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Electromyographic Biofeedback Applications to Stroke Patients A Critical Review STEVEN L. WOLF

This article critically reviews publications on EMG biofeedback applications to stroke patients. The state of the art on specificity of treatment effects, consistency across training procedures, measurement techniques, outcome assessments, transfer of treatment effect, and mechanism of action is discussed. Although EMG biofeedback may augment movement capabilities, at least as well as exercise regimens, data relating neuromuscular changes to function are limited. The deficiencies in our current knowledge about this application to stroke patients are identified, and suggestions for items requiring future clarification are delineated. Key Words: Biofeedback; Cerebrovascular disorders; Rehabilitation.

Feedback of raw electromyographic (EMG) signals has been used by rehabilitation practitioners for more than 20 years to improve movement capabilities of patients with neuromuscular and musculoskeletal pathology. In 1969, the term "biofeedback" was coined to mean the use of instrumentation to make covert physiological processes more overt to the patient. Since that time, biofeedback devices have grown in number and complexity as clinician demand for them has increased. Today, these devices vary from lightweight portable units to table models possessing multiple microprocessor components. Contemporary use of EMG biofeedback among rehabilitation clients has been aided by a National Institute of Mental Health report on biofeedback that noted: Without question the most widely accepted use of biofeedback is for the movement disorders. Usually done with electromyographic (EMG) feedback, the training is considered an adjunct to other procedures used in the rehabilitation of patients suffering from disabilities associated with neuromuscular disease.1(p74) Dr. Wolf is a senior investigator at the Emory University Rehabilitation Research and Training Center, 1441 Clifton Rd NE, Atlanta, GA 30322 (USA); and Associate Professor, Department of Rehabilitation Medicine, and Assistant Professor, Departments of Anatomy, Surgery, and Community Health Sciences, Emory University School of Medicine, Atlanta, GA. Components of work described within this review were supported by Grant No. G008003042 from the Department of Education, National Institute of Handicapped Research, Washington, DC. This article was submitted February 23, 1983; was with the author for revision two weeks; and was accepted April 13, 1983.

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A review of EMG biofeedback applications for rehabilitation patients was presented to the Biofeedback Society of America (BSA) in 1978 as a task force report by Fernando and Basmajian, who deduced that EMG feedback treatment for hemiplegic patients was now beyond the experimental mode.2 At the same time, Keefe and Surwit adopted a more conservative perspective that EMG biofeedback may be helpful for some stroke patients when incorporated as part of a neuromuscular reeducation program.3 Furthermore, they argued that more sophisticated methodological approaches should be undertaken in researching the efficacy of EMG biofeedback in rehabilitation. This notion has been supported more recently by Hume, who expressed a need for more regulated control data in this type of research.4 The other major review by Engel-Sittenfeld recognized the importance of attributing variable results to subtle differences between patients with similar (or identical) diagnoses and of relating outcomes to functionally meaningful activities undertaken in environments other than the laboratory.5 Researchers and clinicians alike have been fascinated by and encouraged to use EMG biofeedback for stroke patients because the modality and training strategies associated with its use have allegedly produced functional gains that transcend improvement obtained by more conventional therapeutic approaches. Although it has been argued that the unique attributes of EMG biofeedback reside in the specificity of information about muscle activity and the speed at which this information is provided to the patient,6 PHYSICAL THERAPY

PRACTICE a contemporary review to analyze the benefits of this modality for the treatment of stroke patients appears warranted, especially in light of the numerous reports on the subject within the last three years. The purpose of this review is to examine published data on EMG biofeedback applied to stroke patients as the data relate to specific elements underlying use of this modality. During this examination, a perspective on the current status of EMG biofeedback for stroke clients will be offered, and suggestions for issues requiring further clarification will be made. Readers may use the elements presented in this review for critical reading of future biofeedback literature. Quantity of Reports The Figure shows the distribution of clinical research publications (excluding textbook chapters and audiovisual materials) on EMG biofeedback applications to stroke patients between 1960 and 1982. Of these 33 reports, 14 (42.4%) included a control group. Control is interpreted to mean inclusion of a no feedback, false feedback, or alternative therapeutic application group. Seven of these 14 control studies (50%) have been reported since 1980. This observation clearly suggests that between 1960 and 1980, the majority of reports provided descriptive or anecdotal information as more clinicians sought to gain impressions about the potential efficacy of biofeedback for stroke populations. During this interval, biofeedback was gaining considerable attention in the press and among the lay public. EMG biofeedback for neuromuscular disorders was particularly intriguing. Unlike feedback applications addressing problems for which visual indications of improvement are not obvious, such as with hypertension, cardiac arrhythmia, migraine headache, and peripheral vasculature disease, changes from feedback to restore movement are easily observable, particularly among patients with prolonged CNS dysfunction. Therefore, visual proof of functional changes in gait or arm movements, for example, helped to promote a favorable impression about the use of biofeedback to enhance motor capabilities. Benefits from use of this modality appeared all the more potent when functional changes could be demonstrated among patient populations, such as stroke clients, who were either resistant to past treatment formats or had plateaued following administration of more traditional or conventional therapeutic interventions. Within the last three years, biofeedback applications to stroke patients have been more carefully scrutinized to determine if the modality really affords specific treatment effects and lives up to either past impressions or future expectations. Appendices 1 and 2 provide a chronological synopsis of EMG biofeed-

Volume 63 / Number 9, September, 1983

back applications to hemiplegic upper and lower extremities, respectively. Many of the articles cited in these appendices are referenced to the concepts addressed in the following material. Several of these reports have yielded encouraging yet only anecdotal information.7-22 Fewer studies have addressed crucial issues which include specificity of treatment effects, consistency of training procedures, neuromuscular measurements, outcome criteria, transfer of treatment effect, and mechanism of action. SPECIFICITY OF TREATMENT EFFECT Within the context of biofeedback, specificity of treatment effect relates to the notion that favorable outcomes are caused by the independent variable (EMG biofeedback, equipment, or training) and not to uncontrolled variables (patient motivational levels, client-therapist interactions, or use of adjunctive therapies such as resistive exercise, vibration, and icing.) Audio and visual information about motor unit activity enables healthy individuals to change discharge frequency or to recruit additional motor units in a systematic fashion. These observations have been consistently verified through numerous replication studies following the pioneering work of Basmajian.23 Surprisingly, an extension of this work to observations on EMG changes resulting from contraction efforts for an entire muscle was not reported until Middaugh et al demonstrated that both healthy individuals and neurological patients could augment muscle activity more significantly when provided with feedback as opposed to no feedback conditions.24, 25 These studies lend considerable credence to the specificity of effect provided by EMG biofeedback. From an analytic perspective, however, the work was performed on a group of neurological patients with mixed diagnoses; the relationship between ability to increase muscle responses accurately and the specific muscle being activated was not analyzed; the number of testing sessions was limited; and the training goal for neurological patients interfaced with feedback instrumentation emphasized recruitment rather than inhibition of muscle activity. Attention and Motivation Clinical studies designed to convince clinicians that functional improvement is specifically attributable to biofeedback intervention must differentiate this contention from other intervening variables. Therefore, the attention given by the clinician to the patient interacting with this "black box" and to patient motivation must be considered. Steiner and Dince note that, contrary to traditional research protocol, there is nothing wrong with clinicians showing enthusiasm and concern for the patient and, in this case, enthu-

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siasm for use of the modality, as long as this attitude is consistent throughout the clinical study.26 They believe that positive therapist-patient interactions are clinically realistic and should, therefore, be included within the research component. Furthermore, this element is a crucial factor in obtaining patient compliance for the treatment strategy. Motivational factors are also important. Undoubtedly, a stroke patient's motivation regarding feedback training (or other treatment regimens) is governed by degree of cognition, past clinical experiences, and psychosocial factors such as family support or demands. Yet behavioral assessments of stroke patients and efforts to relate motivation or other behavioral correlates to outcome are sorely lacking in the stroke patient biofeedback literature. Implications about relating poor outcomes to apparent patient apathy have been made.10, 15, 16, 21, 22, 27 Only a study by Santee and co-workers has peripherally addressed this issue.28 In that report, monetary rewards were thought to enhance stroke patients' motivation to increase anterior tibialis and to reduce gastrocnemius activity. The results, however, were equivocal, and a monetary incentive is an impractical approach to employ among adult patients within a clinical environment.

Experimental Design To demonstrate a specific training effect implies some degree of methodological sophistication.3 The feedback modality or the technique used with the stroke patient must be shown to cause an increase in range of motion (ROM), strength, EMG, function, muscle relaxation, or some combination of these elements. Specifically, the improvement in outcome measure must be causally related to the feedback intervention. Furthermore, the appropriate direction of these measures should be greatest for feedback patients when compared to either no treatment groups or patients receiving another specified procedure. To attribute improvement to the specificity of the treatment rather than therapist interaction or other uncontrollable variable, the ideal experimental design should be double blind; neither the clinician nor the patient should be aware of when the treatment is given (true feedback versus false or yoked feedback) or what the outcome measures tell with respect to the treatment alternatives. This approach is impractical and unrealistic for most EMG biofeedback interventions within a rehabilitation context. One solution is to permit clinicians who have not treated the patient to do the periodic measures of performance without informing the experimenter or patient until feedback treatment is terminated. Unfortunately, this single blind approach was used in only one study cited in the appendices. In defense of most studies where 1450

outcomes following biofeedback training were equivocal and, hence the null hypothesis (biofeedback was not more beneficial than another intervention) was met, the inference that biofeedback training is not beneficial is incorrect. An inability to show an effect is not equivalent to proving the absence of an effect. As Steiner and Dince state, "If a study demonstrates that a particular treatment and its placebo control result in equal clinical improvement, the efficacy of the biofeedback treatment has not been refuted. The conclusion from data such as these is that the treatment may or may not work, but that the particular study was unable to separate treatment effects."26(p277)

Comparative Groups Although Hume has argued that controls are not necessary for biofeedback studies on chronic (greater than one year after insult) stroke patients because stabilization of function has occurred during past conventional therapy,4 this notion fails on two counts. From a scientific perspective, an astute clinician would not be easily convinced that for a neurological patient, variable lengths of time since treatment constitute a control (unless functional measures could be taken at the end of traditional therapy repeated at a future time, and proven to be unchanged). From a practical viewpoint, the clinical reality is that, stroke patients do often show changes (for better or worse) when examined during repeated outpatient visits. Therefore, the remaining options are to compare a group of patients scheduled to receive biofeedback training with 1) a control group who will receive no treatment, 2) a group who will be given a specific exercise regimen, 3) patients who will have the identical feedback training as a supplement to specific exercises or integrated within an exercise program, or 4) a group of patients who will be provided with false feedback. These possibilities are considered in all the controlled clinical biofeedback studies on stroke patients. The majority of studies on both chronic and acute patients indicate the feedback and exercise yield superior results; yet this opinion is not unanimous.29"31

Site of Injury Given the experimental possibilities, specificity of effect can only be demonstrated when other factors are identified and, preferably, controlled. The sites of cerebrovascular accident are quite varied, and the magnitude of sensory and motor deficits are different depending upon the extent of these lesions.32 Only the study reported by Shahani and colleagues has attempted to relate outcome with feedback training

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PRACTICE

to specificity of lesion.33 In that study, patients with lacunar lesions showed greater improvement in gait and lower extremity motor power than patients with middle cerebral artery compromise. All other experimental studies have simply combined stroke patients without respect to location or type of cerebrovascular accident. Brudny and co-workers have identified the causes of stroke for their patients but did not use this information in analyzing outcomes.9, 10, 13, 14 Other investigators have only grouped feedback data from patients with different types of head injuries including stroke.22'24

Stroke If the time since stroke (acute, chronic) is not controlled within the experimental design, the results may be questionable or unclear. Although the report from Shahani and colleagues33 included data on lesion site, that report and several others were about acute stroke patients29, 34, 35 or had combined data about both acute and chronic stroke clients.24, 35, 36 Biofeedback training studies on acute (less than six months after injury) patients pose the problem of isolating specificity of effect from spontaneous recovery or ongoing CNS plasticity. Even if a "no treatment" acute stroke group were possible, such studies would still be criticized because it is impossible to control for the interaction between locus of injury and amount of spontaneous recovery. Basmajian and co-workers have tried to deal with this reality by grouping acute stroke patients by Brunnstrom's stages of recovery.35 Among the 37 acute stroke patients examined in that study, a combined biofeedbackbehavioral technique appeared more effective than conventional therapy in improving function if patients were either at a Stage 5-6 of recovery four to five months after the stroke or at a Stage 3-4 recovery and treated within three months following stroke. This approach should be meaningful for clinicians who believe that Brunnstrom recovery stages are sufficiently defined and possess valid correlations to function. Fish and colleagues accurately note that biofeedback experimental studies in which acute and chronic stroke patients are grouped together present difficult analytic problems because researchers must differentiate specific treatment effects from spontaneous recovery.37 This consideration could be addressed if sufficiently large numbers of both acute and chronic stroke patients are used in a group design experiment. Outcome results could then be examined by duration of injury as well as treatment choice. To date, all experimental biofeedback studies on stroke patients have had insufficient sample sizes to permit the suggested analyses.


Age and Other Variables Evidence is accumulating that among stroke patients receiving EMG biofeedback, no relationship exists between outcome and age, sex, duration of previous rehabilitation, presence of expressive aphasia, or side of cerebral insult.15, 16, 24 These data should be viewed cautiously. Considerably more studies will have to draw similar conclusions before these variables can be dismissed from influencing treatment effect. For example, the issue of left versus right cerebral injury and outcome must be examined more closely in feedback studies because the type and location of stroke can profoundly influence factors, such as cognition, spatial orientation, and awareness of limb activities. Although the presence of receptive aphasia has been shown to minimize the effectiveness of EMG biofeedback training for stroke patients,15, 16, 38 the extent of proprioceptive loss as a factor governing treatment outcome requires further systematic evaluation. Wolf and co-workers suggested that proprioceptive impairment may negatively influence treatment efficacy to the hemiplegic upper extremity; however, their treatment procedure always involved training to the lower extremity before the upper extremity.15 Their observation may have been due to an ordering effect with patients subsequently more resistant to upper extremity treatment. In the few cases in which only the upper extremity was treated, proprioceptive loss did not influence outcome. Preliminary data from Skelly and Kenedi indicate that initial limitation in active shoulder ROM rather than sensory loss influenced specificity of feedback training to the shoulder musculature.31

Instruction and Cognition Specificity of training effect can also be influenced by how instructions are delivered to patients. In clinical situations, clear and simple instructions for braininjured patients are important. In addition, particularly in research, instruction for all subjects must be consistent in content and presentation. Surprisingly, only the study by Binder and colleagues has addressed this issue and provided readers with specific content on how they interacted with their stroke clients.39 None of the studies in the appendices evaluated patients for cognition or motivation. Hence, neither treatment effectiveness nor outcome can be assessed for these components. These elements can have a substantial effect upon training. In our own experiences, we have often observed chronic stroke patients who appeared most congenial and cooperative but were unable to process or recall simple instructions during feedback training. Furthermore, review of past medical records failed to mention any cognitive deficits.

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CONSISTENCY OF TRAINING PROCEDURES

The literature on EMG biofeedback applications to stroke patients has been remiss in failing to provide readers with the specific elements contributing to treatment. Some studies have provided almost overwhelming detail on training procedures.15, 16, 30, 40, 41 Most studies have not only omitted information on training procedure but have also not addressed 1) type of electrodes, 2) electrode placements, 3) descriptions of the feedback displays or devices, 4) use of ongoing feedback or shaping to achieve threshold (contingent feedback), 5) sequence of muscles trained and the amount of time per session spent on each muscle, 6) time constant of the integrator, or 7) total number of treatment sessions. The last of these elements is often provided, but as can be gleaned from the appendices, most of these reports include a total number of treatment sessions that, compared with normal clinical routine, are entirely too few, or, in some reports, far too many.9, 25 In one study, the experimental sessions were limited to one day for each of three procedures, and each contraction effort lasted for 20 seconds.42 Only after provision of the details outlined above can replication of these studies become possible. In addition, experimental protocols that do not parallel clinical reality, especially for duration and total number of treatments, will fail to convince clinicians of the importance or value of the feedback procedure. MEASUREMENTS

In all biofeedback studies applied to stroke patients, neuromuscular measurements have been reported as ROM values, manual muscle test scores, or average or peak EMG (in microvolts or microvolt-seconds). Such quantification lends itself nicely to statistical analyses. In fact, many of the experimental biofeedback studies report substantial improvement in ROM or strength at the wrist,41 shoulder,29, 31 or ankle.27-29,34,36,38,39,43,44Range of motion and manual muscle test data may be unreliable, especially if undertaken by the investigator.2, 3 Furthermore, as noted by Ethridge, microvolt values obtained from active or passive muscle movement, although amenable to statistical analyses, provide limited functional information.45 Statistical (in)significance does not necessarily form a relationship with clinical (in)significance. These EMG, ROM, and muscle tests are the best measures available to clinicians investigating the efficacy of EMG biofeedback. What do they truly reveal? For example, does a significant increase in active ankle dorsiflexion range of motion following feedback training mean that the hemiplegic walks better? Does increased wrist extension activity imply 1452

greater manipulative ability? Does any measure undertaken statically or in isolation translate to improved function dynamically? Electromyographic biofeedback research applied to stroke patients has provided substantial neuromuscular data, but few studies have addressed the questions noted above, and therein lies the greatest shortcoming in this (or perhaps any other) area of rehabilitation—a failure to extrapolate physiological measures to quantified functional changes. OUTCOME CRITERIA

Functional Scores Clearly, then, process must be intimately related to outcome. Few studies have correlated lower extremity activity changes with functional changes following feedback training. Basmajian and colleagues34, 36 developed a six-point scale that has been used by others performing feedback research.29 This scale provides no quantitative measures, however, and can easily be interpreted with reasonable subjectivity. Much the same can be said for the five-point scale used by Brudny and his colleagues to assess functional changes in the hemiplegic upper extremity following feedback training.910 Recently, Basmajian and coworkers made use of an upper-extremity functional scale that lists activities in order of ascending complexity in 10-point increments.35 Although this scale does help to further delineate upper extremity capabilities, it cannot be used for parametric analyses because continuous integers in real values are not used. A more meaningful approach appears to be the measurement of functional activity by continuous values. Three such measures of practical significance are time, distance, and force. By relating biofeedback treatment to functional tasks measured in these domains, data meaningful to researchers and clinicians can be generated whether one uses parametric or nonparametric tests of significance. Only one EMG biofeedback study of training for lower extremities of stroke patients39 and two for upper extremity treatments30, 35 have used such measures. Future studies must include practical, yet meaningful, functional scores to convince both clinicians and third party payers of the efficacy entailed with use of this modality. Evaluators

Indications are that in only two studies were evaluators not also the investigators.27, 39 This approach may be impractical within a clinical environment but PHYSICAL THERAPY

PRACTICE is preferable for research designs to help maintain objectivity. Follow-up Several studies have followed patients from six weeks to four years after completion of treatment to determine if the beneficial effects accrued during feedback training were preserved.9, 10, 16, 27 It would appear safe to conclude that if patients do not sustain further medical complications, then the beneficial effects of feedback to chronic stroke patients are maintained. TRANSFER OF TREATMENT EFFECT From a research perspective, evaluating a patient's response to feedback training outside the clinical or laboratory setting and demonstrating an improved functional capacity would offer convincing evidence for a transfer effect. If, in addition, all other variables could be optimally controlled, then a specific treatment effect would also be demonstrable. Unfortunately, in both clinical and research contexts, demonstrating an effect outside the medical setting is both expensive and impractical. These approaches have not been reported in the stroke-biofeedback literature. One way to remedy this situation would be to develop a functional, yet simple, check list of activities that would be filled by the patient or a family member. If more activities could be accomplished after feedback training than after other forms of treatment, a statement could be made about the transfer of training effects from clinical to other environments. For cost-effectiveness and to strengthen training effects, home practice with biofeedback instrumentation is valuable. Only one anecdotal report has included this procedure as a phase of treatment for study.20 This approach is difficult to incorporate within an experimental protocol because control over frequency or accuracy of home training is almost impossible. MECHANISM OF ACTION Most research studies on biofeedback applications to stroke patients have not addressed the issue of mechanisms to account for results. Not knowing the mechanism(s) should not imply lack of clinical effectiveness. Considering that the complex neurophysiology underlying a simple motor act is unclear,46 it is not surprising that explanations for integration of sensory and motor behaviors to effect functional changes among stroke patients using feedback become exercises in educated speculation. Brudny and colleagues have proposed that visual and auditory feedback to patients with CNS dysfunc-


Figure. Relationship between publication year and number of publications (through 1982) on EMG biofeedback applications to stroke patients (excludes articles on technique, abstracts, reviews, book chapters, videotapes, audiotapes, and documented oral presentations). Closed circles are total number of articles; open circles are the number of articles within the total for which control or comparison groups were included. tion may rely upon conceptualizations such as 1) over-ride: feedback information about muscle length changes may reach the somatosensory cortical areas by entering at a level higher than the locus of pathology and act directly upon corticospinal tract neurons; and 2) by-pass: using the thalamus as a key substrate, feedback information may operate at a subcortical level by making use of brain stem motor nuclei to operate on appropriate motor-sensory feed-forward systems.13 I have speculated that a primary role of visual and auditory feedback might be to activate central synapses previously unused or underused in executing motor commands.32 As visual and auditory input of EMG activity are continuously processed by the cerebellum or sensory and motor cortices directly, available and responsive motor cells are called into play. With continued training, stroke patients would be capable of improving performance by establishing new sensory engrams and eliminating one or both forms of feedback. Feedback may facilitate plastic changes within the CNS.47 Mechanisms that might be invoked include one or more of the following: elimination of active inhibitory influences, unmasking of existing pathways to subserve new functions,48 development of new movement strategies,49 transfer of function to intact neural structures,50 use of alternative pathways, or sprouting of collateral axons to form new synapses.51

Future Considerations Considering that most research in EMG biofeedback applications to stroke patients is comparatively recent (Figure), tremendous advances in our appreciation for the efficacy of this modality have been provided by dedicated clinicians. At the same time, limitations and shortcomings have been exposed.

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Without preference to order, future research should address the following concerns: 1. Interdisciplinary approach to the stroke patient, including measurable behavioral assessments before and after feedback training. 2. Precise data on location of lesion and subgrouping patients accordingly. 3. Segregation of acute from chronic stroke patients in research designs. 4. Specificity in treatment protocol so that stroke patients receiving biofeedback are matched to a group that homogeneously receives an alternative intervention. 5. Delineation and replication of a specific biofeedback training strategy. 6. Identification and uniformity between electrode placements and method of instrumentation used. 7. Independent clinical evaluators who, preferably, assess stroke patients in an environment that differs from the treatment site. 8. An assessment of EMG biofeedback efficacy for treatment of upper or lower extremities among stroke patients with profound proprioceptive deficits, exclusively. 9. Prolonged follow-up assessments using identical evaluation protocol whenever possible. 10. Quantification of function. 11. Use of position-emission tomography (PET) scans during feedback training to delineate neural structures involved in sensory and motor processing of feedback signals. 12. Multiple clinical facilities engaged in a common project

using identical protocols that incorporate all of the above concerns to amass larger sample sizes. SUMMARY The current state of knowledge on EMG biofeedback applications among stroke patients has been presented in a critical fashion. Specificity of treatment effects, consistency across training procedures, measurement techniques, outcome criteria, transfer of treatment effect, and mechanism of action were addressed. Despite the remarkable advances made in such a short time toward understanding this subject area, many inconsistencies and uncertainties exist. The prevailing information indicates that EMG biofeedback applications to stroke patients can enhance function. This enhancement can have an additive effect to previous rehabilitation efforts. Research governing appropriate patient selection and training procedures is still needed if optimal use of the modality is to be achieved. Areas needing further investigation are presented. Acknowledgments. The critical comments offered on initial drafts of this manuscript by my colleagues at the Emory Rehabilitation Research and Training Center are very much appreciated, as are the diligent typing efforts by Gloria Bassett.

REFERENCES 1. Runck B: Biofeedback: Issues in Treatment and Assessment, National Institute of Mental Health, Department of Health and Human Services, Washington, DC, Publication No. (ADM)801032,1980 2. Fernando CK, Basmajian JV: Biofeedback in physical medicine and rehabilitation. Biofeedback Self Regul 3:435-455, 1978 3. Keefe FJ, Surwit RS: Electromyographic biofeedback: Behavioral treatment of neuromuscular disorders. Journal of Behavioral Medicine 1:13-24, 1978 4. Hume Wl: Biofeedback. New York, NY, Human Sciences Press, Inc, 1981, vol 3, pp 9 - 1 6 5. Engel-Sittenfeld P: Biofeedback in the treatment of neuromuscular disorders. In Beatty J, Legewie H (eds): Biofeedback and Behavior, New York, NY, Plenum Publishing Corp, 1977, pp 4 2 7 - 4 3 8 6. Wolf SL: Essential considerations in the use of EMG biofeedback. Phys Ther 58:25-31, 1978 7. Marinacci AA, Horande M: Electromyogram in neuromuscular re-education. Bull Los Angeles Neurol Soc 2 5 : 5 7 - 7 1 , 1960 8. Andrews JM: Neuromuscular re-education of the hemiplegic with the aid of the electromyograph. Arch Phys Med Rehabil 45:530-532, 1964 9. Brudny J, Korein J, Levidow L, et al: Sensory feedback therapy as modality of treatment in central nervous system disorders of voluntary movement. Neurology 24:925-932, 1974 10. Brudny J, Korein J, Grynbaum BB, et al: EMG feedback therapy: Review of 114 patients. Arch Phys Med Rehabil 5 7 : 5 5 - 6 1 , 1976

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11. Gavin J, Stephan K: Biofeedback muscle re-education: A clinical review of ten cases. Biofeedback Self Regul 1:330331,1976 12. Inglis J, Sproule M, Leicht M, et al: Electromyographic biofeedback treatment of residual neuromuscular disabilities after cerebrovascular accident. Physiotherapy (Canada) 28:260-264, 1976 13. Brudny J, Korein J, Grynbaum BB, et al: Sensory feedback therapy in patients with brain insult. Scand J Rehabil Med 9:155-163, 1977 14. Brudny J, Korein J, Grynbaum BB, et al: Helping hemiparetics to help themselves: Sensory feedback therapy. JAMA 241:814-818, 1979 15. Wolf SL, Baker MP, Kelly JL: EMG biofeedback in stroke: Effect of patient characteristics. Arch Phys Med Rehabil 60:96-102, 1979 16. Wolf SL, Baker MP, Kelly JL: EMG biofeedback in stroke: A 1 -year follow up on the effect of patient characteristics. Arch Phys Med Rehabil 61:351 - 3 5 5 , 1980 17. Marsh RW: Electromyographic feedback treatment of hemiplegia. New Zealand Medical Journal 91:96-97, 1980 18. Honer J, Mohr T, Roth R: Electromyographic biofeedback to dissociate an upper extremity synergy pattern. Phys Ther 62:299-303, 1982 19. Amato A, Hermsmeyer CA, Kleinman KM: Use of electromyographic feedback to increase inhibitory control of spastic muscles. Phys Ther 53:1063-1066, 1973 20. Johnson HE, Garton WH: Muscle re-education in hemiplegia by use of electromyographic device. Arch Phys Med Rehabil 54:320-323, 1973

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PRACTICE 21. Flom RP, Quast JE, Boiler JD, et al: Biofeedback training to overcome poststroke foot-drop. Geriatrics 31:47-51, 1976 22. Basmajian JV, Baker MP, Regenos ER: Rehabilitating stroke patients with biofeedback. Geriatrics 32:85-88, 1977 23. Basmajian JV: Conscious control and training of motor units and motor neurons. In Basmajian JV (ed): Muscles Alive: Their Functions Revealed by Electromyography, ed 4. Baltimore, MD, The Williams & Wilkins Co, 1978, pp 1 1 5 - 1 2 9 24. Middaugh SJ, Miller MC: Electromyographic feedback: Effect on voluntary muscle contractions in paretic subjects. Arch Phys Med Rehabil 61:24-29, 1980 25. Middaugh SJ, Miller MC, Foster G, et al: Electromyographic feedback: Effects on voluntary contractions in normal subjects. Arch Phys Med Rehabil 63:254-260, 1982 26. Steiner SS, Dince WM: Biofeedback efficacy studies: A critique of critiques. Biofeedback Self Regul 6:275-288, 1981 27. Burnside IG, Tobias S, Bursill D: Electromyographic feedback in the remobilization of stroke patients: A controlled trial. Arch Phys Med Rehabil 63:217-222, 1982 28. Santee JL, Keister ME, Kleinman KM: Incentives to enhance the effects of electromyographic feedback training in stroke patients. Biofeedback Self Regul 5:51-56, 1980 29. Hurd WW, Pegram V, Nepumuceno C: Comparison of actual and simulated EMG biofeedback in the treatment of hemiplegic patients. Am J Phys Med 59:73-82, 1980 30. Prevo AJH, Visser SL, Vogelaar TW: Effect of EMG feedback on paretic muscles and abnormal co-contraction in the hemiplegic arm, compared with conventional physical therapy. Scand J Rehabil Med 14:121-131, 1982 31. Skelly AM, Kenedi RM: EMG biofeedback therapy in the reeducation of the hemiplegic shoulder in patients with sensory loss. Physiotherapy 68:34-38, 1982 32. Wolf SL: Neurophysiological factors in electromyographic feedback for neuromotor disturbances. In Basmajian JV (ed): Biofeedback: Principles and Practice for Clinicians, ed 2. Baltimore, MD, The Williams & Wilkins Co, to be published. 33. Shahani BT, Connors L, Mohr JP: Electromyographic audiovisual feedback training effect on the motor performance in patients with lesions of the central nervous system. Arch Phys Med Rehabil 58:519, 1977 34. Takebe K, Basmajian JV: Gait analysis in stroke paients to assess treatments of foot-drop. Arch Phys Med Rehabil 57:305-310, 1976 35. Basmajian JV, Gowland C, Brandstater ME, et al: EMG feedback treatment of upper limb in hemiplegic stroke patients: A pilot study. Arch Phys Med Rehabil 63:613-616, 1982 36. Basmajian JV, Kukulka CG, Narayan MG, et al: Biofeedback treatment of foot-drop after stroke compared with standard


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rehabilitation technique: Effects on voluntary control and strength. Arch Phys Med Rehabil 56:231-236, 1975 Fish D, Mayer N, Herman R: Letter to the editor: Biofeedback. Arch Phys Med Rehabil 57:152, 1976 Shiavi RG, Champion SA, Freeman FR, et al: Efficacy of myofeedback therapy in regaining control of lower extremity musculature following stroke. Am J Phys Med 58:185-194, 1979 Binder SA, Moll CB, Wolf SL: Evaluation of electromyographic biofeedback as an adjunct to therapeutic exercise in treating the lower extremities of hemiplegic patients. Phys Ther 61:886-893, 1981 Gianutsos J, Eberstein A, Krasilowsky G, et al: EMG feedback in the rehabilitation of upper extremity function: Single case studies of chronic hemiplegics. International Neuropsychological Society Bulletin, Symposium Issue, 1979, pp 1 12 Mroczek N, Halpern D, McHugh R: Electromyographic feedback and physical therapy for neuromuscular retraining in hemiplegia. Arch Phys Med Rehabil 59:258-267, 1978 Lee K-H, Hill E, Johnston R, et al: Myofeedback for muscle retraining in hemiplegic patients. Arch Phys Med Rehabil 57:588-591,1976 Swaan D, vanWieringen PCW, Fokkema SD: Auditory electromyographic feedback therapy to inhibit undesired motor activity. Arch Phys Med Rehabil 55:251-254, 1974 Teng EL, McNeal DR, Kralj A, et al: Electrical stimulation and feedback training: Effect on the voluntary control of paretic muscles. Arch Phys Med Rehabil 57:228-233, 1976 Ethridge D: Comments. Am J Occup Ther 22:420-425, 1968 Talbot RE, Humphrey DR (eds): Posture and Movement, New York, NY, Raven Press, 1979 Davis AE, Lee RG: EMG biofeedback in patients with motor disorders: An aid for co-ordinating activity in antagonistic muscle groups. Can J Neurol Sci 7:199-206, 1980 Bach-y-Rita P: Central nervous system lesions: Sprouting and unmasking in rehabilitation. Arch Phys Med Rehabil 62:413-417, 1981 Luria AR, Naydin VL, Tsvetkova LS, et al: Restoration of higher cortical function following local brain damage. In Winken PJ, Bruyn GW (eds): Handbook of Clinical Neurology, Amsterdam, North Holland, 1969, Vol 3 Geschwind N: Late changes in the nervous system: An overview. In Stein DG, Rosen JJ, Butters N (eds): Plasticity and Recovery of Function in the Central Nervous System, New York, NY, Academic Press Inc, 1974, pp 4 6 7 - 5 0 8 Nicholls JG (ed): Repair and Regeneration of the Nervous System, Berlin, Germany, Springer-Verlag, 1982

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APPENDIX 1

18

45

10

1

60 70

9

Leeetal, 1976

Brudny et al, 1974, 1976

Gavin and Stephan, 1976

Ingliset al, 1976

Brudny et al, 1977 1979

Mroczek et al, 1978

5

20

Andrews, 1964

Gianutsos et al, 1979

1

Experimental Sample Size

Marinacci and Horande, 1960

Investigator(s)

baseline

crossover

none none

none

none

none

feedback; no feedback; noncontingent feedback

none

none

Control Group

Seventeen of 20 chronic patients gained some elbow control after 5 minutes of feedback training. All patients received the 3 conditions for weak deltoid muscle. Three conditions (counterbalanced) on each of three days; each contraction for 20 seconds; no difference in EMG changes across conditions but older and more poorly motivated patients showed increasing muscle output. Treatment 3-5 times a week for 2-3 months; 39 of 45 patients required additional retraining; 20 of these 39 gained assistive or functional use of upper extremity which was retained at follow-up (3 mo to 3 yrs). Relaxation and targeted muscle training supplemented by relaxation tapes led to improvement in all patients. Specific treatment to involved upper and lower extremity led to increased endurance and a reduction in limb atrophy ascertained by girth measurements; hand function appears to improve. The 1979 report probably adds 10 patients to 1977 report; greater than 50 percent gained assistive or functional use of upper extremity, which was retained at follow-up (up to 3 years). Each chronic patient served as own control; 4 weeks of feedback followed by 4 weeks of conventional therapy or vice versa (cross-over design); goal of increasing wrist extensor EMG was greater for feedback interval but not different from therapy to increase ROM; biofeedback after physical therapy appeared to be less effective. Forty-two to 54 feedback sessions for 5 chronic stroke patients with treatment progressing for targeted muscle training from shoulder to hand; best able to gain elbow function; poorest gain in finger extension.

Twenty percent improvement in upper extremity function.

Major Findings

Considering detail of data acquisition, no statistical analyses provided and no reference to baseline data; method to record peak average EMG is questionable; outcomes not provided.

Treatment techniques tailored to each patient; functional scale vague; description to replicate systematically procedures not provided; data totally descriptive; patients lacking motivation excluded. Excellent data analyses with physical therapy well controlled but no true control group; no specific training with feedback particularly with respect to reducing wrist flexor activity; no measures of arm function.

Quantification of muscle changes, specific and functional measures not provided.

Feedback training tailored to each patient; lacks specific quantification and analysis; no follow-up.

Treatment technique tailored to each patient; functional scale vague; description to replicate systematically not provided; data totally descriptive.

Anecdotal; no follow-up; lacks specific data; only deltoid muscle examined; recognized as initial feedback report. Other treatments also provided; no definition of function; no follow-up; no analysis of data. Testing situation too short and unrealistic; both acute and chronic stroke patients included; only one session for each condition.

Critique

REVIEW OF EMG BIOFEEDBACK FINDINGS ON APPLICATIONS TO STROKE PATIENTS' UPPER EXTREMITIES

conventional therapy; feedback-behavioral training

11 feedback; 9 control

3 CVA 2 gunshot 1 closed head injury

4

1

18

37

20

Middaugh and Miller, 1980

Marsh, 1980

Honer et al, 1982


Prevoet al, 1982

Basmajian et al, 1982

Skelly and Kenedi, 1982

9 conventional PT; 9 biofeedback

none

none

alternate feedback/no feedback trials

no feedback testing

2

Davis and Lee, 1980

none

52 34

Wolf et al, 1979 1980

Case study that failed to show feedback to anterior deltoid and triceps brachii capable of disrupting flexor synergy; limited to 22 sessions. Train chronic patients receiving feedback to reduce muscle activity in 2 proximal and 2 distal muscles and increase activity in 1 proximal and 2 distal muscles. All patients treated for 2 months (28 sessions, 3 times a week); after treatment feedback group showed reduced cocontractions in trained muscles but not in untrained muscle groups; no change in muscles of patients receiving conventional therapy. Five weeks of treatment, 3 times a week; outcomes measured in upper extremity functional scores; patients randomly assigned to groups; feedback-behavioral intervention appears more effective if upper limb involvement not as severe (Brunnstrom recovery Stages 5-6) and duration of stroke longer (4-5 months) or, for severe (Brunnstrom, Stages 3-4), cases if treatment started within 3 months. Goal to increase shoulder flexion; training 3 times weekly for 4 weeks; both feedback and control patients gained increased shoulder flexion that was positively related to initial active ROM and not to treatment.

Following specific treatment protocol for 48 upper extremities, outcome shows no relationship to age, sex, side involved, duration of stroke, or previous rehabilitation; lower extremities responded better than upper; no decrements at 1 year follow-up. Provide novel visual display based upon EMG power spectrum from wrist flexors and extensors; these patients able to reverse muscle action without cocontraction following training (2-3 times a week). Patients asked to make specific 30 second contractions from any 1 of 6 paretic muscles; 12 contractions over 2 sessions; feedback-no feedback trials were alternated and counterbalanced; patients generated significantly more EMG with feedback, particularly during first 10 seconds of 30 second trial; no correlation between ability to do task and age, sex, or duration of injury. Treatments for 15 minutes, twice a week for 8 weeks; all patients improved.

Control situation poorly defined; lacks complete data analyses; no functional correlates provided.

Uncertain of number of patients in each group; all patients in acute phase of stroke; no description of treatment; lacks correlation between intervention and specific functional changes.

Implied improved function but no measures reported; no details on treatment; all accounts are vaguely descriptive and lack any analyses. Profound spasticity, proprioceptive loss, and hyperarousal may have made patient inappropriate candidate; lacks quantitative analyses. Lacks true control group but does provide substantial data analyses; functional tests for hand as time motion measurements yet no detail provided; conventional therapy regimen not explained.

Involves both acute and chronic patients who were receiving concomitant rehabilitation; no functional scores; only 2 sessions, no follow-up; not analyzed for muscle being tested; mixed population with respect to cerebral insult.

Duration of training not defined; lacks true control group; no statistical analyses; insufficient information to replicate work; no functional measures.

Lacks quantitative analyses of neuromuscular and functional measures; no control group; all data are analyzed as discrete rather than continuous data.

PRACTICE

1457

1458

PHYSICAL THERAPY

4

20

6

9

15

6

Swaan et al, 1974


Brudny et al, 1976

Teng et al, 1976

Takebe and Basmajian, 1976

Flom etal, 1976

16

10

Johnson and Garton, 1973

Shahani etal, 1977

1


Amato et al, 1973

Investigator(s)

APPENDIX 2

8 feedback; 8 feedback and conventional PT

3 peroneal nerve stim.; 6 intensive PT; 6 PT and biofeedback none

all patients received 3 types of treatment

none

10 ther. ex.; 10 ther. ex. followed by biofeedback

4

none

none

Control Group

Twelve weeks of training to increase tibialis anterior output; measured ROM and ankle dorsiflexor strength. Feedback group (3 treatments a week for 6 weeks) improved faster in gait, motor power; patients with lacunar lesions showed more improvement than patients with middle cerebral artery lesion.

Three of 6 patients without anterior tibialis activity in static posture, showed some use of this muscle during ambulation. Fixed sequence of treatment: first, peroneal nerve stimulation; second, stimulation and feedback; third, feedback only; four patients increased voluntary ankle dorsiflexion; effect seems to be most attributable to feedback. Treatment for 5 weeks at 3 times a week; measured gait before and after treatment; nerve stimulator and feedback groups showed improved gait patterns; feedback to weak anterior tibialis muscle.

Following 2 months of home training to reduce gastrocnemius activity during voluntary ankle dorsiflexion, activity and gait had improved. After three 30-minute treatments (to tibialis anterior) and multiple home practice, 3 patients discard short leg braces and 2 patients show some functional improvement. Patients receiving feedback to reduce peroneus longus activity for 6 treatment sessions (10 min each) counterbalance by alternating conventional therapy (control); only 1 of 4 patients could inhibit muscle activity with feedback. Between-groups design; patients receiving combined therapeutic exercise and biofeedback gained twice as much ankle dorsiflexion and strength as exercise groups; gains maintained at 4 to 16 week follow-up.

Major Findings

Critique

Described only 3 patients; no control; no consistency in treatment; no quantitative analyses. Only study to relate outcome to specificity of lesion; all patients in acute phase of stroke; analysis of outcomes largely subjective.

Used acute stroke patients, no quantification of findings; no specifics on treatment protocol for patients in any group.

Data presented on only 4 patients; no statistical treatment of data; no baseline data or control group; order of treatment not counterbalanced; treatment intervals not fixed; could have been additive effect.

No statistical analyses; lacks true control group; more recent (subchronic) stroke patients in biofeedback group; inadequate treatment of data; functional scales vague; treatment regimen of each patient, known to evaluator. No description of treatment technique; no functional analysis; no follow-up; no data analyses.

Did not control for cumulative treatment effects so cannot decipher whether EMG changes due to feedback or therapy; first controlled study.

Acute and chronic patients; change based exclusively on muscle test results; no data analysis; no follow-up.

Lacks repeated measurements, gait improvement subjectively assessed; no follow-up.

REVIEW OF EMG BIOFEEDBACK FINDINGS ON APPLICATIONS TO STROKE PATIENTS' LOWER EXTREMITIES


control; instrumental; feedback

none

actual feedback; simulated feedback control

22

52 34

24

5

10

22

Shiavi et al, 1979

Wolf et al, 1979 1980

Hurd et al, 1980

Santee et al, 1980

Binder et al, 1981

Burnside et al, 1982

11 exercise; 11 exercise with feedback

baseline; EMG feedback; EMG feedback and incentives; EMG feedback; follow-up measures 5 feedback with exercise; 5 exercise

none

Control Group

39



Investigator(s)

Three patients received all 5 conditions; 2 patients did not receive second series of EMG feedback sessions; feedback to decrease gastrocnemius and increase tibialis anterior activity; feedback interval produced greatest increase in ankle ROM and muscle activity; incentive (money) may enhance performance via motivational effect. Chronic stroke patients in both groups increased ankle dorsiflexion ROM but feedback within exercise group increased ambulation speed; limited to 12 treatment sessions for all but 2 patients. Treatment for 6 weeks with 2 sessions of 15 minute duration a week; goal was to increase dorsiflexion of ankle; exercise group set-up for feedback but did not receive any; follow-up at 6 weeks; both groups improved but feedback group significantly increased in dorsiflexion strength; exercise group decreased in ROM and in ankle dorsiflexion strength at follow-up.

General description of improvement at shoulder (reduced subluxation), ankle and hand. Three groups (randomly assigned); grade muscle strength for each of 6 muscles treated; feedback group gained greater "control" but not greater strength. Following specific treatment, protocol for 44 lower extremities outcome shows no relationship to age, sex, side involved, duration of stroke, or previous rehabilitation; lower extremities responded better than upper; no decrements at 1 year follow-up. Treated shoulder or ankle with true feedback or simulated feedback based on therapist's impression of patient efforts; both groups showed similar changes in EMG and ROM; changes attributed to motivational factors because patients were encouraged and praised.

Major Findings

Gait analysis outcomes were nonspecific; although evaluations were blind, treatment given by nonprofessional; no statement made on changes in quality of gait.

First study to integrate feedback-within exercise program; lacks true control group; measures quantified ambulation function; limited number of treatments.

All were acute stroke patients; no true control group because these patients received feedback training to either upper or lower limb while monitoring changes in the other limb (more like generalizing effect); number of feedback sessions not given; no functional correlates; combined data from changes in anterior deltoid and tibialis anterior; verbalization of praise confounds data. Lacks true control group; incentive approach clinical unrealistic; ROM results were equivocal; ROM increases were marginal; no correlation to function.

Primarily anecdotal; lacks specific information regarding treatment regimen or assessment of outcome. Term "control" poorly defined; control group receivd undefined conventional PT; lacks comprehensive data analyses; no true control group; not certain of treatment or post-stroke time. Lacks quantitative analyses of neuromuscular and functional measures; no control group; all data are analyzed as discrete rather than continuous data.

Critique

PRACTICE

1459