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Acute Effects of Muscle Fatigue on Anticipatory and Reactive Postural Control in Older Individuals: A Systematic Review of the Evidence

Papa, Evan V. PT, DPT, PhD, MA1; Garg, Hina PT, MS2; Dibble, Leland E. PT, PhD, ATC2

Journal of Geriatric Physical Therapy: January/March 2015 - Volume 38 - Issue 1 - p 40–48
doi: 10.1519/JPT.0000000000000026
Systematic Reviews

Background: Falls are the leading cause of traumatic brain injury and fractures and the No. 1 cause of emergency department visits by older adults. Although declines in muscle strength and sensory function contribute to increased falls in older adults, skeletal muscle fatigue is often overlooked as an additional contributor to fall risk. In an effort to increase awareness of the detrimental effects of skeletal muscle fatigue on postural control, we sought to systematically review research studies examining this issue.

Purpose: The specific purpose of this review was to provide a detailed assessment of how anticipatory and reactive postural control tasks are influenced by acute muscle fatigue in healthy older individuals.

Methods: An extensive search was performed using the CINAHL, Scopus, PubMed, SPORTDiscus, and AgeLine databases for the period from inception of each database to June 2013. This systematic review used standardized search criteria and quality assessments via the American Academy for Cerebral Palsy and Developmental Medicine Methodology to Develop Systematic Reviews of Treatment Interventions (2008 version, revision 1.2, AACPDM, Milwaukee, Wisconsin).

Results: A total of 334 citations were found. Six studies were selected for inclusion, whereas 328 studies were excluded from the analytical review. The majority of articles (5 of 6) utilized reactive postural control paradigms. All studies incorporated extrinsic measures of muscle fatigue, such as declines in maximal voluntary contraction or available active range of motion. The most common biomechanical postural control task outcomes were spatial measures, temporal measures, and end-points of lower extremity joint kinetics.

Conclusion: On the basis of systematic review of relevant literature, it appears that muscle fatigue induces clear deteriorations in reactive postural control. A paucity of high-quality studies examining anticipatory postural control supports the need for further research in this area. These results should serve to heighten awareness regarding the potential negative effects of acute muscle fatigue on postural control and support the examination of muscle endurance training as a fall risk intervention in future studies.

1Department of Physical Therapy, University of North Texas Health Science Center, Fort Worth.

2Department of Physical Therapy, University of Utah, Salt Lake City.

Address correspondence to: Evan V. Papa, DPT, PhD, MA, Department of Physical Therapy, University of North Texas Health Science Center, 3500 Camp Bowie Blvd, MET 533, Fort Worth, TX 76107 (evan.papa@unthsc.edu).

Conflicts of interest and source of funding: none declared.

Richard Bohannon was the Decision Editor.

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INTRODUCTION

Muscular fatigue has been defined as any exercise-induced reduction in the ability to exert muscle force or power1 and is known to modify the neuromuscular system leading to impaired muscle performance. In addition to decrements in muscular contractile ability, muscle fatigue modifies both the peripheral proprioceptive system and the central processing of sensory inputs,2 producing clumsiness and diminished precision of motor control.3 Extensive studies of both general and local exercises producing acute muscle fatigue have been shown to contribute to altering the effectiveness of sensory inputs and motor output of postural control (Table 1). Also, a preponderance of metabolic factors are altered following localized muscle fatigue,9 which may have an effect on postural control. These changes are not benign in terms of postural control as it has been shown that fatiguing lower extremity muscles by performing repetitive dynamic contractions induces changes in postural steadiness10 and increases postural sway during quiet stance.10–12

Table 1

Table 1

Although fatigue degrades postural control during static stance, relatively few studies have examined the effects of fatigue during more dynamic postural tasks. A recent review highlighted 7 articles in healthy older individuals, which suggested that some components of postural control were significantly diminished immediately following muscle fatigue.13 Despite stating an emphasis on “functional tasks,” this review included several articles investigating static stance postural stability. Recently there has been a shift away from static postural stability testing toward testing dynamic postural control as it may be more functional14 and serve to uncover underlying sensorimotor control issues in at-risk populations.15 Furthermore, static stance postural stability testing neglects an important discussion of the particular biomechanical outcomes utilized during daily functional tasks, specifically anticipatory and reactive aspects of postural control.

Anticipatory aspects of postural control are processed internally when individuals prepare sensory and motor systems for postural demands based on previous experience and learning.16 Anticipatory postural adjustments occur in an “expectant” or feedforward manner prior to action of the prime mover.17 Examples of anticipatory postural control actions include transitions to single limb stance18 and rise-to-toes tasks,19 as well as the initiation of gait20 and functional reach tests.18

Reactive postural control is defined by modifying sensory and motor systems in response to changing tasks and externally induced environmental demands.16 Contrary to anticipatory actions, reactive postural control mechanisms occur in a “compensatory” or feedback manner in response to some external perturbation.21 Models of reactive postural control research paradigms include sliding force plates,22 treadmill perturbation training,23 vibratory platforms,24 and trigger-release load cell devices.25

Anticipatory and reactive postural controls are utilized daily in dynamic conditions such as walking, lifting, and carrying objects. Increased variability of gait during walking is associated with fall risk in older adults aged 50 to 75 years.26 Furthermore, it has been reported that delayed muscle latency responses in older persons may increase the risk of injurious falls during tasks requiring reactive postural control appropriations.27 In addition, the chances of sustaining a fall are particularly high during slipping or tripping situations in fatigued conditions28,29 as may be present at the end of a day.30,31 Despite the apparent negative effect of fatigue on postural control, a paucity of information was found for clinicians regarding how acute muscle fatigue impacts anticipatory and reactive aspects of postural control. To address these gaps in the literature, the purpose of this study was to systematically review how anticipatory and reactive postural controls are affected by acute bouts of muscle fatigue in healthy older individuals. Such information is important in that it may influence clinical fall risk examinations, postexercise treatment precautions for patients at risk of falls, as well as providing insight into a potential target for therapeutic intervention.

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METHODS

Search Procedures

Our goal was to capture studies in international medical journals, published in the English language through June 2013, that examined the effects of acute muscular fatigue on postural control outcomes during anticipatory and reactive control tasks in persons older than 50 years.13 To generate the list of articles, we conducted an extensive search of the following research literature databases: Cumulative Index to Nursing and Allied Health Literature (CINAHL), Scopus, PubMed, SPORTDiscus, and AgeLine. The key words fatigue, muscle, posture, postural control, and postural stability were used to conduct the searches. In addition, literature was identified by bibliographic review from included studies. Initial screening of search results was performed using titles and abstracts.

A study was included if it met the following criteria: (1) a controlled clinical trial was used (meeting definitions for levels I, II, and III evidence according to the Methodology to Develop Systematic Reviews of Treatment Interventions developed by the American Academy for Cerebral Palsy and Developmental Medicine (AACPDM) (2008 version, revision 1.2)32,33; (2) the target population included healthy individuals older than 50 years; (4) the independent variable was acute skeletal muscle fatigue of the lower extremities or trunk muscles (except diaphragm or pelvic floor muscles); (5) the outcomes included dynamic anticipatory and reactive postural control assessments; and (6) the article was available in English.

Articles excluded were review papers, methodological or descriptive papers, and articles on postural control in bilateral stance static conditions (eg, postural sway). Articles using participants diagnosed with musculoskeletal, neurological, or other disease were also excluded, as well as studies performed in animals or in vitro, or any articles examining the effect of resistance training protocols (ie, > a single-exercise session). Secondary review of articles in question was made by the third author and inclusion or exclusion decisions were made as a result of consensus decisions from the authors. On the basis of these criteria, a list of final citations was generated and full text articles were procured for full article review. Figure 1 illustrates the process of the search strategy using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow sheet guidelines.

Figure 1

Figure 1

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Full Article Review: Level of Evidence, Quality Assessment, and Data Extraction

Two authors, using standardized methods, independently extracted the data from each article selected for full review. The data extraction forms included general study information (manuscript title, authors, publication year, journal), study characteristics (sample data, groups, outcome measures), and results. Study quality assessments were also performed independently using the AACPDM guidelines. Any discrepancies in data extraction or quality assessment were resolved by reference to the original article and discussion between both researchers.35 If there were questions and it was possible, the original investigators were asked for additional data or clarification of methods. If the first 2 authors reached no consensus, the third author made the final judgment.

The AACPDM tool rates the level of evidence on a 5-category scale founded on Sackett's levels of evidence and the National Health Service Research and Development Centre for Evidence Based Medicine (CEBM, Oxford, England) (level 1 = systematic review, level 5 = expert opinion case study). In addition, it quantifies study quality by awarding one point for each of the following internal and external validity study characteristics: (1) well-defined inclusion and exclusion criteria, (2) intervention adequately described and adherence to intervention, (3) measures used were valid and reliable, (4) outcome assessor was blinded, (5) authors conducted tests of and reported statistical power, (6) dropouts were reported and were less than 20%, and (7) appropriate methods for controlling confounding variables were used. A score of 3 or less was considered to be low quality, a score of 4 or 5 was considered to be moderate quality, and a score of 6 or greater was considered to reflect a high-quality trial.

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RESULTS

General Aspects

A total of 334 citations were found, with 152 from SPORTDiscus, 75 from PubMed, 53 from CINHAL, 51 from Scopus, and 3 from AgeLine. Titles were scanned for evidence of a skeletal muscle fatigue intervention with postural control outcomes in older adults. Relevant articles were recorded and duplicates were removed, leaving 294 studies. After screening titles, an additional 197 articles were excluded and the abstracts of the remaining 97 articles were then reviewed with attention to the exclusion criteria, leaving a total of 7 studies. These articles were then subjected to a full-text review (Figure 1).

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Study Design and Quality

Six of 7 articles were 2-group, prospective cohort studies, with healthy young subjects acting as controls on the main effect of age. These 6 articles were classified as level III on the AACPDM level of evidence scale. One study did not have a control group and was, therefore, classified as level IV evidence.18 This resulted in its exclusion from further synthesis, leaving a total of 6 articles for inclusion and qualitative analysis. Two of the 6 articles were assessed a weak study quality rating,24,36 whereas the remaining 4 articles were considered to provide moderate individual study quality.37–40

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Study Samples

All older participants were considered healthy, community-dwelling adults, with a mean age of 67.5 years (mean range, 62.2-71.7 years). The healthy young control subjects had a mean age of 24.1 years and a mean range of 19.4 to 32.0 years. All studies, except for 2, described the older subjects as having no history of falls within the past year, and those 2 reports described their subjects as being “physically active”40 or “active in sports.”36 Two studies employed solely female subjects,24,37 2 utilized a strict male cohort36,40 and 2 other articles were published examining both sexes.38,39

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Fatigue Protocols

All fatigue protocols focused on lower extremity muscles with the exception of 2 articles, which fatigued the lumbar extensors in addition to the ankle plantar flexors.38,39 Specific muscles and/or muscle groups as well as muscle contraction types (concentric, isometric, etc) used during fatiguing protocols are shown in Tables 2 and 3.

Table 2

Table 2

Table 3

Table 3

Each study reported the time interval between postfatiguing exercise and initiation of posttesting differently. The time latency between the end of the fatigue bout and the initiation of postfatigue postural control testing ranged from “immediately after” exercise24,37,40 to 338 and 4 minutes.39 A single study examined postexercise recovery at 4 time points up 20 minutes.24

In 3 of the 6 studies, the endpoint for fatigue protocols was based on a load related to the participants' maximum voluntary contraction (MVC).38–40 These endpoints differed for each study, ranging from 50% to 70% of patients' MVC. One study determined the exercising endpoint by a failure to complete the task.24 Two other articles used available active range of motion (AROM) as the benchmark for fatigue. For example, Bellew et al37 defined fatigue as when subjects “failed to reach 50% AROM of their exercises” (or also a failure to keep pace with a metronome) while Mademli et al 36 declared that subjects were fatigued when they could not lift the given weight through “the whole range of motion.”

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Postural Control Paradigms

Five of the 6 articles reviewed utilized reactive postural control paradigms. The remaining study used an anticipatory postural control design.

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Reactive postural control paradigms

Two of the studies38,39 utilized a swinging pendulum to apply externally driven perturbations. The design provoked the largest possible perturbation that could be withstood without inducing a stepping response. Adlerton and Moritz24 also examined recovery from perturbation without taking a step by using vibration-induced center-of-pressure oscillations. Two other studies allowed stepping responses but utilized either a treadmill-induced perturbation or a tether-release induced perturbation.36,40

Three of 5 studies investigating the effects of fatigue using external perturbations found that postural control was diminished in older individuals after acute muscle fatiguing exercise relative to prefatigue.24,38,40 Davidson et al38 found that changes in the center-of-mass (COM) trajectory were consistent with a localized muscle fatigue-induced decrement in the ability to recover from perturbations without stepping (COM peak displacement P < .001). Likewise, Adlerton and Moritz24 reported an immediate but short-lasting effect of fatiguing exercise on vibration-induced center-of-pressure (COP) oscillations via increased COP displacement in single-limb stance (P = .03). Using alternating treadmill speeds, Granacher et al40 reported that acute ankle fatigue decreased functional reflex activity of the tibialis anterior (P < .001) and increased antagonist muscle coactivity (P = 0.03), which impacted the older individuals' ability to compensate for gait perturbations.

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Anticipatory postural control paradigms

One of the 6 articles reviewed investigated the effects of fatigue on anticipatory postural control tasks.37 This article examined the anticipatory aspect of postural stability by having subjects voluntarily initiate movement into single limb stance. Accordingly, the Lower Extremity Reach Test and a single limb balance test were used. The Lower Extremity Reach Test is a lower extremity analog of the Functional Reach Test and has been previously described by Bellew et al.41

Bellew et al37 investigated postural control after fatigue to musculature responsible for frontal plane stability (hip abductor muscles). The authors reported no significant differences in prefatigue and postfatigue performance on the study outcomes despite reports that the subjects used considerably altered movement strategies following fatigue.

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Biomechanical Postural Control Task Outcomes

The postural control task outcomes can be broadly categorized into 3 biomechanical classes: temporal measures, spatial measures, and end-points focused on lower extremity joint kinetics (Table 4). Four24,36,37,39 of the 6 articles utilizing temporal outcomes assessments failed to approach statistical significance in their measures. Several of these studies noted deteriorations following muscle fatigue including slowing of reaction time,36 shorter time to complete the postural control task,37 and decreases in COP average angular velocity,24 though these did not reach statistical significance. Just 2 of 5 articles employing spatial measures reported statistically significant effects of fatigue on spatial postural control outcomes, specifically increases in peak COM38 and COP displacements were reported.24 Only 1 article used lower extremity kinetic measures to explore the effect of fatigue on postural control, reporting statistically significant declines in the support limb knee extension moment and vertical ground reaction forces until touchdown by the stepping limb after a fall.36

Table 4

Table 4

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Statistical Analysis Considerations

The inclusion of relevant statistical design details varied between studies. Two studies provided an adjustment of the level of significance as a control for type I statistical error risk.24,37 For outcome measures where no statistical differences between pre- and postfatigue existed, none of the studies reported post hoc power calculations to provide estimates of type II statistical error risk. Two38,40 of the 6 studies provided post hoc effect sizes. In addition, no studies included an a priori sample size estimate based on previous studies. In terms of reliability, 2 authors37,40 reported on tester or instrument reliability of their outcome measures. Intention-to-treat analyses and blinding of evaluators were not reported in any of the studies.

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DISCUSSION

Accidental or environment-related falls are the most frequently cited causes of falling in older individuals, accounting for 30% to 50% of cases. The second most common cause is postural instability and/or gait problems.42 When muscle fatigue is added to these inherent fall risks, older individuals may become increasingly susceptible to falls.28,29,31 This systematic review provides insight into the effects of lower limb and trunk muscle fatigue on reactive and anticipatory postural control in older individuals. To expand upon a previous narrative review,13 this study utilized systematic procedures to consolidate biomechanical data from multiple studies utilizing dynamic postural control tasks (no static stance). Although the study methodologies varied considerably (sample sizes, fatigue protocols, and outcome measures), the composite results appear to indicate that fatigue induces postural control deficits in older individuals during tasks requiring reactive postural control (externally induced destabilizing conditions). Because of a lack of studies examining anticipatory postural control outcomes, the effects of fatigue on this type of postural adjustment remain unclear. These results are important to clinical fall risk examinations, post exercise precautions, and to identify potential targets for therapeutic intervention.

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Clinical Examination of Fatigue-Related Declines in Postural Control

The majority of research reviewed here coupled with studies reporting the alteration of the effectiveness of sensory inputs and motor output of postural control strongly suggests that fatigue has a measurable clinical effect on stability and potentially on fall risk. Despite this evidence, we are not aware of any clinical guidelines that suggest both pre- and postfatigue examination of postural control. In addition, this review emphasizes that the effects of fatigue extend beyond increases in postural sway during static stance. Such results point to the need to conduct postfatigue postural control examinations using reactive postural control tasks. Further research is needed to understand the effects of fatigue on anticipatory postural control tasks.

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Postexercise Postural Control Precautions

There is no question that one of the goals of exercise in older patients is to improve function and reduce fall risk. Unfortunately, little thought is given to the potential for fatigue-induced iatrogenic falls. The research designs used in the reviewed studies all examined the acute effects of fatigue on postural control outcomes in older individuals. With the exception of 1 study, no regard for the time course for recovery of prefatigue levels of postural control was examined. Adlerton and Moritz24 reported that the amplitude of COP displacement increased immediately after fatigue in the sagittal plane but returned to baseline within 5 minutes and remained there at 2 other time points up to 15 minutes. Unfortunately, little evidence-based guidance exists beyond this regarding the recovery time after fatigue for postural control measures. Reports in healthy young individuals have indicated that postural control returns to baseline in as little as 75 seconds43 or as long as 20 minutes11 after acute bouts of localized muscle fatigue. Lin et al44 found that localized muscle fatigue recovery was significantly shorter in a group of older individuals (aged 55-65 years) than in a younger cohort (aged 18-24 years) but the outcome measure was based purely on static stance recovery. Additional research is needed to examine appropriate recovery periods after localized muscle fatiguing exercises for older individuals during more dynamic movement tasks.

In the meantime, clinicians should be careful to organize training conditions so as to minimize the impact of fatigue on older individuals. Proper nutrition and hydration, cardiovascular monitoring, adequately designed training programs, and postexercise recovery time should all be incorporated into the safe practice of clinical and community-based exercise settings.

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A Potential Target for Fall Risk Intervention

The degradation of postural control by acute muscle fatigue would appear to reveal a potential target for intervention. If exercise programs were explicitly designed to make lower extremity muscles more fatigue resistant, the participant might derive postural control benefits. To date, several chronic muscle endurance-training studies have been employed using an amalgam of postural control outcomes.45–49 However, these studies have employed clinical balance correlates like static stance posture, gait speed, the Berg balance test, the Dynamic Gait Index and others, which fail to incorporate measures of reactive postural control. While multidimensional fall risk assessment and exercise interventions have shown promise in reducing falls,50 these interventions are generally composites of neuromuscular reeducation and lower extremity muscle strength and endurance activities. Because of this, the differential benefits of muscle endurance training versus coordination training are unclear. Controlled trials are needed to examine the efficacy of training regimens on muscle fatigue-induced instability.

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Experimental Design Considerations

The heterogeneity in procedures used to induce and to measure fatigue, as well as the poorly controlled threats to internal validity (small sample sizes, consistent lack of control groups), may have influenced the observed results. In addition, several studies reported a lack of specificity of the muscles fatigued relative to the postural control task.24,37,40

The acute muscle fatigue induced in these studies can be categorized into 2 approaches. One method centered around subjects' MVC and the other focused on the ability to perform repetitions of exercises within an available AROM. Two of the 3 articles that induced fatigue via measurements of MVC produced statistically significant reductions in measurements of postural control.38,40 Meanwhile, both of the articles that induced fatigue via an AROM index failed to produce significant changes.36,37 In the future, fatigue-inducing protocols should be based more rigorously on objective measurements of muscle force such as MVC than on less direct measures of force production like available AROM.

The various biomechanical postural control task outcomes employed in these studies included temporal, spatial and lower extremity kinetic measures. Despite significant alterations to postural control occurring across the 3 broad categories, the lack of a unanimous approach with clear sensitivity to postural control changes makes it difficult to suggest a particular biomechanical paradigm for future investigations.

The relevance of the dependent measure to the fatigue task may also have influenced the results of the reviewed studies. While previous research has reported older individuals to be more fatigable than young during velocity-dependent power tasks,51 none of the dependent measures in the reviewed studies examined such tasks. To develop a more clear understanding of the effects of acute muscle fatigue on postural control, future research should examine various postural control tasks including but not limited to rapid force production of reactive or anticipatory tasks.

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Study Limitations

We recognize that the study quality of articles included in this review does not meet the highest standards for quality as provided by standard systematic review guidelines and therefore the results should be interpreted cautiously. Certainly, additional controlled trials examining the acute effects of muscle fatigue on anticipatory and reactive postural control in healthy older individuals are needed. Another limitation to this study may be the inclusion of English-language publications only, causing potentially valuable data to have been overlooked.

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Conclusions and Directions for Future Research

Using systematic review, this study has demonstrated that there is a negative effect of acute muscle fatigue on postural control in older individuals. This fatigue-induced decline in postural control is apparent in dynamic conditions of reactive postural control. Collectively, this evidence points to the potential for transient exercise-induced iatrogenic increases in fall risk. Such results have implications in the examination and management of fall risk and may be even more important in populations with preexisting fall risk factors. Meanwhile, more work is needed to define the effect of fatigue on healthy older individuals in anticipatory postural control conditions. Future research is also needed to examine the clinical merit of pre- and postfatigue postural control examinations, the need for dissipation of fatigue effects after exercise bouts, and for the improvement of muscle endurance as a target for postural control interventions in persons with increased fall risk.

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    Keywords:

    aging muscle fatigue; postural control

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