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Peduncolopontine DBS improves balance in progressive supranuclear palsy: Instrumental analysis
Clinical Neurophysiology 127 (2016) 3470–3471
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Letter to the Editor Peduncolopontine DBS improves balance in progressive supranuclear palsy: Instrumental analysis
Progressive supranuclear palsy (PSP) is a neurodegenerative disease that presents generally with gait and balance disorders. So far, no treatment has been able to improve consistently any of those disabling symptoms. The PPN is part of the rostral locomotor region of the brainstem playing a central role in the initiation and maintenance of gait and balance (Takakusaki et al., 2016). Deep brain stimulation of the pedunculopontine nucleus (PPN-DBS) has emerged as a potential intervention for patients with balance disorders. However, very few reports have clinically assessed the effects of DBS on postural control in PSP (Hazrati et al., 2012; Servello et al., 2014; Doshi et al., 2015; Mazzone et al., 2016). Herein, we present the first report that addresses objectively the effect of PPN-DBS on postural control in a PSP patient assessing balance with force plate. A 74-year-old, female diagnosed with PSP according to the criteria proposed by Litvan et al. (1996), with progressive course, vertical supranuclear gaze palsy, slowing of vertical saccades, prominent parkinsonism and postural instability, participated in this report after local committee approval and under informed consent. The patient presented with very disabling postural instability and was mostly unable to walk alone, scoring 54 in the UPDRS III (Unified Parkinson’s Disease Rating Scale – Motor Score). Bilateral implantation of electrodes in the PPN was performed uneventfully. Targets were defined not only based on classical anatomical references seen in T1-weighted images (Zrinzo et al., 2008), but those coordinates were also compared to histological sections of a MRI scanned brain and its fractional anisotropy (FA) measurements (Alho et al., 2016). The coordinates in the posterolateral pons in the level of the inferior colliculus were selected in the patient’s MRI followed by intraoperative stimulation control. The second of four contacts was selected as the active point of stimulation with low frequency (20 Hz, pulse width 60 ls and voltage between 2 and 4 V) (Ferraye et al., 2010; Florence et al., 2016) three weeks after the implant (Fig. 1A and B). The patient was followed clinically for over 3 months with no changes in the medication and doses during this period. Balance was assessed with and without visual control (eyes open/closed) while standing on a malleable surface set on a force platform (AMTI, OR6-WP). Evaluations were performed at base line, before the PPN surgery (BS), 30 days (30AS) and 60 days (60AS) after the surgery. The patient performed 3 trials of 30 s in each condition after dopaminergic
medication withdraw for at least 12 h. The variables chosen to represent the performance on postural sway were the area of the center of pressure (CoP area – average and SD) and average velocity of center of pressure mediolateral sway (CoPml velocity – average and SD). Under visual control (eyes open), we detected stable values for the CoP area, such as 8.10 ± 3.69 cm2 BS and 10.10 ± 4.53 cm2 at 30AS, changing remarkably at 60AS, 4.87 ± 2.04 cm2. Conversely, with no visual control, the CoP area dropped from 34.32 ± 10.81 cm2 at BS to 15.04 ± 4.43 cm2 at 30AS and to 11.00 ± 4.54 cm2 at 60AS (Fig. 1C). The CoPml velocity under visual control also changed from 2.65 ± 0.23 cm/s at BS to 2.34 ± 0.38 cm/ s at 30AS and 2.24 ± 0.23 cm/s at 60AS. Differences were greater under no visual control, changing from 3.57 ± 0.31 cm/s at BS to 2.95 ± 0.39 cm/s at 30AS and to 2.84 ± 0.35 cm/s at 60AS (Fig. 1D). We also recorded in the UPDRS III scores, improving from 54 before surgery to 43, at 30 days and to 41, 60 days of continuous stimulation. No changes were observed in other clinical domains such as swallowing and speech. Our results suggest that PPN-DBS was able to positively affect postural control in this severely disabled PSP patient by decreasing body oscillations and the CoP velocity. Yet, considering that the control body oscillations is highly automatic, it is unlikely that the improvement observed would have been related to learning effects between the conditions in a few trials. Subjects with low velocity and small CoP displacement are more prone to have reasonably stable posture in the sense that the center of mass does not approach the limits of the base of support, which could lead to falls (Corriveau et al., 2001; Abrahamova and Hlavacka, 2008). The present data, derived from objective measurements of postural control, give a more robust support to previous findings of gait improvement and reduction of falls after PPN-DBS (Servello et al., 2014). Such findings also corroborate the beneficial effects on balance after PPN-DBS in PD patients (Yousif et al., 2016). PPN is apparently involved in motor and sensory coupling and processing vestibular information as part of the mechanism of posture control (Takakusaki et al., 2004, 2016). In conclusion, our findings suggest that PPN-DBS can objectively improve balance of a severe PSP patient also in conditions that posture is challenged by the absence of visual control. Conflict of interest statement On behalf of all authors, the corresponding author states that there is no conflict of interest.
http://dx.doi.org/10.1016/j.clinph.2016.09.006 1388-2457/Ó 2016 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
Letter to the Editor / Clinical Neurophysiology 127 (2016) 3470–3471
3471
Fig. 1. (A) Axial section of post-operative T1-weighted magnetic resonance image of the pontine region showing the electrode artifacts as two round dark spots right anterior to colicular formation. (B) Sagittal section of the same MRI showing the longitudinal electrode artifacts and illustrative outline of the four contacts. (C and D) Average and standard deviation of 3 trials for CoP area (C) and velocity (D) in both visual conditions before the DBS surgery (BS), 30 days after surgery (30AS) and 60 days after surgery (60AS).
References Abrahamova D, Hlavacka F. Age-related changes of human balance during quiet stance. Physiol Res 2008;57:957–64. Alho A, Hamani C, Alho E, da Silva R, Santos G, Neves R, et al. Magnetic resonance diffusion tensor imaging for the pedunculopontine nucleus: proof of concept and histological correlation. Brain Struct Funct 2016 [in press]. Corriveau H, Hebert R, Prince F, Raiche M. Postural control in the elderly: an analysis of test-retest and interrater reliability of the COP-COM variable. Arch Phys Med Rehabil 2001;82:80–5. Doshi PK, Desai JD, Karkera B, Wadia PM. Bilateral pedunculopontine nucleus stimulation for progressive supranuclear palsy. Stereotact Funct Neurosurg 2015;93:59–65. Ferraye MU, Debu B, Fraix V, Goetz L, Ardouin C, Yelnik J, et al. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain 2010;133:205–14. Florence G, Sameshima K, Fonoff ET, Hamani C. Deep brain stimulation: more complex than the inhibition of cells and excitation of fibers. Neuroscientist 2016;22:332–45. Hazrati LN, Wong JC, Hamani C, Lozano AM, Poon YY, Dostrovsky JO, et al. Clinicopathological study in progressive supranuclear palsy with pedunculopontine stimulation. Mov Disord 2012;27:1304–7. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson– Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1–9. Mazzone P, Vilela Filho O, Viselli F, Insola A, Sposato S, Vitale F, et al. Our first decade of experience in deep brain stimulation of the brainstem: elucidating the mechanism of action of stimulation of the ventrolateral pontine tegmentum. J Neural Transm (Vienna) 2016;123:751–67. Servello D, Zekaj E, Saleh C, Menghetti C, Porta M. Long-term follow-up of deep brain stimulation of pedunculopontine nucleus in progressive supranuclear palsy: report of three cases. Surg Neurol Int 2014;5:S416–20. Takakusaki K, Chiba R, Nozu T, Okumura T. Brainstem control of locomotion and muscle tone with special reference to the role of the mesopontine tegmentum and medullary reticulospinal systems. J Neural Transm (Vienna) 2016;123:695–729. Takakusaki K, Oohinata-Sugimoto J, Saitoh K, Habaguchi T. Role of basal gangliabrainstem systems in the control of postural muscle tone and locomotion. Prog Brain Res 2004;143:231–7. Yousif N, Bhatt H, Bain PG, Nandi D, Seemungal BM. The effect of pedunculopontine nucleus deep brain stimulation on postural sway and vestibular perception. Eur J Neurol 2016;23:668–70. Zrinzo L, Zrinzo LV, Tisch S, Limousin PD, Yousry TA, Afshar F, et al. Stereotactic localization of the human pedunculopontine nucleus: atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. Brain 2008;131:1588–98.
Carolina de Oliveira Souza 1 Movement Disorders Clinic, Department of Neurology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil
Andrea Cristina de Lima-Pardini 1 Institute of Radiology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil
⇑
Daniel Boari Coelho ,1 Human Motor Systems Laboratory, School of Physical Education and Sport, University of São Paulo, São Paulo, Brazil ⇑ Corresponding author at: Av. Prof. Mello Moraes, 65, São Paulo, SP 05508-030, Brazil. E-mail address: [email protected] Rachael Brant Machado Movement Disorders Clinic, Department of Neurology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Eduardo Joaquim Lopes Alho Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Ana Tereza Di Lorenzo Alho Institute of Radiology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Luis Augusto Teixeira Human Motor Systems Laboratory, School of Physical Education and Sport, University of São Paulo, São Paulo, Brazil Manoel Jacobsen Teixeira Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Egberto Reis Barbosa Movement Disorders Clinic, Department of Neurology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil
⇑
Erich Talamoni Fonoff Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil ⇑ Corresponding author at: Ovideo Pires de Campos 785, Sao Paulo, SP 01231-000, Brazil. E-mail address: [email protected] Available online 15 September 2016
1
The first three authors have the same contribution to the research.
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Letter to the Editor Peduncolopontine DBS improves balance in progressive supranuclear palsy: Instrumental analysis
Progressive supranuclear palsy (PSP) is a neurodegenerative disease that presents generally with gait and balance disorders. So far, no treatment has been able to improve consistently any of those disabling symptoms. The PPN is part of the rostral locomotor region of the brainstem playing a central role in the initiation and maintenance of gait and balance (Takakusaki et al., 2016). Deep brain stimulation of the pedunculopontine nucleus (PPN-DBS) has emerged as a potential intervention for patients with balance disorders. However, very few reports have clinically assessed the effects of DBS on postural control in PSP (Hazrati et al., 2012; Servello et al., 2014; Doshi et al., 2015; Mazzone et al., 2016). Herein, we present the first report that addresses objectively the effect of PPN-DBS on postural control in a PSP patient assessing balance with force plate. A 74-year-old, female diagnosed with PSP according to the criteria proposed by Litvan et al. (1996), with progressive course, vertical supranuclear gaze palsy, slowing of vertical saccades, prominent parkinsonism and postural instability, participated in this report after local committee approval and under informed consent. The patient presented with very disabling postural instability and was mostly unable to walk alone, scoring 54 in the UPDRS III (Unified Parkinson’s Disease Rating Scale – Motor Score). Bilateral implantation of electrodes in the PPN was performed uneventfully. Targets were defined not only based on classical anatomical references seen in T1-weighted images (Zrinzo et al., 2008), but those coordinates were also compared to histological sections of a MRI scanned brain and its fractional anisotropy (FA) measurements (Alho et al., 2016). The coordinates in the posterolateral pons in the level of the inferior colliculus were selected in the patient’s MRI followed by intraoperative stimulation control. The second of four contacts was selected as the active point of stimulation with low frequency (20 Hz, pulse width 60 ls and voltage between 2 and 4 V) (Ferraye et al., 2010; Florence et al., 2016) three weeks after the implant (Fig. 1A and B). The patient was followed clinically for over 3 months with no changes in the medication and doses during this period. Balance was assessed with and without visual control (eyes open/closed) while standing on a malleable surface set on a force platform (AMTI, OR6-WP). Evaluations were performed at base line, before the PPN surgery (BS), 30 days (30AS) and 60 days (60AS) after the surgery. The patient performed 3 trials of 30 s in each condition after dopaminergic
medication withdraw for at least 12 h. The variables chosen to represent the performance on postural sway were the area of the center of pressure (CoP area – average and SD) and average velocity of center of pressure mediolateral sway (CoPml velocity – average and SD). Under visual control (eyes open), we detected stable values for the CoP area, such as 8.10 ± 3.69 cm2 BS and 10.10 ± 4.53 cm2 at 30AS, changing remarkably at 60AS, 4.87 ± 2.04 cm2. Conversely, with no visual control, the CoP area dropped from 34.32 ± 10.81 cm2 at BS to 15.04 ± 4.43 cm2 at 30AS and to 11.00 ± 4.54 cm2 at 60AS (Fig. 1C). The CoPml velocity under visual control also changed from 2.65 ± 0.23 cm/s at BS to 2.34 ± 0.38 cm/ s at 30AS and 2.24 ± 0.23 cm/s at 60AS. Differences were greater under no visual control, changing from 3.57 ± 0.31 cm/s at BS to 2.95 ± 0.39 cm/s at 30AS and to 2.84 ± 0.35 cm/s at 60AS (Fig. 1D). We also recorded in the UPDRS III scores, improving from 54 before surgery to 43, at 30 days and to 41, 60 days of continuous stimulation. No changes were observed in other clinical domains such as swallowing and speech. Our results suggest that PPN-DBS was able to positively affect postural control in this severely disabled PSP patient by decreasing body oscillations and the CoP velocity. Yet, considering that the control body oscillations is highly automatic, it is unlikely that the improvement observed would have been related to learning effects between the conditions in a few trials. Subjects with low velocity and small CoP displacement are more prone to have reasonably stable posture in the sense that the center of mass does not approach the limits of the base of support, which could lead to falls (Corriveau et al., 2001; Abrahamova and Hlavacka, 2008). The present data, derived from objective measurements of postural control, give a more robust support to previous findings of gait improvement and reduction of falls after PPN-DBS (Servello et al., 2014). Such findings also corroborate the beneficial effects on balance after PPN-DBS in PD patients (Yousif et al., 2016). PPN is apparently involved in motor and sensory coupling and processing vestibular information as part of the mechanism of posture control (Takakusaki et al., 2004, 2016). In conclusion, our findings suggest that PPN-DBS can objectively improve balance of a severe PSP patient also in conditions that posture is challenged by the absence of visual control. Conflict of interest statement On behalf of all authors, the corresponding author states that there is no conflict of interest.
http://dx.doi.org/10.1016/j.clinph.2016.09.006 1388-2457/Ó 2016 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
Letter to the Editor / Clinical Neurophysiology 127 (2016) 3470–3471
3471
Fig. 1. (A) Axial section of post-operative T1-weighted magnetic resonance image of the pontine region showing the electrode artifacts as two round dark spots right anterior to colicular formation. (B) Sagittal section of the same MRI showing the longitudinal electrode artifacts and illustrative outline of the four contacts. (C and D) Average and standard deviation of 3 trials for CoP area (C) and velocity (D) in both visual conditions before the DBS surgery (BS), 30 days after surgery (30AS) and 60 days after surgery (60AS).
References Abrahamova D, Hlavacka F. Age-related changes of human balance during quiet stance. Physiol Res 2008;57:957–64. Alho A, Hamani C, Alho E, da Silva R, Santos G, Neves R, et al. Magnetic resonance diffusion tensor imaging for the pedunculopontine nucleus: proof of concept and histological correlation. Brain Struct Funct 2016 [in press]. Corriveau H, Hebert R, Prince F, Raiche M. Postural control in the elderly: an analysis of test-retest and interrater reliability of the COP-COM variable. Arch Phys Med Rehabil 2001;82:80–5. Doshi PK, Desai JD, Karkera B, Wadia PM. Bilateral pedunculopontine nucleus stimulation for progressive supranuclear palsy. Stereotact Funct Neurosurg 2015;93:59–65. Ferraye MU, Debu B, Fraix V, Goetz L, Ardouin C, Yelnik J, et al. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain 2010;133:205–14. Florence G, Sameshima K, Fonoff ET, Hamani C. Deep brain stimulation: more complex than the inhibition of cells and excitation of fibers. Neuroscientist 2016;22:332–45. Hazrati LN, Wong JC, Hamani C, Lozano AM, Poon YY, Dostrovsky JO, et al. Clinicopathological study in progressive supranuclear palsy with pedunculopontine stimulation. Mov Disord 2012;27:1304–7. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson– Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 1996;47:1–9. Mazzone P, Vilela Filho O, Viselli F, Insola A, Sposato S, Vitale F, et al. Our first decade of experience in deep brain stimulation of the brainstem: elucidating the mechanism of action of stimulation of the ventrolateral pontine tegmentum. J Neural Transm (Vienna) 2016;123:751–67. Servello D, Zekaj E, Saleh C, Menghetti C, Porta M. Long-term follow-up of deep brain stimulation of pedunculopontine nucleus in progressive supranuclear palsy: report of three cases. Surg Neurol Int 2014;5:S416–20. Takakusaki K, Chiba R, Nozu T, Okumura T. Brainstem control of locomotion and muscle tone with special reference to the role of the mesopontine tegmentum and medullary reticulospinal systems. J Neural Transm (Vienna) 2016;123:695–729. Takakusaki K, Oohinata-Sugimoto J, Saitoh K, Habaguchi T. Role of basal gangliabrainstem systems in the control of postural muscle tone and locomotion. Prog Brain Res 2004;143:231–7. Yousif N, Bhatt H, Bain PG, Nandi D, Seemungal BM. The effect of pedunculopontine nucleus deep brain stimulation on postural sway and vestibular perception. Eur J Neurol 2016;23:668–70. Zrinzo L, Zrinzo LV, Tisch S, Limousin PD, Yousry TA, Afshar F, et al. Stereotactic localization of the human pedunculopontine nucleus: atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. Brain 2008;131:1588–98.
Carolina de Oliveira Souza 1 Movement Disorders Clinic, Department of Neurology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil
Andrea Cristina de Lima-Pardini 1 Institute of Radiology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil
⇑
Daniel Boari Coelho ,1 Human Motor Systems Laboratory, School of Physical Education and Sport, University of São Paulo, São Paulo, Brazil ⇑ Corresponding author at: Av. Prof. Mello Moraes, 65, São Paulo, SP 05508-030, Brazil. E-mail address: [email protected] Rachael Brant Machado Movement Disorders Clinic, Department of Neurology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Eduardo Joaquim Lopes Alho Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Ana Tereza Di Lorenzo Alho Institute of Radiology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Luis Augusto Teixeira Human Motor Systems Laboratory, School of Physical Education and Sport, University of São Paulo, São Paulo, Brazil Manoel Jacobsen Teixeira Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil Egberto Reis Barbosa Movement Disorders Clinic, Department of Neurology, Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil
⇑
Erich Talamoni Fonoff Department of Neurology, Division of Functional Neurosurgery at Institute of Psychiatry of Hospital das Clínicas of the University of São Paulo, School of Medicine, São Paulo, Brazil ⇑ Corresponding author at: Ovideo Pires de Campos 785, Sao Paulo, SP 01231-000, Brazil. E-mail address: [email protected] Available online 15 September 2016
1
The first three authors have the same contribution to the research.