Subclinical Atherosclerosis in Patients With Inflammatory Bowel Diseases: A Systematic Review and Meta-Analysis.

We evaluated the differences in major markers of cardiovascular (CV) risk between inflammatory bowel diseases (IBDs) and controls by a systematic review and a meta-analysis. We searched PubMed, EMBASE, and Cochrane databases for literature comparing CV risk markers in IBDs and controls. The overall mean carotid intima-media thickness (CIMT), flow-mediated dilation (FMD%), and carotid-femoral pulse wave velocity (cfPWV) difference between patients with IBDs and control groups were calculated. Twenty-eight studies were included in the meta-analysis, including 16 studies with data on CIMT, 7 studies reporting FMD%, and 9 studies on cfPWV. Compared to controls, patients with IBDs showed significantly higher CIMT (standardized mean difference [ SMD]: 0.534 mm; 95% confidence interval [CI], 0.230 to 0.838; P = .001), significantly lower FMD% ( SMD, -0.721%; 95% CI, -1.020 to -0.421; P < .0001), and significantly increased cfPWV ( SMD, 0.849; 95% CI, 0.589 to 1.110; P < .0001). When analyzing subgroups with ulcerative colitis and Crohn disease (CD), all results were still significant except CIMT in CD. Our findings support the current evidence for an elevated CV burden in patients with IBD and support the clinical utility of markers of subclinical atherosclerosis in the management of these patients.

[1]  A. Di Leo,et al.  Endothelial function and cardiovascular risk in patients with inflammatory bowel disease in remission phase , 2016, Scandinavian journal of gastroenterology.

[2]  D. Ye,et al.  Subclinical atherosclerosis in patients with systemic lupus erythematosus: A systemic review and meta-analysis. , 2016, Autoimmunity reviews.

[3]  LiJun Xu,et al.  Risk of Stroke in Patients with Inflammatory Bowel Disease: A Systematic Review and Meta-analysis. , 2015, Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association.

[4]  A. Redler,et al.  Aortic Intima-Media Thickness as an Early Marker of Atherosclerosis in Children With Inflammatory Bowel Disease , 2015, Journal of pediatric gastroenterology and nutrition.

[5]  E. Tremoli,et al.  Cardiovascular risk markers in patients with psoriatic arthritis: A meta-analysis of literature studies , 2015, Annals of medicine.

[6]  H. Demirci,et al.  Pulse Wave Velocity, Intima Media Thickness, and Flow-mediated Dilatation in Patients with Normotensive Normoglycemic Inflammatory Bowel Disease , 2015, Inflammatory bowel diseases.

[7]  M. Storr,et al.  Cardiovascular complications in inflammatory bowel disease. , 2015, Current drug targets.

[8]  A. Di Minno,et al.  Subclinical atherosclerosis in patients with rheumatoid arthritis , 2015, Thrombosis and Haemostasis.

[9]  D. Gladman,et al.  Increased burden of inflammation over time is associated with the extent of atherosclerotic plaques in patients with psoriatic arthritis , 2014, Annals of the rheumatic diseases.

[10]  Nuria Barbarroja,et al.  Gene profiling reveals specific molecular pathways in the pathogenesis of atherosclerosis and cardiovascular disease in antiphospholipid syndrome, systemic lupus erythematosus and antiphospholipid syndrome with lupus , 2014, Annals of the rheumatic diseases.

[11]  B. Baca,et al.  Visual evoked potentials and pulse wave velocity in inflammatory bowel disease. , 2015, The Turkish journal of gastroenterology : the official journal of Turkish Society of Gastroenterology.

[12]  H. Gullu,et al.  Impaired coronary microvascular and left ventricular diastolic function in patients with inflammatory bowel disease. , 2015, Microvascular research.

[13]  M. Karakaş,et al.  Evaluation of increased subclinical atherosclerosis risk with carotid intima-media thickness and pulse wave velocity in inflamatory bowel disease. , 2015, The Turkish journal of gastroenterology : the official journal of Turkish Society of Gastroenterology.

[14]  Y. Yoon,et al.  Common carotid intima-media thickness as a risk factor for outcomes in Asian patients with acute ST-elevation myocardial infarction. , 2014, The Canadian journal of cardiology.

[15]  S. Rajalingham,et al.  Subclinical atherosclerosis among rheumatoid arthritis patients without overt cardiovascular risk factors , 2014, Modern rheumatology.

[16]  B. Mulder,et al.  Increased carotid intima-media thickness predicts cardiovascular events in aortic coarctation. , 2014, International journal of cardiology.

[17]  F. Cicuttini,et al.  Comparison of inflammation, arterial stiffness and traditional cardiovascular risk factors between rheumatoid arthritis and inflammatory bowel disease , 2014, Journal of Inflammation.

[18]  Kyeong Ok Kim,et al.  Does Carotid Intima-Media Thickness Increase in Patients With Inflammatory Bowel Disease? , 2014, Intestinal research.

[19]  O. Giouleme,et al.  Lipoprotein-associated phospholipase A2 and arterial stiffness evaluation in patients with inflammatory bowel diseases. , 2014, Journal of Crohn's & colitis.

[20]  T. Jess,et al.  Risk of cardiovascular disease in inflammatory bowel disease. , 2014, World journal of gastrointestinal pathophysiology.

[21]  H. Tian,et al.  Association of lipoprotein subclasses and carotid intima-media thickness in the Chinese population , 2014 .

[22]  K. Shimada,et al.  Serial assessment of arterial stiffness by cardio-ankle vascular index for prediction of future cardiovascular events in patients with coronary artery disease , 2013, Hypertension Research.

[23]  S. Douma,et al.  Is There an Association Between Inflammatory Bowel Diseases and Carotid Intima-media Thickness? Preliminary Data , 2014, Angiology.

[24]  F. Şahin,et al.  Increased pulse wave velocity and relationship with inflammation, insulin, and insulin resistance in inflammatory bowel disease , 2014, European journal of gastroenterology & hepatology.

[25]  C. Tsai,et al.  Inflammatory bowel diseases increase future ischemic stroke risk: a Taiwanese population-based retrospective cohort study. , 2014, European journal of internal medicine.

[26]  D. Ye,et al.  Decreased Flow-Mediated Dilatation in Patients with Systemic Lupus Erythematosus: a Meta-analysis , 2014, Inflammation.

[27]  S. Laurent,et al.  Increased arterial stiffness in inflammatory bowel diseases is dependent upon inflammation and reduced by immunomodulatory drugs. , 2014, Atherosclerosis.

[28]  O. Giouleme,et al.  Carotid Intima-Media Thickness in Patients With Inflammatory Bowel Disease , 2014, Angiology.

[29]  Siddharth Singh,et al.  Risk of cerebrovascular accidents and ischemic heart disease in patients with inflammatory bowel disease: a systematic review and meta-analysis. , 2014, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[30]  Sýkora Josef,et al.  Reactive hyperaemia index as a marker of endothelial dysfunction in children with Crohn's disease is significantly lower than healthy controls , 2014, Acta paediatrica.

[31]  F. Nagy,et al.  Increased aortic stiffness in ulcerative colitis , 2014 .

[32]  A. Di Leo,et al.  Endothelial function and cardiovascular risk in active inflammatory bowel diseases. , 2013, Journal of Crohn's & colitis.

[33]  A. Ribeiro,et al.  Progression of carotid atherosclerosis in patients with systemic lupus erythematosus , 2013, Clinical Rheumatology.

[34]  T. Durakoğlugil,et al.  Increased Pulse Wave Velocity and Carotid Intima-Media Thickness in Patients with Ulcerative Colitis , 2013, Digestive Diseases and Sciences.

[35]  M. Budoff,et al.  The Role of Carotid Intimal Thickness Testing and Risk Prediction in the Development of Coronary Atherosclerosis , 2013, Current Atherosclerosis Reports.

[36]  M. Farkouh,et al.  Are patients with inflammatory bowel disease at increased risk of coronary artery disease? , 2012, The American journal of medicine.

[37]  S. Laurent,et al.  Arterial stiffness is increased in patients with inflammatory bowel disease , 2012, Journal of hypertension.

[38]  N. Çullu,et al.  Evaluation of Early Atherosclerosis in Patients with Inflammatory Bowel Disease , 2012, Digestive Diseases and Sciences.

[39]  M. Turiel,et al.  Validated methods for assessment of subclinical atherosclerosis in rheumatology , 2012, Nature Reviews Rheumatology.

[40]  J. Aviña-Zubieta,et al.  Risk of incident cardiovascular events in patients with rheumatoid arthritis: a meta-analysis of observational studies , 2012, Annals of the rheumatic diseases.

[41]  A. Amouri,et al.  P128 Intima media thickness of the common carotid artery is significantly higher in inflammatory bowel disease patients compared to healthy population , 2012 .

[42]  S. Bergmann,et al.  Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. , 2011, Atherosclerosis.

[43]  Umakant Nadkar,et al.  Increased prevalence of subclinical atherosclerosis in rheumatoid arthritis patients of Indian descent. , 2012, Experimental and clinical cardiology.

[44]  E. Boerwinkle,et al.  Common carotid artery intima-media thickness is as good as carotid intima-media thickness of all carotid artery segments in improving prediction of coronary heart disease risk in the Atherosclerosis Risk in Communities (ARIC) study. , 2012, European heart journal.

[45]  M. Szklo,et al.  Longitudinal predictors of progression of carotid atherosclerosis in rheumatoid arthritis. , 2011, Arthritis and rheumatism.

[46]  B. Spiegel,et al.  Atherosclerosis in systemic sclerosis: a systematic review and meta-analysis. , 2011, Arthritis and rheumatism.

[47]  G. Valesini,et al.  Premature Subclinical Atherosclerosis in Pediatric Inflammatory Bowel Disease , 2011 .

[48]  C. Vlachopoulos,et al.  Prediction of Cardiovascular Events and All-Cause Mortality With Arterial Stiffness , 2011 .

[49]  S. Bergmann,et al.  Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis , 2010, The International Journal of Cardiovascular Imaging.

[50]  O. Poyrazoglu,et al.  Is Inflammatory Bowel Disease a Risk Factor for Early Atherosclerosis? , 2010, Angiology.

[51]  E. Scapa,et al.  Intima-Media Thickness of the Common Carotid Artery Is Not Significantly Higher in Crohn’s Disease Patients Compared to Healthy Population , 2010, Digestive Diseases and Sciences.

[52]  Paul M Ridker,et al.  Inflammation in atherosclerosis: from pathophysiology to practice. , 2009, Journal of the American College of Cardiology.

[53]  B. Benzaquen,et al.  Screening for subclinical coronary artery disease measuring carotid intima media thickness. , 2009, The American journal of cardiology.

[54]  R. D'Incà,et al.  Reduced Endothelial Progenitor Cell Number and Function in Inflammatory Bowel Disease: A Possible Link to the Pathogenesis , 2009, The American Journal of Gastroenterology.

[55]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement , 2009, BMJ.

[56]  I. Roifman,et al.  Evidence of endothelial dysfunction in patients with inflammatory bowel disease. , 2009, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[57]  Mohsen Sadatsafavi,et al.  Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. , 2008, Arthritis and rheumatism.

[58]  D. Hommes,et al.  Enhanced atherogenesis and altered high density lipoprotein in patients with Crohn's disease Published, JLR Papers in Press, September 22, 2007. , 2007, Journal of Lipid Research.

[59]  Alex J Sutton,et al.  Performance of the trim and fill method in the presence of publication bias and between‐study heterogeneity , 2007, Statistics in medicine.

[60]  F. Hsu,et al.  Brachial Flow-Mediated Dilation Predicts Incident Cardiovascular Events in Older Adults: The Cardiovascular Health Study , 2007, Circulation.

[61]  Z. Halpern,et al.  Inflammatory Bowel Disease Is Not Associated With Increased Intimal Media Thickening , 2007, The American Journal of Gastroenterology.

[62]  R. Sacco,et al.  The association between endothelial dysfunction and cardiovascular outcomes in a population-based multi-ethnic cohort. , 2007, Atherosclerosis.

[63]  H. Struijker‐Boudier,et al.  Expert consensus document on arterial stiffness: methodological issues and clinical applications. , 2006, European heart journal.

[64]  Gilles Chironi,et al.  Performance of Subclinical Arterial Disease Detection as a Screening Test for Coronary Heart Disease , 2006, Hypertension.

[65]  O. Kocaman,et al.  Endothelial dysfunction in patients with ulcerative colitis , 2006, Inflammatory bowel diseases.

[66]  A. Gasbarrini,et al.  Early atherosclerosis in patients with inflammatory bowel disease. , 2006, European review for medical and pharmacological sciences.

[67]  A. Gasbarrini,et al.  Increased carotid intima–media thickness in patients with inflammatory bowel disease , 2005, Alimentary pharmacology & therapeutics.

[68]  A. Smit,et al.  Measurement of arterial wall thickness as a surrogate marker for atherosclerosis. , 2004, Circulation.

[69]  S. Feinstein,et al.  Emerging, noninvasive surrogate markers of atherosclerosis , 2004, Current atherosclerosis reports.

[70]  J. Schwartz,et al.  Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. , 2003, The New England journal of medicine.

[71]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

[72]  S. Thompson,et al.  Quantifying heterogeneity in a meta‐analysis , 2002, Statistics in medicine.

[73]  G. McColl,et al.  Accelerated atherosclerosis: an extraarticular feature of rheumatoid arthritis? , 2002, Arthritis and rheumatism.

[74]  P. Libby,et al.  Inflammation and Atherosclerosis , 2002, Circulation.

[75]  F. Ruschitzka,et al.  Anti–Tumor Necrosis Factor-&agr; Treatment Improves Endothelial Function in Patients With Rheumatoid Arthritis , 2002, Circulation.

[76]  Jonathan A C Sterne,et al.  Systematic reviews in health care: Investigating and dealing with publication and other biases in meta-analysis. , 2001, BMJ.

[77]  Eary,et al.  CAROTID-ARTERY INTIMA AND MEDIA THICKNESS AS A RISK FACTOR FOR MYOCARDIAL INFARCTION AND STROKE IN OLDER ADULTS , 2000 .

[78]  R. Kronmal,et al.  Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. , 1999, The New England journal of medicine.

[79]  J. Salonen,et al.  ULTRASONOGRAPHY: INTER- AND INTRA-OBSERVER VARIABILITY , 1991 .

[80]  N. Laird,et al.  Meta-analysis in clinical trials. , 1986, Controlled clinical trials.