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Gender-specific patterns of carotid atherosclerosis in patients with inflammatory bowel disease: a case-control study

https://doi.org/10.15829/1728-8800-2026-4457

EDN: TKYZRX

Abstract

Aim. To study the influence of sex on the ultrasound plaque morphology and the burden of atherosclerosis in patients with inflammatory bowel disease (IBD) and carotid atherosclerosis.

Material and methods. This case-control study included 59 patients (28 women and 31 men) aged 40-64 years with IBD and carotid atherosclerosis. The control group (n=149, 56 women and 93 men) was recruited from a database of patients with carotid plaques. All patients underwent carotid duplex ultrasound to determine plaque echogenicity and measure the maximum height, total height, and total area of plaques.

Results. The carotid plaque echogenicity was significantly lower in women with IBD compared to the control group (p=0,011). The maximum and total heights of carotid plaques, as well as the total area of carotid plaques, were higher in women with IBD compared to the control group (p=0,001; p=0,003; p=0,026, respectively). IBD in women was associated with a 4,14-fold increase in the odds ratio of hypoechoic carotid plaques (95% confidence interval: 1,11-15,5; p=0,035) after adjusting for age, obesity, smoking, hypertension, low-density lipoprotein cholesterol, triglyceride, glucose levels, and lipid-lowering therapy.

Conclusion. Women with IBD had lower echogenicity of carotid plaques and higher carotid atherosclerosis burden scores compared with age-matched controls. IBD is associated with an increased probability of hypoechoic carotid plaques among women.

About the Authors

V. V. Genkel
South Ural State Medical University
Russian Federation

MD, Dr. Sci. (Med.), Associate Professor, Associate Professor of the Department of Internal Medicine Propaedeutics, South Ural State Medical University

Chelyabinsk



Ya. I. Zaripova
South Ural State Medical University
Russian Federation

Assistant of the Department of Internal Medicine Propaedeutics, South Ural State Medical University

Chelyabinsk



A. S. Sluchanko
South Ural State Medical University
Russian Federation

Assistant of the Department of Hospital Therapy, South Ural State Medical University

Chelyabinsk



E. V. Lebedev
South Ural State Medical University
Russian Federation

MD, Cand. Sci. (Med.), Associate Professor, Associate Professor of the Department of Internal Medicine Propaedeutics, South Ural State Medical University

Chelyabinsk



L. R. Pykhova
South Ural State Medical University
Russian Federation

Cand. Sci. (Biol.), Associate Professor of the Department of Microbiology, Virology and Immunology, South Ural State Medical University

Chelyabinsk



V. A. Sumerkina
South Ural State Medical University
Russian Federation

MD, Cand. Sci. (Med.), Associate Professor, Head of the Central Research Laboratory, South Ural State Medical University

Chelyabinsk



K. V. Nikushkina
South Ural State Medical University
Russian Federation

Cand. Sci. (Med.), Clinical Laboratory Diagnostics Doctor of the Research Institute of Immunology, South Ural State Medical University

Chelyabinsk



A. S. Kuznetsova
South Ural State Medical University
Russian Federation

MD, Cand. Sci. (Med.), Associate Professor, Associate Professor of the Department of Hospital Therapy, South Ural State Medical University

Chelyabinsk



A. A. Saenko
South Ural State Medical University
Russian Federation

MD, Cand. Sci. (Med.), Associate Professor of the Department of Hospital Therapy, South Ural State Medical University

Chelyabinsk



S. A. Merkulova
South Ural State Medical University
Russian Federation

Head of the Gastroenterology Department, City Clinical Hospital №1 of Chelyabinsk

Chelyabinsk



A. I. Dolgushina
South Ural State Medical University
Russian Federation

MD, Dr. Sci. (Med.), Professor, Head of the Department of Hospital Therapy, South Ural State Medical University

Chelyabinsk



References

1. Fomicheva OA, Balakhonova TV, Pogorelova OA, et al. Peripheral plaque burden in the diagnosis of coronary atherosclerosis in rheumatoid arthritis. Russian Journal of Cardiology. 2024;29(8): 5902. (In Russ.) doi:10.15829/1560-4071-2024-5902.

2. Follin-Arbelet B, Cvancarova Småstuen M, Hovde Ø, et al. Mortality in Patients with Inflammatory Bowel Disease: Results from 30 Years of Follow-up in a Norwegian Inception Cohort (the IBSEN study). J Crohns Colitis. 2023;17(4):497-503. doi:10.1093/ecco-jcc/jjac156.

3. Bikbavova GB, Livzan MA. Cardiovascular risks in patients with inflammatory bowel disease: what should be taken into account? Experimental and Clinical Gastroenterology. 2021;1(6):112-20. (In Russ.) doi:10.31146/1682-8658-ecg-190-6-112-120.

4. D'Ascenzo F, Bruno F, Iannaccone M, et al. Patients with inflammatory bowel disease are at increased risk of atherothrombotic disease: A systematic review with meta-analysis. Int J Cardiol. 2023;378:96-104. doi:10.1016/j.ijcard.2023.02.042.

5. Sleutjes JAM, van der Woude CJ, Verploegh PJP, et al. Cardiovascular risk profiles in patients with inflammatory bowel disease differ from matched controls from the general population. Eur J Prev Cardiol. 2023;30(15):1615-22. doi:10.1093/eurjpc/zwad124.

6. Sinh P, Cross RK. Cardiovascular Comorbidities and Inflammatory Bowel Disease: Causes and Consequences. Gastroenterol Hepatol (N Y). 2024;20(4):204-15.

7. Marín-Jiménez I, Carpio D, Hernández V, et al. Spanish Working Group in Crohn's Disease and Ulcerative Colitis (GETECCU) position paper on cardiovascular disease in patients with inflammatory bowel disease. Gastroenterol Hepatol. 2025;48(5):502314. doi:10.1016/j.gastrohep.2024.502314.

8. Isaev GO, Trushina OIu, Isaikina MA, et al. The effect of inflammatory bowel diseases on the risk of atherosclerosis: assessment according to ultrasound imaging and sphygmometry. Terapevticheskii Arkhiv. 2025;97(1):29-34. (In Russ.) doi:10.26442/00403660.2025.01.203028.

9. Nasir K, Acquah I, Dey AK, et al. Inflammatory bowel disease and atherosclerotic cardiovascular disease in U.S. adults-A population-level analysis in the national health interview survey. Am J Prev Cardiol. 2022;9:100316. doi:10.1016/j.ajpc.2022.100316.

10. Alayo QA, Loftus EV Jr, Yarur A, et al. Inflammatory Bowel Disease Is Associated With an Increased Risk of Incident Acute Arterial Events: Analysis of the United Kingdom Biobank. Clin Gastroenterol Hepatol. 2023;21(3):761-70.e13. doi:10.1016/j.cgh.2022.08.035.

11. Fang L, Gao H, Gao X, et al. Risks of Cardiovascular Events in Patients With Inflammatory Bowel Disease in China: A Retrospective Multicenter Cohort Study. Inflamm Bowel Dis. 2022;28:52-8. doi:10.1093/ibd/izab326.

12. Olivera PA, Zuily S, Kotze PG, et al. International consensus on the prevention of venous and arterial thrombotic events in patients with inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2021;18(12):857-73. doi:10.1038/s41575-021-00492-8.

13. Naami R, Tashtish N, Neeland IJ, et al. Coronary artery calcium scoring for cardiovascular risk assessment in patients with inflammatory bowel disease. Am Heart J. 2023;266:120-7. doi:10.1016/j.ahj.2023.08.011.

14. Genkel VV, Kuznetsova AS, Lebedev EV, et al. Factors associated with atherosclerotic plaque echogenicity in patients aged 40-64 with carotid atherosclerosis. Kardiologiia. 2021;61(6):35-40. (In Russ.) doi:10.18087/cardio.2021.6.n1536.

15. Pogorelova OA, Tripoten MA, Hamchieva LSh, et al. Echogenicity of atherosclerotic plaque — a criterion for assessing the dynamics and prognosis of cardiovascular diseases. Ultrasound & Functional Diagnostics. 2023;(4):35-48. (In Russ.) 24835/1607-0771-2023-4-35-48.

16. Genkel V, Kuznetsova A, Lebedev E, et al. Carotid total plaque area as an independent predictor of short-term subclinical polyvascular atherosclerosis progression and major adverse cardiac and cerebrovascular events. Ther Adv Cardiovasc Dis. 2023; 17:17539447231194861. doi:10.1177/17539447231194861.

17. Magni P. The sex-associated burden of atherosclerotic cardiovascular diseases: An update on prevention strategies. Mech Ageing Dev. 2023;212:111805. doi:10.1016/j.mad.2023.111805.

18. Man JJ, Beckman JA, Jaffe IZ. Sex as a Biological Variable in Atherosclerosis. Circ Res. 2020;126(9):1297-319. doi:10.1161/ CIRCRESAHA.120.315930.

19. Drapkina OM, Kim OT. Sex and gender differences in health and disease. Part II. Clinical and medical-social. Cardiovascular Therapy and Prevention. 2023;22(12):3831. (In Russ.) doi:10. 15829/1728-8800-2023-3831. EDN: WJNNUC.

20. Kim HL. Differences in Risk Factors for Coronary Atherosclerosis According to Sex. J Lipid Atheroscler. 2024;13(2):97-110. doi:10.12997/jla.2024.13.2.97.

21. Rajendran A, Minhas AS, Kazzi B, et al. Sex-specific differences in cardiovascular risk factors and implications for cardiovascular disease prevention in women. Atherosclerosis. 2023;384:117269. doi:10.1016/j.atherosclerosis.2023.117269.

22. Ajoolabady A, Pratico D, Lin L, et al. Inflammation in atherosclerosis: pathophysiology and mechanisms. Cell Death Dis. 2024; 15(11):817. doi:10.1038/s41419-024-07166-8.

23. Ershova AI, Balakhonova TV, Meshkov AN, et al. Prevalence of carotid and femoral artery atherosclerosis among the Ivanovo Oblast population: data from the ATEROGEN-Ivanovo study. Cardiovascular Therapy and Prevention. 2021;20(5):2994. (In Russ.) doi:10.15829/1728-8800-2021-2994.

24. Bermúdez-López M, Martínez-Alonso M, Castro-Boqué E, et al. Subclinical atheromatosis localization and burden in a lowto- moderate cardiovascular risk population: the ILERVAS study. Rev Esp Cardiol (Engl Ed). 2021;74(12):1042-53. doi:10.1016/j.rec.2020.09.015.

25. Ha C, Magowan S, Accortt NA, et al. Risk of arterial thrombotic events in inflammatory bowel disease. Am J Gastroenterol. 2009; 104(6):1445-51. doi:10.1038/ajg.2009.81.

26. Singh S, Singh H, Loftus EV Jr, et al. 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(3):382-93.e1:quiz e22. doi:10.1016/j.cgh. 2013.08.023.

27. Choi YJ, Lee DH, Shin DW, et al. Patients with inflammatory bowel disease have an increased risk of myocardial infarction: a nationwide study. Aliment Pharmacol Ther. 2019;50(7):769-79. doi:10. 1111/apt.15446.

28. Bigeh A, Sanchez A, Maestas C, et al. Inflammatory bowel disease and the risk for cardiovascular disease: Does all inflammation lead to heart disease? Trends Cardiovasc Med. 2020;30(8):463-9. doi:10.1016/j.tcm.2019.10.001.

29. Lungaro L, Costanzini A, Manza F, et al. Impact of Female Gender in Inflammatory Bowel Diseases: A Narrative Review. J Pers Med. 2023;13(2):165. doi:10.3390/jpm13020165.

30. Salem DA, El-Ijla R, AbuMusameh RR, et al. Sex-related differences in profiles and clinical outcomes of Inflammatory bowel disease: a systematic review and meta-analysis. BMC Gastroenterol. 2024;24(1):425. doi:10.1186/s12876-024-03514-2.

31. Civieri G, Abohashem S, Grewal SS, et al. Anxiety and Depression Associated With Increased Cardiovascular Disease Risk Through Accelerated Development of Risk Factors. JACC Adv. 2024;3(9): 101208. doi:10.1016/j.jacadv.2024.101208.

32. Rustgi SD, Kayal M, Shah SC. Sex-based differences in inflammatory bowel diseases: a review. Therap Adv Gastroenterol. 2020; 13:1756284820915043. doi:10.1177/1756284820915043.

33. Khlynova OV, Stepina EA. Disturbance of intestinal permeability and its role in the development of cardiovascular complications in persons with inflammatory bowel diseases. Experimental and Clinical Gastroenterology. 2022;(11):36-45. (In Russ.) doi:10.31146/1682-8658-ecg-207-11-36-45.

34. Li J, Chen Y, Yu Q, et al. Estrogen receptor β alleviates colitis in intestinal epithelial cells and activates HIF-1a and ATG-9a-mediated autophagy. Exp Cell Res. 2025;447(2):114520. doi:10.1016/j.yexcr.2025.114520.

35. Dong W, Peng Q, Liu Z, et al. Estrogen plays an important role by influencing the NLRP3 inflammasome. Biomed Pharmacother. 2023;167:115554. doi:10.1016/j.biopha.2023.115554.

36. Merrheim J, Villegas J, Van Wassenhove J, et al. Estrogen, estrogen- like molecules and autoimmune diseases. Autoimmun Rev. 2020;19(3):102468. doi:10.1016/j.autrev.2020.102468.

37. Constantin AM, Baicus C. Estradiol in Systemic Lupus Erythematosus. Acta Endocrinol (Buchar). 2023;19(2):274-6. doi:10.4183/aeb.2023.274.

38. Moran CA, Collins LF, Beydoun N, et al. Cardiovascular Implications of Immune Disorders in Women. Circ Res. 2022;130(4):593-610. doi:10.1161/CIRCRESAHA.121.319877.

39. Blumenstein I, Sonnenberg E. Sex- and gender-related differences in inflammatory bowel diseases. Front. Gastroenterol. 2023;2: 1199687. doi:10.3389/fgstr.2023.1199687.


What is already known about the subject?

  • Inflammatory bowel disease (IBD) increases the risk of atherosclerotic cardiovascular disease, despi­te a lower prevalence of traditional risk factors.
  • Data on the influence of sex on the risk of cardio­vas­cular disease in patients with IBD are incon­sis­tent.

What might this study add?

  • Women with IBD and carotid atherosclerosis are cha­rac­terized by lower echogenicity of carotid pla­ques and higher atherosclerotic burden compa­red with age-matched controls.
  • A diagnosis of IBD was associated with an increa­sed odds ratio for hypoechoic carotid plaques in a model adjusted for age, obesity, smoking, hyper­ten­sion, low-density lipoprotein cholesterol, trigly­ce­ri­des, glucose, and lipid-­lowering therapy among wo­men only.

Review

For citations:


Genkel V.V., Zaripova Ya.I., Sluchanko A.S., Lebedev E.V., Pykhova L.R., Sumerkina V.A., Nikushkina K.V., Kuznetsova A.S., Saenko A.A., Merkulova S.A., Dolgushina A.I. Gender-specific patterns of carotid atherosclerosis in patients with inflammatory bowel disease: a case-control study. Cardiovascular Therapy and Prevention. 2026;25(1):4457. (In Russ.) https://doi.org/10.15829/1728-8800-2026-4457. EDN: TKYZRX

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ISSN 1728-8800 (Print)
ISSN 2619-0125 (Online)