Skip to main content

Main menu

  • Home
  • Current issue
  • Authors/reviewers
    • Instructions for authors
    • Submit a manuscript
    • COVID-19 submission information
    • Institutional open access agreements
    • Peer reviewer login
  • Alerts
  • Subscriptions
  • ERS Publications
    • European Respiratory Journal
    • ERJ Open Research
    • European Respiratory Review
    • Breathe
    • ERS Books
    • ERS publications home

User menu

  • Log in
  • Subscribe
  • Contact Us
  • My Cart

Search

  • Advanced search
  • ERS Publications
    • European Respiratory Journal
    • ERJ Open Research
    • European Respiratory Review
    • Breathe
    • ERS Books
    • ERS publications home

Login

European Respiratory Society

Advanced Search

  • Home
  • Current issue
  • Authors/reviewers
    • Instructions for authors
    • Submit a manuscript
    • COVID-19 submission information
    • Institutional open access agreements
    • Peer reviewer login
  • Alerts
  • Subscriptions

Cardiac consequences of intermittent hypoxia: a matter of dose? A systematic review and meta-analysis in rodents

Elise Belaidi, Charles Khouri, Olfa Harki, Sébastien Baillieul, Gilles Faury, Anne Briançon-Marjollet, Jean-Louis Pépin, Claire Arnaud
European Respiratory Review 2022 31: 210269; DOI: 10.1183/16000617.0269-2021
Elise Belaidi
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
3These authors contributed equally to this work
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: elise.belaidi-corsat@univ-grenoble-alpes.fr
Charles Khouri
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
2Pharmacovigilance Unit and Clinical Pharmacology Dept, Grenoble Alpes University Hospital, Grenoble, France
3These authors contributed equally to this work
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Charles Khouri
Olfa Harki
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sébastien Baillieul
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gilles Faury
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Anne Briançon-Marjollet
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Anne Briançon-Marjollet
Jean-Louis Pépin
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Claire Arnaud
1Univ. Grenoble Alpes, INSERM, CHU Grenoble Alpes, HP2, Grenoble, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Claire Arnaud
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Figures

  • Tables
  • Supplementary Materials
  • FIGURE 1
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 1

    Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) study flowchart.

  • FIGURE 2
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 2

    Characteristics of intermittent hypoxia (IH) protocols. NR: not reported.

  • FIGURE 3
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 3

    Risk of bias assessment according to the SYstematic Review Center for Laboratory animal Experimentation (SYRCLE) (overall score).

  • FIGURE 4
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 4

    Orchard plots of the effect of intermittent hypoxia (IH) on a) mean arterial blood pressure (MAP); b) heart rate (HR); and c) ejection fraction (EF). Data were extracted in IH and control groups from primary studies and expressed as standardised mean differences. The pooled estimate (yellow) indicates an increase in MAP and HR and a reduction in EF upon IH exposure compared to control normoxic groups.

  • FIGURE 5
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 5

    Orchard plots of the effect of intermittent hypoxia (IH) on cardiac remodelling. a) cardiac dimensions; b) fibrosis and c) apoptosis. Data were extracted in IH and control groups from primary studies and expressed as standardised mean differences. The pooled estimate (yellow) indicates that IH induces an overall cardiac hypertrophy (HW_TL: heart weight to tibia length; CSA: cross-sectional area) and dilation (LVDd: left ventricular diameter in diastole), associated with increased perivascular (PVF) and interstitial fibrosis (IF) and apoptosis (Casp3: caspase 3). CTGF: connective tissue growth factor; TUNEL: terminal deoxynucleotidyl transferase dUTP nick end labelling.

  • FIGURE 6
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 6

    Impact of intermittent hypoxia (IH) on myocardial infarct size. a) Orchard plot indicates a high heterogeneity of IH response to ischaemia and reveals two distinct groups, one exhibiting a reduction in infarct size and the other an increase. Data were extracted in IH and control groups from primary studies and expressed as standardised mean differences (SMDs). Univariate analysis demonstrated that b) inspired oxygen fraction (FIO2) and c) IH duration per day were key parameters influencing myocardial infarct size.

  • FIGURE 7
    • Download figure
    • Open in new tab
    • Download powerpoint
    FIGURE 7

    Impact of intermittent hypoxia (IH) on cardiac function, structure and response to ischaemia–reperfusion. a) Deleterious effect of IH characterised by a decrease in left ventricle (LV) ejection fraction, an increase in diastolic left ventricular diameter (LVDd), as well as hypertrophy, fibrosis and apoptosis. b) Dual effect of IH on infarct size following ischaemia–reperfusion depending on FIO2 severity and IH duration per day. FIO2: inspired oxygen fraction.

Tables

  • Figures
  • Supplementary Materials
  • TABLE 1

    Study characteristics

    Animal characteristicsIH protocol characteristicsHaemodynamic parameterCardiac functionCardiac remodellingResponse to ischaemia
    Article#SpeciesStrainSexBody weight (g)Age (weeks)FIO2 (%)Hypoxia/Reox (s)IH duration (h per day)Protocol duration (day)MAPHREjection fractionStructureHypertrophyFibrosisApoptosisInfarct size
    LVDdHW/TLCSAPVFIFCasp3TUNEL
    Bao et al. 2020 [S1]MiceC57Bl6JMnd9530/301228xxxxx
    Béguin et al. 2005 [S2]RatWistarM350nd5–1040/200.5–4.01x
    Béguin et al. 2007 [S3]RatWistarM350nd1040/2041x
    Belaidi et al. 2008 [S4]RatWistarM340nd1040/2041x
    Belaidi et al. 2009 [S5]RatSHR and WKYMnd9540/20814xx
    Belaidi et al. 2016 [S6]MiceS129 and C57Bl6JMnd8530/30814x
    Bober et al. 2018 [S7]RatSDM340nd6.580/12087
    Bourdier et al. 2016 [S8]RatWistarM3258530/30821xxxx
    Cai et al. 2003 [S9]MicendM25nd6360/36011x
    Castro-Grattoni et al. 2016 [S10]MiceC57Bl6JMnd6520/40642xx
    Castro-Grattoni et al. 2019 [S11]MiceC57Bl6JFnd8–72520/40656x
    Chen et al. 2005 [S12]RatSDM250nd530/30835xxxx
    Chen et al. 2008 [S13]RatSDM185nd520/100842xxxx
    Chen et al. 2010 [S14]MiceC57Bl6JMnd264.5451056xxxxxxx
    Chen et al. 2011 [S15]RatSDM2909430/45612x
    Chen et al. 2011 [S16]RatWKY and SHRM2559430/45610–30x
    Chen et al. 2015 [S17]RatSDM3259630/45612xx
    Chen et al. 2016 [S18]RatSDMnd9430/45814xx
    Chen et al. 2016 [S19]RatSDMnd16430/45814x
    Del Rio et al. 2016 [S20]RatSDM250nd5nd828xxx
    Détrait et al. 2020 [S21]MiceC57Bl6JMnd19530/30828–42xxxxxx
    Ding et al. 2014 [S22]RatWistarM21585.560/60835xxxxx
    Ding et al. 2014 [S23]RatWistarMnd85.520/100nd35x
    Du et al. 2019 [S24]MiceC57Bl6JMnd45.5120/601256x
    Farré et al. 2018 [S25]MiceC57Bl6Jndnd8–72620/40642
    Fu et al. 2016 [S26]RatSDM22594.5120/120nd21–56xxx
    Guan et al. 2019 [S27]RatSDM205nd915/90835xxxx
    Guo et al. 2015 [S28]RatWistarM21087120/12087–28x
    Han et al. 2014 [S29]RatSDM151nd10240/120614–28x
    Han et al. 2018 [S30]RatSDM165nd10240/120842xxxxx
    Hayashi et al. 2008 [S31]MiceC57Bl6JMnd10530/30810xxxx
    Hayashi et al. 2011 [S32]MiceC57Bl6JMnd8560/6087xx
    Imano et al. 2018 [S33]MiceC57Bl6JMnd8590/300828xxxx
    Inamoto et al. 2010 [S34]MiceC57Bl6JMnd8530/30810x
    Jiang et al. 2020 [S35]RatSDM225nd590/90828xxx
    Joyeux-Faure et al. 2005 [S36]RatWistarM230nd540/20835xx
    Lai et al. 2015 [S37]MiceC57Bl6Jndnd22760/60856xxx
    Lai et al. 2015 [S38]MiceC57Bl6JMnd22760/60856xxxx
    Li et al. 2016 [S39]RatWistarMnd16530/90828x
    Li et al. 2017 [S40]RatSDM225nd9240/350842xxx
    Lu et al. 2020 [S41]RatSDM20067.590/90842x
    Lucking et al. 2014 [S42]RatWistarM225nd590/210814xxx
    Ma et al. 2020 [S43]RatSDM19088210/90642xxxx
    Maeda et al. 2013 [S44]RatSDMnd74nd821x
    Matsumoto et al. 2009 [S45]MiceC57Bl6JMnd10530/30810x
    Milano et al. 2013 [S46]MiceC57Bl6JMnd97180/1201.714x
    Morand et al. 2018 [S47]RatWistarM3408530/30814xx
    Moreau et al. 2015 [S48]RatSDMndnd6.580/12087–95xx
    Moulin et al. 2020 [S49]MiceSwiss×S129Mndnd530/30821xx
    Moulin et al. 2020 [S50]MiceSwiss×S129Mnd10530/30821xx
    Naghshin et al. 2009 [S51]MiceC57Bl6JM2311530/301228xxx
    Naghshin et al. 2012 [S52]MiceFVBMnd115.530/301228xx
    Nakagawa et al. 2019 [S53]MicendMndnd560/300814
    Nishioka et al. 2013 [S54]MiceC57Bl6JMnd8530/30810xx
    Pai et al. 2016 [S55]RatSDMnd20540/40828xxxx
    Park et al. 2007 [S56]MiceC57Bl6JMnd106120/12087–28xxx
    Ramirez et al. 2012 [S57]RatSDMndnd10180/18087xx
    Ramond et al. 2007 [S58]RatWistarM300nd540/2041x
    Ramond et al. 2013 [S59]RatWistarM300nd530/30814xx
    Ray et al. 2015 [S60]RatWistarMndnd590/330814xxx
    Rodriguez et al. 2014 [S61]MiceC57Bl6J and ob/obMnd105.530/301228xx
    Sun et al. 2020 [S62]RatSDM220nd915/30835xx
    Tao et al. 2019 [S63]MiceC57Bl6JMnd8530/30828xxxx
    Tong et al. 2019 [S64]MiceC57Bl6JM226520/40813x
    Totoson et al. 2013 [S65]RatWistarM290nd530/30814–28x
    Wang et al. 2013 [S66]RatWistarM250nd7.630/3041–28xx
    Wang et al. 2017 [S67]RatSDnd260nd990/90821
    Wang et al. 2017 [S68]RatSDM200nd990/90821xx
    Wang et al. 2018 [S69]MiceC57Bl6JM23nd5.560/60884x
    Wang et al. 2018 [S70]RatSDM2259890/210528xxx
    Wang et al. 2020 [S71]MiceC57Bl6JMnd8820/401256xxxx
    Wei et al. 2017 [S72]RatSDM250107.630/30835xx
    Williams et al. 2010 [S73]RatSDM180nd530/30810xxx
    Xie et al. 2015 [S74]RatSDM200nd8240/350842xxx
    Xu et al. 2015 [S75]RatSDM200nd8.510/80835x
    Yang et al. 2011 [S76]MiceC57Bl6J and ob/obMnd10530/301228xxx
    Yang et al. 2018 [S77]RatSDM20086120842xxxx
    Yang et al. 2019 [S78]RatSDM2009680/40842
    Yeung et al. 2015 [S79]RatSDM704515/45828xx
    Yin et al. 2014 [S80]MiceFVB and 129S1Mnd9820/100127–56xxx
    Yuan et al. 2014 [S81]RatWistarM200nd530/30842
    Yuan et al. 2015 [S82]RatSDM235nd8240/350842x
    Zhang et al. 2018 [S83]RatSDM300nd8nd630xxx
    Zhang et al. 2017 [S84]MiceC57Bl6JM226520/40884xxx
    Zhang et al. 2018 [S85]RatSDMndnd8nd630xx
    Zhang et al. 2018 [S86]RatSDMndnd8nd630xxx
    Zhao et al. 2019 [S87]RatSDM205nd990/90835xx
    Zhou et al. 2014 [S88]Mice129S1 and FVBMnd9860/60nd21–28xx
    Zhou et al. 2017 [S89]MiceC57Bl6J and FVBMndnd820/100123–28xx
    Zhou et al. 2018 [S90]Mice129s1 and C57Bl6Jndndnd830/301228xxx
    Zhou et al. 2018 [S91]RatSDM165nd4.530/60821xxxx
    Zhu et al. 2020 [S92]RatSDM190nd1030/60835x

    #: For full details of the studies included in the meta-analysis see supplementary file S3, references listed in this table refer to this file. Casp3: caspase 3; CSA: cross-sectional area; F: female; FIO2: inspired oxygen fraction (in percentage); HR: heart rate; Hypoxia/Reox (s): duration of hypoxia and reoxygenation (in seconds); HW/TL: heart weight to tibia length ratio; IF: interstitial fibrosis; IH: intermittent hypoxia; LVDd: left ventricular diameter in diastole; M: male; MAP: mean arterial pressure; nd: no data; PVF: perivascular fibrosis; SD: Sprague–Dawley; SHR: spontaneously hypertensive rat; TUNEL: terminal deoxynucleotidyl transferase dUTP nick end labelling; WKY: Wistar Kyoto.

    Supplementary Materials

    • Figures
    • Tables
    • Supplementary Material

      Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

      Supplementary material ERR-0269-2021.SUPPLEMENT

    PreviousNext
    Back to top
    View this article with LENS
    Vol 31 Issue 164 Table of Contents
    European Respiratory Review: 31 (164)
    • Table of Contents
    • Index by author
    Email

    Thank you for your interest in spreading the word on European Respiratory Society .

    NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

    Enter multiple addresses on separate lines or separate them with commas.
    Cardiac consequences of intermittent hypoxia: a matter of dose? A systematic review and meta-analysis in rodents
    (Your Name) has sent you a message from European Respiratory Society
    (Your Name) thought you would like to see the European Respiratory Society web site.
    CAPTCHA
    This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
    Print
    Citation Tools
    Cardiac consequences of intermittent hypoxia: a matter of dose? A systematic review and meta-analysis in rodents
    Elise Belaidi, Charles Khouri, Olfa Harki, Sébastien Baillieul, Gilles Faury, Anne Briançon-Marjollet, Jean-Louis Pépin, Claire Arnaud
    European Respiratory Review Jun 2022, 31 (164) 210269; DOI: 10.1183/16000617.0269-2021

    Citation Manager Formats

    • BibTeX
    • Bookends
    • EasyBib
    • EndNote (tagged)
    • EndNote 8 (xml)
    • Medlars
    • Mendeley
    • Papers
    • RefWorks Tagged
    • Ref Manager
    • RIS
    • Zotero

    Share
    Cardiac consequences of intermittent hypoxia: a matter of dose? A systematic review and meta-analysis in rodents
    Elise Belaidi, Charles Khouri, Olfa Harki, Sébastien Baillieul, Gilles Faury, Anne Briançon-Marjollet, Jean-Louis Pépin, Claire Arnaud
    European Respiratory Review Jun 2022, 31 (164) 210269; DOI: 10.1183/16000617.0269-2021
    del.icio.us logo Digg logo Reddit logo Technorati logo Twitter logo CiteULike logo Connotea logo Facebook logo Google logo Mendeley logo
    Full Text (PDF)

    Jump To

    • Article
      • Abstract
      • Abstract
      • Introduction
      • Methods
      • Results
      • Discussion
      • Conclusion
      • Supplementary material
      • Acknowledgements
      • Footnotes
      • References
    • Figures & Data
    • Info & Metrics
    • PDF

    Subjects

    • Lung biology and experimental studies
    • Tweet Widget
    • Facebook Like
    • Google Plus One

    More in this TOC Section

    • TLR-agonist-based therapies for respiratory viral diseases
    • Impact of LAMAs on mucus hypersecretion and cough in COPD
    • Bidirectional relationships of comorbidity with OSA
    Show more Reviews

    Related Articles

    Navigate

    • Home
    • Current issue

    About the ERR

    • Journal information
    • Editorial board
    • Reviewers
    • Press
    • Permissions and reprints
    • Advertising
    • Sponsorship

    The European Respiratory Society

    • Society home
    • myERS
    • Privacy policy
    • Accessibility

    ERS publications

    • European Respiratory Journal
    • ERJ Open Research
    • European Respiratory Review
    • Breathe
    • ERS books online
    • ERS Bookshop

    Help

    • Feedback

    For authors

    • Instructions for authors
    • Publication ethics and malpractice
    • Submit a manuscript

    For readers

    • Alerts
    • Subjects
    • RSS

    Subscriptions

    • Accessing the ERS publications

    Contact us

    European Respiratory Society
    442 Glossop Road
    Sheffield S10 2PX
    United Kingdom
    Tel: +44 114 2672860
    Email: journals@ersnet.org

    ISSN

    Print ISSN: 0905-9180
    Online ISSN: 1600-0617

    Copyright © 2022 by the European Respiratory Society