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Trans-spinal magnetic stimulation combined with kinesiotherapy as a new method for enhancing functional recovery in patients with spinal cord injury due to neuromyelitis optica: a case report

Journal of Medical Case Reports volume 18, Article number: 386 (2024) Cite this article

Abstract

Background

Experimental studies have shown that repetitive trans-spinal magnetic stimulation (TsMS) decreases demyelination and enables recovery after spinal cord injury (SCI). However, the usefulness of TsMS in humans with SCI remains unclear. Therefore, the main objective of this study is to evaluate the effects of TsMS combined with kinesiotherapy on SCI symptoms. We describe a protocol treatment with TsMS and kinesiotherapy in a patient with SCI due to neuromyelitis optica (NMO)-associated transverse myelitis.

Case presentation

A 23-year-old white male with NMO spectrum disorders started symptoms in 2014 and included lumbar pain evolving into a mild loss of strength and sensitivity in both lower limbs. Five months later, the symptoms improved spontaneously, and there were no sensorimotor deficits. Two years later, in 2016, the symptoms recurred with a total loss of strength and sensitivity in both lower limbs. Initially, physiotherapy was provided in 15 sessions with goals of motor-sensory recovery and improving balance and functional mobility. Subsequently, TsMS (10 Hz, 600 pulses, 20-seconds inter-trains interval, at 90% of resting motor threshold of the paravertebral muscle) was applied at the 10th thoracic vertebral spinous process before physiotherapy in 12 sessions. Outcomes were assessed at three time points: prior to physiotherapy alone (T-1), before the first session of TsMS combined with kinesiotherapy (T0), and after 12 sessions of TsMS combined with kinesiotherapy (T1). The patient showed a 25% improvement in walking independence, a 125% improvement in balance, and an 18.8% improvement in functional mobility. The Patient Global Impression of Change Scale assessed the patient’s global impression of change as ‘much improved’.

Conclusion

TsMS combined with kinesiotherapy may safely and effectively improve balance, walking independence, and functional mobility of patients with SCI due to NMO-associated transverse myelitis.

Peer Review reports

Introduction

Neuromyelitis optica (NMO) is an autoimmune astrocytopathic disease of the central nervous system with a predilection for the spinal cord and optic nerves and may cause transverse myelitis and optic neuritis, respectively, if these regions are affected [47, 49]. The symptoms associated with transverse myelitis are similar to those of spinal cord injury (SCI), including sensorimotor symptoms, pain, cardiovascular symptoms, and symptoms of bladder, bowel, and sexual dysfunction [22].

Regarding recovery from NMO-associated transverse myelitis, physiotherapy does not seem to result in the deterioration of symptoms in most patients [38]; however, few cases with poor functional recovery have been reported [43, 45]. Despite the proposal of a variety of treatment approaches, such as surgery, physiotherapy, and cell-based therapy, either individually or in combination, their limited efficacy in fully restoring functionality for many patients underscores the need for exploring innovative interventions [12, 15]. Non-invasive brain stimulation (NIBS) is a promising tool for altering cortical and spinal excitability safely and painlessly [42]. Experimental studies in mice with SCI have shown a reduction in demyelination and axonal and walking recovery after trans-spinal magnetic stimulation (TsMS) [8, 31].

These studies provide evidence that TsMS induces therapeutic effects in an experimental animal model and suggest a possible translation of the results to clinical application in humans [8]. The usefulness of TsMS in human patients with SCI has not been documented. In this case report, we describe the usefulness and safety of repetitive TsMS combined with physiotherapy provided to improve mobility of a patient with chronic incomplete SCI due to NMO-associated transverse myelitis.

Case description

Publication of this case report was approved by the local ethics committee (4.755.012), and all study procedures were conducted following the principles stated in the Declaration of Helsinki. The patient underwent physiotherapy at the Applied Neuroscience Laboratory (LANA) at Universidade Federal de Pernambuco (Recife, Pernambuco, Brazil).

The patient was a 23-year-old white male diagnosed with NMO spectrum disorders, presenting no relevant family history. The symptoms started in 2014, when the patient was 18 years old, initially manifesting as lumbar pain evolving into a mild loss of strength and sensitivity in both lower limbs. Five months later, the symptoms improved spontaneously, and there were no sensorimotor deficits. However, 2 years later, in 2016, the symptoms recurred with a total loss of strength and sensitivity in both lower limbs. During this period, the patient did not exhibit any visual symptoms. Over the past 3 years, the patient underwent physiotherapy twice a week, each lasting 35 min, but reported only minimal improvement in their functional sensory-motor symptoms. Consequently, the patient contacted our research group seeking further treatment options.

According to the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI) by the American Spinal Injuries Association (ASIA) [24], the patient had ASIA Impairment Scale (AIS) grade D (motor function is preserved below the neurological level, and at least half of the key muscles below the neurological level have a muscle grade of 3 or more) with sensory level at T5 and motor level at L2 in both right and left sides, and the neurological level was at T5. The patient was independent in activities of daily living such as self-care, dressing, feeding, and movement. Based on the Walking Index for Spinal Cord Injury II (WISCI II) scale [14], the patient ambulated with two crutches both indoor and outdoor, with no braces and physical assistance.

Initially, we opted for an exclusive kinesiotherapy-based treatment for the patient, conducting 15 sessions. Unfortunately, this strategy failed to produce any noticeable gains in motor function. Given the insights from emerging studies, such as those by Ainhoa Insausti-Delgado et al. [21], which highlighted TsMS capacity to promote neuroplasticity in the motor cortex, we decided to integrate TsMS into our kinesiotherapy protocol [21]. After checking the safety criteria for transcranial magnetic stimulation [42] and obtaining written informed consent for participation in the research, the patient underwent 12 sessions of trans-spinal magnetic stimulation (TsMS) in conjunction with kinesiotherapy, tailored to the patient’s specific functional requirements.

Interventions

The initial plan of rehabilitation

The patient underwent 15 sessions of physiotherapy; each session lasted for approximately 2 hours, and the therapy was provided two times a week. Each treatment session had the following goals: (i) to regain muscle strength in lower limbs, (ii) to achieve sensory recovery, (iii) to achieve balance, and (iv) to achieve functional mobility. All proposed exercises were performed considering principles of motor learning theory and principles of neuroplasticity [25]. The physiotherapy protocol is shown in Table 1.

Table 1 Protocol of physical therapy during the initial plan of rehabilitation and with trans-spinal magnetic stimulation
Full size table

Trans-spinal magnetic stimulation protocol

The patient was asked to lie prone on a stretcher during the TsMS session. The resting motor threshold (rMT) of the paraspinal muscle at the 10th thoracic vertebral level was assessed (Fig. 1). rMT was defined as the lowest intensity of TsMS output that was able to produce visible muscular contraction in the target muscle in more than 5 of 10 trials. TsMS was performed using a figure-of-eight coil attached to a MagStim Super Rapid magnetic stimulator (MagStim Company, Whitland, UK) and placed over the spinous process of the 10th thoracic vertebra. A 10-Hz stimulus was delivered with 600 pulses (60 pulses, 10 trains) and 20-seconds inter-trains intervals at 90% rMT.

Fig. 1
figure 1

Positioning of the figure-of-eight coil for assessing the resting motor threshold of the paraspinal muscle at the level of the 10th thoracic vertebra

Full size image

Physiotherapy was conducted immediately after TsMS in another 12 sessions (10 sessions were held daily for five times a week [induction phase], and two sessions were performed with a 48-hours interval between them [maintenance phase]). The protocol and main goals of the physiotherapy were the same as those of the initial plan of rehabilitation.

Outcomes

Except for the ISNCSCI grading, all evaluations were performed at the baseline (T-1), before starting TsMS (T0), and immediately after the completion of the 12th TsMS session (T1). The outcome measures were chosen based on the body structure, body function, and activity domains of the International Classification of Functioning, Disability, and Health (ICF) framework.

The activity was assessed using the WISCI II scale for walking independence. The WISCI II scale assesses the extent of physical assistance and devices required for walking following paralysis that results from SCI. There are 20 levels of assessment; higher levels indicate more independent mobility [13], and a change of one WISCI level can be considered a substantial difference in the clinical context (minimal detectable change [MDC]) [6]. At baseline, the patient had a WISCI II score of 16 (ambulation with two crutches with no braces and physical assistance), and the score remained the same during the initial rehabilitation period. The WISCI II score changed only after initiating TsMS treatment, reaching the maximum level (20; ambulation with no device, braces, and physical assistance). The patient achieved four times the MDC in the WISCI II scale assessment (Fig. 2, Table 2).

Fig. 2
figure 2

Graphical representation of quantitative assessment before and after 12 sessions of repetitive trans-spinal magnetic stimulation combined with physical therapy. Mini-BEST: short version of the Balance Evaluation Systems test; WISCI II: Walking Index for Spinal Cord Injury scale; TUG: timed get up and go test, before TsMS represent the “T0: before starting TsMS”, after TsMS represent the “T1: after TsMS”; % Change: [(value after TsMS − value before TsMS)/value before TsMS] × 100; TsMS: trans-spinal magnetic stimulation

Full size image
Table 2 Quantitative assessment before and after 12 sessions of repetitive trans-spinal spinal magnetic stimulation combined with physical therapy
Full size table

In addition, the activity was assessed using the timed get up and go (TUG) test [41] for functional mobility. The TUG test requires the patient to get up from a chair, walk a distance of 3 m, turn around, and return to the chair. During this activity, the time is measured, and a shorter time indicates better functional mobility [41]. The MDC is 10.8 s or a reduction of 30% [29]. The time required by the patient to perform the TUG test was reduced by 18% after TsMS. Although the MDC was not attained, a substantial reduction was possible after TsMS (Fig. 2, Table 2).

Body function was assessed using the short version of the Balance Evaluation Systems Test (Mini-BEST) [20]. The Mini-BEST is a 14-item test scored on a 3-level ordinal scale, where higher scores indicate better balance, and aims to target and identify six different balance control systems [17, 20]. Therefore, it assesses the activity as well as ICF domains. There is no MDC suggested for SCI, however, the score for Parkinson’s disease is 5.52 points [30] and for vestibular disorders is 3.5 points [18]. Even though the MDC for SCI was not available, we observed that the patient achieved a score comparable with those for the other patient populations (10 points) (Fig. 2, Table 2). This improvement was scored based on anticipatory adjustment (2 to 5 points), reactive postural control (1 to 5 points), sensory orientation (2 to 3 points), and dynamic gait (3 to 5 points).

Finally, the Patient Global Impression of Change Scale (PGICS) that assesses a patient’s belief about the efficacy of treatment was used at the end of the TsMS sessions [16]. The patient reported “an improvement that has made a real and worthwhile difference” (level 6). The presence of adverse effects was also assessed after the end of each TsMS session. No adverse effects were reported. Thus, TsMS may be considered a safe and non-invasive tool.

Discussion

The present case demonstrated that improvement in balance, walking independence, and functional mobility occurred after adding TsMS protocol in a physiotherapy program for a patient with SCI. The use of repetitive transcranial magnetic stimulation (rTMS) of the motor cortex to improve functional recovery in patients with chronic incomplete SCI is well-established [2, 7, 28, 34, 39]. However, to the best of our knowledge, this is the first case report on the trans-spinal application of magnetic field for improving functional recovery in a patient with SCI.

We hypothesized that TsMS could augment the effects of physiotherapy by causing changes in spinal reflexes, especially a decrease in the amplitude of H-reflex [26, 27, 36]. H-reflex is a control measure of spinal motoneuronal excitability. An increase in the amplitude of H-reflex reflects a clinical sign of spasticity [11, 33]. There is high variability in the observed effects of rTMS on H-reflex (a decrease, increase, or no change in the amplitude of H-reflex) [40], depending on the intensity, frequency, and duration of the stimuli used [46, 48] as well as the time since SCI [3]. Consequently, we preferred to use TsMS in the present case.

Only a few studies have assessed the modulatory effects of TsMS on spinal cord functions. Nielsen et al. [35] performed the first investigation using TsMS for modifying spasticity in patients with multiple sclerosis. Later, clinical trials were performed to confirm the modulatory effects of TsMS on multiple sclerosis [36, 37], SCI, and healthy subjects [26]. However, these studies only evaluated bodily functions and structures (spasticity) and electrophysiological assessment (stretch reflex), whereas our study evaluated functional and activity recovery and the priming effect of TsMS, since motor recovery improved after the addition of TsMS to the physiotherapy program.

rTMS can augment motor training and enhance the sensitivity of the brain to physiotherapy by increasing cortical excitability [5, 44]. Although no study has proved the relationship between spinal and cortical excitability after TsMS, studies on trans-spinal direct current stimulation (tsDCS) have suggested this relationship [1, 4]. Consequently, we assumed that TsMS also might be a tool for priming the brain to learn. The patient had a history of non-improvement in motor functions with physiotherapy, which could be noted in T-1 and T0 assessments. TsMS could improve balance, allowing the patient to progress from walking with two crutches to walking with no device, braces, and physical assistance. This improvement was reported as “an improvement that has made a real and worthwhile difference” in the PGICS assessment.

From a clinical perspective, we hypothesize that functional recovery could be achieved through improvement in balance. Maintenance of balance is a complex task that requires coordination among somatosensory/proprioceptive, visual, and vestibular systems [19]. It is necessary to activate the muscular fuse through stretch reflex that is directly related to the spinal interneurons for activating the somatosensory system [32]. Previous studies with tsDCS had shown that excitatory stimulation of the spinal cord could modulate polysynaptic and multisegmental spinal reflexes in the case of a nociceptive stimulus [1, 9, 10]. As high-frequency TsMS is also an excitatory stimulation, it may have positively influenced these reflexes and supported the balance recovery in the patient.

Additionally, the patient had improvement in walking independence and functional mobility assessed using the WISCI II scale and TUG test, respectively. In a similar situation such as traumatic SCI, rTMS of the motor cortex area [2] combined with locomotor training [28] was not able to improve walking independence. These researchers chose the technique of transcranial application because of its ability to modify corticospinal projections and change cortical and spinal excitability [2]. However, studies on rTMS for modifying H-reflex have reported uncertain results [40]. H-reflex depends on the intensity, frequency, and duration of rTMS [46, 48] and the time since SCI [3]. Therefore, we chose trans-spinal instead of transcranial application in the present case.

An experimental study with TsMS had shown a decrease in demyelination, an increase in axonal plasticity, and locomotor recovery after SCI in a rodent model [8]. Additionally, there may be a relevant center called Central Pattern Generator (CPG) in the thoracolumbar region that regulates locomotor behavior [23]. During walking, descending commands from neurons of the midbrain and brain stem provide feedback to the CPG, which then generates the walking rhythm and coordinates muscle activation [23]. Thus, in the present case, TsMS applied in combination with a rhythmic locomotor training program, such as a treadmill training program, might have activated the CPG, which, in turn, might have played a very important role in achieving the results of the treatment.

It’s important to highlight the relapsing–remitting nature of NMO, characterized by phases of acute exacerbations followed by spontaneous remissions. Given this cycling pattern of NMO, we must approach the observed therapeutic benefits of combining TsMS with kinesiotherapy with caution. The improvements seen in patient outcomes could coincide with natural fluctuation of the disease, making it challenging to attribute changes directly to the treatment. Therefore, further studies are necessary to explore the efficacy of these interventions, considering the cyclic dynamics of NMO. However, this case report contributes to the body of knowledge on TsMS and also opens avenues for future investigations into its application in neurorehabilitation.

Conclusion

TsMS in combination with kinesiotherapy could improve the balance and walking independence of a patient with NMO-associated transverse myelitis. The patient showed an improvement of 10 points in balance, assessed using Mini-BEST, and an increase of four levels in the WISCI-II scale for walking independence. This recovery implies an MDC and a patient global impression of “much improved.” Therefore, the present case suggests that TsMS is a safe and promising tool for enabling functional recovery in patients with SCI due to NMO-associated transverse myelitis. However, randomized, sham-controlled clinical trials are required to confirm the results of this study and strengthen the evidence regarding the usefulness of TsMS for motor recovery in patients with SCI.

Availability of data and materials

Not applicable.

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Acknowledgements

We would like to thank Editage (www.editage.com) for English language editing.

Funding

Katia Monte-Silva is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq, Brazil (Grant 311224/2019-9). Rodrigo Brito was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Finance Code 001). English language editing was funded by PROPG/UFPE n.02/2021.

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Authors and Affiliations

  1. Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, Jornalista Aníbal Fernandes Avenue, Recife, PE, 50740-560, Brazil

    Rodrigo Brito, Bárbara Marroquim, Lívia Shirahige, Adriana Baltar, Sérgio Rocha, Alexia Perruci & Katia Monte-Silva

  2. NAPeN Network (Núcleo de Assistência e Pesquisa em Neuromodulação), Recife, Brazil

    Rodrigo Brito, Lívia Shirahige, Adriana Baltar & Katia Monte-Silva

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Contributions

RB, LS, AB, SR and KMS were responsible for planning the treatment; RB, BM, LS and SR conducted the physiotherapy; BM was responsible for data assessment; RB and AP participated in design and organization of the data in this manuscript; RB and KMS analyzed and interpreted the patient data and were a major contributor in writing and the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Katia Monte-Silva.

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Ethics approval and consent to participate

Approved by the local ethics committee (Universidade Federal de Pernambuco—Brazil: 4.755.012). Informed written consent to participate was obtained from the patient.

Consent for publication

Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Competing interests

The authors report there are no competing interests to declare.

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Brito, R., Marroquim, B., Shirahige, L. et al. Trans-spinal magnetic stimulation combined with kinesiotherapy as a new method for enhancing functional recovery in patients with spinal cord injury due to neuromyelitis optica: a case report. J Med Case Reports 18, 386 (2024). https://doi.org/10.1186/s13256-024-04636-7

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Keywords

Journal of Medical Case Reports

ISSN: 1752-1947