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High ultrasensitive serum C-reactive protein may be related to freezing of gait in Parkinson’s disease patients

Journal of Neural Transmission volume 126, pages 1599–1608 (2019)Cite this article

Abstract

C-reactive protein (CRP) is a biomarker of systemic inflammation that has been linked to accelerated decline in walking speed in older adults. The aim of the present study was to compare the CRP levels of PD patients with vs patients without freezing of gait (FOG). Patients and controls participating in the COPPADIS-2015 study that performed blood extraction for determining molecular serum biomarkers were included. 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). Immunoassay was used for determining ultrasensitive CRP (US-CRP) level (mg/dL). In the PD group (n = 225; 61.8 ± 9.5 years old, 61.8% males), 32% of the patients presented FOG but none in the control group (n = 65; 60.3 ± 6.1 years old, 56.9% males) (p < 0.0001). Differences in US-CRP level were significant in patients with FOG vs patients without FOG and vs controls (0.31 ± 0.52 vs 0.16 ± 0.21 vs 0.21 ± 0.22; p = 0.04). Significant differences were also observed between patients with vs without FOG (p = 0.001) but not between patients and controls (p = 0.163). US-CRP level was related to FOG (OR = 4.369; 95% CI 1.105–17.275; p = 0.036) along with H&Y (OR = 2.974; 95% CI 1.113–7.943; p = 0.030) and non-motor symptoms burden (NMSS total score; OR = 1.017; 95% CI 1.005–1.029; p = 0.006) after adjusting for age, gender, disease duration, equivalent daily levodopa dose, number of non-antiparkinsonian drugs per day, motor fluctuations, cognition, motor phenotype, and chronic use of anti-inflammatory drugs. The present study suggests that serum US-CRP level is related to FOG in PD patients. Inflammation could be linked to FOG development.

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Abbreviations

BDI-II:

Beck depression inventory-II

CRP:

C-reactive protein

FOG:

Freezing of gait

FOG-Q:

Freezing of Gait Questionnaire

NMSS:

Non-motor Symptoms Scale

NPI:

Neuropsychiatric inventory

PD:

Parkinson’s disease

PD-CRS:

Parkinson’s Disease Cognitive Rating Scale

PDQ-39SI:

39-item Parkinson’s Disease Quality of Life Questionnaire Summary Index

PDSS:

Parkinson’s Disease Sleep Scale

PIGD:

Postural instability gait difficulty

QUIP-RS:

Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Rating Scale

S&E:

Schwab & England Activities of Daily Living Scale

UPDRS:

Unified Parkinson’s Disease Rating Scale

VAFS:

Visual Analog Fatigue Scale

VAS Pain:

Visual analog scale pain

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Acknowledgements

Collaborators (COPPADIS STUDY GROUP): Adarmes Astrid D, Almeria M, Alonso Losada MG, Alonso Cánovas A, Alonso Frech F, Álvarez Sauco M, Arnáiz S, Arribas S, Ascunce Vidondo A, Ávila MA, Bejr-Kasem H, Blázquez Estrada M, Botí M, Borrue C, Cabello González C, Cabo López I, Caballol N, Cámara Lorenzo A, Carrillo F, Casas E, Catalán MJ, Clavero P, Cortina Fernández A, Cubo E, Díez-Fairen M, Erro E, Estelrich Peyret E, Fernández Guillán N, Gámez P, Gallego M, García Caldentey J, García Campos C, García Moreno JM, Gastón I, 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, Kulisevsky J, Kurtis M, Labandeira C, Labrador MA, Lacruz F, Lage Castro M, Legarda I, López Ariztegui N, López Díaz LM, López Manzanares L, López Seoane B, 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, Pérez Fuertes A, Pérez Noguera R, Planellas L, Prats MA, Prieto Jurczynska C, Redondo Rafales N, Rodríguez Méndez L, Rodríguez Pérez AB, Roldán F, Ruíz De Arcos M, Ruíz Martínez J, Sánchez Alonso P, Sánchez-Carpintero M, Sánchez Díez G, Sánchez Rodríguez A, Santacruz P, Segundo Rodríguez JC, Seijo M, Serarols A, Sierra Peña M, Tartari JP, Valero C, Vargas L, Vázquez Gómez R, Vela L, Villanueva C, Vives B, 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. Aneiros Díaz A: None. Paz González JM. has received honoraria for educational presentations and/or advice service by UCB Pharma, Lundbeck, KRKA, and Zambon. Feal Panceiras MJ: None. García Sancho C: None. Jesús S. has received honoraria from Abbvie, Bial, Merz, UCB, and Zambon. She holds the competitive contract “Juan Rodés” supported by the Instituto de Salud Carlos III. Also, she has received grants from the Spanish Ministry of Economy and Competitiveness (PI18/01898) as well as 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. 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). He also received grants from 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. Aguilar M: UCB and Schwabe with assistance to a Congress; Nutricia with assistance to a Congress and payment of lecture. Pastor P: None. 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. de Fábregues-Boixar O. has received honoraria for educational presentations and advice service by Bial, Zambon, Abbvie, KRKA, and Teva. Puente V. has served as consultant for Abbvie and Zambon; has received grant/research from Abbvie. Crespo Cuevas A: None. González-Aramburu I: None. Infante J. has received travel bursaries and honoraria for educational presentations from Abbvie and Zambon. Carrillo Padilla F. has received honoraria from Zambon (SEN Congress assistance). Pueyo M. has received honoraria from Zambon for educational presentations and SEN Congress assistance and of Medtronic for course assistance. Escalante S. has received honoraria for educational presentations and advice service by Abbvie, Zambon, and Bial. Bernardo N: None. Solano B. has received honoraria for educational presentations and advice service by UCB, Zambon, Teva, Abbvie, and Bial. Cots Foraster A has received honoraria for educational presentations by UCB and Zambon, Has received financial help to Master courses (Master en Trastornos del Movimiento, Ed Viguera, 2017–2018) from UCB an Zambon. Martinez-Martin P: Honoraria: from Editorial Viguera for lecturing in courses; International Parkinson and Movement Disorder Society for management of the Program on Rating Scales; Air Liquide, Abbvie, and HM Hospitales de Madrid for advice in clinic-epidemiological studies. License fee payments for the King’s Parkinson’s Disease Pain scale.

Author information

Authors and Affiliations

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

    Diego Santos-García, J. M. Paz González, M. J. Feal Panceiras & C. García Sancho

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

    T. de Deus Fonticoba, E. Suárez Castro & A. Aneiros Díaz

  3. Hospital Universitario Virgen del Rocío, Instituto de Biomedicina de Sevilla, Universidad de Sevilla/CSIC, Seville, Spain

    S. Jesús & P. Mir

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

    S. Jesús, P. Mir, I. González-Aramburu, J. Infante & P. Martinez-Martin

  5. Hospital Universitari Mutua de Terrassa, Terrassa, Barcelona, Spain

    M. Aguilar & P. Pastor

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

    J. Hernández Vara & O. de Fábregues-Boixar

  7. Hospital del Mar, Barcelona, Spain

    V. Puente & A. Crespo Cuevas

  8. Hospital Universitario Marqués de Valdecilla, Santander, Spain

    I. González-Aramburu & J. Infante

  9. Hospital Universitario de Canarias, San Cristóbal de la Laguna, Santa Cruz de Tenerife, Spain

    F. Carrillo Padilla & M. Pueyo

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

    S. Escalante & N. Bernardo

  11. Institut d’Assistència Sanitària (IAS), Instituí Cátala de la Salud, Girona, Spain

    B. Solano & A. Cots Foraster

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

    P. Martinez-Martin

Authors
  1. Diego Santos-García
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  2. T. de Deus Fonticoba
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  3. E. Suárez Castro
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  4. A. Aneiros Díaz
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  5. J. M. Paz González
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  6. M. J. Feal Panceiras
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  7. C. García Sancho
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  8. S. Jesús
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  9. P. Mir
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  10. M. Aguilar
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  11. P. Pastor
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  12. J. Hernández Vara
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  13. O. de Fábregues-Boixar
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  14. V. Puente
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  15. A. Crespo Cuevas
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  16. I. González-Aramburu
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  17. J. Infante
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  18. F. Carrillo Padilla
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  19. M. Pueyo
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  20. S. Escalante
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  21. N. Bernardo
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  22. B. Solano
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  23. A. Cots Foraster
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  24. P. Martinez-Martin
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Consortia

on behalf of the COPPADIS Study Group

  • D. Adarmes Astrid
  • , M. Almeria
  • , M. G. Alonso Losada
  • , A. Alonso Cánovas
  • , F. Alonso Frech
  • , M. Álvarez Sauco
  • , S. Arnáiz
  • , S. Arribas
  • , A. Ascunce Vidondo
  • , M. A. Ávila
  • , H. Bejr-Kasem
  • , M. Blázquez Estrada
  • , M. Botí
  • , C. Borrue
  • , C. Cabello González
  • , I. Cabo López
  • , N. Caballol
  • , A. Cámara Lorenzo
  • , F. Carrillo
  • , E. Casas
  • , M. J. Catalán
  • , P. Clavero
  • , A. Cortina Fernández
  • , E. Cubo
  • , M. Díez-Fairen
  • , E. Erro
  • , E. Estelrich Peyret
  • , N. Fernández Guillán
  • , P. Gámez
  • , M. Gallego
  • , J. García Caldentey
  • , C. García Campos
  • , J. M. García Moreno
  • , I. Gastón
  • , M. P. Gómez Garre
  • , J. González Aloy
  • , J. González Ardura
  • , B. González García
  • , M. J. González Palmás
  • , G. R. González Toledo
  • , A. Golpe Díaz
  • , M. Grau Solá
  • , G. Guardia
  • , A. Horta-Barba
  • , J. Kulisevsky
  • , M. Kurtis
  • , C. Labandeira
  • , M. A. Labrador
  • , F. Lacruz
  • , M. Lage Castro
  • , I. Legarda
  • , N. López Ariztegui
  • , L. M. López Díaz
  • , L. López Manzanares
  • , B. López Seoane
  • , Y. Macías
  • , M. Mata
  • , G. Martí Andres
  • , M. J. Martí
  • , J. C. Martínez Castrillo
  • , D. McAfee
  • , M. T. Meitín
  • , M. Menéndez González
  • , C. Méndez del Barrio
  • , J. Miranda Santiago
  • , M. I. Morales Casado
  • , A. Moreno Diéguez
  • , V. Nogueira
  • , A. Novo Amado
  • , S. Novo Ponte
  • , C. Ordás
  • , J. Pagonabarraga
  • , I. Pareés
  • , B. Pascual-Sedano
  • , A. Pérez Fuertes
  • , R. Pérez Noguera
  • , L. Planellas
  • , M. A. Prats
  • , C. Prieto Jurczynska
  • , N. Redondo Rafales
  • , L. Rodríguez Méndez
  • , A. B. 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
  • , J. C. Segundo Rodríguez
  • , M. Seijo
  • , A. Serarols
  • , M. Sierra Peña
  • , J. P. Tartari
  • , C. Valero
  • , L. Vargas
  • , R. Vázquez Gómez
  • , L. Vela
  • , C. Villanueva
  • , B. Vives
  •  & M. D. Villar

Contributions

DSG: conception, organization, and execution of the project; statistical analysis; writing of the first draft of the manuscript; recruitment and/or evaluation of participants. DF: review and critique; recruitment and/or evaluation of participants. ESC: review and critique. AAD: review and critique. JMPG: review and critique. MJFP: review and critique. CGS: review and critique. SJ: review and critique; recruitment and/or evaluation of participants. PM: review and critique; recruitment and/or evaluation of participants. MA: review and critique; recruitment and/or evaluation of participants. PP: review and critique; recruitment and/or evaluation of participants. JHV: review and critique; recruitment and/or evaluation of participants. OFB: review and critique; recruitment and/or evaluation of participants. VP: review and critique; recruitment and/or evaluation of participants. ACC: review and critique; recruitment and/or evaluation of participants. IGA: review and critique; recruitment and/or evaluation of participants. JI: review and critique; recruitment and/or evaluation of participants. FCP: review and critique; recruitment and/or evaluation of participants. MP: review and critique; recruitment and/or evaluation of participants. SE: review and critique; recruitment and/or evaluation of participants. NB: review and critique; recruitment and/or evaluation of participants. BS: review and critique; recruitment and/or evaluation of participants. ACF: review and critique; recruitment and/or evaluation of participants. PMM: 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. High ultrasensitive serum C-reactive protein may be related to freezing of gait in Parkinson’s disease patients. J Neural Transm 126, 1599–1608 (2019). https://doi.org/10.1007/s00702-019-02096-8

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Keywords

  • C-Reactive protein
  • Freezing
  • Inflammation
  • Gait
  • Parkinson’s disease