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Background: Pentraxin 3 (PTX3) is a well-established inflammatory biomarker with significant implications in the pathogenesis and prognostic assessment of cardiovascular diseases. This study aimed to investigate the potential value of serum PTX3 as a circulating biomarker when combined with the high-resolution magnetic resonance vessel wall imaging (HR-VWI) for identifying carotid vulnerable plaque (CVP) and its specific vulnerable features. Methods: This prospective cross-sectional study enrolled 86 patients with carotid atherosclerosis who underwent HR-VWI. Patients were classified into CVP and non-carotid vulnerable plaque (NCVP) groups, and CVP was divided into unilateral carotid vulnerable plaque (UCVP) and bilateral carotid vulnerable plaque (BCVP). CVP was defined as meeting ≥ 1 major criteria: lipid-rich necrotic core (LRNC) maximum area percentage > 40% combined with thin fibrous cap (FC), intraplaque hemorrhage (IPH), FC discontinuity, and focal inflammation. Multivariate logistic regression analysis identified factors influencing CVP and the formation of specific vulnerable features. Results: Serum PTX3 levels progressively increased across the NCVP, UCVP, and BCVP groups (median 638.23, 858.52, 1113.62 pg/mL; p < 0.001). PTX3 independently predicted the presence of CVP (OR = 2.88; 95% CI: 1.16-8.91; p = 0.039) and specific vulnerable features, including FC discontinuity (OR = 2.47; 95% CI: 1.32-4.63; p = 0.005) and focal inflammation (OR = 2.25; 95% CI: 1.18-4.32; p = 0.014) with high diagnostic performance for these conditions. PTX3 levels exhibited a moderate positive correlation with the number of vulnerable features (r = 0.610, p < 0.01). Conclusions: Elevated serum PTX3 levels were significantly associated with HR-VWI-defined carotid plaque vulnerability and its severity, serving as a reliable circulating biomarker for identifying FC discontinuity and focal inflammation.