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The impact of freezing of gait on functional dependency in Parkinson’s disease with regard to motor phenotype

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Abstract

Background and objective

Freezing of gait (FOG) is a disabling symptom more frequent in Parkinson’s disease (PD) patients with postural instability gait difficulty (PIGD) phenotype. The aim of this study was to determine the prevalence of self-reported FOG in a large group of PD patients as well as assess its relationship with functional dependency with regard to motor phenotype.

Methods

The data correspond to the baseline evaluation of the COPPADIS-2015 study. Patients with FOG were identified as those with a score of 1 or greater on item-3 of the freezing of gait questionnaire (FOG-Q). Functional dependency was defined as a Schwab and England (S&E) ADL scale score less than 80%. PIGD and non-PIGD (tremor dominant + indeterminate) groups were considered regarding to motor phenotype.

Results

Among the 689 PD patients (62.6 ± 8.9 years old, 59.8% males), 240 reported FOG (34.8%), whereas 63 presented functional dependency (9.1%). A total of 22.1% of patients with FOG presented functional dependency vs. only 2.2% of those without FOG (p < 0.0001). FOG was related to functional dependency (OR = 3.470; 95%CI 1.411–8.530; p = 0.007) after adjustment to age, gender, disease duration, daily equivalent levodopa dose, comorbidity (number of non-antiparkinsonian drugs/day), motor status (UPDRS-III), PIGD phenotype, motor complications (UPDRS-IV), NMS burden (NMSS total score), cognition (PD-CRS), and mood (BDI-II). However, according to motor phenotype, FOG was related to functional dependency only in PIGD patients (OR = 7.163; 95%CI 1.206–42.564; p = 0.030).

Conclusions

Self-reported FOG is associated with functional dependency in PIGD but not in non-PIGD motor phenotype patients.

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Abbreviations

FOG:

Freezing of gait

FOG-Q:

Freezing of gait questionnaire

NMSS:

Non-motor symptoms scale

PD:

Parkinson’s disease

PD-CRS:

Parkinson’s disease cognitive rating scale

PIGD:

Postural instability gait difficulty

S&E:

Schwab & England activities of daily living scale

TD:

Tremor dominant

UPDRS:

Unified Parkinson’s disease rating scale

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Acknowledgments

We would like to thank all patients, caregivers, and all persons, companies, or institutions collaborating in this project. Especially, many thanks to Fundación Curemos el Parkinson (www.curemoselparkinson.org) and Alphabioresearch (www.alphabioresearch.com). The following are the collaborators of the COPPADIS STUDY GROUP: Adarmes Astrid D, Almeria M, Alonso Cánovas A, Alonso Frech F, Arnáiz S, Arribas S, Ascunce Vidondo A, Aguilar M, Bernardo Lambrich N, Bejr-Kasem H, Blázquez Estrada M, Botí M, Borrue C, Cabello González C, Cabo López I, Cámara Lorenzo A, Carrillo F, Carrillo Padilla FJ, Casas E, Clavero P, Cortina Fernández A, Cosgaya M, Cots Foraster A, Crespo Cuevas A, de Fábregues-Boixar O, Díez-Fairen M, Erro E, Estelrich Peyret E, Fernández Guillán N, Gámez P, Gallego M, García Campos C, García Moreno JM, Gastón I, Guillén Fopiani D, Gómez Garre MP, González Aloy J, González Ardura J, González García B, González Palmás MJ, González Toledo GR, Golpe Díaz A, Grau Solá M, Guardia G, Horta-Barba A, Idoate Calderón D, Infante J, Kulisevsky J, Kurtis M, Labandeira C, Labrador MA, Lacruz F, Lage Castro M, López Díaz LM, López Manzanares L, López Seoane B, Lucas del Pozo, Macías Y, Mata M, Martí Andres G, Martí MJ, Martínez Castrillo JC, McAfee D, Meitín MT, Menéndez González M, Méndez del Barrio C, Miranda Santiago J, Morales Casado MI, Moreno Diéguez A, Nogueira V, Novo Amado A, Novo Ponte S, Ordás C, Pagonabarraga J, Pareés I, Pascual-Sedano B, Pastor P, Pérez Fuertes A, Pérez Noguera R, Prats MA, Prieto Jurczynska C, Puente V, Pueyo Morlans M, Redondo Rafales N, Rodríguez Méndez L, Rodríguez Pérez AB, Roldán F, Ruíz De Arcos M, Ruíz Martínez J, Sánchez-Carpintero M, Sánchez Díez G, Sánchez Rodríguez A, Santacruz P, Segundo Rodríguez JC, Seijo M, Sierra Peña M, Solano Vila B, Tartari JP, Valero C, Vargas L, Villanueva C, Vives B, and Villar MD.

Funding

Santos-García D. has received honoraria for educational presentations and/or advice service by Abbvie, UCB Pharma, Lundbeck, KRKA, Zambon, Bial, and Teva.

de Deus Fonticoba T. has received honoraria for educational presentations and advice service by Abbvie. Suárez Castro E: None. Ángel Aneiros Díaz: None. Feal Painceiras M: None. Paz González JM has received honoraria for educational presentations and/or advice service by UCB Pharma, Lundbeck, KRKA y Zambon. García Sancho C: None. Jesús S. has received honoraria from AbbVie, Bial, Merz, UCB, and Zambon. She also holds the competitive contract “Juan Rodés” supported by the Instituto de Salud Carlos III. She has received grants from the Spanish Ministry of Economy and Competitiveness (PI18/01898) and the Consejería de Salud de la Junta de Andalucía (PI-0459-2018). Mir P. has received honoraria from AbbVie, Abbott, Allergan, Bial, Merz, UCB, and Zambon. Also, he has received grants from the Spanish Ministry of Economy and Competitiveness (PI16/01575) co-founded by ISCIII (Subdirección General de Evaluación y Fomento de la Investigación), Fondo Europeo de Desarrollo Regional (FEDER), the Consejería de Economía, Innovación, Ciencia y Empleo de la Junta de Andalucía (CVI-02526, CTS-7685), the Consejería de Salud y Bienestar Social de la Junta de Andalucía (PI-0437-2012, PI-0471-2013), the Sociedad Andaluza de Neurología, the Jacques and Gloria Gossweiler Foundation, the Fundación Alicia Koplowitz, and the Fundación Mutua Madrileña. Planellas LL. has received travel bursaries grant from Abbvie. García Caldentey J. has received honoraria for educational presentations and advice service by Qualigen, Nutricia, Abbvie, Italfarmaco, UCB Pharma, Lundbeck, Zambon, Bial, and Teva. Caballol N. has received honoraria for educational presentations and advice service by Qualigen, Nutricia, Abbvie, Italfarmaco, UCB Pharma, Lundbeck, Zambon, Bial, and Teva. Legarda I. has received honoraria for educational presentations and advice service by Abbvie, UCB Pharma, Zambon, Bial, and Teva. Hernández Vara J. has received travel bursaries and educational grants from Abbvie and has received honoraria for educational presentations from Abbvie, Teva, Bial, Zambon, Italfarmaco, and Sanofi-Genzyme. González Aramburu I: None. Ávila Rivera MA. has received honoraria from Zambon, UCB Pharma, Qualigen, Bial, and Teva, and sponsorship from Zambon and Teva for attending conferences. Catalán MJ: None. Nogueira V: None. Álvarez Sauco M. has received honoraria for educational presentations and advice service by Abbvie, UCB Pharma, Zambon, Bial, and Teva. Vela L. has received honoraria for educational presentations and advice service by Abbvie, UCB Pharma, Lundbeck, KRKA, Zambon, Bial, and Teva. Escalante S. has received honoraria for educational presentations and advice service by Abbvie, Zambon, and Bial. Cubo E: travel grants: Abbvie, Allergan, Boston; lecturing honoraria: Abbvie, International Parkinson’s disease Movement Disorder Society. Sánchez Alonso P. has received honoraria for educational presentations and advice service by Abbvie, UCB Pharma, Lundbeck, KRKA, Zambon, Bial, and Teva. Alonso Losada MG. has received honoraria for educational presentations and advice service by Zambon and Bial. López Ariztegui N. has received honoraria for educational presentations and advice service by Abbvie, Italfarmaco, Zambon, and Bial. Martinez-Martin P: Honoraria: from Editorial Viguera and National School of Health for lecturing in courses; International Parkinson and Movement Disorder Society for management of the Program on Rating Scales; Abbvie and Zambon for advice in clinic-epidemiological studies www.curemoselparkinson.org.

Author information

Authors and Affiliations

  1. Section of Neurology, Complejo Hospitalario Universitario de A Coruña (CHUAC), HUAC, C / As Xubias 84, 15006, A Coruña, Spain

    Diego Santos-García, María J Feal-Painceiras, Jose M Paz-González & Carlos García-Sancho

  2. Hospital Arquitecto Marcide y Hospital Naval, Complejo Hospitalario Universitario de Ferrol (CHUF), Ferrol, A Coruña, Spain

    Teres de Deus-Fonticoba, Ester Suárez Castro & Ángel M Aneiros Díaz

  3. Unidad de Trastornos del Movimiento, Servicio de Neurología y Neurofisiología Clínica, Instituto de Biomedicina de Sevilla, Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla, Seville, Spain

    Silvia Jesús & Pablo Mir

  4. Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain

    Silvia Jesús, Pablo Mir & Pablo Martinez-Martin

  5. Hospital Clínic de Barcelona, Barcelona, Spain

    Lluís Planellas

  6. Centro Neurológico Oms 42, Palma de Mallorca, Spain

    Juan García-Caldentey

  7. Consorci Sanitari Integral, Hospital Moisés Broggi, Sant Joan Despí, Barcelona, Spain

    Nuria Caballol

  8. Hospital Universitario Son Espases, Palma de Mallorca, Spain

    Inés Legarda

  9. Hospital Universitario Vall d’Hebron, Barcelona, Spain

    Jorge Hernández-Vara

  10. Hospital Universitario Marqués de Valdecilla, Santander, Spain

    Isabel González-Aramburu

  11. Consorci Sanitari Integral, Hospital General de L’Hospitalet, L’Hospitalet de Llobregat, Barcelona, Spain

    María A Ávila-Rivera

  12. Hospital Universitario Clínico San Carlos, Madrid, Spain

    María J Catalán

  13. Hospital Da Costa de Burela, Lugo, Spain

    Víctor Nogueira

  14. Hospital General Universitario de Elche, Elche, Spain

    María Álvarez-Sauco

  15. Fundación Hospital de Alcorcón, Madrid, Spain

    Lydia Vela

  16. Hospital de Tortosa Verge de la Cinta (HTVC), Tortosa, Tarragona, Spain

    Sonia Escalante

  17. Complejo Asistencial Universitario de Burgos, Burgos, Spain

    Esther Cubo

  18. Hospital Universitario Puerta de Hierro, Madrid, Spain

    Pilar Sánchez-Alonso

  19. Hospital Álvaro Cunqueiro, Complejo Hospitalario Universitario de Vigo (CHUVI), Vigo, Spain

    María G Alonso-Losada

  20. Complejo Hospitalario de Toledo, Toledo, Spain

    Nuria López-Ariztegui

  21. Centro Nacional de Epidemiología, Instituto de Salud Carlos III, Madrid, Spain

    Pablo Martinez-Martin

Authors
  1. Diego Santos-García
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  2. Teres de Deus-Fonticoba
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  3. Ester Suárez Castro
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  4. Ángel M Aneiros Díaz
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  5. María J Feal-Painceiras
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  6. Jose M Paz-González
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  7. Carlos García-Sancho
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  8. Silvia Jesús
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  9. Pablo Mir
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  10. Lluís Planellas
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  11. Juan García-Caldentey
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  12. Nuria Caballol
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  13. Inés Legarda
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  14. Jorge Hernández-Vara
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  15. Isabel González-Aramburu
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  16. María A Ávila-Rivera
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  17. María J Catalán
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  18. Víctor Nogueira
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  19. María Álvarez-Sauco
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  20. Lydia Vela
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  21. Sonia Escalante
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  22. Esther Cubo
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  23. Pilar Sánchez-Alonso
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  24. María G Alonso-Losada
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  25. Nuria López-Ariztegui
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  26. Pablo Martinez-Martin
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Consortia

on behalf of the COPPADIS Study Group

  • AD Adarmes
  • , M Almeria
  • , MG Alonso Losada
  • , A Alonso Cánovas
  • , F Alonso Frech
  • , I Álvarez
  • , M Álvarez Sauco
  • , A Aneiros Díaz
  • , S Arnáiz
  • , S Arribas
  • , A Ascunce Vidondo
  • , M Aguilar
  • , MA Ávila
  • , N Bernardo Lambrich
  • , H Bejr-Kasem
  • , M Blázquez Estrada
  • , M Botí
  • , C Borrue
  • , MT Buongiorno
  • , C Cabello González
  • , I Cabo López
  • , N Caballol
  • , A Cámara Lorenzo
  • , F Carrillo
  • , FJ Carrillo Padilla
  • , E Casas
  • , MJ Catalán
  • , P Clavero
  • , A Cortina Fernández
  • , M Cosgaya
  • , A Cots Foraster
  • , A Crespo Cuevas
  • , E Cubo
  • , T de Deus Fonticoba
  • , O de Fábregues-Boixar
  • , M Díez-Fairen
  • , E Erro
  • , S Escalante
  • , E Estelrich Peyret
  • , N Fernández Guillán
  • , P Gámez
  • , M Gallego
  • , J García Caldentey
  • , C García Campos
  • , JM García Moreno
  • , I Gastón
  • , D Guillén Fopiani
  • , MP Gómez Garre
  • , J González Aloy
  • , I González-Aramburu
  • , J González Ardura
  • , B González García
  • , MJ González Palmás
  • , GR González Toledo
  • , A Golpe Díaz
  • , M Grau Solá
  • , G Guardia
  • , J Hernández Vara
  • , A Horta-Barba
  • , D Idoate Calderón
  • , J Infante
  • , S Jesús
  • , J Kulisevsky
  • , M Kurtis
  • , C Labandeira
  • , MA Labrador
  • , F Lacruz
  • , M Lage Castro
  • , I Legarda
  • , N López Ariztegui
  • , LM López Díaz
  • , L López Manzanares
  • , B López Seoane
  • , S Lucas del Pozo
  • , Y Macías
  • , M Mata
  • , G Martí Andres
  • , MJ Martí
  • , JC Martínez Castrillo
  • , P Martinez-Martin
  • , D McAfee
  • , MT Meitín
  • , M Menéndez González
  • , C Méndez del Barrio
  • , P Mir
  • , J Miranda Santiago
  • , MI Morales Casado
  • , A Moreno Diéguez
  • , V Nogueira
  • , A Novo Amado
  • , S Novo Ponte
  • , C Ordás
  • , J Pagonabarraga
  • , I Pareés
  • , B Pascual-Sedano
  • , P Pastor
  • , A Pérez Fuertes
  • , R Pérez Noguera
  • , L Planellas
  • , MA Prats
  • , C Prieto Jurczynska
  • , V Puente
  • , M Pueyo Morlans
  • , N Redondo Rafales
  • , L Rodríguez Méndez
  • , AB Rodríguez Pérez
  • , F Roldán
  • , M Ruíz De Arcos
  • , J Ruíz Martínez
  • , P Sánchez Alonso
  • , M Sánchez-Carpintero
  • , G Sánchez Díez
  • , A Sánchez Rodríguez
  • , P Santacruz
  • , D Santos García
  • , JC Segundo Rodríguez
  • , M Seijo
  • , M Sierra Peña
  • , B Solano Vila
  • , E Suárez Castro
  • , JP Tartari
  • , C Valero
  • , L Vargas
  • , L Vela
  • , C Villanueva
  • , B Vives
  •  & MD Villar

Contributions

Santos-García D: conception, organization, and execution of the project; statistical analysis; writing of the first draft of the manuscript; recruitment and/or evaluation of participants. De Deus Fonticoba T: review and critique; recruitment and/or evaluation of participants. Suárez Castro E: review and critique; recruitment and/or evaluation of participants. Ángel Aneiros Díaz: review and critique; recruitment and/or evaluation of participants. Feal Painceiras M: review and critique. Paz González JM: review and critique. García Sancho C: review and critique. Jesús S: review and critique; recruitment and/or evaluation of participants. Mir P: review and critique; recruitment and/or evaluation of participants. Planellas LL: review and critique; recruitment and/or evaluation of participants. García Caldentey J: review and critique; recruitment and/or evaluation of participants. Caballol N: review and critique; recruitment and/or evaluation of participants. Legarda I: review and critique; recruitment and/or evaluation of participants. Hernández Vara J: review and critique; recruitment and/or evaluation of participants. González Aramburu I: review and critique; recruitment and/or evaluation of participants. Ávila Rivera MA: review and critique; recruitment and/or evaluation of participants. Catalán MJ: review and critique; recruitment and/or evaluation of participants. Víctor Nogueira: review and critique; recruitment and/or evaluation of participants. Álvarez Sauco M: review and critique; recruitment and/or evaluation of participants. Vela L: review and critique; recruitment and/or evaluation of participants. Escalante S: review and critique; recruitment and/or evaluation of participants. Cubo E: review and critique; recruitment and/or evaluation of participants. Sánchez Alonso P: review and critique; recruitment and/or evaluation of participants. Alonso Losada MG: review and critique; recruitment and/or evaluation of participants. López Ariztegui N: review and critique; recruitment and/or evaluation of participants. Martinez-Martin P: review and critique; overall supervision.

Corresponding author

Correspondence to Diego Santos-García.

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Santos-García, D., de Deus-Fonticoba, T., Suárez Castro, E. et al. The impact of freezing of gait on functional dependency in Parkinson’s disease with regard to motor phenotype. Neurol Sci 41, 2883–2892 (2020). https://doi.org/10.1007/s10072-020-04404-7

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