.7 Falls can lead to more serious injuries such as an increased risk of fractures and hospitalizations, thereby decreasing the QOL and level of independence for survivors.8 It is important, therefore, to accurately identify impairments in muscular performance in order to initiate early intervention to mitigate the effects of ADT and subsequent functional decline among PCS.

In 2010, the American Physical Therapy Association's (APTA) Oncology Section created the EDGE (Evaluation Database to Guide Effectiveness) Task Force to develop recommendations for outcome measures to be used when assessing the status of survivors of cancer.14 This systematic review evaluates the ways in which strength and muscular endurance are measured clinically in individuals with prostate cancer. The reliability, validity, minimal detectable change (MDC), and/or minimally clinically important difference (MCID) are important psychometric properties that need to be evaluated to justify clinical use of outcome measures.15 Tools used to track and measure patient outcomes should be validated in the population in which they are used to be most beneficial. Additionally, these tools need to be assessed in light of clinical utility, including the availability of resources, cost, ease of use, and availability of normative data. The purpose of this systematic review is to identify commonly used methods of evaluating strength and muscular endurance in PCS and to make recommendations of the best methods based on psychometric properties and clinical utility.

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METHODS

Search strategy

The authors systematically searched the literature for outcome measures that directly measured strength and muscular endurance to evaluate the psychometric properties and clinical utility of such measures. The primary search was conducted in February 2014 in PubMed/Medline and CINAHL, with secondary searches occurring through July 2014 using Web of Science, Ovid, Google Scholar, Sports Discus, Cochrane Review, PEDro, and Academic Search Premier. Search terms used alone and in combination included: Prostate cancer or neoplasm and; strength measure/measurement/test, muscular endurance measure/measurement/test, manual muscle test, psychometric properties, clinometrics, dynamometer/dynamometry, power, and energy, along with the following MESH terms: “Muscle strength dynamometer” OR “Muscle Strength” OR “Hand Strength.” Relevant articles and journals focusing on orthopedics or fitness measures were reviewed recursively for other potential studies. The prostate cancer population took first priority within the search, however, if no studies included this population, patients with other cancers, geriatric patients, and the general population were considered for review.

Included studies of tests of muscle strength and muscular endurance had to report psychometric properties, present clinically feasible methods, have adults (preferably male) as participants, and be published in the English language. The publication dates were limited to 1/1/1995 and after, as long as the inclusion criteria were met. Studies were excluded if they focused on nonclinical measures of strength and muscular endurance, or were functional mobility measures (eg, Timed Up and Go, sit-to-stand, gait speed, etc.).

After completion of the literature search, relevant articles were classified into 4 strength categories and one additional category for muscular endurance. The 4 strength categories were: manual muscle test (MMT), 1 repetition maximum (1-RM) testing, hand-grip strength (HGS) using dynamometry, and hand-held dynamometry (HHD). These categories for strength measurement tools were selected based on characteristics of each measurement tool described in the available literature. Each outcome measure was appraised by two reviewers independently using the Cancer EDGE Outcome Measure Rating Form.14 Outcome measures were then rated on the 1-4 Cancer EDGE Task Force Rating Scale taking into consideration both psychometric properties and clinical utility (Figure 1).14 If an outcome measure rating was found to be in disagreement between the two independent reviewers, the disagreement was resolved by discussion with all 5 reviewers until consensus was obtained. Finally, all articles reviewed for an outcome measure were included in a reference section of the EDGE form for each appropriate measure.

Figure 1.

Figure 1.

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Data Extraction and Synthesis

Relevant psychometric data, when available, were extracted and recorded on the Cancer EDGE Task Force Outcome Measure Rating Form for each study. This data included: intra-, inter-, and test-retest reliability values, with confidence intervals as available, validity, MDC, standard error of measurement (SEM), and MCID. Reliability and validity were determined by either the Pearson (r) or Intraclass Correlation Coefficient (ICC), or Kappa values (K). Correlation coefficients of greater than 0.75 are considered good to excellent, 0.5-0.74 moderate, and below 0.5 considered poor.16 Kappa values greater than 80% demonstrated excellent agreement, 61% to 80% substantial agreement, 41% to 60% adequate agreement, and less than 40% showed poor agreement.16 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.

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RESULTS

The initial literature search for muscle strength and endurance resulted in 683 articles. The titles were screened and any duplicates removed by the assessors. Article titles and abstracts were then reviewed to identify studies that specifically addressed the purpose of this review. Eighty-two articles were retrieved and assessed for eligibility. Thirty articles were included in the study after exclusions were applied. Figure 2, the PRISMA Flow diagram, details the literature search process.

Figure 2.

Figure 2.

By category, the number of articles reviewed were: MMT = 2, 1-RM = 4, HGS = 8, and HHD = 24. No articles were found which met inclusion criteria to assess muscular endurance measures, although such tests have been used in prostate cancer research. Note that some research studies evaluated multiple tools, such that the number of articles for each category is not mutually exclusive. Table 1 demonstrates the clinical usefulness of strength and muscle endurance testing methods.

Table 1

Table 1

Two measures were recommended (rated 3) by the Prostate Cancer EDGE Task Force members: HGS and HHD.5 These measures are recommended for clinical use to objectify strength measures. One repetition maximum testing was scored a 2A, unable to recommend at this time, because of a lack of high clinical feasibility, although there is evidence of use in prostate cancer research for chest and leg press strength assessment. Manual muscle testing and muscle endurance were scored a 2B, unable to recommend at this time, due to lack of psychometric support. 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. See Table 2 for Task Force ratings and clinical utility comments. Table 3 details the psychometric properties of the clinical measures of strength.

Table 2

Table 2

Table 3

Table 3

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DISCUSSION

The measurement of strength and muscular endurance in men who have been treated with ADT for prostate cancer is essential to the rehabilitation continuum. The effect of ADT on muscular tissue is well documented,4-6 and the loss of strength and muscular endurance impairs functional mobility6 and subsequent QOL.4,7 Therefore, valid and reliable measures of strength and muscular endurance are critical for this population in order to identify deficits, to establish a comprehensive picture of the patient's functional goals and needs, and to monitor progress throughout the course of treatment and beyond.

Findings from this systematic review indicate that the measurement of strength is best performed using objective dynamometry for both hand grip and extremity measures. No recommendations for the clinical measurement of muscular endurance can be made at this time.

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Strength

Accurate measurement of strength using dynamometry is achieved through a method that is valid, reliable, and sensitive to change. Importantly, by quantifying force output as a measure of strength, clinicians can measure strength objectively to determine deficits, plan treatment, and measure progress. Although used widely, MMT, which ranks strength on a 0-5 scale (0 representing no muscular contraction and a 5 indicating full strength),17 has limitations which need to be considered in light of emerging affordable and clinically feasible alternatives which provide greater validity and reliability. Manual muscle testing is a subjective measure of strength. This is particularly true for the antigravity grades of 3 or greater, which lend themselves to personal interpretation of the evaluator. Although reliability measures indicate that there is adequate intrarater consistency within a single evaluator, the amount of force exerted by multiple testers of a 3+ for the same participant are quite variable.18 Another important limitation to be considered is that the MMT scale is ordinal rather than interval; the difference between a muscle graded a 3 and one graded a 4 is not necessarily the same as the difference between a 4 and a 5. This limitation in grading and lack of precision of measurement does not allow the clinician to accurately describe strength gains made through rehabilitative measures, and generally lacks the sensitivity needed to appreciate small gains in strength.

Tools which are considered accurate possess a small level of error. The SEM of the two HHD examined in this review varies from 4.9-12.5N.19,20 One kilogram is equivalent to 2.2 pounds or 9.8N. With a SEM of no greater than 12.5N, the error of measurement in the HHD is less than 1.3 kg (2.9 pounds). The hand grip dynamometers evaluated have a SEM of 0.76 - 1.25 kg.21 Any amount of change in strength measures greater than the SEM, 1.3 kg, is real change. Research and analysis establishing the MDC or MCID for dynamometry is slight, but studies reported MDC values of 1.75-5.58 kg in cancer populations,20,22 and up to 7.3 kg in a healthy population.19 What 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 will require the judgment of the clinician.

The validity and reliability of HHD is well established in the literature. These psychometric properties have been described for multiple populations: healthy individuals, chronically ill, and those with cancer.20,23-27 Overall, validity with strength measured using isokinetic dynamometry is good to excellent.25,26 Although reliability is reported as good to excellent in most studies,23,24,26,27 it can be improved through the use of a fixation method. Because research shows that the tester gender, body weight, or grip strength can influence the force values obtained using HHD,28 it is important to create a mechanism of consistent resistance. Research supports using some external fixation for the dynamometer to improve the interrater reliability of dynamometry in a clinical setting. Studies have investigated different devices including brackets,29-31 or straps.32,33 The studies whose psychometric properties are reported in this review did not use external stabilization, and it is reasonable to conclude that reliability measures would improve with this use. In a clinical situation, a mobilization belt can be strapped around the dynamometer and fixed in opposition to the force vector to provide a consistent resistance for maximal voluntary contractions.

Sensitivity to change is impacted by the tool used, as well as the unit of measure for that tool. Manual muscle testing lacks properties of measurement which are sensitive. Force is often measured by Newtons (N), pounds (lb), or kilograms (kg). The unit of force output for MMT remains an ordinal number whereas the output on dynamometers is in pounds or kilograms. Muscles graded a 4 may have as little as 10% of the maximum strength of a muscle.34 Hand-held dynamometry uses a unit of measure that is an interval scale; the amount of difference between a 3 and a 4 is the same as between a 4 and a 5. Sensitivity to change over time can then be accurately described. Furthermore, clinicians consistently evaluate patient performance against an expected normal level of performance. Use of HHD allows this comparison to be made as normative values have been established for human strength measures. Although outside the scope of this paper, the reader is encouraged to reference the numerous studies reporting these values.35-37

Measurement of strength is most accurate using dynamometry. The use of dynamometry in the prostate cancer population is limited to two smaller studies20,22 which used a strain-gauge rather than a force gauge typically seen clinically. This limited the authors' ratings of HHD and HGS to a 3 (recommended) in this review, however, both HGS and HHD offer the clinician a clinically feasible method to measure strength that has the necessary psychometric properties to support good validity, reliability, MDC, MCID, and sensitivity to change, and have been used in other cancer populations. The use of 1-RM cannot be recommended secondary to low clinical utility and weaker psychometric properties.

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Muscular Endurance

Clinically feasible methods of measuring muscular endurance with accompanying sound psychometric properties and normative values remain elusive. Because of this, muscular endurance, the ability to sustain force output over time, is seldom assessed in a clinical setting. Yet understanding overall muscular fitness after treatment with ADT is an important consideration given the effects of ADT on muscle tissue, including sarcopenia.38 A component of muscular fitness is muscular endurance. Research is emerging suggesting that muscular endurance is lower in men treated for prostate cancer with ADT.7,9 Therefore, finding appropriate means to assess this clinically is important for monitoring patient status.

The most available method to measure muscular endurance is some variation of a repetition to failure loading test. An early study examining muscular fitness among men treated with ADT compared a group engaged in a resistance exercise program to a group without exercise using a fixed load repeatedly lifted at a standard rate, and counted the number of repetitions correctly completed.7 Findings from this study showed an increase in the number of repetitions after 3 months of resistance exercise training, with an accompanying decrease in self-reported fatigue using the Functional Assessment of Cancer Therapy - Fatigue.7 Another study recorded the number of repetitions of 70% of 1RM lifted until failure comparing a group of men on ADT to a group of healthy controls. This study found no differences between groups for muscular endurance repetitions to failure using 70% of 1 RM.6 To better understand the implications of these results, it is important to examine how muscular endurance should be measured.

The American College of Sports Medicine recommends that lifting 40-60% of a maximum resistance repeatedly in training will increase muscular endurance.39 Intuitively, then, measuring endurance should be completed using repetitions to failure of 40-60% of 1RM. Neither study purporting to measure muscular endurance utilized this method, although findings that an increase in repetitions suggest an increase in muscular endurance among men using ADT. The limitation to this study was the lack of a healthy control comparison to determine whether deficits in muscular endurance were present at baseline.

Measuring muscular endurance with a repetition to failure using 40-60% of 1 RM is not without merit. Establishing a baseline measure for an individual is possible, and repeating the measure postintervention can inform change. The limitation of this methodology is the lack of normative data for age, gender, and muscle group. Such data is difficult to gather, as the number of repetitions to failure is largely dependent upon the muscle mass of the individual.40

What is needed is a test for muscular endurance which possesses good clinical feasibility, along with strong psychometric properties. Isokinetic dynamometry offers a more reliable and valid method to measure muscular endurance, but lacks clinical feasibility. However, a study of muscular endurance using a Biodex stationary dynamometer, measuring maximal voluntary isometric contraction (MVIC) levels pre- and post-endurance activity, shows promise.41 Findings from this study suggest that rather than measuring repetitions to failure as a unit to quantify endurance, perhaps measuring MVIC pre- and post-activity may provide a more reliable and valid method to measure endurance. It may be possible that using HHD to measure MVIC before and after some fatiguing activity holds promise for a more clinically realistic measure of muscular endurance. At this time, measuring muscle endurance clinically is not feasible and this systematic review does not support it.

Further investigation is needed in designing a clinically feasible, reliable, valid, and standardized method to measure muscular endurance. A clinical method of measuring muscle endurance should utilize the guiding principles of 40% to 60% of maximum resistance lifted over time. The clinical method should also be responsive enough to detect differences between healthy and injured tissue, as well as have a reliable and quantifiable normative unit of measure.

Other research in cancer outcome measures should focus on the specific needs of the population. More studies with men who have been treated for prostate cancer examining reliability and validity as well as responsiveness to change are needed to determine intervention effectiveness. Cutoff scores should be established to assess the severity of impairment and functional limitations. Tools for specific practice settings across the continuum of care need to be explored; it is reasonable to believe that responses of individuals will vary based on whether they are in the acute stage of recovery or a more long-term stage, as the impact of treatment changes with time.

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CONCLUSION

Psychometrically strong and clinically feasible outcome measures need to be utilized in evidence-based practice of physical therapy. Measuring strength and muscular endurance precisely in men with prostate cancer allows clinical decisionmaking to accurately identify impairments in body structures which may impact activity and participation. Both HGS and HHD are recommended as valid and reliable methods to assess strength in PCS. No clinical measures for muscle endurance could be recommended at this time. Further research is necessary to devise a clinically feasible muscular endurance test with sound psychometric properties for clinical use in this population.

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ACKNOWLEDGEMENTS

Support was provided through Graduate Research Assistants at the University of Michigan-Flint and the University of Dayton. Library Search Assistance was provided at University of Michigan-Flint, Baptist Health Lexington, and University of Dayton.

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          Keywords:

          prostate neoplasms; muscle performance; dynamometry; outcome measures; psychometrics

          ©2015 (C) Academy of Oncologic Physical Therapy, APTA