Monitoring Upper Limb Recovery after Cervical Spinal Cord Injury: Insights beyond Assessment Scores

Michael Brogioli, Sophie Schneider, Werner L Popp, Urs Albisser, Anne K Brust, Inge-Marie Velstra, Roger Gassert, Armin Curt, Michelle L Starkey, Michael Brogioli, Sophie Schneider, Werner L Popp, Urs Albisser, Anne K Brust, Inge-Marie Velstra, Roger Gassert, Armin Curt, Michelle L Starkey

Abstract

Background: Preclinical investigations in animal models demonstrate that enhanced upper limb (UL) activity during rehabilitation promotes motor recovery following spinal cord injury (SCI). Despite this, following SCI in humans, no commonly applied training protocols exist, and therefore, activity-based rehabilitative therapies (ABRT) vary in frequency, duration, and intensity. Quantification of UL recovery is limited to subjective questionnaires or scattered measures of muscle function and movement tasks.

Objective: To objectively measure changes in UL activity during acute SCI rehabilitation and to assess the value of wearable sensors as novel measurement tools that are complimentary to standard clinical assessments tools.

Methods: The overall amount of UL activity and kinematics of wheeling were measured longitudinally with wearable sensors in 12 thoracic and 19 cervical acute SCI patients (complete and incomplete). The measurements were performed for up to seven consecutive days, and simultaneously, SCI-specific assessments were made during rehabilitation sessions 1, 3, and 6 months after injury. Changes in UL activity and function over time were analyzed using linear mixed models.

Results: During acute rehabilitation, the overall amount of UL activity and the active distance wheeled significantly increased in tetraplegic patients, but remained constant in paraplegic patients. The same tendency was shown in clinical scores with the exception of those for independence, which showed improvements at the beginning of the rehabilitation period, even in paraplegic subjects. In the later stages of acute rehabilitation, the quantity of UL activity in tetraplegic individuals matched that of their paraplegic counterparts, despite their greater motor impairments. Both subject groups showed higher UL activity during therapy time compared to the time outside of therapy time.

Conclusion: Tracking day-to-day UL activity is necessary to gain insights into the real impact of a patient's impairments on their UL movements during therapy and during their leisure time. In the future, this novel methodology may be used to reliably control and adjust ABRT and to evaluate the progress of UL rehabilitation in clinical trials.

Keywords: long-term monitoring; rehabilitation; spinal cord injury; upper limb; wearable sensors.

Figures

Figure 1
Figure 1
Flow diagram depicting the study groups and the measurement performed in each time frame. Stage A1: 1 month after injury; Stage A2: 3 months after injury; Stage A3: 6 months after injury; GRASSP, Graded and Redefined Assessment of Strength, Sensibility and Prehension; SCIM, Spinal Cord Independence Measure; HHD, hand-held dynamometer; N, sample size; MMT, Manual Muscle Testing; ISNCSCI, International Standards for Neurological Classification of Spinal Cord Injury.
Figure 2
Figure 2
Changes in sensor-based and clinical measures over time among a group of paraplegic and tetraplegic patients. Lines represent the means; error bars represent the 95% confidence interval. Paraplegic patients are displayed with empty squares, whereas tetraplegic patients are displayed with full circles. (A,B) illustrate the changes in clinical scores during rehabilitation, (C–F) changes in sensor-based metrics. Proximal muscle strength was assessed with the manual muscle testing (MMT); independence in self-care was assessed with the Spinal Cord Independence Measure (SCIM). Stage A1 – 1 month after injury; Stage A2 – 3 months after injury; and Stage A3 – 6 months after injury.
Figure 3
Figure 3
Cross-sectional relationship between proximal muscle function and overall upper limb activity across time. Paraplegic patients are displayed with empty squares, whereas tetraplegic patients are displayed with full circles. The relationship at 1 month (A) and 3 months (B) after injury was strong and significant (N = 29 and N = 31, p < 0.01, r = 0.562 and r = 0.605, Spearman correlation, respectively), whereas it was not significant at 6 months (C) after injury (N = 27, p = 0.178, r = 0.273, Spearman correlation). MMT, manual muscle testing.
Figure 4
Figure 4
Comparison of activity count (AC) categories between paraplegic and tetraplegic patients 6 months after injury. Bars represent the means; error bars represent the 95% confidence interval. Paraplegic patients are displayed in white, whereas tetraplegic patients are displayed in black. Differences are not statistically significant. ADL, activities of daily living.
Figure 5
Figure 5
Comparison of strength values between paraplegic and tetraplegic patients 6 months after injury. (A) The boxplot shows the median of each strength measurement. The bottom represents the first quartile, whereas the top represents the third quartile. The whisker is 1.5 times the interquartile range. Outliers are displayed with points. Significant differences are represented with stars (one star represents alpha ≤ 0.05; two stars represent alpha = 0.01). (B) Relationship between AC during active wheeling and HHD scores of shoulder extension. Paraplegic patients are displayed in white or with empty squares, whereas tetraplegic patients are displayed in black or full circles. HHD, hand-held dynamometer.
Figure 6
Figure 6
Center differences in overall activity counts and in scores of proximal muscle strength at 6 months after injury for all patients. (A) The bars represent the means of overall activity counts; error bars represent the 95% confidence interval. Significant differences are represented with stars (two stars equal alpha = 0.01). (B) The boxplot shows the median of each strength measurement. The bottom represents the first quartile, whereas the top represents the third quartile. The whisker is 1.5 times the interquartile range. Outliers are displayed with points. MMT, manual muscle testing.

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