Quantifying Real-World Upper-Limb Activity Via Patient-Initiated Movement After Nerve Reconstruction for Upper Brachial Plexus Injury

Abstract

BACKGROUND

A critical concept in brachial plexus reconstruction is the accurate assessment of functional outcomes. The current standard for motor outcome assessment is clinician-elicited, outpatient clinic-based, serial evaluation of range of motion and muscle power. However, discrepancies exist between such clinical measurements and actual patient-initiated use. We employed emerging technology in the form of accelerometry-based motion detectors to quantify real-world arm use after brachial plexus surgery.

OBJECTIVE

To evaluate (1) the ability of accelerometry-based motion detectors to assess functional outcome and (2) the real-world arm use of patients after nerve transfer for brachial plexus injury, through a pilot study.

METHODS

Five male patients who underwent nerve transfer after brachial plexus injury wore bilateral motion detectors for 7 d. The patients also underwent range-of-motion evaluation and completed multiple patient-reported outcome surveys.

RESULTS

The average age of the recruits was 41 yr (±17 yr), and the average time from operation was 2 yr (±1 yr). The VT (time of use ratio) for the affected side compared to the unaffected side was 0.73 (±0.27), and the VM (magnitude ratio) was 0.63 (±0.59). VT strongly and positively correlated with shoulder flexion and shoulder abduction: 0.97 (P = .008) and 0.99 (P = .002), respectively.

CONCLUSION

Accelerometry-based activity monitors can successfully assess real-world functional outcomes after brachial plexus reconstruction. This pilot study demonstrates that patients after nerve transfer are utilizing their affected limbs significantly in daily activities and that recovery of shoulder function is critical.

ABBREVIATIONS

AROM

active range of motion

DN4

Douleur Neuropathique 4 questionnaire

IPAQ

International Physical Activity Questionnaire

MRC

Medical Research Council

PROM

passive range of motion

PROMIS

Patient-Reported Outcomes Measurement Information System

QuickDASH

shortened Disability of Arm, Shoulder, and Hand questionnaire

SPADI

Shoulder Pain and Disability Index

VM

magnitude ratio

VT

time of use ratio

The goal of every surgical procedure is to achieve a successful outcome. This is true with brachial plexus reconstruction surgery; however, the definition of a successful outcome to this procedure continues to evolve. Current outcomes assessment is based on clinician-elicited measures in the outpatient clinic (eg, muscle strength using the Medical Research Council [MRC] grading criteria, active range of motion [AROM], and video/pictorial recordings). These measures do not assess real-world use of the reconstructed arm.

Subjective patient input regarding the perception of surgical outcome via various surveys that define “patient-reported outcomes” can augment the assessment of outcome. The World Health Organization (www.who.int/classifications/icf) emphasizes the evaluation of the “Activity and Participation” domains (versus clinician-elicited measures in the “Body Function and Structure” domains); however, these subjective disability surveys generally rely on questions assessing the ability to perform global tasks and thus provide little insight into outcomes specific to a surgically reconstructed upper extremity. Hence, the applicability of our current outcomes assessments to the “real-world” use of the reconstructed arm—beyond the exam room—is controversial, and true assessment of arm use in everyday activities remains elusive.

Recent advances in body-worn sensor technology provide a promising improved method for assessing outcomes after brachial plexus reconstruction surgery by quantifying patient-initiated arm movement in remote settings: for example, wrist-worn accelerometers have been used successfully to monitor changes in arm function in chronic stroke.¹ In this novel application of accelerometry to assessing true outcomes after nerve reconstruction for brachial plexus injury, we present the results of a pilot study demonstrating the applicability of accelerometry to evaluate arm use after nerve reconstruction and examine the relationship between patient-initiated real-world arm use and our current clinician-elicited assessment methods.

METHODS

Study Design

This prospective pilot case series recruited 5 adults with upper brachial plexopathy who underwent nerve transfer procedure in a single institute in 2014 and 2015. The participants completed surveys regarding patient demographics, pain, Patient-Reported Outcomes Measurement Information System (PROMIS), and patient-reported upper extremity function at the study visit. One of two certified occupational therapists conducted standard clinician-elicited physical measurements at the same visit. Participants then wore an activity monitoring device on both the injured (after nerve reconstruction) and noninjured arms for 7 d. The devices were returned at the end of the study for data analysis. Participants were financially compensated for their participation. The study protocol was approved by the Institutional Review Board (HUM103135); informed consent was acquired from all patients prior to study participation.

Accelerometry

Activity monitors (GT9X Link ActiGraph; ActiGraph LLC, Pensacola, Florida) were worn on each wrist during waking hours for 7 consecutive days, of note the patients did not participate in physical therapy during testing. These devices have been shown to be a valid and reliable means of monitoring movements of the upper extremity in motor impairments following central nervous system insult, including stroke^1,2 and cerebral palsy.³ Each device contains a solid-state accelerometer that records raw acceleration in 3 axes at 30 Hz and can store data locally for up to 14 d. Devices were calibrated prior to use and were attached to the wrist using adjustable watch bands. Accelerometry data were downloaded and filtered using commercial software (ActiLife v6.13.3; ActiGraph LLC). This software was also used to visually inspect data to ensure that participants followed the established protocol for wearing the devices during waking hours over the 7-d period.

Analysis of arm acceleration followed methods previously reported⁴ and focused on the amount of time per day that the devices detected movement (VT) and vector magnitude (VM). The latter is a measure of the intensity of upper extremity activity, where, for each second of data, accelerations in the 3 planes of motion were combined into a single vector magnitude value. To compare the daily contribution of each arm to overall time of use and vector magnitude, time and magnitude ratios were calculated by dividing values associated with the affected limb by unaffected limb values.

Demographic and Clinical Measures

Patient demographics included age, surgery to study duration, gender, race, involved side, and dominant hand. Active and passive range of motion (AROM and PROM) of shoulder flexion, shoulder abduction, shoulder extension, shoulder external rotation in adduction, shoulder internal rotation in adduction, elbow flexion in adduction, elbow extension, and forearm supination were measured, as these joints are targeted for functional recovery in patients with upper brachial plexopathy.

Patient-Reported Pain, Upper Extremity Function, and Physical Activity Measures

Pain was assessed using the Douleur Neuropathique 4 (DN4) questionnaire and the Shoulder Pain and Disability Index (SPADI). The DN4 is a 10-item questionnaire commonly used to assess neuropathic pain. It comprises 7 patient-reported measures of pain quality and 3 items based on clinical examination. Scores range from 0 to 10, with scores above 4 indicative of neuropathic pain.⁵ The 13-item self-report SPADI comprises 2 subscales: pain and disability. Patients are asked to rate the amount of pain experienced during different activities and the degree to which they are impaired by their injury or condition. Subscale scores range from 0 to 100, with 0 indicating no pain or difficulty and 100 indicating worst pain imaginable and help needed because of the injury. Scores are combined and range from 0 (best) to 100 (worst).⁶

Upper extremity function was self-reported using the shortened version of the widely used Disability of Arm, Shoulder, and Hand (QuickDASH). It is validated for a wide range of musculoskeletal conditions and includes 11 items scored 1 to 5. Total scores are calculated, with the highest score of 100 indicating the greatest amount of disability.⁷ Manual ability was assessed using 1 of 5 validated ABILHAND questionnaires that measure the ability of specific clinical populations to perform activities of daily living using the upper extremity.⁸ The ABILHAND questionnaire designed for stroke was chosen since it focuses primarily on bimanual activities. It consists of 23 items using a 3-level scale from impossible (0), difficult (1), or easy (2). An online Rasch analysis is used for scoring, with lower scores (0-42) indicating greater disability.⁹

Self-reported physical activity was measured using the International Physical Activity Questionnaire (IPAQ). The IPAQ is a validated and reliable assessment of physical activity measured across four domains: occupational, transport, domestic, and leisure.¹⁰ Participants reported their physical activity in hours over the preceding 7 d, with higher scores indicative of greater physical activity. Participants were then classified (low, moderate, or high) based on their scores.

Quality of Life

PROMIS is a generic measure of health-related quality of life that can be applied to the general population and patients with neurological conditions (http://www.nihpromis.org). We reported fatigue, informational support, emotional support, anxiety, anger, and depression domains in this study.

Statistical Analysis

We assessed descriptive statistics for patient demographic data and ActiGraph data. Pearson correlation was applied to investigate the relationship between ActiGraph arm use data and physical measurements, patient-reported pain, upper extremity functionality, and PROMIS. P < .05 was considered as statistically significant. Commercially available software was used for all analyses (SPSS version 22; IBM Corporation, Armonk, New York).

RESULTS

Five patients were recruited for this pilot study. All 5 (100%) patients had nonrecovering brachial plexus injuries for which surgical nerve reconstruction was recommended. The mean age was 41 yr (±17 yr) at the time of surgery, and the average time from surgery to the inclusion of the study was 2 yr (±1 yr). All 5 (100%) patients included in this study were white males. Three (60%) of the injuries were right sided, and 3 (60%) of the injuries involved the dominant arm (Table 1). Patient 1 underwent C5 to posterior division, spinal accessory to suprascapular transfer, and median to musculocutaneous, and patients 2 to 5 all underwent triple transfer repairs (spinal accessory to suprascapular, radial to axillary, and ulnar to musculocutaneous). Shoulder flexion AROM and shoulder abduction AROM ranged from 10 to 160 and 0 to 160, respectively. MRC grading for shoulder flexion and shoulder abduction ranged from 0 to 4- in both. Elbow flexion AROM ranged from 0 to 150, and MRC ranged from 2 to 4-.

TABLE 1.

Patient Demographic Data

	n (%) n = 5
Mean age (y) ± standard deviation (SD)	41 ± 17
Time from operating room to study (y) ± SD	2 ± 1
Sex
Male	5 (100%)
Race
Caucasian	5 (100%)
Involved side
Left	2 (40%)
Right	3 (60%)
Dominance
Right	5 (100%)
Lesion type
Brachial plexopathy	5 (100%)

The VT reflects the ratio of movement in the injured (reconstructed) arm to the unaffected arm: VT averaged 0.73 (±0.27) over the entire cohort. The range for VT was 0.53 to 1.19. The VM averaged 0.63 (±0.59). The range for VM was 0.23 to 1.66 (Table 2). There was a positive correlation of VT with shoulder flexion and shoulder abduction: 0.97 (P = .008) and 0.99 (P = .002), respectively. No statistically significant correlation was noted between VT and elbow flexion (0.73, P = .17) or forearm supination (0.43, P = .47; Table 3). There was a positive correlation of VM with shoulder flexion and shoulder abduction: 0.93 (P = .022) and 0.96 (P = .009), respectively. Again, no statistically significant correlation was found between VM and elbow flexion (0.66, P = .23) or forearm supination (0.39, P = .52; Table 3). Both the percentage time of use and the magnitude of movement demonstrate that nerve reconstruction conveys adequate patient-initiated arm use.

TABLE 2.

The Percentage of Time of Use and Magnitude of Movement Demonstrate That Nerve Reconstruction Conveys Adequate Patient-Initiated Arm Use

Patient	Time of use ratio (VT)	Magnitude ratio (VM)
1	0.53	0.23
2	1.19	1.66
3	0.62	0.41
4	0.56	0.33
5	0.75	0.5
Total mean ± SD (percentage of unaffected arm)	0.73 ± 0.27 (73%)	0.63 ± 0.59 (63%)

TABLE 3.

Pearson Correlations With PROM/AROM: VT and VM Correlate With Shoulder Flexion and Shoulder Abduction

	Time of use ratio (VT)				Magnitude ratio (VM)
	AROM correlation	P value	PROM correlation	P value	AROM correlation	P value	PROM correlation	P value
Shoulder flexion	0.97	.008	0.52	.38	0.93	.022	0.60	.29
Shoulder abduction	0.99	.002	0.47	.43	0.96	.009	0.39	.52
Shoulder extension	0.48	.41	0.41	.49	0.51	.38	0.38	.53
Shoulder external rotation adduction	0.73	.17	0.42	.48	0.61	.28	0.32	.60
Shoulder internal rotation adduction	0.41	.49	0.68	.21	0.38	.53	0.66	.22
Elbow flexion in adduction	0.73	.17	0.53	.36	0.66	.23	0.47	.42
Forearm supination	0.43	.47	0.41	.49	0.39	.52	0.38	.53

AROM and PROM, active and passive range of motion. Bold P value indicates significance.

Self-reported pain scales were used for correlations with the activity ratios (VT and VM). There was a positive correlation between the DN4 score and VT (0.96, P = .011); however, there was no correlation between the SPADI pain score and VT (0.31, P = .61; Table 4). Likewise, there was a positive correlation between the DN4 score and VM (0.94, P = .018), but no correlation between the SPADI pain score and VM (0.21, P = .73; Table 4). Therefore, pain assessment methods that measure neuropathic pain were more valuable for outcome assessments than general pain measures.

TABLE 4.

Pearson Correlations With Patient-Reported Pain and Upper Extremity Functional Disability: Pain Assessment Methods (DN4) That Measure Neuropathic Pain Are More Valuable for Outcome Assessments Than General Pain Measures

	Time of use ratio (VT)		Magnitude ratio (VM)
	Correlation	P value	Correlation	P value
Pain
DN4	0.96	.011	0.94	.018
SPADI pain	0.31	.61	0.21	.73
Functional disability
QuickDASH	−0.90	.039	−0.86	.061
ABILHAND	0.91	.033	0.92	.025
SPADI disability	−0.43	.47	−0.43	.47
IPAQ MET min/wk	0.70	.19	0.58	.31
IPAQ category	−0.35	.56	−0.28	.65

DN4, Douleur Neuropathique 4 questionnaire; SPADI, Shoulder Pain and Disability Index; QuickDASH, shortened Disability of Arm, Shoulder, and Hand questionnaire; IPAQ, International Physical Activity Questionnaire. Bold P value indicates significance.

Functional disability scales were used for correlations with arm use ratios. The correlations between QuickDASH and VT and VM arm use ratios were −0.90 (P = .039) and −0.86 (P = .061), respectively. The statistically significant correlation between QuickDASH and arm time use ratio can be interpreted as patients with higher VT consider themselves to have better upper extremity function. The correlations between ABILHAND score and VT and VM were 0.91 (P = .033) and .92 (P = .025), respectively. There were no significant correlations between VT or VM and SPADI disability scores or the IPAQ scores (Table 4). Therefore, patient-reported outcomes that are directed at arm and hand use are more relevant than general subjective activity surveys.

The arm use ratios were also correlated with the PROMIS scores (Table 5). There was a correlation between the fatigue subscore and VT and VM, −0.95 (P = .014) and −0.97 (P = .006), respectively. However, the informational support, emotional support, anxiety, anger and depression subscores showed no significant correlations with either VT or VM.

TABLE 5.

Pearson Correlations With PROMIS: Fatigue Correlates With Decreased Patient-Initiated Arm Use

	Time of use ratio (VT)		Magnitude ratio (VM)
PROMIS	Correlation	P value	Correlation	P value
Fatigue	−0.95	.014	−0.97	.006
Informational support	−0.18	.77	−0.07	.92
Emotional support	0.43	.47	0.39	.52
Anxiety	0.12	.85	0.25	.69
Anger	−0.14	.82	−0.16	.80
Depression	−0.44	.46	−0.47	.43

PROMIS, Patient-Reported Outcomes Measurement Information System. Bold P value indicates significance.

DISCUSSION

Traumatic injury to the brachial plexus is a devastating event for the adult patient, resulting in decreased function of the upper extremity.¹¹ Fortunately, the treatment of brachial plexus injury has advanced dramatically over the past 25 yr.¹¹ Brachial plexus surgeries, including nerve grafting and nerve transfers, have given hope to a once dismal prognosis.¹² Until now, the focus of research has been on the surgical techniques and therapeutic approaches, but little has been done to further refine the evaluation of these patients.

Evaluating patients with brachial plexus injuries requires serial clinical examinations as well as electro-diagnostic testing with electromyography and nerve conduction studies. Though this focused testing allows us to evaluate each muscle and joint individually, understanding the functional arm use once the patient leaves clinic remains elusive. Attempts to understand the real-world use of the arm have been limited to patient recall and various surveys. This project attempted to not only capture patient-initiated movement, but also to quantify the frequency and quality of the movement through the use of bilateral upper extremity accelerometers. These devices successfully captured and quantified the timing and magnitude of arm movements over the course of 7 d, and showed that patients used their affected arm up to 73% as much as the time they used their unaffected arm and with approximately 63% of the magnitude of movement after a brachial plexus reconstruction. These data on the remote capture of patient-initiated movements are critical in describing the real-world use of the upper extremities. Additionally, these are the first quantifiable data demonstrating how patients do when they leave the clinic, and the results are quite promising. These findings add to the ever-increasing base of knowledge that brachial plexus reconstruction is creating favorable outcomes in our patients.

Brachial plexus functional outcomes are not the only condition in which out-of-clinic evaluations are useful. Cardiac arrhythmias and sleep disturbances are among other conditions where prolonged observation is important. Though the idea of take-home technology may be daunting, holter monitors and at-home sleep studies have been widely and successfully adopted in cardiology and sleep medicine. The accelerometry devices that we employed are small wristwatch-like detectors that are much simpler and less intrusive than holter monitors and at-home sleep studies.

Prior to capturing patient-initiated movement with motion detectors, we focused our evaluations on multiple domains: AROM, MRC, patient satisfaction, and patient reporting.^13,14 Although these domains have been widely used, their relationships to one another have demonstrated conflicting messages. For instance, Franzblau et al¹⁵ and Rasulić et al¹⁶ demonstrated that there appeared to be no correlation between clinician-elicited outcomes and patient satisfaction. The apparent disconnect between objective clinical outcomes like MRC grading and subjective clinical outcomes such as patient satisfaction should raise concern that we may be missing the mark in evaluating one or both.

Although widely used and often the main focus of clinical evaluation and research, the utilization of AROM and MRC in the evaluation of these patients has major pitfalls. These outcome measures test single joints and the movements are not patient initiated. As the main goal of surgery is to restore a limb for use in everyday activities, it is a concern that clinical evaluation focuses on two characteristics of movement that are not reflective of daily use. A majority of our movements involve multiple joints and are spontaneously initiated, and an ideal evaluation should reflect these characteristics. In addition to the questionable applicability of these tests to real life, the tests require subjective calls by the evaluator. The interrater reliability between various providers administering these tests has its inherent variance and has been thoroughly described.^17,18 Together, these factors can explain why some patients report limited use despite good outcomes of clinical recovery in the ways that we have previously tested. The ActiGraph measurements address these issues by gathering objective data on patient-initiated, multijoint movements throughout various points in the patient's normal day.

It is unfair to blame clinical evaluations alone for this disconnect. The utilization of patient-reported outcomes, including patient satisfaction queries, comes with its own set of limitations. Franzblau et al¹⁵ demonstrated that patient satisfaction after brachial plexus injury is largely varied and depends on which specific questions about satisfaction are asked and on preoperative expectations. Additionally, patients in the Franzblau et al¹⁵ study stated that they were satisfied with their surgical outcomes and the care provided and would have surgery again; however, they were not satisfied when asked about the function of their arm. Kretschmer et al¹⁹ demonstrated high levels of satisfaction in patients despite persistently severe levels of disability as well as the inability to resume work in their prior profession. Rasulić et al¹⁶ demonstrated a slight disagreement between patients’ improvement in quality of life and satisfaction with surgical outcome. Despite patient satisfaction being so broad, varied in its evaluation, and varied in its results, it has an ever evolving role in the health care system, including linkage to reimbursement. This further heightens the importance of understanding its evaluation.

Additional patient-reported outcome surveys have been utilized after brachial plexus repair. These range from broad evaluations like the NIH initiative PROMIS to more specific surveys aimed at nerve issues like IPAQ, DASH, DN4, SPADI, and ABILHAND. We utilized two scales to evaluate pain, DN4 and SPADI pain, which showed conflicting results. The DN4 directly correlated to both time of use and quality of use as defined by the ActiGraph. Although the DN4 had a direct correlation, the SPADI pain scale showed no relationship to movement. Multiple functional disability scales were included in this study as well: DASH, ABILHAND, SPADI disability, and IPAQ. Again, amongst the patient-reported scales focused on disability, there were differing associations with arm movement frequency and arm movement quality. The DASH and ABILHAND surveys showed clear correlations, while the SPADI disability and IPAQ surveys did not. Despite the robust nature of the PROMIS survey data, the only correlation between arm movement and subscores was fatigue, while the informational support, emotional support, anxiety, anger, and depression subscores demonstrated no relationship to arm use and quality of movement. These data and other publications showing conflicting results and interpretations with theses scales in nerve injuries support the recent advocacy for the creation of more specific brachial plexus questionnaires.¹⁵ Similar to the surveys on satisfaction, these data demonstrate the importance of understanding the questions we ask to evaluate disability and the outcomes to which they are correlated.

Although the initial goal of this project was to test motion detectors in patients with brachial plexus repair, an interesting finding came to the forefront during data analysis. The only joint function that demonstrated a clear association with both the time of arm use and the quality of arm movement in these patients was the shoulder AROM. The patients with better shoulder function used the affected arm significantly more often and with significantly better quality. The importance of the shoulder has been recognized for many years, and was championed by Dr Gilbert; however, no data until now have been able to demonstrate the importance of shoulder function on overall arm use. These preliminary data demonstrate that the shoulder could be the limiting factor in meaningful arm use and support the importance of focusing our efforts to improve the restoration of shoulder function, especially given that adequate reanimation of the shoulder remains elusive. In areas other than brachial plexus and nerve repair, the importance of a functioning shoulder is recognized. Shoulder and rotator cuff injuries can be career ending in athletes and patients with physically demanding professions.

Although shoulder function showed the strongest correlation with arm use in this cohort, this does not devalue the importance of the restoration of elbow flexion. Brachial plexus surgery and the development of nerve transfers for elbow restoration have demonstrated huge leaps in functional outcomes. It is possible that the correlation with elbow flexion was not yet demonstrated due to a type 2 error and low sample size. Further studies with larger numbers will be necessary to more clearly define this relationship.

Limitations

This manuscript presents pilot data on the use of accelerometry in the evaluation of brachial plexus repair after injury. Limitations inherent to pilot data are the low number of patients included in the study and the homogeneity of the subjects (young males); however, this study neatly demonstrates the applicability of accelerometry, and the patients accurately represent the demographic that is likely to be afflicted with adult brachial plexus injuries. The third major limitation in the interpretation of results is the lack of preoperative accelerometry data. Further work will be pursued in the prospective evaluation of brachial plexus patients using accelerometry.

CONCLUSION

The current evaluation of success in brachial plexus surgery continues to be limited by clinician-elicited methods and patient recall. The use of accelerometry can overcome some of these barriers, while providing objective data on real-world use of the affected limb. Additionally, we demonstrate clearly that unless the shoulder has been reconstructed enough to place the hand in space, patients do not use the arm in real life. Therefore, the shoulder may be the limiting factor in the real-world use of the affected limb. We suggest that the shoulder joint deserves increased attention in the context of improving and advancing brachial plexus reconstruction.

Disclosures

Supported, in part, by grants from the Michigan Institute for Clinical and Health Research to Dr Lynda J.-S. Yang, and the University of Michigan MCubed Program and the Blue Cross Blue Shield of Michigan Foundation to Dr Susan H. Brown. Research reported in this publication was also supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases of the National Institutes of Health under Award Number 2 K24-AR053120-06 to Dr Kevin C. Chung. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

COMMENT

This is a well-written pilot study in which the authors evaluate the use of an accelerometry-based motion detector to assess functional outcome and the real-world use of an upper extremity that has suffered an upper brachial plexus injury and underwent nerve transfers for reconstruction. Although the n is only 5, the authors present promising data that may well change the paradigm that is used to assess the outcomes of these complex nerve reconstructive strategies. The findings indicate that timely and well-performed brachial plexus reconstruction is very useful in terms of real-world functional recovery. One somewhat surprising finding is that the time of use and the magnitude of limb movement correlated with shoulder flexion and abduction, but not with other limb movements. I suspect that with a larger n, the importance of recovery of elbow flexion will also become evident statistically.

Eric L. Zager

Philadelphia, Pennsylvania