†These authors contributed equally.
Ankle-foot orthoses (AFOs) are widely prescribed for stroke rehabilitation. We
investigated the potential of transcranial magnetic stimulation (TMS) at an early
stage, after stroke, to predict the need of using AFOs in stroke patients. We
recruited 35 patients who could walk with intermittent support of one person or
independently 3 months after onset of stroke. The patients included in the study
were classified into two groups: a TMS (+) group (n
Stroke is a common disorder which can result in a functional deficit in humans [1, 2, 3]. Motor impairment after stroke is one of the most disabling sequelae, which can hinder patients’ independent living and decrease their quality of life [2, 4, 5]. Motor impairment, in the lower limb especially, disturbs gait function, and approximately 54% to 80% of patients are reported to have walking problems 3 months after the onset of stroke .
Impaired function of muscles around the ankle is a major cause of gait disturbance after stroke, resulting in instability of the ankle during stance phase and reduced clearance during swing phase [7, 8, 9]. An ankle-foot orthosis (AFO) can provide medial-lateral stability at the ankle during stance phase, and aid clearance during swing phase by keeping the foot in a neutral plantigrade position [2, 6, 10, 11, 12, 13, 14]. Therefore, AFOs are widely prescribed within stroke rehabilitation. It was reported that 39% of stroke inpatients needed an AFO at discharge from rehabilitation [10, 15, 16, 17, 18].
However, in clinical practice, the following scenario frequently occurs. In a patient with weakness of ankle dorsiflexors (Medical Research Council [MRC]: grade 1-2), one month after stroke, the clinician prescribes an AFO. However, the dorsiflexors may quickly improve to MRC 4. In this case, further application of an AFO may not be necessary. Accordingly, the prediction of the need of using an AFO would be useful in early stroke rehabilitation.
The corticospinal tract (CST) is one of the most important neural tracts for motor function in the human brain [19, 20, 21]. The CST mainly controls the distal musculature; thus, injury of the CST frequently results in weakness of ankle dorsiflexors [19, 22, 23]. Patients in whom the CST innervating the tibialis anterior (TA) muscle is disrupted, show poor outcome for the recovery of the ankle dorsiflexor and need to wear an AFO while walking, whereas patients who have a preserved CST to the TA muscle have a good recovery outcome and do not need to wear an AFO [22, 24]. The recovery of motor weakness in the TA is correlated with the need of using an AFO. Transcranial magnetic stimulation (TMS) is a useful tool for evaluating the state of the CST and predicting the motor outcome in stroke patients [20, 22, 25]. Therefore, by evaluating the status of the CST using TMS, clinicians can predict motor outcome and the need of using an AFO early on. This can allow for appropriate planning of the rehabilitation strategy for stroke patients, leading to a good therapeutic outcome.
In the current study, we evaluated the potential of TMS to reliably predict the need of using AFOs in stroke patients.
Thirty-five consecutive patients (24 males and 11 females; 58.1
Three months after the onset of stroke, we investigated whether patients were using the AFOs or not. We also checked the motor function of the affected lower extremity using the MRC scale, and the walking ability using the FAC. The FAC score consists of six categories as follows: 0, non-ambulatory; 1, a need for continuous support from one person; 2, a need for intermittent support from one person; 3, a requirement for verbal supervision only; 4, help required on stairs and uneven surfaces; and 5, able to walk independently anywhere. Its reliability and validity were well established.
A Magstim Novametrix 200 magnetic stimulator with a 9 cm diameter circular coil
(Novametrix, Woburn, MA, USA) was used for TMS. Cortical stimulation was
performed with the coil held tangentially over the vertex. A cloth marked with 1
cm spacing and Cz referenced to the intersection of the midsagittal and
interaural lines was placed on the scalp. Stimulation of the left hemisphere was
provided by a counterclockwise current and stimulation of the right hemisphere
was provided by a clockwise current. MEPs were obtained from the TA muscle in a
relaxed state. The motor threshold was defined as the minimum stimulus required
to elicit a MEP with a peak-to-peak amplitude of 50
Classification according to the results of transcranial magnetic stimulation (TMS) study of the corticospinal tract to tibialis anterior (TA). Axial T2-weighted magnetic resonance images (top panel) and the results of the TMS study (bottom panel) are presented. In the TMS (+) group, motor evoked potential (MEP) appeared in the affected TA; in the TMS (-) group, MEP was not evoked in the affected TA.
We used SPSS version 23.0 software (SPSS, Chicago, IL, USA) for statistical
analysis. The Fisher’s exact was used for evaluating intergroup differences in
use of the AFO, stroke type, and sex distribution. The Mann-Whiney test was used
to analyze the intergroup differences of age, time from stroke onset to the TMS
study, and motor function. Statistical significance was set at P
The number of patients in the TMS (+) group was 10, and that in the TMS (-)
group was 25. The type of stroke, age of the patient, time to TMS evaluation, and
MRC and FAC at admission to the Department of Physical Medicine and
Rehabilitation were not significantly different between the two groups
|TMS (+) group||TMS (-) group||P|
|Stroke type (infarct: hemorrhage), n||7 : 3||14 : 11||0.704|
|Sex (male: female), n||6 : 4||18 : 7||0.689|
|Time point from stroke onset to the TMS study, in days||13.0
|Motor function at admission to PM & R|
|MRC (hip flexor)||1.7
|MRC (knee extensor)||1.4
|MRC (ankle dorsiflexor)||0.5
|FAC, functional ambulation category; MRC, Medical Research Council; PM & R, department of physical medicine and rehabilitation; TMS, transcranial magnetic stimulation.|
|TMS (+) group||TMS (-) group||P|
|Use of AFO, n (%)||4 (40%)||21 (84%)||0.016|
|MRC (hip flexor)||3.1
|MRC (knee extensor)||3.2
|MRC (ankle dorsiflexor)||2.7
|AFO, ankle-foot orthosis; FAC, functional ambulation category; MRC, Medical
Research Council; TMS, transcranial magnetic stimulation; Bold values denote
statistical significance at the P |
In the current study, we evaluated whether a TMS study during the early stage of recovery from stroke can help predict the need of using AFOs.
The most characteristic abnormal walking pattern after stroke is impairment of ankle dorsiflexion or hyper-plantarflexion in the swing phase and the genu recurvatum due to hyperextension of the knee while in the stance phase . These abnormal gait patterns are explained by the loss of optimal muscle control, muscle strength, and a sense of balance [7, 16, 26]. The application of an AFO improves the gait-pattern and gait-stability of stroke patients by inhibiting hyper-plantarflexion in the swing phase and the genu recurvatum in the stance phase [6, 11, 17, 26, 27, 28]. An AFO is most frequently prescribed for orthosis in stroke patients [10, 15, 16, 17, 27], but sometimes motor recovery during recovery phase eliminates the need for AFOs [15, 29]. Because the preservation of CST is the most important factor that affects motor recovery [23, 24], we tried to assess the ability of a TMS study to predict the need of using AFOs. We evaluated for the presence of MEP in the CST of the affected TA because the functional state of the TA (ankle dorsiflexor) is a decisive factor for the application of AFOs. The presence of MEP indicates that the CST innervating the affected TA is preserved after stroke. In contrast, if MEP is not evoked from the affected TA, it indicates that the CST to the TA is interrupted.
In patients whose CST to the TA is preserved, 40% of them needed to apply an AFO during ambulation at 3 months after stroke onset. However, when CST was interrupted, 84% applied an AFO during ambulation. The ratio of using AFO at 3 months after the onset of stroke was significantly higher in patients with interrupted CST to the TA. The intergroup difference of these ratios seems to result from the recovery of motor weakness of the ankle dorsiflexor. The mean MRC score of the ankle dorsiflexor of patients with preserved CST was 2.7 at 3 months after the onset, whereas that of patients with interrupted CST was 1.3. An MRC score of 1.3 implies that patients cannot perform ankle dorsiflexion against gravity; these patients need an AFO during ambulation to prevent the toe dragging on the ground. In addition, an improvement of medial-lateral stability at the ankle by an AFO helps the patients to walk stably and gait pattern to be normalized.
Considering the results that 40% of patients with preserved CST used an AFO and 16% of patients with interrupted CST did not use an AFO at the 3-month follow-up, we believe that it would be difficult for clinicians to clearly decide to apply AFOs to patients with severe weakness of the ankle dorsiflexor based on the findings of MEP. However, when MEP on the affected TA is present at an early stage after the onset of stroke, clinicians can delay the decision of application of AFOs while observing the motor recovery even if the weakness of the ankle dorsiflexor is severe. In addition, when clinicians apply AFOs to the stroke patients, the patients would be able to provide detailed information about the possibility of throwing away the AFO at a later stage.
In addition, we observed that the motor function of hip flexor, knee extensor, and ankle dorsiflexor muscles was additionally improved when MEP to the affected TA was present. This result corresponded to the results of several previous studies. Chang et al.  assessed the presence of MEP to the affected TA in 14 stroke patients within 7-28 days of onset. The motor function of lower limb at 6 months after onset was better in patients with preserved MEP, compared to patients with interrupted MEP. Thus, TMS evaluation at an early stage is useful for predicting recovery of motor function of lower limb in stroke patients.
Regarding the prediction of necessity of using AFO, in 2001, Teasell et al.  investigated factors associated with AFO use in 423 stroke patients. They found that patients with lower upper and lower limb functions at admission were more likely to need an AFO at discharge.
Our study has some limitations. First, this study was conducted retrospectively. Second, the number of recruited patients was relatively small. Third, AFOs may affect the lower limb in various ways; however, this study has primarily considered AFOs role in compensation for ankle dorsiflexion weakness only. Further studies complementing these limitations should be conducted in the future.
We suggest that a TMS study is beneficial for deciding whether clinicians apply AFOs to stroke patients during the recovery phase or not, which could optimize outcomes and make the most efficient use of resources. In addition, this study adds to the literature on motor recovery which will inform clinical practice and future research in this area.
AFO, Ankle-foot orthosis; CST, corticospinal tract; FAC, functional ambulation category; MEP, motor-evoked potential; MRC, Medical Research Council; TA, tibialis anterior; TMS, transcranial magnetic stimulation.
Y.J.C., J.K. and M.C.C. conceived and designed the experiments; Y.J.C. and M.C.C. performed the experiments; Y.J.C. and M.C.C. analyzed the data; Y.J.C., J.K. and M.C.C. wrote the paper.
This research was retrospectively conducted without randomization or blinding, and approved by the institutional review board of Yeungnam University Hospital (YUMC 2019-10-046).
We thank two anonymous reviewers for excellent criticism of the article.
This study was supported by a National Research Foundation of Korea grand funded by the Korean government (grant no. NRF-2019M3E5D1A02068106).
The authors declare no conflict of interest.