ORIGINAL RESEARCH ARTICLE published: 17 April 2014 HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2014.00207 Effects of robot assisted gait training in progressive supranuclear palsy (PSP): a preliminary report Patrizio Sale 1*, Fabrizio Stocchi 1, Daniele Galafate 1, Maria Francesca De Pandis 2, Domenica Le Pera 1, Ivan Sova 1, Manuela Galli 1,3, Calogero Foti 4 and Marco Franceschini 1 1 Department of Neurorehabilitation, IRCCS San Raffaele Pisana, Rome, Italy 2 San Raffaele Cassino, Cassino, Italy 3 Dipartimento di Elettronica, Informazione e Bioingegneria-Politecnico di Milano, Milano, Italy 4 Physical Rehabilitation Medicine Chair, Clinical Sciences and Translational Medicine DPT, Tor Vergata University, Roma, Italy Edited by: Background and Purpose: Progressive supranuclear palsy (PSP) is a rare Marco Iosa, Fondazione Santa Lucia, neurodegenerative disease clinically characterized by prominent axial extrapyramidal Italy motor symptoms with frequent falls. Over the last years the introduction of robotic Reviewed by: technologies to recover lower limb function has been greatly employed in the Leonardo Gizzi, University Hospital Göttingen, Germany rehabilitative practice. This observational trial is aimed at investigating the changes Giovanni Morone, IRCCS Santa in the main spatiotemporal following end-effector robot training in people with PSP. Lucia Foundation, Italy Method: Pilot observational trial. *Correspondence: Patrizio Sale, Department of Participants: Five cognitively intact participants with PSP and gait disorders. Neurorehabilitation, IRCCS San Raffaele Pisana, Via della Pisana Interventions: Patients were submitted to a rehabilitative program of robot-assisted 235, 00163, Rome, Italy walking sessions for 45 min, 5 times a week for 4 weeks. e-mail: [email protected] Main outcome measures: The spatiotemporal parameters at the beginning (T0) and at the end of treatment (T1) were recorded by a gait analysis laboratory. Results: Robot training was feasible, acceptable and safe and all participants completed the prescribed training sessions. All patients showed an improvement in the gait spatiotemporal index (Mean velocity, Cadence, Step length, and Step width) (T0 vs. T1). Conclusions: Robot training is a feasible and safe form of rehabilitation for cognitively intact people with PSP. The lack of side effects and the positive results in the gait parameter index in all patients support the recommendation to extend the trials of this treatment. Further investigation regarding the effectiveness of robot training in time is necessary. Trial registration: ClinicalTrials.gov NCT01668407. Keywords: progressive supranuclear palsy, PSP, gait analysis, lower limb, robot INTRODUCTION The PSP subject shows a short, shuffling stepped gait, gait freez- Progressive supranuclear palsy (PSP) is a rare neurodegenerative ing, lurching, unsteady gait or spontaneous falls (Lubarsky and disease that causes the gradual deterioration and death of spe- Juncos, 2008). In particular, subjects with PSP have decreased cific volumes of the brain (Richardson et al., 1963; Steele et al., step length, step velocity, and a significantly slower ability to 1964). Ludolph and colleagues showed that the neuropathologic break a fall from the center of gravity than controls (Welter et al., features of PSP include marked midbrain atrophy and atrophy of 2007). Although some disorders are similar to those found in the pallidum, thalamus, subthalamic nucleus, and frontal lobes Parkinsonism (rigidity, bradykinesia, postural instability), PSP (Ludolph et al., 2009). Clinical criteria for the diagnosis of PSP differs in several ways. The PSP subject does not have a forward are: a gradually progressive disorder, an onset at the age of 40 flexed posture like the Parkinson Disease (PD) subject and falls years or later, a presence of vertical supranuclear palsy, a slow- in PSP tend to be backwards (Boeve, 2007). Pharmacotherapy ing of vertical saccades and a postural instability with falls in the with carbidopa/levodopa and with dopamine agonists typically first year of disease onset. In particular, the first symptoms in is ineffective in managing the disorders (Rampello et al., 2005). two-thirds of the cases are: loss of balance, lunging forward when Non-pharmacologic therapies such as physical therapy and occu- mobilizing, fast walking, bumping into objects or people, and pational therapy are potentially useful, with the main goals being falls (Lubarsky and Juncos, 2008). Other common early symp- the maintenance of functional ambulation and the reduction of toms are changes in personality, general slowing of movement falls and associated injuries (Steffen et al., 2007). Gait recovery and visual symptoms. Postural instability and gait impairment are in all patients with impairments of the central nervous system the most important disorders in the early phases of the disease. (CNS) is an integral part of rehabilitation and often influences Frontiers in Human Neuroscience www.frontiersin.org April 2014 | Volume 8 | Article 207 | 1 Sale et al. Robot and progressive supranuclear Palsy the possibility of a patient returning home or to work (Schmidt were: (a) diagnosis of idiopathic PSP according to the UK Brain et al., 2007). Neurologic motor rehabilitation is directed toward Bank criteria, without any other significant neurological or the re-learning of motor skills. In particular, the recovery of walk- orthopaedic disorder; (b) age between 18 and 90 years old; (c) ing is a crucial aspect of rehabilitation, improving the quality ability to walk, unassisted or with little assistance, for at least 25 of life and patient’s independence. For non-ambulatory neuro- feet. The following exclusion criteria were identified: (d) inability logical patients, mechanically assisted walking with body weight to understand instructions required by the study (Informed support (BWS) has been suggested as a strategy to facilitate walk- Consent Test of Comprehension); (e) primarily wheelchair ing (Richards et al., 1993; Hesse et al., 2001) because it provides bound; (f) chronic and ongoing alcohol or drug abuse, active the opportunity to complete more practice of the whole task depression, anxiety or psychosis that might interfere with the use than would be possible by assisting overground walking. In the of the equipment or testing. last years, robot-aided walking is considered a promising tool for gait rehabilitation (Colombo et al., 2000) in various neu- INSTRUMENTAL ASSESSMENTS rological disease (Beer et al., 2008; Lo and Triche, 2008; Hesse Trained professionals, who were not involved in the research et al., 2010). The robotic devices have been developed to relieve treatment and blind to patients’ treatment, performed all instru- physical therapists from the strenuous and not ergonomic bur- mental and clinical assessments. All outcome assessments were den of manual BWS (Volpe et al., 2001; Winchester and Querry, collected in the ON phase 1 h and half after oral assumption of 2006; Steffen et al., 2007). Furthermore, the use of robotic devices the usual dose of medication. The 3D-Gait analysis (3D-GA) was is currently advised to prevent the risk of falls and to improve conducted using the following equipment: a 12-camera opto- gait velocity with the total safety of the patient (Morone et al., electronic system with passive markers (ELITE2002, BTS, Italy) 2014). Moreover, robot devices can be used to give inpatients to measure the kinematics of the movement; 2 force platforms an intensive program (in terms of many repetitions) of complex (Kistler, CH) to obtain the kinetic data of the movement (i.e., gait cycles. The robotic machines, offering practice up to 1000 ground reaction forces); 2 TV camera Video systems (BTS, Italy) steps per session, used either an exoskeleton or an end-effector synchronized with the optoelectronic and force platform systems approach. Currently, a robotic task-specific repetitive approach, for video recording. To evaluate the kinematics of each body i.e., numerous practices of complex gait cycles, is regarded as the segment, markers were positioned as described by Davis and most promising to restore motor function after neurological dis- colleagues (Sale et al., 2012, 2013a). Subjects were asked to walk ease (Dobkin, 2004; Dobkin and Duncan, 2012). Evidence-based barefoot, at their own natural pace (self-selected and comfortable approaches of rehabilitation in PSP are lacking and currently the speed), along a 10-meter walkway where the two force platforms majority of research on these subjects consists of case reports were placed. At least seven trials were collected for each subject involving only a small number of patients. Until now, only few in order to ensure data consistency. All graphs obtained from GA studies have been carried out on physiotherapy intervention in were normalized as a % of the gait cycle and kinetic data were the PSP gait and balance disorder (Izzo et al., 1986; Sosner et al., normalized for individual body weights. In order to quantify 1993; Suteerawattananon et al., 2002; Steffen et al., 2014). Usually the gait pattern of participants involved in this study, a specific the subject with PSP needs rehabilitative training to improve bal- software (Smartanalyser, BTS, Italy) enabled the calculation of ance and gait problems and to prevent the frequent falls. The some indices (time/distance parameters, joint angles values in rehabilitation programs for patients with PSP generally include specific gait cycle instant, peak values in ankle power