Rehabilitation in primary lateral sclerosis mimicking parkinsonism: A case report

Abstract

BACKGROUND:

Primary lateral sclerosis (PLS) is an upper motor neurons disease that on rare occasions may determine bradykinesia and motor fatigue. To date, no rehabilitative treatment has been described as useful for these patients.

CASE PRESENTATION:

A 68-year-old male developed dysarthria, spastic laugh, impairments of handwriting and fine motor, gait and dysphagia disorders for both solids and liquids over the period from 2015 to December 2018, with normal DaT scans and no clinical benefits from therapy with levodopa, pramipexole and baclofen. The patient underwent exercises for gait training and balance control with sensory treadmill and stabilometric platform and kinesiotherapy to improve fine motor skills of both hands and postural changes, five days a week for two weeks. Based on our data, the patient showed an improvement in balance and gait parameters in T2 compared to T1.

CONCLUSION:

Thanks to the synergistic action of a combined treatment of physical and instrumental therapy, despite the rare pathology and complex disability, the patient had important benefits in terms of performance and independence in daily activity.

Keywords

Primary lateral sclerosis parkinsonism rehabilitation motor neuron disease

1 Introduction

Amyotrophic lateral sclerosis (ALS) is a progressive degenerative motoneuron disease involving motor cortex, corticospinal tract, brain stem, and spinal anterior horn neurons. It is a rare and unfamiliar neurodegenerative disease. Primary lateral sclerosis (PLS) is characterized by slowly progressive spinobulbar spasticity reflecting exclusive involvement of upper motor neurons (Kuipers-Upmeijer, 2001). On rare occasions, motor neuron disease (MND) may determine bradykinesia and motor fatigue, probably resulting from generalized spasticity. However, gait freezing and severe postural instability suggest an involvement of more widespread system and have not been well described (Mabuchi, 2004). Norlinah identified a subgroup of patients with PLS with evident slowness in movement and spasticity which can be easily confused with extrapyramidal rigidity. In these patients, absence of nigrostriatal involvement in DaT scan allowed to exclude diagnosis of atypical parkinsonism (Norlinah, 2007). Gordon et al. described presence of apparent extrapyramidal features in two cases of PLS with hypomimia, slow stride and “bradykinesia” without postural instability or response to levodopa (Gordon, 2006). In a longitudinal study, Le Forestier et al. found that five of 20 patients developed facial hypokinesia and amimia (Le Forestier, 2001). Mabuchi et al. described three cases of PLS with prominent parkinsonian-like features in form of gait freezing and postural instability in addition to “bradykinesia” (Mabuchi, 2004; Norlinah, 2007). Unfortunately, it is possible to administer only symptomatic remedy such as anti-spasticity medications (Baclofen and Dantrolene) for which most patients had transient responses (Pringle, 1992). Regarding characteristics similar to parkinsonism, as mentioned above, response to levodopa is poor and short-lived (Gordon, 2006). Moreover, no rehabilitative treatment has been described in literature as useful for these patients. This case reports the effectiveness of a combined treatment of kinesiotherapy and instrumental therapy and its impact on performance and independence on the activities of daily living (ADL).

2 Case presentation

Informed consent was obtained in writing from the patient before the start of the treatment. A 68-year-old male came to outpatient service in December 2018 referring neurological symptoms, such as dysarthria and spastic laugh. In 2015 the patient suffered a first episode of impairments of handwriting and fine motor skills of hands. In 2016, he underwent a DaT scan, reported as normal, and was given levodopa and pramipexole, without clinical benefits. An EMG examination of triceps surae bilaterally was performed to exclude any signs of peripheral motoneuron involvement. In the same year, the patient reported a progressive worsening of disease with difficulty in climbing stairs and feeling of weakness in legs. In 2017, after several episodes of falls, the neurologist suspended levodopa and pramipexole, excluded any form of parkinsonism and pyramidal tract disease and formulated diagnosis of PLS; also gave baclofen, with no clinical benefits. In January 2018, he developed gait and dysphagia disorders for solids and liquids. After being discharged from the Neurology Unit of our University Hospital, he was admitted to our ward to assess disability and plan an adequate rehabilitation program.

His clinical examination was difficult because of slow and disarticulated language and gait disorder such as small movements and episodic inability to generate effective steps, especially during beginning and at turning point. He showed good trunk control in static and dynamic conditions. Romberg’s test was negative with open and closed eyes. The pROM in all main joints of upper and lower limbs was normal. Ankle clonus was present with duration of 39 seconds at the right ankle and 35 seconds at the left one. The osteo-tendinous reflexes of superior and inferior limbs were increased and Hoffman and Babinsky signs were present on the left side. A plastic stiffness was bilaterally identified on wrist, without fatigue or decrease with repeated finger/foot percussion.

On the right side, both in upper and lower limbs, hypopallesthesia, tactile hypoesthesia and a decrease in sensation of pain were recognized. Fine motor skills were symmetrically reduced in upper limbs, mainly on the right side.

Before the start of the rehabilitation program, the patient underwent the following functional and instrumental evaluations: Box and Block Test, Nine Hole Peg Test, trunk control test, Berg Balance Scale, and gait analysis with inertial sensor.

The patient underwent exercises for gait training and balance control with sensory treadmill (Gait Trainer Treadmill Biodex^©; BTS Italy) and stabilometric platform (Balance System Biodex^©; BTS Italy), and passive and active kinesiotherapy to improve fine motor skills of hands and postural changes.

Exercises with treadmill were prescribed five days a week for two weeks. The protocol included: 10 minutes of warm-up, 30 minutes of exercise on treadmill and 10 minutes of cooling. Speed, length of gait cycle and length of step were lower at beginning of treatment and gradually increased reaching target levels. During this exercise, acoustic feedback was used (Schenkman, 2018). Auditory cueing is a rhythmic auditory stimulation that consistently increase speed and stride length in subject affected by Parkinson disease. These cues were administered with a metronome at 90 bpm and/or by rhythmic beats and music (Rutz, 2020).

Specific balance exercises were also proposed five days a week for two weeks to evaluate response to change in center of body mass and improve postural stability. The exercise protocol included: weight percentage, weight shift, postural stability and motor control. The training sessions were customized according to needs of patient, referring to scientific evidence and clinical experience. The sessions, lasting about 1,5 hour, were composed in sequence by: active stretching exercises, muscle strengthening, functional activity training and, again, active stretching exercises (da Silva Rocha Paz, 2019). To analyze gait cycle Kinovea was used. Kinovea is a free 2D motion analysis software with which to measure kinematic parameters. It can be used to analyze distances, angles, coordinates and spatial-temporal parameters, frame by frame, from a video recording in different perspectives, from 90 to 45 degrees (Puig-Divì, 2019). To observe trajectory and angles of knee and ankle on both sides, markers were positioned on lateral malleolus, condyle of the femur and on middle point between superior-anterior iliac spine and lateral condyle.

The patient followed this rehabilitation protocol for two weeks and functional and instrumental evaluations were performed at the end of treatment (T1) and after one month from the end (T2).

At the end of treatment, after 15 days, the patient showed an improvement in most of the analyzed parameters.

The highest values were observed in data on motor skills. At hospitalization, the patient needed 1 minute and 24 seconds to complete the Nine Hole Peg Test, compared to only 38 seconds at discharge.

The gait analysis with inertial sensor also showed an improvement in all skills between T0 and T2. In particular, a lengthening in stride and greater stability of gait cycle, as well as greater resistance demonstrated by the Timed Up and Go test, which the patient did not perform at T0, but performed at T2. Results are reported in Table 1 and Fig. 1 and 2.

Table 1
Berg Balance Scale, fall risk test at stabilometric platform, Box and Block Test, Nine Hole Peg Test, Timed Up and Go, and gait analysis with inertial sensor data at T0, T1 and T2

T0 T1 T2

Berg Balance Scale 31/56 30/56 28/56

Balance (fall risk test) 1.8 (DS 0.52) 1.8 (DS 0.51) 2.00 (DS 0.69)

Box and Block Test R 17, L 14 R 21, L 16 R 21, L 18

Nine Hole Peg Test 1 m24 s 1 m17 s 38 s

Gait cycle duration right 1.61±0.27 1.74±0.24 3.72±0.46

Gait cycle duration left 1.63±0.3 1.76±0.19 3.63±0.48

Stance phase duration right 0.97±0.1 0.94±0.12 2.13±0.51

Stance phase duration left 1.09±0.21 1.21±0.22 1.89±0.26

Swing phase duration right 0.64±0.23 0.8±0.2 1.59±0.3

Swing phase duration left 0.55±0.1 0.55±0.12 1.74±0.5

Single stance phase (%) right 33.4±3.2 31.6±6.8 46.1±7.9

Single stance phase (%) left 39.3±7.4 46.9±16.1 44.8±11.6

Average cadence 75.3±11.5 69.6±3.8 33.2±3.9

Gait quality index right 85.9±8.1 87.1±10.8 85±8.8

Gait quality index left 87.1±3.7 82.4±13.4 85.6±15.9

Timed Up and Go Not executable Not completed 15s (without aid)

	T0	T1	T2
Berg Balance Scale	31/56	30/56	28/56
Balance (fall risk test)	1.8 (DS 0.52)	1.8 (DS 0.51)	2.00 (DS 0.69)
Box and Block Test	R 17, L 14	R 21, L 16	R 21, L 18
Nine Hole Peg Test	1 m24 s	1 m17 s	38 s
Gait cycle duration right	1.61±0.27	1.74±0.24	3.72±0.46
Gait cycle duration left	1.63±0.3	1.76±0.19	3.63±0.48
Stance phase duration right	0.97±0.1	0.94±0.12	2.13±0.51
Stance phase duration left	1.09±0.21	1.21±0.22	1.89±0.26
Swing phase duration right	0.64±0.23	0.8±0.2	1.59±0.3
Swing phase duration left	0.55±0.1	0.55±0.12	1.74±0.5
Single stance phase (%) right	33.4±3.2	31.6±6.8	46.1±7.9
Single stance phase (%) left	39.3±7.4	46.9±16.1	44.8±11.6
Average cadence	75.3±11.5	69.6±3.8	33.2±3.9
Gait quality index right	85.9±8.1	87.1±10.8	85±8.8
Gait quality index left	87.1±3.7	82.4±13.4	85.6±15.9
Timed Up and Go	Not executable	Not completed	15s (without aid)

Fig. 1

Knee and ankle trajectory in T0 (A, upper picture) and T2 (B, lower picture).

Fig. 2

Angles of ankle in initial swing phase, midswing phase, initial contact phase, loading response phase at T0 (A, upper pictures) and T2 (B, lower pictures).

3 Discussion

PLS is characterized by slowly progressive spinobulbar spasticity that reflects exclusive involvement of the UMN but does not respond to pharmacological therapies normally administered for treatment of MND (Kuipers-Upmeijer, 2001). Also, as regards extrapyramidal-like signs described in some subjects with a diagnosis of PLS, patients seem to respond poorly to treatment with levodopa, as reported by Norlinah et al. (Norlinah, 2007). Furthermore, no rehabilitative treatment has been described in literature as useful for these subjects.

This case evaluates effectiveness of a combined treatment of kinesiotherapy and instrumental therapy on performance and independency on ADL in a patient affected by PLS. Basing on our data, the patient showed an improvement in balance and gait parameters in T2 compared to T1. Notably, there was a reduction of fall risk instrumentally assessed with stabilometric platform, a better manual dexterity analyzed by the Box and Block Test and Nine Hole Peg Test, and an increase in values referable to quality of gait, in terms of average speed and endurance examined with inertial sensor. Treadmill training improved spatiotemporal gait measures in people with Parkinson’s disease. In our patient, we were able to improve gait parameters using treadmill with acoustic feedback and acoustic cues during kinesiotherapy (Schenkman, 2018). In addition, combined treatment of kinesiotherapy and instrumental therapy have also allowed a reduction in brady/akinesia. This superficial brady/akinesia aspect in our patient was probably due to pyramidal slowdown because, conversely, in case of true extrapyramidal akinesia, fatigue or decrease on repeated finger/foot percussion has not been demonstrated. Thanks to gait analysis, it was possible to verify how gait pattern radically changed, in particular as regards to type of contact of foot with ground. At T0 the patient showed a reduction in ankle dorsiflexion and whole foot initial contact, with exhaustion of push and swing phase. This has been drastically modified to T2, with recovery of physiological roll of heel, ankle and forefoot, followed by an adequate and effective thrust.

Kinovea allowed to objectively analyze angles of knee and ankle and to identify an increase in flexion of these joints during gait, confirming what was observed with analysis of gait.

We concluded that, thanks to synergistic action of a combined treatment of kinesiotherapy and instrumental therapy, the patient, despite rare pathology and complex disability, had important benefits in terms of performance and independence in daily activity.

Conflict of interest

The authors declare that they have no conflicts of interest and nothing to disclose.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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