Right Atrial Adaptation to Precapillary Pulmonary Hypertension: Pressure-Volume, Cardiomyocyte, and Histological Analysis.

pressure-volume loop pulmonary arterial hypertension right atrioventricular coupling right atrium right ventricle

Journal

Journal of the American College of Cardiology
ISSN: 1558-3597
Titre abrégé: J Am Coll Cardiol
Pays: United States
ID NLM: 8301365

Informations de publication

Date de publication:
22 08 2023
Historique:
received: 18 01 2023
revised: 25 05 2023
accepted: 31 05 2023
medline: 18 8 2023
pubmed: 17 8 2023
entrez: 17 8 2023
Statut: ppublish

Résumé

Precapillary pulmonary hypertension (precPH) patients have altered right atrial (RA) function and right ventricular (RV) diastolic stiffness. This study aimed to investigate RA function using pressure-volume (PV) loops, isolated cardiomyocyte, and histological analyses. RA PV loops were constructed in control subjects (n = 9) and precPH patients (n = 27) using magnetic resonance and catheterization data. RA stiffness (pressure rise during atrial filling) and right atrioventricular coupling index (RA minimal volume / RV end-diastolic volume) were compared in a larger cohort of patients with moderate (n = 39) or severe (n = 41) RV diastolic stiffness. Cardiomyocytes were isolated from RA tissue collected from control subjects (n = 6) and precPH patients (n = 9) undergoing surgery. Autopsy material was collected from control subjects (n = 6) and precPH patients (n = 4) to study RA hypertrophy, capillarization, and fibrosis. RA PV loops showed 3 RA cardiac phases (reservoir, passive emptying, and contraction) with dilatation and elevated pressure in precPH. PrecPH patients with severe RV diastolic stiffness had increased RA stiffness and worse right atrioventricular coupling index. Cardiomyocyte cross-sectional area was increased 2- to 3-fold in precPH, but active tension generated by the sarcomeres was unaltered. There was no increase in passive tension of the cardiomyocytes, but end-stage precPH showed reduced number of capillaries per mm RA PV loops show increased RA stiffness and suggest atrioventricular uncoupling in patients with severe RV diastolic stiffness. Isolated RA cardiomyocytes of precPH patients are hypertrophied, without intrinsic sarcomeric changes. In end-stage precPH, reduced capillary density is accompanied by interstitial and perivascular fibrosis.

Sections du résumé

BACKGROUND
Precapillary pulmonary hypertension (precPH) patients have altered right atrial (RA) function and right ventricular (RV) diastolic stiffness.
OBJECTIVES
This study aimed to investigate RA function using pressure-volume (PV) loops, isolated cardiomyocyte, and histological analyses.
METHODS
RA PV loops were constructed in control subjects (n = 9) and precPH patients (n = 27) using magnetic resonance and catheterization data. RA stiffness (pressure rise during atrial filling) and right atrioventricular coupling index (RA minimal volume / RV end-diastolic volume) were compared in a larger cohort of patients with moderate (n = 39) or severe (n = 41) RV diastolic stiffness. Cardiomyocytes were isolated from RA tissue collected from control subjects (n = 6) and precPH patients (n = 9) undergoing surgery. Autopsy material was collected from control subjects (n = 6) and precPH patients (n = 4) to study RA hypertrophy, capillarization, and fibrosis.
RESULTS
RA PV loops showed 3 RA cardiac phases (reservoir, passive emptying, and contraction) with dilatation and elevated pressure in precPH. PrecPH patients with severe RV diastolic stiffness had increased RA stiffness and worse right atrioventricular coupling index. Cardiomyocyte cross-sectional area was increased 2- to 3-fold in precPH, but active tension generated by the sarcomeres was unaltered. There was no increase in passive tension of the cardiomyocytes, but end-stage precPH showed reduced number of capillaries per mm
CONCLUSIONS
RA PV loops show increased RA stiffness and suggest atrioventricular uncoupling in patients with severe RV diastolic stiffness. Isolated RA cardiomyocytes of precPH patients are hypertrophied, without intrinsic sarcomeric changes. In end-stage precPH, reduced capillary density is accompanied by interstitial and perivascular fibrosis.

Identifiants

pubmed: 37587582
pii: S0735-1097(23)05978-8
doi: 10.1016/j.jacc.2023.05.063
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

704-717

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Funding Support and Author Disclosures Drs Bogaard, Vonk Noordegraaf, Goumans, and de Man were supported by the Netherlands CardioVascular Research Initiative: the Dutch Heart Foundation, Dutch Federation of University Medical Centres, the Netherlands Organisation for Health Research and Development, and the Royal Netherlands Academy of Sciences (CVON-2012-08 PHAEDRA, CVON-2018-29 PHAEDRA-IMPACT, and CVON-2017-10 Dolphin-Genesis). Drs Vonk Noordegraaf and de Man were further supported by the Netherlands Organization for Scientific Research (NWO-VICI: 918.16.610, NWO-VIDI: 917.18.338). Dr de Man was supported by a Dutch Heart Foundation Dekker senior postdoc grant (2018T059). Drs Bogaard and Vonk Noordegraaf have received research grant support from Actelion, GSK, and Ferrer (Therabel). Dr de Man has received research grant support from Janssen and BIAL. Dr Handoko has received consultancy/speaker fees from Novartis, Boehringer Ingelheim, AstraZeneca, Vifor, Bayer, MSD, and Abbott. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.

Auteurs

Jeroen N Wessels (JN)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Jessie van Wezenbeek (J)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Jari de Rover (J)

Cardiovascular and Respiratory Physiology, Faculty of Science and Technology, Technical Medical Centre, University of Twente, Enschede, the Netherlands.

Rowan Smal (R)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Aida Llucià-Valldeperas (A)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Lucas R Celant (LR)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

J Tim Marcus (JT)

Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands; Department of Radiology and Nuclear Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.

Lilian J Meijboom (LJ)

Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands; Department of Radiology and Nuclear Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.

Joanne A Groeneveldt (JA)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Frank P T Oosterveer (FPT)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Toon A Winkelman (TA)

Department of Cardiothoracic Surgery, Amsterdam UMC location University of Amsterdam, Amsterdam, the Netherlands.

Hans W M Niessen (HWM)

Department of Pathology, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.

Marie-José Goumans (MJ)

Department of Cell and Chemical Biology, Leiden UMC, Leiden, the Netherlands.

Harm Jan Bogaard (HJ)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Anton Vonk Noordegraaf (AV)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Gustav J Strijkers (GJ)

Department of Biomedical Engineering and Physics, Amsterdam UMC location University of Amsterdam, Amsterdam, the Netherlands.

M Louis Handoko (ML)

Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands; Department of Cardiology, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.

Berend E Westerhof (BE)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands.

Frances S de Man (FS)

PHEniX Laboratory, Department of Pulmonary Medicine, Amsterdam UMC location Vrije Universiteit Amsterdam, Amsterdam, the Netherlands; Pulmonary Hypertension and Thrombosis, Amsterdam Cardiovascular Sciences, Amsterdam, the Netherlands. Electronic address: fs.deman@amsterdamumc.nl.

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Classifications MeSH