Berlin Bimanual Test for Tetraplegia (BeBiTT)
The BeBiTT consists of 9 test items, all representing relevant bimanual tasks of daily living that are impaired in individuals with tetraplegia (Table 1). The BeBiTT test items cover all grasp patterns relevant to everyday life (tripod pinch, tip pinch, lateral pinch, power grip, spherical grip, and extension grip) and address multiple ADL categories such as eating and drinking, dressing, and personal hygiene (Table 1). The BeBiTT test items include various types of bimanual actions according to the taxonomy of Kantak et al. (2017), i.e., symmetric and asymmetric bimanual movements with common and independent task goals (Table 1). While originally designed for stroke populations, we reasoned that considering Kantak´s taxonomy in the BeBiTT would be important to include a broad range of bimanual actions with varying requirements for coordination. The required material for the BeBiTT is commonly available in clinics and research laboratories and can purchased anywhere in the world (Table 1). Being based on a comprehensive theoretical framework (Fig. 1) and due to its fast and easy administration (< 20 minutes), the BeBiTT can be carried out in both research and clinical routine.
Table 1
Berlin Bimanual Test for Tetraplegia
Bimanual items | Material | Grasp pattern | Bimanual action | ADL category |
Charge a smart phone | Common smart phone (e.g., iPhone 6, Samsung Galaxy S20) Corresponding charging cable | Extension grip (smart phone) Tip pinch (charging cable) | Symmetric, independent goal, bimanual action | Communication |
Open a water bottle | 1-liter plastic bottle of water (filled), screwed on by hand | Power grip (bottle) Tip pinch (lid) | Asymmetric, common goal, bimanual action | Eating and Drinking |
Pour glass of water | 1-liter plastic bottle of water (filled) Water glass (200ml, empty) | Power grip (bottle) Power grip (glass) | Symmetric, common goal, bimanual action | Eating and Drinking |
Rinse a plate | Dinner plate (approx. 25 cm in diameter) Kitchen sponge | Extension grip (plate) Spherical grip (sponge) | Asymmetric, common goal, bimanual action | Housekeeping |
Cut meat-like putty | Medium resistance putty resembling the consistency of a piece of meat Knife and fork | Lateral pinch (both hands) | Asymmetric, common goal, cooperative bimanual action | Eating and Drinking |
Open toothpaste | Normal 75ml toothpaste with screwed lid, > 50% full | Lateral pinch (toothpaste) Tip pinch (lid) | Asymmetric, common goal, bimanual action | Body Hygiene |
Apply toothpaste on toothbrush | Normal 75ml toothpaste with screw lid, > 50% full Toothbrush | Lateral pinch (both hands) | Asymmetric, common goal, bimanual action | Body Hygiene |
Take note out of wallet | Common leader wallet 10 Euro or 20 US Dollar note | Lateral pinch (bank note) Extension grip (wallet) | Asymmetric, common goal, bimanual action | Managing Finance |
Close zipper of a jacket | Metal zipper in a jacket | Tip pinch (both hands) | Asymmetric, independent goal, bimanual action | Dressing |
To reliably assess the BeBiTT score, raters are provided with a systematic scoring system (Appendix 1). The scoring system is designed to evaluate the main components of bimanual function in daily activities, i.e., grasping, manipulating, and lifting. For grasping, the scoring system pays special attention whether an active or passive grip is used to accomplish the task. Passive grip refers to the concept of grasping objects with the help of passive tension in the fingers, e.g., by extending the wrist in the so-called tenodesis grasp. While a passive grip is often not very dexterous and powerful (Smaby et al., 2004), exerting active finger strength contributes to good control and ability to manipulate an object. Accordingly, 2 points are assigned in case an active/firm grip is performed and 1 point is assigned if a passive/loose grip is performed (evaluated for each hand). Moreover, the scoring systems accounts for the level of difficulty the participant experiences during bimanual manipulation and considers the use of compensatory mechanisms. Compensatory mechanisms refer to the use of body parts or functions that are usually not involved in a particular action to compensate for impaired function (e.g., using both hands for a one-handed activity or pinching objects between legs for manipulation). No difficulty in manipulating results in 4 points, slight difficulty in 3 points, great difficulty in 2 points, and 1 point is assigned when solely compensatory strategies are used. Lifting is a good way to evaluate bilateral arm and shoulder function and 2 points are assigned if the bimanual manipulation is performed in a lifted position. Altogether, a maximum of 10 points can be achieved per task (4 for grasping, 4 for manipulating and 2 for lifting or, in case a task does not involve any meaningful lifting component, 4 for grasping and 6 for manipulating). With 9 test items, this results in a score ranging from 0 to 90 points, with 0 points indicating no bimanual function and 90 points indicating unimpaired bimanual function in tetraplegia.
Participants
14 individuals with tetraplegia were recruited (13 male, mean age 48.6 ± 18.5 years) with complete (n = 6; ASIA grade A) and incomplete (n = 8; ASIA grades B – C) cSCI (C4 to C6). Recruitment took place at the University Hospital of Tübingen, the Charité – Universitätsmedizin Berlin, and the Neurological Rehabilitation Clinic Beelitz-Heilstätten (Germany). Participants were selected based on the following inclusion criteria: Age between 18 and 85 years, interval after SCI at least six months, lesion height C4 – C6, ASIA grade A – C. Exclusion criteria were the following: Consumption of illegal drugs or more than two alcoholic beverages per day, history of severe neurological injuries or conditions other than SCI (e.g., multiple sclerosis, stroke and cerebral palsy), severe medical conditions (e.g., renal/liver/heart failure; malignant tumor disease), serious cognitive impairment and severe spasticity.
All 14 participants took part in the baseline test of the BeBiTT (without intervention). For further validation using an exoskeleton, ten participants (all male, mean age 44.7 ± 14.6 years) with complete (n = 5; ASIA grade A) and incomplete (n = 5; ASIA grades B to D) cSCI (C5 to C6) repeated the BeBiTT using a B/NHE (intervention). All participants were BCI naïve, i.e., they had never taken part in any BCI training or application. Four participants had to be excluded from the intervention due to incapability to wear the hand exoskeleton, arthritic pain, impending hand surgery and skepticism about brain-controlled technology.
Study procedure
The study protocol complied with the Declaration of Helsinki. Ethical approval was obtained from the Ethical Committee of the Medical Faculty of the University of Tübingen (201/2018BO1). After providing written informed consent, participants were comfortably seated in front of a desk for the BeBiTT baseline assessment. The BeBiTT tasks were explained, and their proper execution was demonstrated by the instructor. The participant was encouraged to perform the tasks as close to the instructor’s demonstration as possible. The participant was reminded of the importance to use both hands and to avoid compensatory strategies if possible. There was no time limit to perform the tasks. The participant could also repeat each task to reach a higher score. After completing the BeBiTT without assistance (baseline), the B/NHE was attached to the participants’ hand and fingers. Then, the BeBiTT was repeated in the exact same manner as in the baseline condition (intervention). The whole session was videotaped, and videos stored for later review. At the end of the session, all participants were interviewed on the self-care category of Spinal Cord Independence Measure III (SCIM III) and Quadriplegia Index of Function (QIF) and completed a questionnaire assessing safety and feasibility of the BeBiTT.
Hybrid brain/neural hand exoskeleton (B/NHE)
For the intervention, a wearable hand exoskeleton with nine motor units (HandyRehab from Zunosaki Ltd., Hong Kong) was donned to the participant´s left or right hand, depending on the participant’s choice. Control of the exoskeleton was established by a hybrid BCI, translating EEG and EOG signals into open and close commands. Sensorimotor rhythm event-related desynchronization (SMR-ERD) associated with intended grasping motions was detected by EEG and translated into exoskeleton closing motions. Horizontal oculoversions (HOV) detected by EOG were used to control exoskeleton opening motions or to stop unintended closing (Soekadar, Witkowski, et al., 2015). EEG was recorded with a Smarting Mobi system (mBrainTrain, Serbia) and a semi-dry saline-based cap (Greentek Pty. Ltd, Wuhan, China) from 5 conventional recording sites according to the international 10/20 system (C3, Cz, F3, P3, T3 for right hand exoskeleton control, or C4, Cz, F4, P4, T4 for left exoskeleton control). A surface Laplacian filter was applied to reduce signal-to-noise ratio of the target electrodes C3 or C4. Signals were recorded at a sampling frequency of 250 Hz and filtered between 0.1 Hz and 70 Hz with a Butterworth filter. For EOG, two additional electrodes were placed on the right and left outer canthus. The signal amplitude was converted into a bipolar signal and low pass filtered at 1.5 Hz. EEG and EOG signals were processed and classified by a customized version of the BCI2000 software platform (www.bci2000.org) (Schalk et al., 2004).
Internal consistency, interrater-reliability, construct validity, and sensitivity to change
For assessing internal consistency of the BeBiTT´s test items, Cronbach’s alpha and corrected item-total correlation was calculated using SPSS (v.27) for baseline scores. As suggested by Kline (2015), corrected item-total correlation was set below 0.30 for items to be discarded. For assessing interrater reliability, the scorings of the study instructor and three independent raters were obtained. The independent raters were blinded to the participants’ diagnosis and ASIA classification. Raters were given the scoring sheet (Appendix 1) along with a short explanation of the scoring system. They were asked to fill out the scoring sheets for each participant individually and not to discuss the video clips or the assigned scores with each other. Agreement in scores between raters was tested by calculating the intraclass correlation coefficient (ICC) using SPSS (v.27) for both the baseline and intervention. The ICC was calculated based on an absolute-agreement, 2-way mixed-effects model.
To assess construct validity of the BeBiTT, two common ADL tests were assessed by interview: the self-care category of the Spinal Cord Independence Measure III (SCIM III) and the Quadriplegia Index of Function-Short Form (QIF-SF) (Catz et al., 1997; Marino & Goin, 1999). While the self-care category of SCIM III and QIF-SF do not assess hand function exclusively, they include many tasks that require bimanual function and are thus suitable to assess construct validity of the BeBiTT baseline scores. (Rudhe & van Hedel, 2009). The construct validity of the BeBiTT was assessed by computing Pearson’s correlation coefficient between BeBiTT baseline scores and the SCIM III self-care category as well as the QIF-SF.
To assess sensitivity to change between baseline and intervention, a non-parametric bootstrapped paired t-test with 1000 permutations was applied using SPSS. Effect size (Cohen´s D) was calculated. Furthermore, BeBiTT subscores (grasping, lifting, manipulating components) were tested for significance using a bootstrapped paired t-test with 1000 permutations.