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July 30, 2019; 93 (5) Article

Muscle-targeted nutritional support for rehabilitation in patients with parkinsonian syndrome

Michela Barichella, View ORCID ProfileEmanuele Cereda, Giovanna Pinelli, Laura Iorio, Diana Caroli, Irene Masiero, Valentina Ferri, Erica Cassani, Carlotta Bolliri, Serena Caronni, Marcello Maggio, Paola Ortelli, Davide Ferrazzoli, Antonios Maras, Giulio Riboldazzi, Giuseppe Frazzitta, Gianni Pezzoli
First published July 5, 2019, DOI: https://doi.org/10.1212/WNL.0000000000007858
Michela Barichella
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Emanuele Cereda
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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  • ORCID record for Emanuele Cereda
Giovanna Pinelli
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Laura Iorio
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Diana Caroli
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Irene Masiero
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Valentina Ferri
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Erica Cassani
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Carlotta Bolliri
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Serena Caronni
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Marcello Maggio
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Paola Ortelli
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Davide Ferrazzoli
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Antonios Maras
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Giulio Riboldazzi
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Giuseppe Frazzitta
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Gianni Pezzoli
From the Parkinson Institute (M.B., D.C., I.M., V.F., E.C., C.B., S.C., G. Pezzoli), ASST G.Pini-CTO, ex ICP, Milan; Clinical Nutrition and Dietetics Unit (E.C.), Fondazione IRCCS Policlinico San Matteo, Pavia; Dipartimento Riabilitazione Malattia di Parkinson e Disturbi del Movimento (G. Pinelli, P.O., D.F., G.F.), Ospedale Classificato Moriggia Pelascini di Gravedona; U.S. Riabilitazione Parkinson (L.I., A.M., G.R.), Fondazione Gaetano e Piera Borghi di Brebbia; and UOC Clinica Geriatrica (M.M.), Dipartimento Medico-Geriatrico-Riabilitativo, Università-Azienda Ospedaliero-Universitaria di Parma, Italy.
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Citation
Muscle-targeted nutritional support for rehabilitation in patients with parkinsonian syndrome
Michela Barichella, Emanuele Cereda, Giovanna Pinelli, Laura Iorio, Diana Caroli, Irene Masiero, Valentina Ferri, Erica Cassani, Carlotta Bolliri, Serena Caronni, Marcello Maggio, Paola Ortelli, Davide Ferrazzoli, Antonios Maras, Giulio Riboldazzi, Giuseppe Frazzitta, Gianni Pezzoli
Neurology Jul 2019, 93 (5) e485-e496; DOI: 10.1212/WNL.0000000000007858

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Abstract

Objective We evaluated the efficacy of muscle-targeted nutritional support on the functional outcomes of multidisciplinary intensive rehabilitation treatment (MIRT) in patients with Parkinson disease (PD) or parkinsonism.

Methods We conducted a pragmatic, bicentric, randomized (1:1), assessor-blind controlled trial (Protein, Leucine and Vitamin D Enhancing Rehabilitation [PRO-LEADER]; April 2017 to January 2018) in cognitively intact patients with PD or parkinsonism and undergoing a 30-day MIRT. Patients (n = 150) received a standard hospital diet with or without a whey protein–based nutritional supplement enriched with leucine and vitamin D twice daily. The primary efficacy endpoint was the increase in the distance walked during a 6-minute walking test (6MWT). Secondary endpoints were changes in 4-meter walking speed, Timed Up and Go test (TUG), Berg balance scale, handgrip strength, Self-assessment Parkinson's Disease Disability Scale, body weight, and skeletal muscle mass (SMM).

Results Nutritional support resulted in greater increase in the distance walked during 6MWT (mean 69.6 meters [95% confidence interval (CI) 60.7–78.6]) than no support (51.8 meters [95% CI 37.0–66.7]): center-adjusted mean difference, 18.1 meters (95% CI 0.9–35.3) (p = 0.039). Further adjustment for changes in dopaminergic therapy and SMM yielded consistent results: mean difference, 18.0 meters (95% CI 0.7–35.2) (p = 0.043). A meaningful effect was also found for the following secondary endpoints: 4-meter walking speed (p = 0.032), TUG (p = 0.046), SMM, and SMM index (p = 0.029). Six patients discontinued the nutritional therapy due to mild side effects.

Conclusion The consumption of a whey protein–based nutritional formula enriched with leucine and vitamin D with MIRT improved lower extremity function and preserved muscle mass in patients with PD or parkinsonism.

Clinicaltrials.gov identifier NCT03124277.

Classification of evidence This study provides Class I evidence that for patients with parkinsonism undergoing intensive rehabilitation, a whey protein–based nutritional formula enriched with leucine and vitamin D increased distance walked on the 6MWT.

Glossary

6MWT=
6-minute walk test;
BBS=
Berg Balance Scale;
CI=
confidence interval;
HS=
handgrip strength;
ITT=
intent-to-treat;
LEDD=
levodopa equivalent daily dose;
MIRT=
multidisciplinary intensive rehabilitation treatment;
PD=
Parkinson disease;
RCT=
randomized clinical trial;
SMI=
skeletal muscle mass index;
SMM=
skeletal muscle mass;
SPDDS=
Self-assessment Parkinson's Disease Disability Scale;
TUG=
Timed Up and Go test;
UPDRS=
Unified Parkinson’s Disease Rating Scale

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • Class of Evidence: NPub.org/coe

  • Received October 22, 2018.
  • Accepted in final form March 14, 2019.
  • © 2019 American Academy of Neurology
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Disputes & Debates: Rapid online correspondence

  • Author response: Muscle-targeted nutritional support for rehabilitation in patients with parkinsonian syndrome
    • Emanuele Cereda, Physician, Clinical Nutrition and Dietetics Unit, Fondazione IRCCS Policlinico San Matteo (Pavia, Italy)
    • Michela Barichella, Physician, Parkinson Institute, ASST G.Pini-CTO, ex ICP (Milan, Italy)
    • Gianni Pezzoli, Physician, Parkinson Institute, ASST G.Pini-CTO, ex ICP (Milan, Italy)
    Submitted August 28, 2019
  • Reader response: Muscle-targeted nutritional support for rehabilitation in patients with parkinsonian syndrome
    • Cynthia K. López Botello, Nutritionist, Master’s Degree in Public Health, Consulta No.2 de Nutrición, Hospital Universitario “Dr. José E. González”, Universidad Autónoma de Nuevo León
    • Ingrid Estrada-Bellmann, Professor of Neurology, Servicio de Neurología, Hospital Universitario “Dr. José E. González”, Universidad Autónoma de Nuevo León.
    • Sergio A. Castillo-Torres, Neurology Resident, Servicio de Neurología, Hospital Universitario “Dr. José E. González”, Universidad Autónoma de Nuevo León.
    • Denisse G. Martínez-Roque, Social Service Intern, Servicio de Neurología, Hospital Universitario “Dr. José E. González”, Universidad Autónoma de Nuevo León.
    • Carlos A. Soto-Rincón, Neurology Resident, Servicio de Neurología, Hospital Universitario “Dr. José E. González”, Universidad Autónoma de Nuevo León.
    • Beatriz Chavez-Luevanos, Professor of Neurology, Head of Service, Servicio de Neurología, Hospital Universitario “Dr. José E. González”, Universidad Autónoma de Nuevo León.
    • Patricia R. Ancer Rodríguez, Doctorate in Bioethics, University Hospital of the Faculty of Medicine of Uanl City (Monterrey, Mexico)
    Submitted August 11, 2019
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Neurology | Print ISSN:0028-3878
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