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December 13, 2016; 87 (24) Article

Medulla oblongata damage and cardiac autonomic dysfunction in Parkinson disease

Nadya Pyatigorskaya, Marie Mongin, Romain Valabregue, Lydia Yahia-Cherif, Claire Ewenczyk, Cyril Poupon, Eden Debellemaniere, Marie Vidailhet, Isabelle Arnulf, Stephane Lehéricy
First published November 11, 2016, DOI: https://doi.org/10.1212/WNL.0000000000003426
Nadya Pyatigorskaya
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
MD
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Marie Mongin
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Romain Valabregue
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Lydia Yahia-Cherif
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Claire Ewenczyk
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Cyril Poupon
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Eden Debellemaniere
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Marie Vidailhet
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Isabelle Arnulf
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Stephane Lehéricy
From Centre de NeuroImagerie de Recherche–CENIR (N.P., M.M., R.V., L.Y-C., I.A., S.L.), Institut du Cerveau et de la Moelle Épinière (ICM), Paris; UPMC Univ Paris 06, UMR S 1127, CNRS UMR 7225, ICM, F-75013 (N.P., M.M., R.V., L.Y-C., E.D., M.V., I.A., S.L.), Sorbonne Universités; Service de Neuroradiologie (N.P., S.L.), Clinique des Mouvements Anormaux, Département des Maladies du Système Nerveux (C.E., M.V.), INSERM, Centre d’Investigation Clinique (CIC9503), Département des Maladies du Système Nerveux (M.V.), and Service des Pathologies du Sommeil (E.D., I.A.), Assistance Publique Hôpitaux de Paris, Hôpital Pitié-Salpêtrière; and NeuroSpin (C.P.), Commissariat à l'Energie Atomique (CEA), Gif-Sur-Yvette, France.
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Citation
Medulla oblongata damage and cardiac autonomic dysfunction in Parkinson disease
Nadya Pyatigorskaya, Marie Mongin, Romain Valabregue, Lydia Yahia-Cherif, Claire Ewenczyk, Cyril Poupon, Eden Debellemaniere, Marie Vidailhet, Isabelle Arnulf, Stephane Lehéricy
Neurology Dec 2016, 87 (24) 2540-2545; DOI: 10.1212/WNL.0000000000003426

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Abstract

Objective: To characterize medulla oblongata damage using diffusion tensor imaging (DTI) in Parkinson disease (PD) and correlate it with dysfunction of the cardiac sympathetic/vagal balance.

Methods: Fifty-two patients with PD and 24 healthy controls were included in the study. All participants underwent clinical examination and 3T MRI using 3D T1-weighted imaging and DTI. DTI metrics were calculated within manually drawn regions of interest. Heart rate variability was evaluated using spectral analysis of the R–R cardiac interval during REM and slow-wave sleep based on continuous overnight electrocardiographic monitoring. Respiratory frequency was measured in 30-second contiguous epochs of REM and slow-wave sleep. The relationships between imaging and cardiac variables were calculated using partial correlations followed by the multiple comparisons permutation approach.

Results: The changes in heart rate and respiratory frequency variability from slow-wave sleep to REM sleep in healthy controls were no longer detectable in patients with PD. There were significant increases in the mean (p = 0.006), axial (p = 0.006), and radial diffusivities (p = 0.005) in the medulla oblongata of patients with PD. In PD, diffusion changes were specifically correlated with a lower heart rate and respiratory frequency variability during REM sleep.

Conclusions: This study provides evidence that medulla oblongata damage underlies cardiac sympathetic/vagal balance and respiratory dysfunction in patients with PD.

GLOSSARY

AD=
axial diffusivity;
ANOVA=
analysis of variance;
DMV=
dorsal motor nucleus of the vagus;
DTI=
diffusion tensor images;
FA=
fractional anisotropy;
HC=
healthy controls;
HF=
high-frequency components;
HFnu=
high-frequency, normalized units;
iRBD=
idiopathic REM sleep behavior disorder;
LF=
low-frequency components;
LFnu=
low-frequency, normalized units;
MD=
mean diffusivity;
NST=
nucleus of the solitary tract;
PD=
Parkinson disease;
RD=
radial diffusivity;
RF=
respiratory frequency;
ROI=
region of interest;
RVLM=
rostral ventrolateral medulla;
SWS=
slow-wave sleep;
UPDRS-III=
motor disability score of the Unified Parkinson’s Disease Rating Scale

Footnotes

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

  • Editorial, page 2506

  • Received April 10, 2016.
  • Accepted in final form August 22, 2016.
  • © 2016 American Academy of Neurology
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