Skip to main content

Main menu

  • Home
  • Current issue
  • ERJ Early View
  • Past issues
  • ERS Guidelines
  • Authors/reviewers
    • Instructions for authors
    • Submit a manuscript
    • Open access
    • 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
  • ERJ Early View
  • Past issues
  • ERS Guidelines
  • Authors/reviewers
    • Instructions for authors
    • Submit a manuscript
    • Open access
    • Peer reviewer login
  • Alerts
  • Subscriptions

Arterial vascular volume changes with haemodynamics in schistosomiasis-associated pulmonary arterial hypertension

Farbod N. Rahaghi, Joan F. Hilton, Ricardo A. Corrêa, Camila Loureiro, Jaquelina S. Ota-Arakaki, Carlos G.Y. Verrastro, Michael H. Lee, Claudia Mickael, Pietro Nardelli, David A. Systrom, Aaron B. Waxman, George R. Washko, Raúl San José Estépar, Brian B. Graham, Rudolf K.F. Oliveira
European Respiratory Journal 2021 57: 2003914; DOI: 10.1183/13993003.03914-2020
Farbod N. Rahaghi
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joan F. Hilton
2Dept of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ricardo A. Corrêa
3Internal Medicine/Pulmonary Division, Medical School, Federal University of Minas Gerais, Belo Horizonte, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Camila Loureiro
4Pulmonary Medicine, Santa Casa Hospital, Salvador, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jaquelina S. Ota-Arakaki
5Division of Respiratory Diseases, Dept of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Jaquelina S. Ota-Arakaki
Carlos G.Y. Verrastro
6Radiology Dept, Federal University of Sao Paulo (UNIFESP), São Paulo, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Michael H. Lee
7Pulmonary Sciences and Critical Care Medicine, University of California San Francisco, San Francisco, CA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Michael H. Lee
Claudia Mickael
8Pulmonary Sciences and Critical Care Medicine, University of Colorado Anschutz medical campus, Aurora, CO, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Pietro Nardelli
9Applied Chest Imaging Laboratory, Dept of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
David A. Systrom
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Aaron B. Waxman
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
George R. Washko
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Raúl San José Estépar
9Applied Chest Imaging Laboratory, Dept of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Raúl San José Estépar
Brian B. Graham
7Pulmonary Sciences and Critical Care Medicine, University of California San Francisco, San Francisco, CA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Brian B. Graham
Rudolf K.F. Oliveira
5Division of Respiratory Diseases, Dept of Medicine, Federal University of São Paulo (UNIFESP), São Paulo, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Rudolf K.F. Oliveira
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Abstract

Relative loss of vascular volume in small vessels compared to total vascular volume is a marker of pulmonary arterial hypertension in schistosomiasis and is correlated with pulmonary vascular remodelling by haemodynamics https://bit.ly/3bfIlAQ

To the Editor:

Schistosomiasis is a prevalent cause of pulmonary arterial hypertension (PAH), currently classified as group 1 pulmonary hypertension (PH) [1]. In comparison to other aetiologies of PAH, such as idiopathic PAH, schistosomiasis-associated PAH (Sch-PAH) has not been extensively studied. Potential mechanisms of PAH development in schistosomiasis include systemic and localised lung inflammation, involvement of other organs, such as the liver and spleen, and direct blockage of precapillary vessels from parasite egg embolisation. Currently, the diagnosis of Sch-PAH relies on haemodynamic assessment using right heart catheterisation. In several aetiologies of PH, loss of visualised distal vascular volume has been quantified from pulmonary angiography [2, 3] and computed tomography (CT) of the lungs [4–6]. Additionally, loss of distal vascular volume has been shown to be associated with loss of vascular cross-sectional area histologically [7]. In this pilot study, we hypothesised that relative loss of arterial pulmonary vascular volume differentially correlates with haemodynamics in Sch-PAH patients, compared to a group of control subjects.

12 patients with Sch-PAH who had thin-slice chest CT were retrospectively identified at three PH centres where schistosomiasis is prevalent (Federal University of São Paulo, São Paulo, Brazil; Federal University of Minas Gerais, Belo Horizonte, Brazil; Santa Casa of Salvador, Bahia, Brazil). The diagnosis of Sch-PAH was established by: 1) significant exposure to an endemic region, history of treatment for schistosomiasis, or history of presence of Schistosoma mansoni eggs on stool examination or rectal biopsy; 2) presence of hepatosplenic disease on imaging (periportal fibrosis, or enlargement of the left lobe of the liver); 3) no other apparent cause of group 1 PAH; and 4) PAH haemodynamic criteria, including mean pulmonary arterial pressure (mPAP) ≥25 mmHg, pulmonary arterial wedge pressure (PAWP) ≤15 mmHg, and pulmonary vascular resistance (PVR) ≥3 Wood units (WU) (observed ranges: mPAP, 36–86 mmHg; PAWP, 4–15 mmHg; and PVR, 5.7–36.8 WU). 17 control subjects with thin-slice chest CT were identified from a cohort of patients who previously underwent invasive cardiopulmonary exercise testing (CPET) [8] for dyspnoea at Brigham and Women's Hospital (Boston, MA, USA) and were found to have no evidence of PH (observed ranges: mPAP, 9–21 mmHg; PAWP, 7–14 mmHg; PVR, 0.2–2.1 WU) and a normal physiological limit to exercise (IRB#2018P000419).

Automated vascular reconstructions and computation of the vascular volumes by cross-sectional area were performed using the Chest Imaging Platform (www.chestimagingplatform) [9], with the separation of the arteries and veins performed using a convolutional neural network algorithm [10]. All vascular volumes reported were normalised by lung volume (yielding a unitless index representing millilitres of vessel volume per litre of lung volume). We focused on the fraction of blood volume in arteries of area <5 mm2 (“small vessel volume”) relative to total arterial volume, termed arterial small vessel fraction (arterial BV5%), in relation to log(PVR index). Data are represented as median with interquartile range by group (compared using Wilcoxon rank-sum test) with the exception of gender, reported as percentage (p-value from Fisher's exact test). Analyses were conducted using SAS version 9.4 (Cary, NC, USA).

The Sch-PAH group was similar in age to the control group (54 (46–59) versus 52 (44–71) years; p=0.63) but included fewer women (58% versus 88%; p=0.09). In addition to higher mPAP and PVR, and similar PAWP, subjects with Sch-PAH had higher pulmonary vascular stiffness (1.8 (1.1–2.6) versus 0.3 (0.3–0.4) mmHg·mL−1; p=0.0001), lower pulmonary arterial compliance (PAC) (1.0 (0.59–1.73) versus 5.5 (4.1–6.6) mL·mmHg−1; p=0.0001) and lower stroke volume (SV) index (25.4 (21.0–38.6) versus 42.3 (35.8–51.9) mL·m−2; p=0.005) compared to controls. The subgroup of Sch-PAH who underwent CPET (n=6) had a reduced peak oxygen consumption compared to controls (62 (49–69) versus 101 (91–106)% predicted; p=0.003). Pairwise correlations among the haemodynamic metrics stratified by group showed that log(PVR index) was more strongly correlated with log(PAC) and SV index within the Sch-PAH group (R=0.85 and 0.87, respectively) than among controls (R=−0.54 and −0.12, respectively).

The pulmonary vasculature was reconstructed from the chest CT scans, with an example from each group shown in figure 1. There was no statistically significant difference between whole lung volume (3.5 (2.6–4.6) versus 4.0 (2.2–4.7) L; p=0.62) or total arterial volume (28.0 (26.9–36.1) versus 29.5 (24.6–38.3); p=0.42) between Sch-PAH and control groups. However, there was significantly lower arterial small vessel volume (10.7 (9.0–12.6) versus 16.6 (15.2–19.0); p<0.0001) in the Sch-PAH cohort, compensated for by higher large vessel volume (18.1 (13.9–26.2) versus 11.7 (7.9–19.9); p=0.03), as shown in figure 1. We quantified this shift of volume from small to large vessels by the arterial small vessel fraction (arterial BV5%), with the median percentage being 35% in Sch-PAH compared to 60% in controls (p=0.0003).

FIGURE 1
  • Download figure
  • Open in new tab
  • Download powerpoint
FIGURE 1

a) Representative vascular reconstructions from a control subject (left; subject ranked eighth amongst controls based on arterial BV5%) and a patient with schistosomiasis-associated pulmonary arterial hypertension (Sch-PAH) (right, subject ranked seventh amongst Sch-PAH patients based on arterial BV5%) showing comparative loss of distal small vessels and dilation of proximal vessels. b) Relative distribution of arterial small vessel volume (top) and arterial large vessel volume (bottom) showing a decrease in arterial small vessel volume (defined as volume in vessels with cross sectional area ≤5 mm2) and an increase in arterial large vessel volume (defined as volume in vessels with cross sectional area >5 mm2) in patients with Sch-PAH. c) The graph shows each subject's arterial small-vessel fraction (arterial BV5%; defined as arterial small vessel volume divided by total vascular volume) in relation to their log(PVR index), with subjects ranked by group and by arterial BV5%. Arterial BV5% is negatively correlated with log(PVR index) in the Sch-PAH group, showing that loss of small arterial vessel volume relates to greater pulmonary vascular resistance (PVR) (Spearman's correlation, ρ=−0.50). There is no evidence of this link in the control group, where the correlation is positive and weaker (ρ=0.31).

We additionally plotted each individual's arterial BV5% in relation to their log(PVR index) (figure 1). In general, the arterial BV5% was negatively associated with log(PVR index) among Sch-PAH patients (Spearman's correlation, ρ=−0.50) and positively associated among controls (ρ=0.31). Arterial BV5% values were nearly distinct between groups: three Sch-PAH patients had arterial BV5% >42% and only one control had arterial BV5% <42%.

To further quantify the association of arterial small-vessel fraction with log(PVR index), we modelled arterial BV5% as a function of log(PVR index), group, and their interaction using a generalised linear model with log-binomial inference. Per 1-point increase in log(PVR index), the arterial small-vessel fraction declined 0.72-fold (95% CI 0.50 to 1.03) among Sch-PAH patients (e.g. as log(PVR index) increased from 7 to 8, arterial BV5% decreased by a factor of 0.72=28%/39%) but rose 1.13-fold (95% CI 0.95 to 1.34) among controls (e.g. as log(PVR index) increased from 4 to 5, arterial BV5% increased by a factor of 1.13=56%/49%). Comparison of the relative effects between groups identified a clinically and statistically significant greater reduction in arterial BV5% per 1-point increase in log(PVR index) among Sch-PAH patients compared with controls: 0.64 (95% CI 0.43 to 0.94; p=0.026), where 0.64=0.72/1.13.

Relating haemodynamics to the physical pulmonary vascular structure, quantified by CT imaging of the lungs, extends our understanding of Sch-PAH disease. The current findings support the hypothesis that pulmonary vascular remodelling severity, as measured by higher PVR index in Sch-PAH, reflects arterial small vessel loss. Insofar as blood gas exchange occurs in the small arterial vessels of the lungs, this loss helps to explain the devastating experience of PAH progression. Our evidence suggests that Sch-PAH-related loss of distal arterial volume may be due to blood volume shifting from smaller to larger vessels and/or to narrowing of the distal arterial lumen. Proximal dilation of the pulmonary arteries has been observed in other forms of PH [4, 11] and may be an adaptation to higher pressure. In Sch-PAH, previously described [12] arterial aneurysmal dilation may also play a role, which may result from more focal extreme dilations of the spatially uniform proximal dilation we observed. While obstruction of the arterial lumen by Schistosoma eggs has been reported, PH persistence despite effective anthelmintic treatment (as was the case in the Sch-PAH cohort) and modern autopsy studies finding Schistosoma eggs absent from the lungs [13] make it unlikely that egg obstruction is causing the observed decrease in arterial small vessel volume. Rather, it is more likely that a persisting inflammatory response cascade, or the persisting effect of the initial vascular injury, lead to progression of arterial remodelling and development of PAH [14]. The relatively small size of the eggs (short axis diameter 50 µm) is below the resolution of conventional CT imaging (0.5–1 mm), and none of the patients in this study had active infection. To further explore this question, our future studies will compare other biomarkers in conjunction with imaging, as well Sch-PAH to other aetiologies of PAH.

This study is limited by the retrospective nature of the data collection, small sample sizes, limitations inherent to CT imaging resolution, and variations in image acquisition between different sites. Nonetheless, this is the first study, to our knowledge, characterising the pulmonary vascular structure in Sch-PAH, adding to the framework of our understanding of Sch-PAH pathophysiology.

In conclusion, the current pilot study findings suggest that arterial small vessel volume is reduced and inversely associated with PVR index in Sch-PAH. Validation of these methods involving larger prospective cohorts is necessary to evaluate their potential for non-invasive screening, diagnosis, and monitoring in Sch-PAH.

Shareable PDF

Supplementary Material

This one-page PDF can be shared freely online.

Shareable PDF ERJ-03914-2020.Shareable

Footnotes

  • Conflict of interest: F.N. Rahaghi reports grants from NHLBI/NIH, during the conduct of the study.

  • Conflict of interest: J.F. Hilton has nothing to disclose.

  • Conflict of interest: R.A. Corrêa has nothing to disclose.

  • Conflict of interest: C. Loureiro has nothing to disclose.

  • Conflict of interest: J.S. Ota-Arakaki has nothing to disclose.

  • Conflict of interest: C.G.Y. Verrastro has nothing to disclose.

  • Conflict of interest: M.H. Lee owns shares in NANO X IMAGING LTD (NNOX), outside the submitted work.

  • Conflict of interest: C. Mickael has nothing to disclose.

  • Conflict of interest: P. Nardelli has nothing to disclose.

  • Conflict of interest: D.A. Systrom has nothing to disclose.

  • Conflict of interest: A.B. Waxman has nothing to disclose.

  • Conflict of interest: G.R. Washko reports grants from NIH, grants and other (consultant, advisory board member) from Boehringer Ingelheim, other (founder and co-owner) from Quantitative Imaging Solutions, other (consulting, data monitoring committee) from PulmonX, grants and other (consultant) from Janssen Pharmaceuticals, other (consultant) from GlaxoSmithKline and Novartis, other (consultant, advisory board member) from Vertex and CSL Behring, outside the submitted work; and G.R. Washko's spouse works for Biogen.

  • Conflict of interest: R. San José Estépar reports grants from NIH-NHLBI, during the conduct of the study; personal fees from LeukoLabs and Chiesi, grants and personal fees from Boehringer Ingelheim, outside the submitted work; and is also a founder and co-owner of Quantitative Imaging Solutions, which is a company that provides image based consulting and develops software to enable data sharing.

  • Conflict of interest: B.B. Graham reports grants from NIH, during the conduct of the study.

  • Conflict of interest: R.K.F. Oliveira has nothing to disclose.

  • Support statement: This study was supported in part by NHLBI grants 1K23HL136905 (F.N. Rahaghi) 5R01HL116473-08 (R. San José Estépar and G.R. Washko), 1R01HL149877-01 (R. San José Estépar) and P01HL152961 (B.B. Graham). Funding information for this article has been deposited with the Crossref Funder Registry.

  • Received October 20, 2020.
  • Accepted December 19, 2020.
  • Copyright ©The authors 2021. For reproduction rights and permissions contact permissions{at}ersnet.org
https://www.ersjournals.com/user-licence

References

  1. ↵
    1. Simonneau G,
    2. Montani D,
    3. Celermajer DS, et al.
    Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J 2019; 53: 1801913. doi:10.1183/13993003.01913-2018
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Reid L
    . The angiogram and pulmonary artery structure and branching (in the normal and with reference to disease). Proc R Soc Med 1965; 58: 681–684.
    OpenUrlPubMed
  3. ↵
    1. Boxt LM,
    2. Katz J,
    3. Liebovitch LS, et al.
    Fractal analysis of pulmonary arteries: the fractal dimension is lower in pulmonary hypertension. J Thorac Imaging 1994; 9: 8–13. doi:10.1097/00005382-199424000-00002
    OpenUrlPubMed
  4. ↵
    1. Rahaghi FN,
    2. Ross JC,
    3. Agarwal M, et al.
    Pulmonary vascular morphology as an imaging biomarker in chronic thromboembolic pulmonary hypertension. Pulm Circ 2016; 6: 70–81. doi:10.1086/685081
    OpenUrl
    1. Moledina S,
    2. de Bruyn A,
    3. Schievano S, et al.
    Fractal branching quantifies vascular changes and predicts survival in pulmonary hypertension: a proof of principle study. Heart 2011; 97: 1245–1249. doi:10.1136/hrt.2010.214130
    OpenUrlAbstract/FREE Full Text
  5. ↵
    1. Matsuoka S,
    2. Washko GR,
    3. Yamashiro T, et al.
    Pulmonary hypertension and computed tomography measurement of small pulmonary vessels in severe emphysema. Am J Respir Crit Care Med 2010; 181: 218–225. doi:10.1164/rccm.200908-1189OC
    OpenUrlCrossRefPubMed
  6. ↵
    1. Rahaghi FN,
    2. Argemi G,
    3. Nardelli P, et al.
    Pulmonary vascular density: comparison of findings on computed tomography imaging with histology. Eur Respir J 2019; 54: 1900370. doi:10.1183/13993003.00370-2019
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. Oliveira RK,
    2. Agarwal M,
    3. Tracy JA, et al.
    Age-related upper limits of normal for maximum upright exercise pulmonary haemodynamics. Eur Respir J 2016; 47: 1179–1188. doi:10.1183/13993003.01307-2015
    OpenUrlAbstract/FREE Full Text
  8. ↵
    1. San Jose Estepar R,
    2. Ross JC,
    3. Harmouche R, et al.
    Chest imaging platform: an open-source library and workstation for quantitative chest imaging. Am J Respir Crit Care Med 2015; 191: A4975.
    OpenUrl
  9. ↵
    1. Nardelli P,
    2. Jimenez-Carretero D,
    3. Bermejo-Pelaez D, et al.
    Pulmonary artery-vein classification in CT images using deep learning. IEEE Trans Med Imaging 2018; 37: 2428–2440. doi:10.1109/TMI.2018.2833385
    OpenUrl
  10. ↵
    1. Rahaghi FN,
    2. Wells JM,
    3. Come CE, et al.
    Arterial and venous pulmonary vascular morphology and their relationship to findings in cardiac magnetic resonance imaging in smokers. J Comput Assist Tomogr 2016; 40: 948–952. doi:10.1097/RCT.0000000000000465
    OpenUrl
  11. ↵
    1. Butrous G
    . Schistosome infection and its effect on pulmonary circulation. Glob Cardiol Sci Pract 2019; 2019: 5.
    OpenUrl
  12. ↵
    1. Graham BB,
    2. Chabon J,
    3. Bandeira A, et al.
    Significant intrapulmonary Schistosoma egg antigens are not present in schistosomiasis-associated pulmonary hypertension. Pulm Circ 2011; 1: 456–461. doi:10.4103/2045-8932.93544
    OpenUrlPubMed
  13. ↵
    1. Knafl D,
    2. Gerges C,
    3. King CH, et al.
    Schistosomiasis-associated pulmonary arterial hypertension: a systematic review. Eur Respir Rev 2020; 29: 190089. doi:10.1183/16000617.0089-2019
    OpenUrlAbstract/FREE Full Text
PreviousNext
Back to top
View this article with LENS
Vol 57 Issue 5 Table of Contents
European Respiratory Journal: 57 (5)
  • 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.
Arterial vascular volume changes with haemodynamics in schistosomiasis-associated pulmonary arterial hypertension
(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
Arterial vascular volume changes with haemodynamics in schistosomiasis-associated pulmonary arterial hypertension
Farbod N. Rahaghi, Joan F. Hilton, Ricardo A. Corrêa, Camila Loureiro, Jaquelina S. Ota-Arakaki, Carlos G.Y. Verrastro, Michael H. Lee, Claudia Mickael, Pietro Nardelli, David A. Systrom, Aaron B. Waxman, George R. Washko, Raúl San José Estépar, Brian B. Graham, Rudolf K.F. Oliveira
European Respiratory Journal May 2021, 57 (5) 2003914; DOI: 10.1183/13993003.03914-2020

Citation Manager Formats

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

Share
Arterial vascular volume changes with haemodynamics in schistosomiasis-associated pulmonary arterial hypertension
Farbod N. Rahaghi, Joan F. Hilton, Ricardo A. Corrêa, Camila Loureiro, Jaquelina S. Ota-Arakaki, Carlos G.Y. Verrastro, Michael H. Lee, Claudia Mickael, Pietro Nardelli, David A. Systrom, Aaron B. Waxman, George R. Washko, Raúl San José Estépar, Brian B. Graham, Rudolf K.F. Oliveira
European Respiratory Journal May 2021, 57 (5) 2003914; DOI: 10.1183/13993003.03914-2020
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
    • Shareable PDF
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • PDF
  • Tweet Widget
  • Facebook Like
  • Google Plus One

More in this TOC Section

Agora

  • Airway immune responses to COVID-19 vaccination in COPD patients
  • Wider access to rifapentine-based regimens is needed for TB care globally
  • Normative multiple-breath washout data for children corrected for sensor error
Show more Agora

Research letters

  • Lessons from 2 years of use of the Post-COVID-19 Functional Status scale
  • Beta-blockade improves right ventricular diastolic function in exercising PAH
  • Trends in COVID-19-associated mortality in PH
Show more Research letters

Related Articles

Navigate

  • Home
  • Current issue
  • Archive

About the ERJ

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

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
  • Podcasts
  • 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:  0903-1936
Online ISSN: 1399-3003

Copyright © 2023 by the European Respiratory Society