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. 2022 Apr 14:13:849820.
doi: 10.3389/fneur.2022.849820. eCollection 2022.

Non-Invasive Neuromodulation in the Rehabilitation of Pisa Syndrome in Parkinson's Disease: A Randomized Controlled Trial

Roberto De Icco  1   2 , Alessia Putortì  1   2 , Marta Allena  1 , Micol Avenali  1   2 , Carlotta Dagna  1   2 , Daniele Martinelli  1   2 , Silvano Cristina  1 , Valentina Grillo  1 , Mauro Fresia  1 , Vito Bitetto  1 , Giuseppe Cosentino  2   3 , Francesca Valentino  4 , Enrico Alfonsi  3 , Giorgio Sandrini  1   2 , Antonio Pisani  1   2 , Cristina Tassorelli  1   2
Affiliations

Non-Invasive Neuromodulation in the Rehabilitation of Pisa Syndrome in Parkinson's Disease: A Randomized Controlled Trial

Roberto De Icco et al. Front Neurol. .

Abstract

Background: Pisa syndrome (PS) is a frequent postural complication of Parkinson's disease (PD). PS poorly responds to anti-parkinsonian drugs and the improvement achieved with neurorehabilitation tends to fade in 6 months or less. Transcranial direct current stimulation (t-DCS) is a non-invasive neuromodulation technique that showed promising results in improving specific symptoms in different movement disorders.

Objectives: This study aimed to evaluate the role of bi-hemispheric t-DCS as an add-on to a standardized hospital rehabilitation program in the management of PS in PD.

Methods: This study included 28 patients with PD and PS (21 men, aged 72.9 ± 5.1 years) who underwent a 4-week intensive neurorehabilitation treatment and were randomized to receive: i) t-DCS (t-DCS group, n = 13) for 5 daily sessions (20 min-2 mA) with bi-hemispheric stimulation over the primary motor cortex (M1), or ii) sham stimulation (sham group, n = 15) with the same duration and cadence. At baseline (T0), end of rehabilitation (T1), and 6 months later (T2) patients were evaluated with both trunk kinematic analysis and clinical scales, including UPDRS-III, Functional Independence Measure (FIM), and Numerical Rating Scale for lumbar pain.

Results: When compared to the sham group, the t-DCS group achieved a more pronounced improvement in several variables: overall posture (p = 0.014), lateral trunk inclination (p = 0.013) during upright standing position, total range of motion of the trunk (p = 0.012), FIM score (p = 0.048), and lumbar pain intensity (p = 0.017).

Conclusions: Our data support the use of neuromodulation with t-DCS as an add-on to neurorehabilitation for the treatment of patients affected by PS in PD.

Keywords: lateral trunk inclination; movement analysis; movement disorders; neurorehabilitation; parkinsonism; transcranial direct current stimulation (tDCS).

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Conflict of interest statement

RD, APu, MAl, MAv, CD, DM, SC, VG, MF, VB, GC, FV, GS, and EA report no funding in the preceding 12 months. APi holds grants that are not related to the subject of the present study, and he reports no biomedical financial interests or potential conflicts of interest. CT received honoraria for their participation in advisory boards or for oral presentations from Allergan, ElectroCore, Eli-Lilly, Novartis, and Teva. CT has no ownership interest and does not own stocks of any pharmaceutical company. CT serves as Chief Section Editor of Frontiers in Neurology—Section Headache Medicine and Facial Pain and on the editorial board of The Journal of Headache and Pain.

Figures

Figure 1
Figure 1
Flowchart of study procedures. t-DCS: patients randomized to transcranial direct current stimulation (n = 13). sham: patients randomized to sham stimulation (n = 15).
Figure 2
Figure 2
Kinematic analysis of trunk movement in static and dynamic conditions performed by a representative subject. The figure illustrates the static and dynamic tasks performed by a representative healthy subject. C7: the spinous process of the 7th cervical vertebra; Sa: sacral prominence. For the measurement of lateral (A) and anterior (B) trunk deviation, we considered the absolute deviation of the “C7-Sa” segment from the vector perpendicular to the floor of our movement analysis laboratory during the static upright standing position. For the dynamic tasks, we calculated the range of motion (ROM) of the trunk, defined as the maximum angle described by the C7-Sa segment starting from the upright standing position to the end of a right (C) or left (D) trunk bending, a forward trunk flexion (E) and a posterior trunk extension (F).
Figure 3
Figure 3
Effects of t-DCS and sham treatments on the kinematic analysis of trunk parameters and clinical scales scores. t-DCS: patients randomized to transcranial direct current stimulation (n = 13). sham: patients randomized to sham stimulation (n = 15). ROM: range of motion. Error bars: standard deviation. (A) Stat Tot: total postural alteration in the upright standing position. (B) Stat Bend: lateral trunk inclination in the upright standing position. (C) ROM Tot: sum of trunk ROMs of the four dynamic tasks. (D) UPDRS-III: Unified Parkinson's Disease Rating Scale—Part III—Motor examination. (E) FIM, Functional Independence Measure. (F) NRS: 0–10 numerical rating scale NRS for lumbar pain severity. Mixed-model ANOVA: factor “TIME” is the expression of the efficacy of the rehabilitative treatment in the overall population; factor “STIM” is the expression of the comparison between t-DCS and sham groups across all time-points. If the “TIMExSTIM” interaction was not significant, a post-hoc analysis was performed in the overall population: ■ = time-point vs. T0: p < 0.05; in case of a significant “TIMExSTIM” interaction, a post-hoc analysis was separately performed for the t-DCS group and the sham group: Δ = time-point vs. T0: p < 0.05 (the color identifies the group).
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References

    1. Doherty KM, van de Warrenburg BP, Peralta MC, Silveira-Moriyama L, Azulay JP, Gershanik OS, et al. . Postural deformities in Parkinson's disease. Lancet Neurol. (2011) 10:538–49. 10.1016/S1474-4422(11)70067-9 - DOI - PubMed
    1. Tassorelli C, De Icco R, Alfonsi E, Bartolo M, Serrao M, Avenali M, et al. . Botulinum toxin type A potentiates the effect of neuromotor rehabilitation of Pisa syndrome in Parkinson disease: a placebo controlled study. Park Relat Disord. (2014) 20:1140–4. 10.1016/j.parkreldis.2014.07.015 - DOI - PubMed
    1. Tinazzi M, Fasano A, Geroin C, Morgante F, Ceravolo R, Rossi S, et al. . Pisa syndrome in Parkinson disease: an observational multicenter Italian study. Neurology. (2015) 85:1769–79. 10.1212/WNL.0000000000002122 - DOI - PubMed
    1. Artusi CA, Montanaro E, Tuttobene S, Romagnolo A, Zibetti M, Lopiano L. Pisa syndrome in parkinson's disease is associated with specific cognitive alterations. Front Neurol. (2019) 10:577. 10.3389/fneur.2019.00577 - DOI - PMC - PubMed
    1. Yokochi F. Lateral flexion in Parkinson's disease and Pisa syndrome. J Neurol. (2006) 253(Suppl 7):VII17–20. 10.1007/s00415-006-7005-4 - DOI - PubMed