Increase in serum and salivary neutrophil gelatinase-associated lipocalin levels with increased periodontal inflammation

Abstract Objective: This study aimed to determine serum and salivary levels of neutrophil gelatinase-associated lipocalin (NGAL) and evaluate NGAL correlation with key anti-interleukin 10 (IL-10) and pro-inflammatory (IL-1β) cytokines in different severities of periodontal diseases. We also calculated the systemic inflammation using the periodontal inflamed surface area (PISA) to evaluate its correlation with NGAL in the study groups. Methodology: Eighty systemically healthy and non-smoking individuals were separated into four groups of 20: clinically healthy (Group 1), gingivitis (Group 2), stage I generalized periodontitis (Group 3, Grade A), and stage III generalized periodontitis (Group 4, Grade A). Sociodemographic characteristics and periodontal parameters were recorded, and PISA was calculated. The serum and salivary levels of interleukin (IL)-1β, IL-10, and NGAL were determined using the enzyme-linked immunosorbent assay (ELISA). Results: We observed a significant increase in serum and salivary NGAL levels from healthy to periodontitis groups (p=0.000). Group 2 presented significantly higher serum and salivary IL-10 levels and salivary IL-1β levels than Group 3 (p=0.000). Serum and salivary parameters (IL-1β, IL-10, and NGAL levels) were strongly positively correlated to periodontal parameters and PISA values (p=0.000). Groups 2 and 3 showed overlapping PISA values. Conclusion: The overlapping PISA values found in Groups 2 and 3 suggest that gingivitis might progress to a systemic inflammatory burden somewhat comparable to stage I periodontitis. This finding is supported by the higher serum and salivary cytokines/mediators levels in the gingivitis group than in stage I periodontitis group. Serum and salivary NGAL levels increased proportionally to disease severity and PISA. NGAL seems to play a role in the pathogenesis of periodontal disease, within the limitation of our study.

摘要 研究目的：本研究旨在检测中性粒细胞明胶酶相关脂质运载蛋白（neutrophil gelatinase-associated lipocalin, NGAL）在血清与唾液中的水平，并分析不同严重程度牙周病患者体内NGAL与关键抗白细胞介素10（anti-interleukin 10, IL-10）及促炎（IL-1β）细胞因子的相关性。此外，本研究通过牙周炎性表面积（periodontal inflamed surface area, PISA）评估全身炎症状态，并分析其与各组NGAL水平的相关性。
研究方法：招募80名全身健康且无吸烟史的受试者，按20例一组分为4组：临床健康组（第1组）、牙龈炎组（第2组）、I级广泛性牙周炎组（第3组，A级）以及III级广泛性牙周炎组（第4组，A级）。记录受试者的社会人口学特征与牙周参数，并计算PISA值。采用酶联免疫吸附试验（enzyme-linked immunosorbent assay, ELISA）检测血清及唾液中IL-1β、IL-10与NGAL的水平。
研究结果：从健康组至牙周炎组，血清与唾液中的NGAL水平均显著升高（p=0.000）。第2组的血清与唾液IL-10水平、唾液IL-1β水平均显著高于第3组（p=0.000）。血清及唾液中的各项参数（IL-1β、IL-10及NGAL水平）与牙周参数及PISA值均呈显著正相关（p=0.000）。第2组与第3组的PISA值存在重叠。
研究结论：第2组与第3组的PISA值重叠提示，牙龈炎进展所致的全身炎症负荷可能与I级牙周炎相当。这一结论得到了牙龈炎组血清与唾液中的细胞因子/介质水平显著高于I级牙周炎组的结果支持。血清及唾液中的NGAL水平随疾病严重程度与PISA值呈正比升高。本研究存在一定局限性，结果提示NGAL可能参与牙周疾病的发病过程。