University of Manchester
Myocardial involvement in eosinophilic granulomatosis with polyangiitis evaluated with cardiopulmonary magnetic resonanceJakub Lagan LEKARZ PhD,1,2 Josephine H Naish BSc PhD,2 Christien Fortune MBChB,1,2 Joshua Bradley BSc MRes,1,2 David Clark BSc,1 Robert Niven MBChB,1,3 Nazia Chaudhuri MBChB PhD,1,3 Erik B Schelbert MD MS,4-6 Matthias Schmitt MD PhD,1,2 Christopher A Miller MBChB PhD.1,2,7AffiliationsManchester University NHS Foundation Trust, Wythenshawe Hospital, Southmoor Road, Wythenshawe, Manchester, M23 9LT.Division of Cardiovascular Sciences, School of Medical Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, University of Manchester, Oxford Road, Manchester, M13 9PL.Division of Infection, Immunity and Respiratory Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, University of Manchester, Oxford Road, Manchester, M13 9PL Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA, USAUPMC Cardiovascular Magnetic Resonance Center, Heart and Vascular Institute, Pittsburgh, PA, USAClinical and Translational Science Institute, University of Pittsburgh, Pittsburgh, PA, USAWellcome Centre for Cell-Matrix Research, Division of Cell-Matrix Biology & Regenerative Medicine, School of Biology, Faculty of Biology, Medicine & Health, Manchester Academic Health Science Centre, University of Manchester, Oxford Road, Manchester, M13 9PT Word count: 3530CorrespondenceDr Christopher A. Miller, Division of Cardiovascular Sciences, School of Medical Sciences, University of Manchester, Oxford Road, Manchester, M13 9PL, UK. Telephone:00441612912034. Fax:0044 1612912389Email:Christopher.Miller@manchester.ac.ukAcknowledgmentsThe authors would like to express their gratitude to Siemens Healthcare Ltd for technical support.AbstractPurpose: Patients with eosinophilic granulomatosis with polyangiitis (EGPA) most commonly die from cardiac causes, however, cardiac involvement remains poorly characterised and the relationship between cardiac and pulmonary disease is not known. This study aimed to characterise myocardial and pulmonary manifestations of EGPA, and their relationship.Methods: Prospective comprehensive cardiopulmonary investigation, including a novel combined cardiopulmonary magnetic resonance imaging (MRI) technology, was performed in 13 patients with stable EGPA. Comparison was made with 11 prospectively recruited matched healthy volunteers.Results: Stable EGPA was associated with focal replacement and diffuse interstitial myocardial fibrosis (myocardial extracellular volume 26.9% vs. 24.7%; p=0.034), which drove a borderline increase in left ventricular mass (56 ± 9g/m2 vs. 49 ± 8 g/m2; p=0.065). Corrected QT interval was significantly prolonged and was associated with the severity of myocardial fibrosis (r=0.582, p=0.037). Stable EGPA was not associated with increased myocardial capillary permeability or myocardial oedema. Pulmonary tissue perfusion and capillary permeability were normal and there was no evidence of pulmonary tissue oedema or fibrosis. Forced expiratory volume in one second showed a strong inverse relationship with myocardial fibrosis (r=-0.783, p=0.038). Conclusions: In this exploratory study, stable EGPA was associated with focal replacement and diffuse interstitial myocardial fibrosis, but no evidence of myocardial or pulmonary inflammation or pulmonary fibrosis. Myocardial fibrosis was strongly associated with airway obstruction and abnormal cardiac repolarisation. Further investigation is required to determine the mechanisms underlying the association between heart and lung disease in EGPA and whether an immediate immunosuppressive strategy could prevent myocardial fibrosis formation. Key wordsCardiac magnetic resonance scanningParametric mappingDynamic contrast enhanced magnetic resonanceEosinophilic granulomatosis with polyangiitisChurg – Strauss syndromeIntroductionEosinophilic granulomatosis with polyangiitis (EGPA), formerly known as Churg-Strauss syndrome, is a hybrid condition comprising a systemic antineutrophil cytoplasmic antibody (ANCA)-associated vasculitis and a hypereosinophilic disorder with frequent lung involvement that is associated with asthmaPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5KZW5uZXR0ZTwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+
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ADDIN EN.CITE.DATA 3,4. In contrast, up to approximately 90% of patients have evidence of cardiac involvement at post-mortem and between a third and three quarters of patients with EGPA die from cardiac causesPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EZW5uZXJ0PC9BdXRob3I+PFllYXI+MjAxMDwvWWVhcj48
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ADDIN EN.CITE.DATA 5,8-11. However, contemporary cardiac MRI techniques, which provide quantitative characterisation of myocardial injury and adaptation, have been applied sparsely and the relationship between cardiac and pulmonary disease is not known. In this study, we sought to apply a novel combined cardiopulmonary MRI technology, which provides comprehensive and simultaneous interrogation of cardiac and pulmonary structure, function and tissue character, in patients with stable EGPA in order to: (1)Characterise myocardial and pulmonary manifestations of EGPA; and (2)Investigate the relationship between cardiac and pulmonary disease in EGPA.Materials and MethodsStudy designThis prospective research study aimed to apply a combined cardiopulmonary MRI protocol in patients with stable EGPA and matched healthy volunteers in order to investigate myocardial and pulmonary manifestations of EGPA, and their relationship. Study populationStable patients with a clinical diagnosis of EGPA according to the 2012 Chapel Hill consensusPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5KZW5uZXR0ZTwvQXV0aG9yPjxZZWFyPjIwMTM8L1llYXI+
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ADDIN EN.CITE.DATA 1 were prospectively recruited at Manchester University NHS Foundation Trust. Age and gender matched volunteers with no cardiovascular symptoms, no history of any medical condition and normal electrocardiogram (ECG) were prospectively recruited as controls. Exclusion criteria included: history of any cardiovascular disorder other than cardiac disease that was thought, by the attending clinical team, to be secondary to EGPA, contraindication to MRI, hypersensitivity to gadolinium-based contrast agent (GBCA), estimated glomerular filtration rate < 40ml/min/1.73m2. Study proceduresParticipants underwent blood sampling for blood count, renal function, c-reactive protein, high sensitivity troponin I, and B-human chorionic gonadotropin in females of childbearing potential, ECG and MRI scanning on the same day (see below). Clinical pulmonary function tests performed closest to the study visit were bined cardiopulmonary MRIProtocolMRI was performed at 1.5T (Avanto, Siemens Medical Imaging). Scan duration 60 minutes. It included the following sequences (Figure 1):1.Steady-state free precession (SSFP) cine imaging of the heart (standard long- and short-axis views) to provide measurement of cardiac function. 2.T1 mapping (by MOdified Look-Locker Inversion Recovery (MOLLI)) at basal and mid left ventricular (LV) short axis level before and 15 minutes following the final bolus of GBCA (see below) to provide evaluation of myocardial oedema and fibrosis. T2 mapping (by T2-prepared SFFP) at the same locations to provide further assessment of myocardial oedema. Late gadolinium enhancement (LGE) imaging beginning at 6 minutes following the final GBCA bolus (see below) to assess for focal replacement myocardial fibrosis. 3.T1 mapping (by MOLLI) in the central sagittal plane of both lungs to provide evaluation of lung tissue injury. 4.Dynamic contrast enhanced (DCE) imaging using free-breathing 2D saturation-recovery fast low angle shot (FLASH) dynamic acquisitions in four planes (basal and mid LV short axis, left and right lung central sagittal planes) to assess myocardial and pulmonary capillary permeability (transfer constant (Ktrans)), pulmonary extracellular volume fraction (Ve) and blood flow (F). GBCA (gadoterate meglumine (Dotarem), Guerbet, France; 3ml/s) administration was divided into three doses in order to avoid saturation of the peak of the arterial input function (AIF), which occurs as a result of the non-linear relationship between contrast agent concentration and signal intensity, and T2 shortening effects, at higher contrast agent concentrations ADDIN EN.CITE <EndNote><Cite><Author>Roberts</Author><Year>1997</Year><RecNum>34</RecNum><DisplayText><style face="superscript">12</style></DisplayText><record><rec-number>34</rec-number><foreign-keys><key app="EN" db-id="pps22zdapzxe21etw5vppw57wpdsxwf0rwds" timestamp="1552503201">34</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Roberts, T P</author></authors></contributors><auth-address>Department of Radiology, University of California, San Francisco 94143, USA.</auth-address><titles><title>Physiologic measurements by contrast-enhanced MR imaging: expectations and limitations.</title><secondary-title>J Magn Reson Imaging</secondary-title></titles><periodical><full-title>J Magn Reson Imaging</full-title></periodical><pages>82-90</pages><volume>7</volume><number>1</number><dates><year>1997</year><pub-dates><date>Jan</date></pub-dates></dates><accession-num>9039597</accession-num><label>r00294</label><work-type>Review</work-type><urls><related-urls><url>. The initial low dose (0.005 mmol/kg) bolus was used to calculate the AIF first pass peak, followed by 2 minutes of dynamic acquisitions with a temporal resolution equal to 50% of heart rate. Then a higher GBCA dose (0.05mmol/kg) was administered and followed by 6 minutes of dynamic acquisitions. The higher dose provided higher contrast to noise ratio for the tail of the AIF and for the myocardial and pulmonary tissue curves. The low dose curve was multiplied by 10 and combined with the high dose curve to produce the final AIFs for the kinetic analysis. The third contrast agent dose (0.1mmol/kg) was administered after the dynamic acquisition to allow LGE imaging and post-contrast T1 mapping.AnalysisMyocardial function: Cardiac volumetric analysis was performed using Circle CVI42 (Circle Cardiovascular Imaging, Canada) according to current guidelinesPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TY2h1bHotTWVuZ2VyPC9BdXRob3I+PFllYXI+MjAxMzwv
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ADDIN EN.CITE.DATA 14. Myocardial extracellular volume (ECV) was calculated using same-day haematocrit as described previouslyPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NaWxsZXI8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS
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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NaWxsZXI8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS
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ADDIN EN.CITE.DATA 15. LV extracellular matrix mass (g) was calculated by multiplying LV mass by ECVPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NZXNzcm9naGxpPC9BdXRob3I+PFllYXI+MjAxNzwvWWVh
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ADDIN EN.CITE.DATA 16. LV cellular mass (g) was calculated by multiplying LV mass by (100%-ECV).Myocardial and lung blood flow characteristics: DCE imaging was analysed using custom written Matlab code (v9.0, The MathWorks, USA). Cardiac motion correction was achieved using an intensity-based rigid registration algorithm. Lung registration was performed using Advanced Normalisation Tools (ANTs) symmetric normalization non-linear registration algorithm, employing cross-correlation as the similarity measure ADDIN EN.CITE <EndNote><Cite><Author>Avants</Author><Year>2008</Year><RecNum>36</RecNum><DisplayText><style face="superscript">17</style></DisplayText><record><rec-number>36</rec-number><foreign-keys><key app="EN" db-id="pps22zdapzxe21etw5vppw57wpdsxwf0rwds" timestamp="1552546496">36</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Avants, B B</author><author>Epstein, C L</author><author>Grossman, M</author><author>Gee, J C</author></authors></contributors><auth-address>Department of Radiology, University of Pennsylvania, 3600 Market Street, Philadelphia, PA 19104, United States. avants@grasp.cis.upenn.edu</auth-address><titles><title>Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain.</title><secondary-title>Med Image Anal</secondary-title></titles><periodical><full-title>Med Image Anal</full-title></periodical><pages>26-41</pages><volume>12</volume><number>1</number><dates><year>2008</year><pub-dates><date>Feb</date></pub-dates></dates><accession-num>17659998</accession-num><label>r00301</label><urls><related-urls><url>. Epicardial, endocardial and lung ROIs were drawn as described above. AIFs were derived from the right ventricular (RV) blood pool for the lungs and the LV blood pool for the myocardium. Care was taken to avoid any trabeculations or papillary muscles. Contrast agent kinetics were modelled using an extended version of a Kety model on a voxel-by-voxel basis within registered ROIs to calculate Ktrans and Ve ADDIN EN.CITE <EndNote><Cite><Author>Naish</Author><Year>2009</Year><RecNum>24</RecNum><DisplayText><style face="superscript">18</style></DisplayText><record><rec-number>24</rec-number><foreign-keys><key app="EN" db-id="pps22zdapzxe21etw5vppw57wpdsxwf0rwds" timestamp="1552464854">24</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Naish, Josephine H</author><author>Kershaw, Lucy E</author><author>Buckley, David L</author><author>Jackson, Alan</author><author>Waterton, John C</author><author>Parker, Geoffrey J M</author></authors></contributors><auth-address>Imaging Science and Biomedical Engineering, University of Manchester, Manchester, UK. josephine.naish@manchester.ac.uk</auth-address><titles><title>Modeling of contrast agent kinetics in the lung using T1-weighted dynamic contrast-enhanced MRI.</title><secondary-title>Magn Reson Med</secondary-title></titles><periodical><full-title>Magn Reson Med</full-title></periodical><pages>1507-1514</pages><volume>61</volume><number>6</number><dates><year>2009</year><pub-dates><date>Jun</date></pub-dates></dates><publisher>Wiley-Blackwell</publisher><accession-num>19319896</accession-num><label>r00149</label><work-type>Evaluation Study</work-type><urls><related-urls><url>. Pulmonary blood flow (F) was calculated by deconvolution of the first pass dynamic data as described previouslyPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5OYWlzaDwvQXV0aG9yPjxZZWFyPjIwMDk8L1llYXI+PFJl
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ADDIN EN.CITE.DATA 10,11,15. Data distribution was determined using the Shapiro-Wilk test. Data are summarised using mean and standard deviation or median and interquartile range (IQR), and were compared using t tests or non-parametric equivalents, as appropriate. Analyses were performed using SPSS (version 22, IBM, USA).ResultsParticipant characteristicsThirteen patients with stable EGPA and 11 healthy volunteers were recruited (Table 1). Groups were matched for age and gender. Twelve (92%) patients with EGPA were receiving immunosuppressive therapy at the time of the study. Patients with EGPA had a significantly higher white cell count (10.7 vs. 6.0x109/L; p=0.001), however, eosinophil count was no different (0.23 vs. 0.11x109/L; p=0.23). High sensitivity troponin I was within the normal range in all participants. Pulmonary function tests were available in seven patients with EGPA.Two patients with EGPA had a history of cardiac involvement; one patient had previously had a pericardial effusion and a pericardial window formed, one patient had experienced a distal coronary artery dissection at a young age. Corrected QT interval was significantly longer in EGPA than in healthy volunteers (414±17 vs. 398±18ms; p=0.04). Four patients with EGPA exhibited ST segment (ST elevation in one; ST depression in one) or T wave abnormalities (T wave inversion in two). No patients exhibited clinically significant arrhythmias. Cardiopulmonary manifestationsVentricular size, ventricular ejection fraction and atrial size were no different in EGPA compared to control (Table 2). Body surface area-indexed LV mass was borderline higher in EGPA (56±9 vs. 49±8g/m2; p=0.065).EGPA was associated with elevated myocardial ECV (26.9% (25.9-28.5%) vs 24.7% (23.6-26.4%); p=0.034), increased extracellular matrix mass (24±6 vs. 32±9; p=0.015) and elevated native T1 (1063±46 vs. 1003±21ms; p=0.001). Ten patients with EGPA exhibited non-ischaemic LGE (mid myocardial wall in five, epicardial in one, RV insertion point in nine; p<0.001; (some patients displayed more than one type)). Myocardial T2 and capillary permeability were no different in EGPA compared to control. Figure 2 illustrates representative examples of tissue characterisation in a patient with EGPA .There was no relationship between corrected QT interval and medications. Corrected QT interval was significantly associated with myocardial ECV interval (r=0.582, p=0.037; Figure 3A). Two patients had evidence of a myocardial infarction (MI) on LGE imaging: in one patient it was previously unrecognised and the other was the patient with a history of coronary artery dissection. Pulmonary tissue T1, capillary permeability, extracellular volume fraction and blood flow were no different in EGPA compared to healthy volunteers (Table 3).Relationship between cardiac and pulmonary manifestations Forced expiratory volume in one second (FEV1) was strongly negatively correlated to native myocardial T1 (r=-0.816, p=0.025) and ECV (r=-0.783, p=0.038; Figure 3B). There were no significant correlations between myocardial and pulmonary MRI measurements, and no association between circulating eosinophil levels and cardiac findings.DiscussionIn the first study to utilise a combined multiparametric cardiopulmonary MRI protocol in EGPA, we demonstrate a number of novel findings. We show that stable EGPA is associated with focal replacement and diffuse interstitial myocardial fibrosis, which drives a borderline increase in LV mass, but is not associated with myocardial oedema or increased capillary permeability. We show that myocardial fibrosis burden is associated with abnormal cardiac repolarisation. We demonstrate that in the setting of stable disease, EGPA is associated with normal pulmonary tissue perfusion and no evidence of pulmonary inflammation or fibrosis. Finally, we show that myocardial fibrosis burden is strongly related to the severity of airway obstruction.It is increasingly recognised that conditions considered to be primary pulmonary disorders are associated with cardiovascular conditions, particularly heart failure, independent of shared risk factors, and that in turn, cardiovascular conditions independently contribute to all-cause mortality in patients with pulmonary conditions ADDIN EN.CITE <EndNote><Cite><Author>Carter</Author><Year>2019</Year><RecNum>80</RecNum><DisplayText><style face="superscript">20</style></DisplayText><record><rec-number>80</rec-number><foreign-keys><key app="EN" db-id="pps22zdapzxe21etw5vppw57wpdsxwf0rwds" timestamp="1563874384">80</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Carter, Paul</author><author>Lagan, Jakub</author><author>Fortune, Christien</author><author>Bhatt, Deepak L</author><author>Vestbo, J?rgen</author><author>Niven, Robert</author><author>Chaudhuri, Nazia</author><author>Schelbert, Erik B</author><author>Potluri, Rahul</author><author>Miller, Christopher A</author></authors></contributors><auth-address>ACALM Study Unit in collaboration with Aston Medical School, Aston University, Birmingham, United Kingdom; Cambridge Cardiovascular Epidemiology Unit, University of Cambridge, Cambridge, United Kingdom.</auth-address><titles><title>Association of Cardiovascular Disease With Respiratory Disease.</title><secondary-title> J Am Coll Cardiol</secondary-title></titles><pages>2166-2177</pages><volume>73</volume><number>17</number><dates><year>2019</year><pub-dates><date>May 07</date></pub-dates></dates><accession-num>30846341</accession-num><label>r00521</label><urls><related-urls><url>. 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ADDIN EN.CITE.DATA 2. Cardiac involvement often occurs early in the disease processPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5OZXVtYW5uPC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48
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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5OZXVtYW5uPC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48
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ADDIN EN.CITE.DATA 8. Some studies report that cardiac involvement is more common in ANCA-negative patients and is related to the degree of blood eosinophilia, but others have not found these associationsPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5OZXVtYW5uPC9BdXRob3I+PFllYXI+MjAwOTwvWWVhcj48
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ADDIN EN.CITE.DATA 2,3,7Patients all had stable EGPA, as evidenced by low levels of circulating C reactive protein and eosinophil counts (the slightly elevated white cell count is likely because 92% of patients were receiving corticosteroids). Perhaps as a result, we did not find an association between cardiac manifestations and circulating eosinophil levels. Seventy-seven percent of patients were ANCA-negative at diagnosis. The multiparametric nature of MRI, i.e. its ability to measure multiple aspects of tissue structure, function, injury and adaptation within one scan, without radiation, means that it is uniquely placed to elucidate underlying disease mechanisms and understand their relationships. Myocardial ECV, measured using cardiac MRI, quantifies myocardial extracellular matrix volume and in the absence of significant inflammation, is a robust measure of myocardial fibrosis, having been extensively validated against histological collagen volume fractionPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NZXNzcm9naGxpPC9BdXRob3I+PFllYXI+MjAxNzwvWWVh
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ADDIN EN.CITE.DATA 24,25. Myocardial T2 is directly proportional to myocardial water content ADDIN EN.CITE <EndNote><Cite><Author>Higgins</Author><Year>1983</Year><RecNum>76</RecNum><DisplayText><style face="superscript">26</style></DisplayText><record><rec-number>76</rec-number><foreign-keys><key app="EN" db-id="pps22zdapzxe21etw5vppw57wpdsxwf0rwds" timestamp="1559661020">76</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Higgins, C B</author><author>Herfkens, R</author><author>Lipton, M J</author><author>Sievers, R</author><author>Sheldon, P</author><author>Kaufman, L</author><author>Crooks, L E</author></authors></contributors><titles><title>Nuclear magnetic resonance imaging of acute myocardial infarction in dogs: alterations in magnetic relaxation times.</title><secondary-title>Am J Cardiol</secondary-title></titles><periodical><full-title>Am J Cardiol</full-title></periodical><pages>184-188</pages><volume>52</volume><number>1</number><dates><year>1983</year><pub-dates><date>Jul</date></pub-dates></dates><accession-num>6858909</accession-num><label>r00639</label><urls><related-urls><url> and Ktrans measures capillary permeabilityPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MZWFjaDwvQXV0aG9yPjxZZWFyPjIwMDU8L1llYXI+PFJl
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ADDIN EN.CITE.DATA 10. ECV and T1 can be affected by oedema, thus it is unclear whether the elevated ECV and T1 that Greulich et al report represented myocardial oedema or fibrosis. In a study by Cereda et al, elevated ECV was confined to patients with reduced LV ejection fractionPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5DZXJlZGE8L0F1dGhvcj48WWVhcj4yMDE3PC9ZZWFyPjxS
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ADDIN EN.CITE PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5DZXJlZGE8L0F1dGhvcj48WWVhcj4yMDE3PC9ZZWFyPjxS
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ADDIN EN.CITE.DATA 11. The prevalence of non-ischaemic focal replacement fibrosis in our study (77%) is in keeping with that in previous studiesPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TemN6ZWtsaWs8L0F1dGhvcj48WWVhcj4yMDExPC9ZZWFy
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ZT4A
ADDIN EN.CITE.DATA 11,28-30. Although quantitative T2 mapping has only been applied in one previous study in EPGA, studies using semi-quantitative T2-weighted imaging, and positron emission tomography, have generally shown a low prevalence of inflammation in stable EGPA, which is in keeping with the described histology and our findingsPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EZW5uZXJ0PC9BdXRob3I+PFllYXI+MjAxMDwvWWVhcj48
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ADDIN EN.CITE.DATA 32,33 and further work is required to determine the association between myocardial fibrosis and outcome in EGPA. Arrhythmia is a common feature of EGPA and it is of note that we demonstrate an association between myocardial fibrosis and corrected QT interval.The authors of pathological studies demonstrating that myocardial fibrosis develops rapidly during the course of EGPA have suggested immediate and aggressive immunosuppressant treatment may be beneficial in preventing the development of heart failure and other cardiac complicationsPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NYWhyPC9BdXRob3I+PFllYXI+MjAxNDwvWWVhcj48UmVj
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ADDIN EN.CITE.DATA 2,8. Future studies applying MRI in the initial stages of EGPA are required in order to characterise the early myocardial manifestations and evaluate the impact of such an immunosuppressant strategy.Importantly, one patient (8%) was found to have an otherwise unrecognised MI. MI that is not detectable from patient history or ECG is well described in non-EGPA populations. Cardiac MRI with LGE has a sensitivity such that it is able to detect 0.7g of infarcted myocardium ADDIN EN.CITE <EndNote><Cite><Author>Ricciardi</Author><Year>2001</Year><RecNum>78</RecNum><DisplayText><style face="superscript">34</style></DisplayText><record><rec-number>78</rec-number><foreign-keys><key app="EN" db-id="pps22zdapzxe21etw5vppw57wpdsxwf0rwds" timestamp="1559668047">78</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ricciardi, M J</author><author>Wu, E</author><author>Davidson, C J</author><author>Choi, K M</author><author>Klocke, F J</author><author>Bonow, R O</author><author>Judd, R M</author><author>Kim, R J</author></authors></contributors><auth-address>Feinberg Cardiovascular Institute and the Department of Medicine, Northwestern University, Chicago, IL, USA.</auth-address><titles><title>Visualization of discrete microinfarction after percutaneous coronary intervention associated with mild creatine kinase-MB elevation.</title><secondary-title>Circulation</secondary-title></titles><periodical><full-title>Circulation</full-title></periodical><pages>2780-2783</pages><volume>103</volume><number>23</number><dates><year>2001</year><pub-dates><date>Jun 12</date></pub-dates></dates><accession-num>11401931</accession-num><label>r00640</label><work-type>Clinical Trial</work-type><urls><related-urls><url>. Several large community cohort studies (including people with or at risk of cardiovascular disease) utilising cardiac MRI have demonstrated a significant prevalence of otherwise unrecognised MI, and a high associated mortality riskPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TY2hlbGJlcnQ8L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFy
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ADDIN EN.CITE.DATA 35. Subendocardial LGE is well described in EGPA but studies rarely comment on its apparent aetiology (i.e. non-ischaemic eosinophilic subendocardial fibrosis vs. ischaemic), or its context (i.e. history of MI). It is well recognized that EGPA is associated with coronary artery disease, and while our study is small, it suggests that unrecognised MI may not be uncommon. Given that unrecognised MI is only detectable using cardiac MRI, and that its detection allows initiation of secondary preventative therapy, consideration should be given to performing cardiac MRI in all patients with EGPA. Demonstrating the unique utility of cardiac MRI, the cardiac MRI findings were not evident from circulating biomarkers (e.g. high sensitivity troponin) or on ECG. Furthermore, despite there being evidence of significant myocardial injury and adaptation, ventricular size and ejection fraction were normal, which is in keeping with most previous studies in EGPA, demonstrating the low sensitivity of ventricular size and ejection fraction for detecting cardiac injuryPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5TemN6ZWtsaWs8L0F1dGhvcj48WWVhcj4yMDExPC9ZZWFy
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ADDIN EN.CITE.DATA 2,6,43,44 which is in keeping with our findings that showed no reduction in pulmonary T1 and no increase in extracellular volume fraction in EGPA compared to controls. Indeed, a benefit of our combined cardio-pulmonary protocol is that it enabled us to demonstrate that myocardial fibrosis occurs independently of pulmonary fibrosis in EGPA. We found a strong association between myocardial fibrosis and the severity of airflow limitation. This is a novel finding and the underlying mechanism is unclear. Associations between FEV1 and incident heart failure, and between FEV1 and adverse outcome in patients with HF, particularly heart failure with preserved ejection fraction, are widely recognisedPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MYW08L0F1dGhvcj48WWVhcj4yMDExPC9ZZWFyPjxSZWNO
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ADDIN EN.CITE.DATA 50-52. In COPD, it has been hypothesised that systemic inflammation leading to myocardial injury and subsequent myocardial fibrosis may be the unifying mechanism ADDIN EN.CITE <EndNote><Cite><Author>Paulus</Author><Year>2013</Year><RecNum>59</RecNum><DisplayText><style face="superscript">53</style></DisplayText><record><rec-number>59</rec-number><foreign-keys><key app="EN" db-id="xzsavfxwie9vene9ta9p9z2902zxfawz95zr">59</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Paulus, W. J.</author><author>Tschope, C.</author></authors></contributors><auth-address>Department of Physiology, Institute for Cardiovascular Research VU, VU University Medical Center Amsterdam, Amsterdam, the Netherlands. wj.paulus@vumc.nl</auth-address><titles><title>A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation</title><secondary-title>J Am Coll Cardiol</secondary-title><alt-title>Journal of the American College of Cardiology</alt-title></titles><periodical><full-title>J Am Coll Cardiol</full-title></periodical><pages>263-71</pages><volume>62</volume><number>4</number><keywords><keyword>Animals</keyword><keyword>Comorbidity</keyword><keyword>Coronary Circulation/physiology</keyword><keyword>Endothelium, Vascular/metabolism/*pathology</keyword><keyword>Heart Failure/metabolism/*pathology/physiopathology</keyword><keyword>Humans</keyword><keyword>Inflammation/pathology/physiopathology</keyword><keyword>Microcirculation/*physiology</keyword><keyword>Myocardium/metabolism/*pathology</keyword><keyword>Stroke Volume/*physiology</keyword><keyword>Ventricular Remodeling/*physiology</keyword></keywords><dates><year>2013</year><pub-dates><date>Jul 23</date></pub-dates></dates><isbn>1558-3597 (Electronic)
0735-1097 (Linking)</isbn><accession-num>23684677</accession-num><urls><related-urls><url>. It is possible that a similar mechanism may be responsible for the relationship between myocardial fibrosis and airflow limitation that we have demonstrated in EGPA, indeed our findings may shed light on these wider pulmonary-cardiac associations, but further work is required to investigate these mechanisms. LimitationsThe number of patients included was small, although we were able to demonstrate significant results despite the small numbers. EGPA is a rare condition with estimated prevalence of 2 to 22 per/million and the size of our study is in keeping with other recent studiesPEVuZE5vdGU+PENpdGU+PEF1dGhvcj5NYWhyPC9BdXRob3I+PFllYXI+MjAxNDwvWWVhcj48UmVj
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ADDIN EN.CITE.DATA 2,10,11. It was not possible to obtain histological data; it was not felt ethically acceptable to conduct lung and endomyocardial biopsies as part of this study, and these procedures are not generally performed in stable EGPA patients. ConclusionsIn this exploratory study that utilised a combined multiparametric cardiopulmonary MRI protocol, we demonstrate that stable EGPA is associated with focal replacement and diffuse interstitial myocardial fibrosis, but no evidence of myocardial or pulmonary inflammation or pulmonary fibrosis. Myocardial fibrosis is strongly related to airway obstruction and abnormal cardiac repolarisation. Further investigation is required to determine the mechanisms underlying the association between heart and lung disease in EGPA, the impact myocardial fibrosis has on prognosis, and whether an immediate immunosuppressive strategy could prevent myocardial fibrosis formation. Declarations:FundingDr Lagan is funded by a Clinical Research Training Fellowship from the British Heart Foundation (FS/17/47/32805). Dr Miller is?funded by a Clinician Scientist Award (CS-2015-15-003)?from the National Institute for Health Research. The work was also supported in part by a British Heart Foundation Accelerator award to The University of Manchester (AA/18/4/34221). The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research or the Department of Health. None of these funding bodies had a role in study design, data collection, analysis or interpretation or writing of the manuscript.Conflicts of interest / Competing interestsDr Miller received research support provided by Roche and Guerbert. Dr Miller served on an advisory board for Novartis and serves as an advisor for HAYA therapeutics. Other authors declare that they have no competing interests. Authors have full control of all primary data and agree to allow the journal to review the data if requested.Ethics approval and consent to participateA North West – Greater Manchester West Research Ethics Committee of the UK National Research Ethics Service approved the study and written informed consent was obtained from all participants. The work was conducted according to the Helsinki Declaration.Availability of data and materialsThe datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request. Author’s contributionJL – study conceptualisation and design, ethical approval application, recruitment, MRI acquisition and analysis, clinical data analysis, statistical analysis, writing and revision of the manuscript. JHN – MRI protocol and analysis tools design, revision of the manuscript. CF – recruitment and clinical data analysis, revision of the manuscript. JB – MRI analysis, revision of the manuscript. DC – MRI acquisition and analysis, revision of the manuscript. RN, NC – study conceptualisation and design, patient recruitment, revision of the manuscript. EBS, MS – study conceptualisation and design, revision of the manuscript. CAM – chief investigator for the study, study conceptualisation and design, supervision of all study aspects, writing and revision of the manuscript.Consent for publicationNot applicable.References: ADDIN EN.REFLIST 1.Jennette JC, Falk RJ, Bacon PA, et al. 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Paper presented at: Arthritis Rheum; 2013.2.Mahr A, Moosig F, Neumann T, et al. Eosinophilic granulomatosis with polyangiitis (Churg-Strauss): evolutions in classification, etiopathogenesis, assessment and management. Curr Opin Rheumatol. 2014;26:16-23.3.Guillevin L, Cohen P, Gayraud M, et al. Churg-Strauss syndrome. Clinical study and long-term follow-up of 96 patients. 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A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol. 2013;62:263-71.Table 1. Participant characteristics.ParameterControls (n=11)EGPA (n=13)p valueDemographics???Age (years)53 (46-56)54 (49-57)0.543Gender (female,%)4 (36%)6 (46%)0.697BSA (m2)1.98 (1.73-2.21)2.22 (1.8-2.3)0.369EGPA manifestations???ANCA positive0 (0%)3 (23%)?Asthma0 (0%)12 (92%)?History of eosinophilia0 (0%)13 (100%)?Peripheral neuropathy0 (0%)10 (77%)?Paranasal sinus abnormalities0 (0%)6 (46%)?Extravascular eosinophils0 (0%)2 (15%)?Cardiac involvement0 (0%)2 (15%)?Renal involvement0 (0%)2 (15%)?GI involvement0 (0%)2 (15%)?Dermatological involvement0 (0%)2 (15%)?Polymyalgia0 (0%)2 (15%)?Hypertension0 (0%)2 (15%)?Alveolar haemorrhage0 (0%)1 (8%)?Medications???Oral steroids0 (0%)12 (92 %)?Mycophenolate mofetil0 (0%)6 (46%)?Methotrexate0 (0%)2 (15 %)?Inhaled steroids0 (0%)11 (85%)?Inhaled LABAs0 (0%)9 (69%)?Inhaled SABAs0 (0%)12 (92 %)?Inhaled LAMAs0 (0%)4 (31%)?Theophylline0 (0%)2 (15 %)?LTRA0 (0%)2 (15 %)?Macrolides0 (0%)3 (23%)?Statins0 (0%)4 (31%)?ACEI/sartans0 (0%)3 (23%)?B Blockers0 (0%)1 (8%)?Calcium channel blockers0 (0%)1 (8%)?Duretics0 (0%)3 (23%)?Antiplatelets0 (0%)1 (8%)?Anticoagulants0 (0%)2 (15%)?Lung function tests??FEV1 (L/s)?2.4±0.7*?FEV1% (%)?70.6±25.0*?FVC (L)?3.6±1.0*?FVC% (%)?85.0±18.8*?FEV1/FVC?0.68±0.13*?Laboratory findings???CRP (mg/L)1 (0-2)3 (1-10)0.070WBC (x109/L)6 (4.9-7.1)10.7 (9.8-12.85)0.001Eosinophil count (x109/L)0.11 (0.07-0.21)0.23 (0.07-0.44)0.213Troponin I (ng/L)4 (4-4)4 (4-4)0.317ECG findings???PR duration (ms)160 (130-160)160 (140-160)0.975QRS duration (ms)80 (80-100)80 (70-80)0.115QTc (ms)398±18414±170.043ST-T abnormalities (present)0 (0%)4 (31%)0.098Data presented as mean ± standard deviation or median (interquartile range) depending on data distribution. *n=7. ACEI-angiotensin converting enzyme inhibitor; ANCA-antineutrophil cytoplasmic antibodies; BSA-body surface area; CRP-c reactive protein; EGPA-eosinophilic granulomatosis with polyangiitis; FEV1-forced expiratory volume in one second; FEV1%-percentage of predicted forced expiratory volume in one second; FVC-forced vital capacity; FVC%-percentage of predicted forced vital capacity GI-gastrointestinal tract; LABA-long acting B agonist; LAMA-long acting muscarinic antagonist; LTRA-leukotriene receptor antagonist; LVH-left ventricular hypertrophy; SABA-short acting B agonist; WBC-white blood cell.Table 2. Myocardial magnetic resonance imaging indices ParameterControls (n=11)EGPA (n=13)p valueLV??LV EDV/BSA (ml/m2)76±1176±180.932LV ESV/BSA (ml/m2)30±631±140.770LV EF (%)62±560±90.645LV mass/BSA (g/m2)49±856±90.065RV??RV EDV/BSA (ml/m2)83±1477±160.305RV ESV/BSA (ml/m2)37±733±100.396RV EF (%)56±456±80.996Pericardium??Pericardial effusion (n,%)0 (0%)1 (8%)1.000Pericardial thickening (n,%)0 (0%)2 (15%)0.482Atria??LA area/BSA (cm2/m2)12±112±30.319RA area/BSA (cm2/m2)12±311±20.221Tissue characterisation??Ischaemic LGE (present)0 (0%)2 (15%)0.482Ischaemic LGE (g)0.00 (0.00-0.00)0.00 (0.00-0.00)0.184Non-ischaemic LGE (present)0 (0%)10 (77%)<0.001Non-ischaemic LGE (g)0.00 (0.00-0.00)0.51 (0.12-3.16)0.001T2 (ms)50±250±30.533T1 (ms)1003±211063±460.001ECV (%)24.7 (23.6-26.4)26.9 (25.9-28.5)0.034Extracellular matrix mass (g)24±632±90.015Cellular mass (g)74±2184±160.191Median Ktrans (min-1)0.32±0.080.31±0.080.762Data presented as mean ± standard deviation or median (interquartile range) depending on data distribution. ECV-extracellular volume fraction; EDV-end systolic volume; EF-ejection fraction; ESV-end systolic volume; Ktrans-transfer constant; LA-left atrium; LGE-late gadolinium enhancement; LV-left ventricle; RA-right atrium; RV-right ventricle; SV-stroke volume. Other abbreviations as per Table 1.Table 3. Pulmonary magnetic resonance imaging indices ParameterControls (n=11)EGPA (n=13)p valueT1 (ms)1261±461290±650.232Median Ve (%)20.8 (18.73-26.86)21.9 (18.62-25.64)0.839Median Ktrans (min-1)0.25±0.070.23±0.090.561Median F (ml blood/ml tissue/min)2.32 (1.76-3.10)2.77 (1.88-3.15)0.794Data presented as mean ± standard deviation or median (interquartile range) depending on data distribution. F – Pulmonary tissue blood flow; Ve - pulmonary extracellular volume fraction. Other abbreviations as per Table 2. Figure Legends:Figure 1. Cardiopulmonary magnetic resonance imaging protocol. DCE-dynamic contrast enhanced; GBCA-gadolinium based contrast agent; HASTE-Half-Fourier-Acquired Single-shot Turbo spin Echo; LGE-Late enhancement imaging.Figure 2. Myocardial tissue characterisation in a patient with eosinophilic granulomatosis with polyangiitis. (A)On late enhancement imaging (arrow) and (B)extracellular volume mapping (extracellular volume in the lateral wall is elevated at 37%), there is evidence of non-ischaemic fibrosis in the lateral wall of the left ventricle. (C)On T2 mapping, there is no evidence of myocardial inflammation (lateral wall: 45ms; septum: 47ms). Figure 3. Relationship between myocardial extracellular volume (ECV) fraction, lung function and cardiac repolarisation in eosinophilic granulomatosis with polyangiitis. (A)Corrected QT interval was significantly associated with myocardial fibrosis burden, measured using extracellular volume fraction (ECV). (B)Forced expiratory volume in one second (FEV1) was significantly negatively correlated to myocardial fibrosis burden, measured using ECV. ................
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