Skip to main content

Advertisement

Log in

Shear wave elastography in evaluation of carotid elasticity in the type 2 diabetes mellitus patients with nonalcoholic fatty liver disease

  • Original Article
  • Published:
International Journal of Diabetes in Developing Countries Aims and scope Submit manuscript

Abstract

Purpose

Using shear wave elastography (SWE) to assess carotid elasticity in the type 2 diabetes mellitus (T2DM) patients with non-alcoholic fatty liver disease (NAFLD).

Methods

There were 98 patients diagnosed T2DM in our hospital, including 35 cases without NAFLD (group A), 33 cases with mild NAFLD (group B), and 30 cases with moderate to severe NAFLD (group C) according to the classification standard of fatty liver. There was no plaque by carotid ultrasound in all the selected patients. The left carotid intima-media thickness (IMT), standard carotid arterial systolic diameter (Ds), standard carotid arterial diastolic diameter (Dd), and systolic peak velocity (PSV) were measured by routine two-dimensional and M-mode ultrasound, and the stiffness coefficient (β) is obtained by calculation. Shear wave elastography (SWE) was used to measure the anterior wall of the left carotid artery values of longitudinal elastic modulus, including the mean values of mean elastic modulus (MEmean), the maximum elastic modulus (MEmax), and minimum elastic modulus (MEmin) at the end of diastole.

Results

There was no significant difference in Ds, Dd, and PSV among the groups (all p > 0.05). In group C, IMT, β, MEmean, MEmax, and MEmin increased significantly compared with groups A and B (all p < 0.05). Compared with group A, MEmean, MEmax, and MEmin increased in group B (all p < 0.05), while IMT and β were no significant difference (both p > 0.05).

Conclusion

SWE can quantitatively evaluate the carotid elasticity of the T2DM patients with NAFLD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Qi JC, Huang JC, Lin QC, Zhao JM, Lin X, Chen LD, Huang JF, Chen X. Relationship between obstructive sleep apnea and nonalcoholic fatty liver disease in nonobese adults. Sleep Breath. 2016;20:529–35. https://doi.org/10.1007/s11325-015-1232-9.

    Article  PubMed  Google Scholar 

  2. Zamirian MM, Samiee EM, Moaref AM, Abtahi FM, Tahamtan MM. Assessment of subclinical myocardial changes in non-alcoholic fatty liver disease: a case-control study using speckle tracking echocardiography. Iran J Med Sci. 2018;43:466–72.

    PubMed  Google Scholar 

  3. Mavrogiannaki AN, Migdalis IN. Nonalcoholic Fatty liver disease, diabetes mellitus and cardiovascular disease: newer data. Int J Endocrinol. 2013;2013:450639. https://doi.org/10.1155/2013/450639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Byrne CD, Targher G. NAFLD: a multisystem disease. J Hepatol. 2015;62:S47–64. https://doi.org/10.1016/j.jhep.2014.12.012.

    Article  PubMed  Google Scholar 

  5. Devaraj NK. Knowledge, attitude, and practice regarding obstructive sleep apnea among primary care physicians. Sleep Breath. 2020;24:1581–90. https://doi.org/10.1007/s11325-020-02040-1.

    Article  PubMed  Google Scholar 

  6. Lee KW, Loh HC, Ching SM, Devaraj NK, Hoo FK. Effects of vegetarian diets on blood pressure lowering: a systematic review with meta-analysis and trial sequential analysis. Nutrients. 2020;12. https://doi.org/10.3390/nu12061604.

  7. Lee DG, Han JH, Kwon KY, Kim JH, Han KH, Lee EJ. Association of 10-year atherosclerotic cardiovascular disease risk score with carotid intima-media thickness and plaque. Korean J Fam Med. 2015;36:310–5. https://doi.org/10.4082/kjfm.2015.36.6.310.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hou JS, Wang CH, Lai YH, Lin YL, Kuo CH, Subeq YM, Hsu BG. Negative correlation of serum adiponectin levels with carotid-femoral pulse wave velocity in patients treated with hemodialysis. Biol Res Nurs. 2018;20:462–8. https://doi.org/10.1177/1099800418768887.

    Article  CAS  PubMed  Google Scholar 

  9. Hekimoglu K, Yildirim Donmez F, Arslan S, Ozdemir A, Demir C, Yazici C. The role of shear wave elastography in the diagnosis of chronic autoimmune thyroiditis. Med Ultrason. 2015;17:322–6. https://doi.org/10.11152/mu.2013.2066.173.khu.

    Article  PubMed  Google Scholar 

  10. Kim JR, Suh CH, Yoon HM, Lee JS, Cho YA, Jung AY. The diagnostic performance of shear-wave elastography for liver fibrosis in children and adolescents: a systematic review and diagnostic meta-analysis. Eur Radiol. 2018;28:1175–86. https://doi.org/10.1007/s00330-017-5078-3.

    Article  PubMed  Google Scholar 

  11. Zeng MD, Fan JG, Lu LG, Li YM, Chen CW, Wang BY, et al. Guidelines for the diagnosis and treatment of nonalcoholic fatty liver diseases. J Dig Dis. 2008;9:108–12. https://doi.org/10.1111/j.1751-2980.2008.00331.x.

    Article  PubMed  Google Scholar 

  12. Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, Harrison SA, Brunt EM, Sanyal AJ. The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67:328–57. https://doi.org/10.1002/hep.29367.

    Article  PubMed  Google Scholar 

  13. Wang Y, Zhao C, Meng P, Yu Y, Li G, Kong F, Mu L, Yang J, Ma C. Incremental value of carotid elasticity modulus using shear wave elastography for identifying coronary artery disease in patients without carotid plaque. J Hypertens. 2021;39:1210–20. https://doi.org/10.1097/hjh.0000000000002773.

    Article  CAS  PubMed  Google Scholar 

  14. Khneizer G, Rizvi S, Gawrieh S. Non-alcoholic fatty liver disease and diabetes mellitus. Adv Exp Med Biol. 2021;1307:417–40. https://doi.org/10.1007/5584_2020_532.

    Article  CAS  PubMed  Google Scholar 

  15. Saponaro C, Gaggini M, Gastaldelli A. Nonalcoholic fatty liver disease and type 2 diabetes: common pathophysiologic mechanisms. Curr Diab Rep. 2015;15:607. https://doi.org/10.1007/s11892-015-0607-4.

    Article  CAS  PubMed  Google Scholar 

  16. George JM, Bhat R, Pai KM, Arun S, Jeganathan J. The carotid intima media thickness: a predictor of the clincal coronary events. J Clin Diagn Res. 2013;7:1082–5. https://doi.org/10.7860/jcdr/2013/4767.3029.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Tada T, Kumada T, Toyoda H, Ito T, Sone Y, Okuda S, Tsuji N, Imayoshi Y, Yasuda E. Utility of real-time shear wave elastography for assessing liver fibrosis in patients with chronic hepatitis C infection without cirrhosis: Comparison of liver fibrosis indices. Hepatol Res. 2015;45:E122–9. https://doi.org/10.1111/hepr.12476.

    Article  CAS  PubMed  Google Scholar 

  18. Marais L, Pernot M, Khettab H, Tanter M, Messas E, Zidi M, Laurent S, Boutouyrie P. Arterial stiffness assessment by shear wave elastography and ultrafast pulse wave imaging: comparison with reference techniques in normotensives and hypertensives. Ultrasound Med Biol. 2019;45:758–72. https://doi.org/10.1016/j.ultrasmedbio.2018.10.032.

    Article  PubMed  Google Scholar 

  19. Alis D, Durmaz ESM, Civcik C, Tutuncu M, Saip S, Kocer N, et al. Assessment of the common carotid artery wall stiffness by Shear Wave Elastography in Behcet's disease. Med Ultrason. 2018;20:446–52. https://doi.org/10.11152/mu-1565.

    Article  PubMed  Google Scholar 

  20. Li Z, Du L, Wang F, Luo X. Assessment of the arterial stiffness in patients with acute ischemic stroke using longitudinal elasticity modulus measurements obtained with Shear Wave Elastography. Med Ultrason. 2016;18:182–9. https://doi.org/10.11152/mu.2013.2066.182.wav.

    Article  PubMed  Google Scholar 

  21. Al-Mutairi FF, Al-Hussaini A, Marsh AM, Samani N, McCann G, Adlam D, et al. Ultrasound shear wave elastography imaging of common carotid arteries in patients with Spontaneous Coronary Artery Dissection (SCAD). J Ultrasound. 2022. https://doi.org/10.1007/s40477-021-00627-2.

  22. Simon A, Megnien JL, Levenson J. Coronary risk estimation and treatment of hypercholesterolemia. Circulation. 1997;96:2449–52. https://doi.org/10.1161/01.cir.96.7.2449.

    Article  CAS  PubMed  Google Scholar 

  23. Sookoian S, Pirola CJ. Non-alcoholic fatty liver disease is strongly associated with carotid atherosclerosis: a systematic review. J Hepatol. 2008;49:600–7. https://doi.org/10.1016/j.jhep.2008.06.012.

    Article  PubMed  Google Scholar 

  24. Abdallah LR, de Matos RC, YPDM ES, Vieira-Soares D, Muller-Machado G, Pollo-Flores P. Non-alcoholic fatty liver disease and its links with inflammation and atherosclerosis. Curr Atheroscler Rep. 2020;22:7. https://doi.org/10.1007/s11883-020-0820-8.

    Article  PubMed  Google Scholar 

  25. Targher G, Bertolini L, Padovani R, Rodella S, Zoppini G, Zenari L, Cigolini M, Falezza G, Arcaro G. Relations between carotid artery wall thickness and liver histology in subjects with nonalcoholic fatty liver disease. Diabetes Care. 2006;29:1325–30. https://doi.org/10.2337/dc06-0135.

    Article  PubMed  Google Scholar 

  26. Silaghi CA, Silaghi H, Crăciun AE, Fărcaș A, Colosi HA, Cosma DT, et al. Age, abdominal obesity, and glycated hemoglobin are associated with carotid atherosclerosis in type 2 diabetes patients with nonalcoholic fatty liver disease. Med Ultrason. 2015;17:300–7. https://doi.org/10.11152/mu.2013.2066.173.cas.

    Article  PubMed  Google Scholar 

  27. Fruci B, Giuliano S, Mazza A, Malaguarnera R, Belfiore A. Nonalcoholic fatty liver: a possible new target for type 2 diabetes prevention and treatment. Int J Mol Sci. 2013;14:22933–66. https://doi.org/10.3390/ijms141122933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mazzotti A, Caletti MT, Marchignoli F, Forlani G, Marchesini G. Which treatment for type 2 diabetes associated with non-alcoholic fatty liver disease? Dig Liver Dis. 2017;49:235–40. https://doi.org/10.1016/j.dld.2016.12.028.

    Article  CAS  PubMed  Google Scholar 

  29. Tanase DM, Gosav EM, Costea CF, Ciocoiu M, Lacatusu CM, Maranduca MA, Ouatu A, Floria M. The intricate relationship between type 2 diabetes mellitus (T2DM), insulin resistance (IR), and nonalcoholic fatty liver disease (NAFLD). J Diabetes Res. 2020;2020:3920196. https://doi.org/10.1155/2020/3920196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Salvi P, Ruffini R, Agnoletti D, Magnani E, Pagliarani G, Comandini G, Praticò A, Borghi C, Benetos A, Pazzi P. Increased arterial stiffness in nonalcoholic fatty liver disease: the Cardio-GOOSE study. J Hypertens. 2010;28:1699–707. https://doi.org/10.1097/HJH.0b013e32833a7de6.

    Article  CAS  PubMed  Google Scholar 

  31. Sinn DH, Cho SJ, Gu S, Seong D, Kang D, Kim H, et al. Persistent nonalcoholic fatty liver disease increases risk for carotid atherosclerosis. Gastroenterology. 2016;151:481–8.e1. https://doi.org/10.1053/j.gastro.2016.06.001.

    Article  PubMed  Google Scholar 

  32. Oni E, Budoff MJ, Zeb I, Li D, Veledar E, Polak JF, Blankstein R, Wong ND, Blaha MJ, Agatston A, Blumenthal RS, Nasir K. Nonalcoholic fatty liver disease is associated with arterial distensibility and carotid intima-media thickness: (from the Multi-Ethnic Study of Atherosclerosis). Am J Cardiol. 2019;124:534–8. https://doi.org/10.1016/j.amjcard.2019.05.028.

    Article  PubMed  Google Scholar 

  33. Zhang L, Yin JK, Duan YY, Liu X, Xu L, Wang J, Yang YL, Yuan LJ, Cao TS. Evaluation of carotid artery elasticity changes in patients with type 2 diabetes. Cardiovasc Diabetol. 2014;13:39. https://doi.org/10.1186/1475-2840-13-39.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Watt MJ, Miotto PM, De Nardo W, Montgomery MK. The liver as an endocrine organ-linking NAFLD and insulin resistance. Endocr Rev. 2019;40:1367–93. https://doi.org/10.1210/er.2019-00034.

    Article  PubMed  Google Scholar 

  35. Utzschneider KM, Kahn SE. Review: The role of insulin resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2006;91:4753–61. https://doi.org/10.1210/jc.2006-0587.

    Article  CAS  PubMed  Google Scholar 

  36. Putz-Bankuti C, Pilz S, Stojakovic T, Scharnagl H, Pieber TR, Trauner M, Obermayer-Pietsch B, Stauber RE. Association of 25-hydroxyvitamin D levels with liver dysfunction and mortality in chronic liver disease. Liver Int. 2012;32:845–51. https://doi.org/10.1111/j.1478-3231.2011.02735.x.

    Article  CAS  PubMed  Google Scholar 

  37. Kotronen A, Westerbacka J, Bergholm R, Pietiläinen KH, Yki-Järvinen H. Liver fat in the metabolic syndrome. J Clin Endocrinol Metab. 2007;92:3490–7. https://doi.org/10.1210/jc.2007-0482.

    Article  CAS  PubMed  Google Scholar 

  38. Bae JC, Cho YK, Lee WY, Seo HI, Rhee EJ, Park SE, Park CY, Oh KW, Sung KC, Kim BI. Impact of nonalcoholic fatty liver disease on insulin resistance in relation to HbA1c levels in nondiabetic subjects. Am J Gastroenterol. 2010;105:2389–95. https://doi.org/10.1038/ajg.2010.275.

    Article  CAS  PubMed  Google Scholar 

  39. Mo Y, Zhou J, Ma X, Zhu W, Zhang L, Li J, Lu J, Hu C, Bao Y, Jia W. Haemoglobin A1c variability as an independent correlate of atherosclerosis and cardiovascular disease in Chinese type 2 diabetes. Diab Vasc Dis Res. 2018;15:402–8. https://doi.org/10.1177/1479164118778850.

    Article  CAS  PubMed  Google Scholar 

  40. James PE, Lang D, Tufnell-Barret T, Milsom AB, Frenneaux MP. Vasorelaxation by red blood cells and impairment in diabetes: reduced nitric oxide and oxygen delivery by glycated hemoglobin. Circ Res. 2004;94:976–83. https://doi.org/10.1161/01.Res.0000122044.21787.01.

    Article  CAS  PubMed  Google Scholar 

  41. Jain SK, McVie R, Duett J, Herbst JJ. Erythrocyte membrane lipid peroxidation and glycosylated hemoglobin in diabetes. Diabetes. 1989;38:1539–43. https://doi.org/10.2337/diab.38.12.1539.

    Article  CAS  PubMed  Google Scholar 

  42. Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation. 2005;111:3481–8. https://doi.org/10.1161/circulationaha.105.537878.

    Article  PubMed  Google Scholar 

  43. Li H, Cui Y, Zhu Y, Yan H, Xu W. Association of high normal HbA1c and TSH levels with the risk of CHD: a 10-year cohort study and SVM analysis. Sci Rep. 2017;7:45406. https://doi.org/10.1038/srep45406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgment

We thank Prof. Li for guidance in study design and manuscript revision. In addition, we gratefully acknowledge the support and help from the Department of Ultrasound of the Second Affiliated Hospital of Dalian Medical University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guangsen Li.

Ethics declarations

Ethics approval

The study acquired the agreement of the local ethics committee and all participants had given written informed consent.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Tang, L., Cui, X. et al. Shear wave elastography in evaluation of carotid elasticity in the type 2 diabetes mellitus patients with nonalcoholic fatty liver disease. Int J Diabetes Dev Ctries 43, 191–198 (2023). https://doi.org/10.1007/s13410-022-01097-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13410-022-01097-w

Keywords

Navigation