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28.04.2020 | original article

Plasma lipids in patients with inflammatory bowel disease

Observations on the associations between lipid indices and coronary flow reserve

verfasst von: Şeref Kul, MD, Zuhal Çalışkan, MD, Tolga Sinan Güvenç, MD, Rengin Çetin Güvenç, MD, Mustafa Çalışkan, MD

Erschienen in: Wiener klinische Wochenschrift | Ausgabe 11-12/2020

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Summary

Background and aims

Patients with inflammatory bowel disease (IBD) are at increased risk for coronary artery disease (CAD), even after adjusting for traditional risk factors for atherosclerosis. While inflammation is widely regarded as the pathophysiologic link between IBD and CAD, the exact mechanisms are largely unknown. This study was conducted to investigate the association of lipid parameters and indices with coronary flow reserve and markers of inflammation in IBD patients.

Methods

A total of 73 patients with IBD and 26 healthy controls were enrolled. Patients in the IBD arm were either in remission or had mild disease activity. Lipid parameters, C‑reactive protein (CRP) and erythrocyte sedimentation rate (ESR) were analyzed using standard laboratory techniques. Coronary flow reserve (CFR) was measured using two-dimensional echocardiography.

Results

Both CRP and ESR were higher and CFR was significantly lower in IBD patients, but there were no differences in terms of lipid parameters or indices; however, patients with IBD and a CFR <2.0 had significantly higher triglyceride (TG) level (155.0 (80.0) mg/dl vs. 108.0 (68.0) mg/dl, p < 0.001) and there was a strong trend towards lower high-density lipoprotein (HDL) cholesterol (40.0 (8.5) mg/dl vs. 45.0 (10.0) mg/dl, p = 0.05) level in the latter group when compared to patients with a CFR ≥2.0. The atherogenic index of plasma (AIP), measured as log(TG/HDL-C) had the best predictive value for CFR in IBD group and was an independent predictor of CFR after multivariate adjustment for confounders (unstandardized coefficient: −0.75, 95% CI: (−1.13)–(−0.37)), β = −0.41, p = <0.001).

Conclusion

The atherogenic index of plasma is a marker for reduced CFR in IBD patients and could be useful to screen those at risk for early atherogenesis and CAD.
Literatur
1.
Zurück zum Zitat Bernstein CN, Wajda A, Blanchard JF. The incidence of arterial thromboembolic diseases in inflammatory bowel disease: a population-based study. Clin Gastroenterol Hepatol. 2008;6:41–5.PubMed Bernstein CN, Wajda A, Blanchard JF. The incidence of arterial thromboembolic diseases in inflammatory bowel disease: a population-based study. Clin Gastroenterol Hepatol. 2008;6:41–5.PubMed
2.
Zurück zum Zitat Ha C, Magowan S, Accortt NA, Chen J, Stone CD. Risk of arterial thrombotic events in inflammatory bowel disease. Am J Gastroenterol. 2009;104:1445–51.PubMed Ha C, Magowan S, Accortt NA, Chen J, Stone CD. Risk of arterial thrombotic events in inflammatory bowel disease. Am J Gastroenterol. 2009;104:1445–51.PubMed
3.
Zurück zum Zitat Yarur AJ, Deshpande AR, Pechman DM, Tamariz L, Abreu MT, Sussman DA. Inflammatory bowel disease is associated with an increased incidence of cardiovascular events. Am J Gastroenterol. 2011;106:741–7.PubMed Yarur AJ, Deshpande AR, Pechman DM, Tamariz L, Abreu MT, Sussman DA. Inflammatory bowel disease is associated with an increased incidence of cardiovascular events. Am J Gastroenterol. 2011;106:741–7.PubMed
4.
Zurück zum Zitat Rungoe C, Basit S, Ranthe MF, Wohlfahrt J, Langholz E, Jess T. Risk of ischaemic heart disease in patients with inflammatory bowel disease: a nationwide Danish cohort study. Gut. 2013;62:689–94.PubMed Rungoe C, Basit S, Ranthe MF, Wohlfahrt J, Langholz E, Jess T. Risk of ischaemic heart disease in patients with inflammatory bowel disease: a nationwide Danish cohort study. Gut. 2013;62:689–94.PubMed
5.
Zurück zum Zitat Singh S, Singh H, Loftus EV Jr, Pardi DS. Risk of cerebrovascular accidents and ischemic heart disease in patients with inflammatory bowel disease: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2014;12:382–93.PubMed Singh S, Singh H, Loftus EV Jr, Pardi DS. Risk of cerebrovascular accidents and ischemic heart disease in patients with inflammatory bowel disease: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2014;12:382–93.PubMed
7.
Zurück zum Zitat Prasad M, Hermann J, Gabriel SE, Weyand CM, Mulvagh S, Mankad R, et al. Cardiorheumatology: cardiac involvement in systemic rheumatic disease. Nat Rev Cardiol. 2014;12(3):168–76.PubMedPubMedCentral Prasad M, Hermann J, Gabriel SE, Weyand CM, Mulvagh S, Mankad R, et al. Cardiorheumatology: cardiac involvement in systemic rheumatic disease. Nat Rev Cardiol. 2014;12(3):168–76.PubMedPubMedCentral
9.
Zurück zum Zitat Sappati Biyyani RS, Putka BS, Mullen KD. Dyslipidemia and lipoprotein profiles in patients with inflammatory bowel disease. J Clin Lipidol. 2010;4:478–82.PubMed Sappati Biyyani RS, Putka BS, Mullen KD. Dyslipidemia and lipoprotein profiles in patients with inflammatory bowel disease. J Clin Lipidol. 2010;4:478–82.PubMed
10.
Zurück zum Zitat Romanato G, Scarpa M, Angriman I, et al. Plasma lipids and inflammation in active inflammatory bowel diseases. Aliment Pharmacol Ther. 2009;29:298–307.PubMed Romanato G, Scarpa M, Angriman I, et al. Plasma lipids and inflammation in active inflammatory bowel diseases. Aliment Pharmacol Ther. 2009;29:298–307.PubMed
11.
Zurück zum Zitat Ripolles Piquer B, Nazih H, Bourreille A, et al. Altered lipid, apolipoprotein, and lipoprotein profiles in inflammatory bowel disease: consequences on the cholesterol efflux capacity of serum using Fu5AH cell system. Metabolism. 2006;55:980–8.PubMed Ripolles Piquer B, Nazih H, Bourreille A, et al. Altered lipid, apolipoprotein, and lipoprotein profiles in inflammatory bowel disease: consequences on the cholesterol efflux capacity of serum using Fu5AH cell system. Metabolism. 2006;55:980–8.PubMed
12.
Zurück zum Zitat Koutroubakis IE, Malliaraki N, Vardas E, et al. Increased levels of lipoprotein (a) in Crohn’s disease: a relation to thrombosis? Eur J Gastroenterol Hepatol. 2001;13:1415–9.PubMed Koutroubakis IE, Malliaraki N, Vardas E, et al. Increased levels of lipoprotein (a) in Crohn’s disease: a relation to thrombosis? Eur J Gastroenterol Hepatol. 2001;13:1415–9.PubMed
13.
Zurück zum Zitat Ingelsson E, Schaefer EJ, Contois JH, McNamara JR, Sullivan L, Keyes MJ, et al. Clinical utility of different lipid measures for prediction of coronary heart disease in men and women. JAMA. 2007;298(7):776.PubMed Ingelsson E, Schaefer EJ, Contois JH, McNamara JR, Sullivan L, Keyes MJ, et al. Clinical utility of different lipid measures for prediction of coronary heart disease in men and women. JAMA. 2007;298(7):776.PubMed
14.
Zurück zum Zitat Emerging Risk Factors Collaboration, Di Angelantonio E, Sarwar N, Perry P, Kaptoge S, Ray KK, et al. Major lipids, apolipoproteins, and risk of vascular disease. JAMA. 2009;302(18):1993–2000. Emerging Risk Factors Collaboration, Di Angelantonio E, Sarwar N, Perry P, Kaptoge S, Ray KK, et al. Major lipids, apolipoproteins, and risk of vascular disease. JAMA. 2009;302(18):1993–2000.
15.
Zurück zum Zitat Onat A, Can G, Kaya H, et al. Atherogenic index of plasma (log10 triglyceride/high-density lipoprotein cholesterol) predicts high blood pressure, diabetes, and vascular events. J Clin Lipidol. 2010;4:89–98.PubMed Onat A, Can G, Kaya H, et al. Atherogenic index of plasma (log10 triglyceride/high-density lipoprotein cholesterol) predicts high blood pressure, diabetes, and vascular events. J Clin Lipidol. 2010;4:89–98.PubMed
17.
Zurück zum Zitat Dobiásová M, Frohlich J. The plasma parameter log (TG/HDL-C) as an atherogenic index: correlation with lipoprotein particle size and esterification rate in apoB-lipoprotein-depleted plasma (FER(HDL)). Clin Biochem. 2001;34(7):583–8.PubMed Dobiásová M, Frohlich J. The plasma parameter log (TG/HDL-C) as an atherogenic index: correlation with lipoprotein particle size and esterification rate in apoB-lipoprotein-depleted plasma (FER(HDL)). Clin Biochem. 2001;34(7):583–8.PubMed
18.
Zurück zum Zitat Quispe R, Manalac RJ, Faridi KF, et al. Relationship of the triglyceride to high-density lipoprotein cholesterol (TG/HDL-C) ratio to the remainder of the lipid profile: the Very Large Database of Lipids‑4 (VLDL-4) study. Atherosclerosis. 2015;242(1):243–50.PubMed Quispe R, Manalac RJ, Faridi KF, et al. Relationship of the triglyceride to high-density lipoprotein cholesterol (TG/HDL-C) ratio to the remainder of the lipid profile: the Very Large Database of Lipids‑4 (VLDL-4) study. Atherosclerosis. 2015;242(1):243–50.PubMed
19.
Zurück zum Zitat Arcaro G, Zenere BM, Travia D, Zenti MG, Covi G, Lechi A, et al. Non-invasive detection of early endothelial dysfunction in hypercholesterolaemic subjects. Atherosclerosis. 1995;114:247–54.PubMed Arcaro G, Zenere BM, Travia D, Zenti MG, Covi G, Lechi A, et al. Non-invasive detection of early endothelial dysfunction in hypercholesterolaemic subjects. Atherosclerosis. 1995;114:247–54.PubMed
20.
Zurück zum Zitat Dayanikli F, Grambow D, Muzik O, Mosca L, Rubenfire M, Schwaiger M. Early detection of abnormal coronary flow reserve in asymptomatic men at high risk for coronary artery disease using positron emission tomography. Circulation. 1994;90:808–17.PubMed Dayanikli F, Grambow D, Muzik O, Mosca L, Rubenfire M, Schwaiger M. Early detection of abnormal coronary flow reserve in asymptomatic men at high risk for coronary artery disease using positron emission tomography. Circulation. 1994;90:808–17.PubMed
21.
Zurück zum Zitat Clarkson P, Celermajer DS, Powe AJ, Donald AE, Henry RM, Deanfield JE. Endothelium-dependent dilatation is impaired in young healthy subjects with a family history of premature coronary disease. Circulation. 1997;96:3378–83.PubMed Clarkson P, Celermajer DS, Powe AJ, Donald AE, Henry RM, Deanfield JE. Endothelium-dependent dilatation is impaired in young healthy subjects with a family history of premature coronary disease. Circulation. 1997;96:3378–83.PubMed
22.
Zurück zum Zitat Bernstein CN, Eliakim A, Fedail S, Fried M, Gearry R, Goh KL, et al. World Gastroenterology Organisation global guidelines inflammatory bowel disease: update August 2015. J Clin Gastroenterol. 2016;50(10):803–18.PubMed Bernstein CN, Eliakim A, Fedail S, Fried M, Gearry R, Goh KL, et al. World Gastroenterology Organisation global guidelines inflammatory bowel disease: update August 2015. J Clin Gastroenterol. 2016;50(10):803–18.PubMed
23.
Zurück zum Zitat Best WR, Becktel JM, Singleton JW, Kern F Jr. Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology. 1976;70:439–44.PubMed Best WR, Becktel JM, Singleton JW, Kern F Jr. Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology. 1976;70:439–44.PubMed
24.
Zurück zum Zitat Turner D, Seow CH, Greenberg GR, Griffiths AM, Silverberg MS, Steinhart AH. A systematic prospective comparison of noninvasive disease activity indices in ulcerative colitis. Clin Gastroenterol Hepatol. 2009;7(10):1081–8.PubMed Turner D, Seow CH, Greenberg GR, Griffiths AM, Silverberg MS, Steinhart AH. A systematic prospective comparison of noninvasive disease activity indices in ulcerative colitis. Clin Gastroenterol Hepatol. 2009;7(10):1081–8.PubMed
25.
Zurück zum Zitat Castelli WP, Abbott RD, McNamara PM. Summary estimates of cholesterol used to predict coronary heart disease. Circulation. 1983;67(4):730–4.PubMed Castelli WP, Abbott RD, McNamara PM. Summary estimates of cholesterol used to predict coronary heart disease. Circulation. 1983;67(4):730–4.PubMed
26.
Zurück zum Zitat Nunes SO, Piccoli de Melo LG, Pizzo de Castro MR, Barbosa DS, Vargas HO, Berk M, et al. Atherogenic index of plasma and atherogenic coefficient are increased in major depression and bipolar disorder, especially when comorbid with tobacco use disorder. J Affect Disord. 2015;172:55–62. https://doi.org/10.1016/j.jad.2014.09.038.CrossRefPubMed Nunes SO, Piccoli de Melo LG, Pizzo de Castro MR, Barbosa DS, Vargas HO, Berk M, et al. Atherogenic index of plasma and atherogenic coefficient are increased in major depression and bipolar disorder, especially when comorbid with tobacco use disorder. J Affect Disord. 2015;172:55–62. https://​doi.​org/​10.​1016/​j.​jad.​2014.​09.​038.CrossRefPubMed
27.
Zurück zum Zitat Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity. 2013;38:1092–104.PubMedPubMedCentral Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity. 2013;38:1092–104.PubMedPubMedCentral
28.
Zurück zum Zitat Theocharidou E, Gossios TD, Giouleme O, Athyros VG, Karagiannis A. Carotid intima-media thickness in patients with inflammatory bowel disease: a systematic review. Angiology. 2014;65:284–93.PubMed Theocharidou E, Gossios TD, Giouleme O, Athyros VG, Karagiannis A. Carotid intima-media thickness in patients with inflammatory bowel disease: a systematic review. Angiology. 2014;65:284–93.PubMed
29.
Zurück zum Zitat Zanoli L, Cannavo M, Rastelli S, Di PL, Monte I, Di GM, et al. Arterial stiffness is increased in patients with inflammatory bowel disease. J Hypertens. 2012;30:1775–81.PubMed Zanoli L, Cannavo M, Rastelli S, Di PL, Monte I, Di GM, et al. Arterial stiffness is increased in patients with inflammatory bowel disease. J Hypertens. 2012;30:1775–81.PubMed
32.
Zurück zum Zitat Sellke FW, Armstrong ML, Harrison DG. Endothelium-dependent vascular relaxation is abnormal in the coronary microcirculation of atherosclerotic primates. Circulation. 1990;81:1586.PubMed Sellke FW, Armstrong ML, Harrison DG. Endothelium-dependent vascular relaxation is abnormal in the coronary microcirculation of atherosclerotic primates. Circulation. 1990;81:1586.PubMed
33.
Zurück zum Zitat Laaksonen R, Janatuinen T, Vesalainen R, Lehtimäki T, Elovaara I, Jaakkola O, et al. High oxidized LDL and elevated plasma homocysteine contribute to the early reduction of myocardial flow reserve in healthy adults. Eur J Clin Invest. 2002;32(11):795–802.PubMed Laaksonen R, Janatuinen T, Vesalainen R, Lehtimäki T, Elovaara I, Jaakkola O, et al. High oxidized LDL and elevated plasma homocysteine contribute to the early reduction of myocardial flow reserve in healthy adults. Eur J Clin Invest. 2002;32(11):795–802.PubMed
34.
Zurück zum Zitat Berliner JA, Navab M, Fogelman AM, Frank JS, Demer LL, Edwards PA, et al. Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation. 1995;91(9):2488.PubMed Berliner JA, Navab M, Fogelman AM, Frank JS, Demer LL, Edwards PA, et al. Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation. 1995;91(9):2488.PubMed
35.
Zurück zum Zitat Nissen SE. The Jupiter trial: key findings, controversies, and implications. Curr Cardiol Rep. 2009;11(2):81–2.PubMed Nissen SE. The Jupiter trial: key findings, controversies, and implications. Curr Cardiol Rep. 2009;11(2):81–2.PubMed
37.
Zurück zum Zitat Austin MA, King MC, Vranizan KM, Krauss RM. Atherogenic lipoprotein phenotype. A proposed genetic marker for coronary heart disease risk. Circulation. 1990;82(2):495–506.PubMed Austin MA, King MC, Vranizan KM, Krauss RM. Atherogenic lipoprotein phenotype. A proposed genetic marker for coronary heart disease risk. Circulation. 1990;82(2):495–506.PubMed
38.
Zurück zum Zitat Fujimoto K, Hozumi T, Watanabe H, Shimada K, Takeuchi M, Sakanoue Y, et al. Effect of fluvastatin therapy on coronary flow reserve in patients with hypercholesterolemia. Am J Cardiol. 2004;93(11):1419–21, A10.PubMed Fujimoto K, Hozumi T, Watanabe H, Shimada K, Takeuchi M, Sakanoue Y, et al. Effect of fluvastatin therapy on coronary flow reserve in patients with hypercholesterolemia. Am J Cardiol. 2004;93(11):1419–21, A10.PubMed
39.
Zurück zum Zitat Yokoyama I, Ohtake T, Momomura S, Nishikawa J, Sasaki Y, Omata M. Reduced coronary flow reserve in hypercholesterolemic patients without overt coronary stenosis. Circulation. 1996;94:3232–8.PubMed Yokoyama I, Ohtake T, Momomura S, Nishikawa J, Sasaki Y, Omata M. Reduced coronary flow reserve in hypercholesterolemic patients without overt coronary stenosis. Circulation. 1996;94:3232–8.PubMed
40.
Zurück zum Zitat Otvos JD, Jeyarajah EJ, Bennett DW, Krauss RM. Development of a proton nuclear magnetic resonance spectroscopic method for determining plasma lipoprotein concentrations and subspecies distributions from a single, rapid measurement. Clin Chem. 1992;38(9):1632.PubMed Otvos JD, Jeyarajah EJ, Bennett DW, Krauss RM. Development of a proton nuclear magnetic resonance spectroscopic method for determining plasma lipoprotein concentrations and subspecies distributions from a single, rapid measurement. Clin Chem. 1992;38(9):1632.PubMed
41.
Zurück zum Zitat Talmud PJ, Edwards KL, Turner CM, Newman B, Palmen JM, Humphries SE, et al. Linkage of the cholesteryl ester transfer protein (CETP) gene to LDL particle size: use of a novel tetranucleotide repeat within the CETP promoter. Circulation. 2000;101(21):2461.PubMed Talmud PJ, Edwards KL, Turner CM, Newman B, Palmen JM, Humphries SE, et al. Linkage of the cholesteryl ester transfer protein (CETP) gene to LDL particle size: use of a novel tetranucleotide repeat within the CETP promoter. Circulation. 2000;101(21):2461.PubMed
42.
Zurück zum Zitat Gardner CD, Fortmann SP, Krauss RM. Association of small low-density lipoprotein particles with the incidence of coronary artery disease in men and women. JAMA. 1996;276(11):875.PubMed Gardner CD, Fortmann SP, Krauss RM. Association of small low-density lipoprotein particles with the incidence of coronary artery disease in men and women. JAMA. 1996;276(11):875.PubMed
43.
Zurück zum Zitat Kathiresan S, Otvos JD, Sullivan LM, Keyes MJ, Schaefer EJ, Wilson PW, et al. Increased small low-density lipoprotein particle number: a prominent feature of the metabolic syndrome in the Framingham Heart Study. Circulation. 2006;113(1):20.PubMed Kathiresan S, Otvos JD, Sullivan LM, Keyes MJ, Schaefer EJ, Wilson PW, et al. Increased small low-density lipoprotein particle number: a prominent feature of the metabolic syndrome in the Framingham Heart Study. Circulation. 2006;113(1):20.PubMed
44.
Zurück zum Zitat Chait A, Brazg RL, Tribble DL, Krauss RM. Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am J Med. 1993;94(4):350.PubMed Chait A, Brazg RL, Tribble DL, Krauss RM. Susceptibility of small, dense, low-density lipoproteins to oxidative modification in subjects with the atherogenic lipoprotein phenotype, pattern B. Am J Med. 1993;94(4):350.PubMed
45.
Zurück zum Zitat Rosenson RS, Davidson MH, Hirsh BJ, Kathiresan S, Gaudet D. Genetics and causality of triglyceride-rich lipoproteins in atherosclerotic cardiovascular disease. J Am Coll Cardiol. 2014;64(23):2525–40.PubMed Rosenson RS, Davidson MH, Hirsh BJ, Kathiresan S, Gaudet D. Genetics and causality of triglyceride-rich lipoproteins in atherosclerotic cardiovascular disease. J Am Coll Cardiol. 2014;64(23):2525–40.PubMed
46.
Zurück zum Zitat Sarwar N, Danesh J, Eiriksdottir G, Sigurdsson G, Wareham N, Bingham S, et al. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies. Circulation. 2007;115(4):450.PubMed Sarwar N, Danesh J, Eiriksdottir G, Sigurdsson G, Wareham N, Bingham S, et al. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies. Circulation. 2007;115(4):450.PubMed
47.
Zurück zum Zitat Ballantyne CM, Grundy SM, Oberman A, Kreisberg RA, Havel RJ, Frost PH, et al. Hyperlipidemia: diagnostic and therapeutic perspectives. J Clin Endocrinol Metab. 2000;85(6):2089.PubMed Ballantyne CM, Grundy SM, Oberman A, Kreisberg RA, Havel RJ, Frost PH, et al. Hyperlipidemia: diagnostic and therapeutic perspectives. J Clin Endocrinol Metab. 2000;85(6):2089.PubMed
48.
Zurück zum Zitat Lundman P, Eriksson M, Schenck-Gustafsson K, Karpe F, Tornvall P. Transient triglyceridemia decreases vascular reactivity in young, healthy men without risk factors for coronary heart disease. Circulation. 1997;96(10):3266–8.PubMed Lundman P, Eriksson M, Schenck-Gustafsson K, Karpe F, Tornvall P. Transient triglyceridemia decreases vascular reactivity in young, healthy men without risk factors for coronary heart disease. Circulation. 1997;96(10):3266–8.PubMed
49.
Zurück zum Zitat Hozumi T, Eisenberg M, Sugioka K, Kokkirala AR, Watanabe H, Teragaki M, et al. Change in coronary flow reserve on transthoracic Doppler echocardiography after a single high-fat meal in young healthy men. Ann Intern Med. 2002;136(7):523–8.PubMed Hozumi T, Eisenberg M, Sugioka K, Kokkirala AR, Watanabe H, Teragaki M, et al. Change in coronary flow reserve on transthoracic Doppler echocardiography after a single high-fat meal in young healthy men. Ann Intern Med. 2002;136(7):523–8.PubMed
50.
Zurück zum Zitat Maddox TM, Stanislawski MA, Grunwald GK, Bradley SM, Ho PM, Tsai TT, et al. Nonobstructive coronary artery disease and risk of myocardial infarction. JAMA. 2014;312(17):1754–63.PubMedPubMedCentral Maddox TM, Stanislawski MA, Grunwald GK, Bradley SM, Ho PM, Tsai TT, et al. Nonobstructive coronary artery disease and risk of myocardial infarction. JAMA. 2014;312(17):1754–63.PubMedPubMedCentral
51.
Zurück zum Zitat Chow BJ, Small G, Yam Y, Chen L, Achenbach S, Al-Mallah M, et al. Incremental prognostic value of cardiac computed tomography in coronary artery disease using CONFIRM: COroNary computed tomography angiography evaluation for clinical outcomes: an InteRnational Multicenter registry. Circ Cardiovasc Imaging. 2011;4(5):463–72.PubMed Chow BJ, Small G, Yam Y, Chen L, Achenbach S, Al-Mallah M, et al. Incremental prognostic value of cardiac computed tomography in coronary artery disease using CONFIRM: COroNary computed tomography angiography evaluation for clinical outcomes: an InteRnational Multicenter registry. Circ Cardiovasc Imaging. 2011;4(5):463–72.PubMed
52.
Zurück zum Zitat Rigo F, Cortigiani L, Pasanisi E, Richieri M, Cutaia V, Celestre M, et al. The additional prognostic value of coronary flow reserve on left anterior descending artery in patients with negative stress echo by wall motion criteria: a transthoracic vasodilator stress echocardiography study. Am Heart J. 2006;151:124–30.PubMed Rigo F, Cortigiani L, Pasanisi E, Richieri M, Cutaia V, Celestre M, et al. The additional prognostic value of coronary flow reserve on left anterior descending artery in patients with negative stress echo by wall motion criteria: a transthoracic vasodilator stress echocardiography study. Am Heart J. 2006;151:124–30.PubMed
Metadaten
Titel
Plasma lipids in patients with inflammatory bowel disease
Observations on the associations between lipid indices and coronary flow reserve
verfasst von
Şeref Kul, MD
Zuhal Çalışkan, MD
Tolga Sinan Güvenç, MD
Rengin Çetin Güvenç, MD
Mustafa Çalışkan, MD
Publikationsdatum
28.04.2020
Verlag
Springer Vienna
Erschienen in
Wiener klinische Wochenschrift / Ausgabe 11-12/2020
Print ISSN: 0043-5325
Elektronische ISSN: 1613-7671
DOI
https://doi.org/10.1007/s00508-020-01649-2

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