Download PDF
Exp Clin Endocrinol Diabetes 2019; 127(01): 41-49
DOI: 10.1055/a-0577-7658
Article
© Georg Thieme Verlag KG Stuttgart · New York

Evaluation of Vascular Remodeling in Carotid Atherosclerosis Among Type 2 Diabetes Mellitus Patients Using High-Frequency Ultrasonography Combined with Serum Resistin

Li-Kun Wang
1   Department of Ultrasound, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Xue-Liang Wu
2   Department of Vascular Gland Surgery, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Li Shi
3   Department of Endocrinology, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Rui-Min Yang
1   Department of Ultrasound, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Wei-Liang Liu
1   Department of Ultrasound, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Zhen-Shun Hu
4   Department of Imaging, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Zhi-Hua Zhang
5   Department of Respiratory, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
,
Yi-Cheng Wang
1   Department of Ultrasound, the First Affiliated Hospital of Hebei North University, Zhangjiakou, P. R. China
› Author Affiliations
Further Information

Publication History

received 06 August 2017
revised 06 February 2018

accepted 09 February 2018

Publication Date:
04 July 2018 (online)

Also available at
    Permissions and Reprints

Abstract

Diabetes remains a long standing public health issue among the Chinese population, with an incidence of up to 11.6%, of which type 2 diabetes mellitus (T2DM) accounts for 85%–95%. During this study, we aimed to elucidate the value of high-frequency ultrasonography (HFUS) combined with serum resistin on vascular remodeling (VR) in carotid atherosclerosis (CA) among patients suffering from T2DM. A total of 432 T2DM were recruited and assigned into the short T2DM duration group (<5 years), middle T2DM duration group (5~10 years) and long T2DM duration group (>10 years), while another 172 healthy cases were recruited as the control group. The intima-media thickness (IMT) as well as plaque score, detection rate and type were detected by the HFUS. The respective blood pressure readings were measured and pulse pressure was calculated accordingly. The serum resistin level, remodeling incidence and type, levels of total cholesterol (TC), fasting blood glucose (FBG), low-density lipoprotein cholesterol (LDL-C), high-density liproprotein cholesterol (HDL-C), and triglyceride (TG) were measured. The correlation between IMT, the plaque detection rate and blood pressure were analyzed. A receiver operating characteristic (ROC) curve was constructed in order to evaluate the impact of VR in CA on T2DM patients who were solely using HFUS and serum resistin respectively, as well as a combination of HFUS with serum resistin. As In comparison with the control group, the short, middle and long T2DM duration groups all displayed increased IMT, plaque score and detection rate, serum resistin level and VR incidence, especially for the long T2DM duration group. Levels of TC, TG, FBG and LDL-C were much higher while HDL-C was lower among patients with T2DM than those in the control group. A positive correlation was detected between the disease course and IMT. The detection rate of plaque with thickening IMT exhibited upregulated levels when compared to those with normal IMT. The HFUS, serum resistin and HFUS combined with serum resistin respective areas under the ROC curve were 0.873, 0.867 and 0.923, respectively, suggesting that the combination of HFUS and serum resistin was superior to that of individual HFUS or individual serum resistin in regard to the impact of VR in CA on T2DM patients. The results of this study revealed that the combination of HFUS and serum resistin was superior to individual HFUS or individual serum resistin in relation to its ability to evaluate the impact of VR in CA in patients with T2DM.

Key words

T2DM - Carotid atherosclerosis - Vascular remodeling - High-frequency ultrasonography - Serum resistin
 

  • References

  • 1 Markowicz-Piasecka M, Sikora J, Szydlowska A. et al. Metformin - a future therapy for neurodegenerative diseases. Pharm Res. 2017; 34 (12): 2614-2627
    CrossrefPubMedGoogle Scholar
  • 2 Quevedo MDP, Palermo M, Serra E. et al. Metabolic surgery: Gastric bypass for the treatment of type 2 diabetes mellitus. Transl Gastroenterol Hepatol 2017; 2: 58
    CrossrefPubMedGoogle Scholar
  • 3 Sami W, Ansari T, Butt NS. et al. Effect of diet on type 2 diabetes mellitus: A review. Int J Health Sci (Qassim) 2017; 11: 65-71
    PubMedGoogle Scholar
  • 4 Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010 87: 4-14
    PubMedGoogle Scholar
  • 5 Vanasse A, Carpentier AC, Courteau J. et al. Stroke and cardiovascular morbidity and mortality associated with rosiglitazone use in elderly diabetic patients. Diab Vasc Dis Res 2009; 6: 87-93
    CrossrefPubMedGoogle Scholar
  • 6 Guerci B, Kearney-Schwartz A, Bohme P. et al. Endothelial dysfunction and type 2 diabetes. Part 1: Physiology and methods for exploring the endothelial function. Diabetes Metab 2001; 27: 425-434
    PubMedGoogle Scholar
  • 7 Gartner V, Eigentler TK. Pathogenesis of diabetic macro- and microangiopathy. Clin Nephrol 2008; 70: 1-9
    CrossrefPubMedGoogle Scholar
  • 8 Wang Y, Zhang H. Serum 25-Hydroxyvitamin D3 levels are associated with carotid intima-media thickness and carotid atherosclerotic plaque in type 2 diabetic patients. J Diabetes Res 2017; 2017: 3510275
    PubMedGoogle Scholar
  • 9 Bauer M, Caviezel S, Teynor A. et al. Carotid intima-media thickness as a biomarker of subclinical atherosclerosis. Swiss Med Wkly 2012; 142: w13705
    PubMedGoogle Scholar
  • 10 Zhang X, Zhang T, Gao F. et al. Fasudil, a Rhokinase inhibitor, prevents intimamedia thickening in a partially ligated carotid artery mouse model: Effects of fasudil in flowinduced vascular remodeling. Mol Med Rep 2015; 12: 7317-7325
    CrossrefPubMedGoogle Scholar
  • 11 Sasaki R, Yamano S, Yamamoto Y. et al. Vascular remodeling of the carotid artery in patients with untreated essential hypertension increases with age. Hypertens Res 2002; 25: 373-379
    CrossrefPubMedGoogle Scholar
  • 12 Domkundwar S, Autkar G, Khadilkar SV. et al. Ultrasound and EMG-NCV study (electromyography and nerve conduction velocity) correlation in diagnosis of nerve pathologies. J Ultrasound 2017; 20: 111-122
    CrossrefPubMedGoogle Scholar
  • 13 Mlosek RK, Malinowska S. Application of high-frequency ultrasonography in closing small blood vessels. J Ultrason 2014; 14: 320-327
    CrossrefPubMedGoogle Scholar
  • 14 Jasaitiene D, Valiukeviciene S, Linkeviciute G. et al. Principles of high-frequency ultrasonography for investigation of skin pathology. J Eur Acad Dermatol Venereol 2011; 25: 375-382
    CrossrefPubMedGoogle Scholar
  • 15 Li X, Yue W, Chen Y. et al. Assessments of carotid adventitial remodeling in metabolic syndrome patients using high-frequency ultrasound. Zhonghua Yi Xue Za Zhi 2015; 95: 52-55
    PubMedGoogle Scholar
  • 16 Qi SD, He ZL, Chen Y. et al. Relevance and clinical significance of serum resistin level in obese T2DM rhesus monkey models. Exp Clin Endocrinol Diabetes 2015; 123: 508-513
    Article in Thieme ConnectPubMedGoogle Scholar
  • 17 Moreno LO, Salvemini L, Mendonca C. et al. Serum resistin and glomerular filtration rate in patients with type 2 diabetes. PLoS One 2015; 10: e0119529
    CrossrefPubMedGoogle Scholar
  • 18 Gharibeh MY, Al Tawallbeh GM, Abboud MM. et al. Correlation of plasma resistin with obesity and insulin resistance in type 2 diabetic patients. Diabetes Metab 2010; 36: 443-449
    CrossrefPubMedGoogle Scholar
  • 19 Rayburn WF. Diagnosis and classification of diabetes mellitus: Highlights from the American Diabetes Association. J Reprod Med 1997; 42: 585-586
    PubMedGoogle Scholar
  • 20 Oike M, Yokokawa H, Fukuda H. et al. Association between abdominal fat distribution and atherosclerotic changes in the carotid artery. Obes Res Clin Pract 2014; 8: e448-e458
    CrossrefPubMedGoogle Scholar
  • 21 Jung JM, Young Kwon D, Han C. et al. Metabolic syndrome and early carotid atherosclerosis in the elderly. J Atheroscler Thromb 2014; 21: 435-444
    CrossrefPubMedGoogle Scholar
  • 22 de Waard EA, van Geel TA, Savelberg HH. et al. Increased fracture risk in patients with type 2 diabetes mellitus: An overview of the underlying mechanisms and the usefulness of imaging modalities and fracture risk assessment tools. Maturitas 2014; 79: 265-274
    CrossrefPubMedGoogle Scholar
  • 23 Zhang YH, Gao Y, Mao X. et al. Assessment of carotid atherosclerosis in type 2 diabetes mellitus patients with microalbuminuria by high-frequency ultrasonography. Int J Endocrinol 2013; 2013: 819584
    PubMedGoogle Scholar
  • 24 Veller MG, Fisher CM, Nicolaides AN. et al. Measurement of the ultrasonic intima-media complex thickness in normal subjects. J Vasc Surg 1993; 17: 719-725
    CrossrefPubMedGoogle Scholar
  • 25 Belcaro G, Nicolaides AN, Laurora G. et al. Ultrasound morphology classification of the arterial wall and cardiovascular events in a 6-year follow-up study. Arterioscler Thromb Vasc Biol 1996; 16: 851-856
    CrossrefPubMedGoogle Scholar
  • 26 Lilje C, Cronan JC, Schwartzenburg EJ. et al. Intima-media thickness at different arterial segments in pediatric type 1 diabetes patients and its relationship with advanced glycation end products. Pediatr Diabetes 2017; 19 (3) 450-456
    PubMedGoogle Scholar
  • 27 Lester SJ, Eleid MF, Khandheria BK. et al. Carotid intima-media thickness and coronary artery calcium score as indications of subclinical atherosclerosis. Mayo Clin Proc 2009; 84: 229-233
    CrossrefPubMedGoogle Scholar
  • 28 Mita T, Katakami N, Shiraiwa T. et al. The effect of sitagliptin on the regression of carotid intima-media thickening in patients with type 2 diabetes mellitus: A Post Hoc analysis of the sitagliptin preventive study of intima-media thickness evaluation. Int J Endocrinol 2017; 2017: 1925305
    PubMedGoogle Scholar
  • 29 Contreras-Rodriguez A, Gomez-Diaz RA, Tanus-Hajj J. et al. Carotid Intima-Media Thickness, Ankle-Arm Index, and Inflammation Profile in Mexican Patients with Early and Late Onset Type 2 Diabetes. Rev Invest Clin 2015; 67: 240-249
    PubMedGoogle Scholar
  • 30 Sturlaugsdottir R, Aspelund T, Bjornsdottir G. et al. Prevalence and determinants of carotid plaque in the cross-sectional REFINE-Reykjavik study. BMJ Open 2016; 6: e012457
    CrossrefPubMedGoogle Scholar
  • 31 Menzaghi C, Bacci S, Salvemini L. et al. Serum resistin, cardiovascular disease and all-cause mortality in patients with type 2 diabetes. PLoS One 2014; 8: e64729
    PubMedGoogle Scholar
  • 32 Youn BS, Yu KY, Park HJ. et al. Plasma resistin concentrations measured by enzyme-linked immunosorbent assay using a newly developed monoclonal antibody are elevated in individuals with type 2 diabetes mellitus. J Clin Endocrinol Metab 2004; 89: 150-156
    CrossrefPubMedGoogle Scholar
  • 33 Porter KE, Riches K. The vascular smooth muscle cell: A therapeutic target in Type 2 diabetes?. Clin Sci (Lond) 2013; 125: 167-182
    CrossrefPubMedGoogle Scholar
  • 34 Barnes RF, Cramer TJ, Hughes TH. et al. The hypertension of hemophilia is associated with vascular remodeling in the joint. Microcirculation 2017; DOI: 10.1111/micc.12387.
    CrossrefPubMedGoogle Scholar
  • 35 Noh M, Kwon H, Jung CH. et al. Impact of diabetes duration and degree of carotid artery stenosis on major adverse cardiovascular events: A single-center, retrospective, observational cohort study. Cardiovasc Diabetol 2017; 16: 74
    CrossrefPubMedGoogle Scholar
  • 36 Melo LC, Dativo-Medeiros J, Menezes-Silva CE. et al. Physical exercise on inflammatory markers in type 2 diabetes patients: A systematic review of randomized controlled trials. Oxid Med Cell Longev 2017; 2017: 8523728
    PubMedGoogle Scholar
  • 37 Emamian M, Hasanian SM, Tayefi M. et al. Association of hematocrit with blood pressure and hypertension. J Clin Lab Anal 2017; 31 (6) DOI: 10.1002/jcla.22124.
    CrossrefPubMedGoogle Scholar
  • 38 Li X, Shen J, Lu Z. et al. High neutrophil-to-lymphocyte ratio is associated with increased carotid artery intima-media thickness in type 2 diabetes. J Diabetes Investig 2017; 8: 101-107
    CrossrefPubMedGoogle Scholar
  • 39 Zureik M, Ducimetiere P, Touboul PJ. et al. Common carotid intima-media thickness predicts occurrence of carotid atherosclerotic plaques: Longitudinal results from the Aging Vascular Study (EVA) study. Arterioscler Thromb Vasc Biol 2000; 20: 1622-1629
    CrossrefPubMedGoogle Scholar
  • 40 Nair SB, Malik R, Khattar RS. Carotid intima-media thickness: Ultrasound measurement, prognostic value and role in clinical practice. Postgrad Med J 2012; 88: 694-699
    CrossrefPubMedGoogle Scholar
  • 41 Wang X, Chen L, Liu W. et al. Early detection of atrophy of foot muscles in Chinese patients of type 2 diabetes mellitus by high-frequency ultrasonography. J Diabetes Res 2014; 2014: 927069
    PubMedGoogle Scholar
  • 42 Zhang Y, Li W, Yan T. et al. Early detection of lesions of dorsal artery of foot in patients with type 2 diabetes mellitus by high-frequency ultrasonography. J Huazhong Univ Sci Technolog Med Sci 2009; 29: 387-390
    CrossrefPubMedGoogle Scholar
  • 43 Lubos E, Messow CM, Schnabel R. et al. Resistin, acute coronary syndrome and prognosis results from the AtheroGene study. Atherosclerosis 2007; 193: 121-128
    CrossrefPubMedGoogle Scholar
  • 44 Hoefle G, Saely CH, Risch L. et al. Relationship between the adipose-tissue hormone resistin and coronary artery disease. Clin Chim Acta 2007; 386: 1-6
    CrossrefPubMedGoogle Scholar
  • 45 Frankel DS, Vasan RS, D'Agostino Sr. RB. et al. Resistin, adiponectin, and risk of heart failure the Framingham offspring study. J Am Coll Cardiol 2009; 53: 754-762
    CrossrefPubMedGoogle Scholar
  • 46 Butler J, Kalogeropoulos A, Georgiopoulou V. et al Serum resistin concentrations and risk of new onset heart failure in older persons: The health, aging, and body composition (Health ABC) study. Arterioscler Thromb Vasc Biol 2009; 29: 1144-1149
    CrossrefPubMedGoogle Scholar
  • 47 Luc G, Empana JP, Morange P. et al. Adipocytokines and the risk of coronary heart disease in healthy middle aged men: The PRIME Study. Int J Obes (Lond) 2010; 34: 118-126
    CrossrefPubMedGoogle Scholar