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Possible role of annexin A1/FPR2 pathway in COX2/NLRP3 inflammasome regulation in alveolar bone cells of estrogen-deficient female rats with diabetes mellitus 膜联蛋白A1/FPR2通路在雌激素缺乏雌性糖尿病大鼠牙槽骨细胞COX2/NLRP3炎性体调控中的可能作用
IF 4.2 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-21 DOI: 10.1002/JPER.23-0530
Gisela Rodrigues Da Silva Sasso, Paulo Sérgio Cerri, Estela Sasso-Cerri, Manuel Jesus Simões, Cristiane Damas Gil, Rinaldo Florencio-Silva

Background

Annexin A1 (ANXA1) and the NOD-like receptor family pyrin domain-containing protein 3 (NLRP3) inflammasome play important roles in bone remodeling. However, expression profiles of these factors in bone cells under diabetes mellitus (DM) and estrogen-deficient conditions are poorly understood. This study investigated the immunoexpression of ANXA1 and its formyl peptide receptor 2 (FPR2), as well as NLRP3 inflammasome mediators, during remodeling of the alveolar process in diabetic and estrogen-deficient rats.

Methods

Twenty adult female Wistar rats were divided into four groups (n = 5): Sham-operated (SHAM) and ovariectomized (OVX) rats received a vehicle solution, and SHAM and OVX rats were intraperitoneally administered 60 mg/kg/body weight (BW) of streptozotocin (STZ) to induce DM (SHAM-Di and OVX-Di groups). After 7 weeks, the rats were euthanized and their maxillae were fixed in phosphate-buffered 4% formaldehyde and embedded in paraffin. Sections were stained with hematoxylin/eosin (H&E) and picrosirius red or subjected to immunohistochemical detection of ANXA1, FPR2, NLRP3, interleukin-1β (IL-1β), and cyclooxygenase-2 (COX2).

Results

Estrogen deficiency and DM were associated with deleterious effects in bone tissue, as evidenced by a lower number of osteocytes and higher number of empty lacunae in the SHAM-Di and OVX-Di groups compared to the nondiabetic groups. Both diabetic groups showed a smaller vascular area and weaker collagen fiber birefringence intensity in alveolar bone tissue. A significantly higher number of ANXA1/FPR2-positive osteoblasts, osteocytes, and osteoclasts was accompanied by a significantly higher number of these cells immunolabeled for COX2, NLRP3, and IL-1β in the diabetic and OVX groups, especially in both estrogen-deficient and diabetic rats.

Conclusion

These results indicate a possible role for the ANXA1/FPR2 pathway as a fine-tuning/anti-inflammatory regulator to counterbalance exacerbated COX2/NLRP3/IL-1β activation in bone cells during bone remodeling under estrogen deficiency and DM.

背景:膜联蛋白A1 (ANXA1)和nod样受体家族pyrin结构域蛋白3 (NLRP3)炎性体在骨重塑中发挥重要作用。然而,在糖尿病(DM)和雌激素缺乏的情况下,这些因子在骨细胞中的表达谱知之甚少。本研究研究了糖尿病和雌激素缺乏大鼠肺泡过程重构过程中ANXA1及其甲酰基肽受体2 (FPR2)以及NLRP3炎症小体介质的免疫表达。方法:将20只成年雌性Wistar大鼠分为4组(n = 5):假手术(SHAM)和去卵巢(OVX)大鼠给予载药液,假手术(SHAM)和去卵巢(OVX)大鼠分别腹腔注射链脲佐菌素(STZ) 60 mg/kg/体重(BW)诱导DM (SHAM- di组和OVX- di组)。7周后处死大鼠,用4%甲醛磷酸盐缓冲液固定上颌骨,石蜡包埋。切片采用苏木精/伊红(H&E)和小红染色或免疫组化检测ANXA1、FPR2、NLRP3、白细胞介素-1β (IL-1β)和环氧化酶-2 (COX2)。结果:雌激素缺乏和糖尿病与骨组织的有害影响有关,与非糖尿病组相比,SHAM-Di和OVX-Di组骨细胞数量减少,空腔隙数量增加。两组患者牙槽骨组织血管面积减小,胶原纤维双折射强度减弱。在糖尿病和OVX组中,尤其是在雌激素缺乏和糖尿病大鼠中,ANXA1/ fpr2阳性的成骨细胞、骨细胞和破骨细胞数量显著增加,同时这些细胞免疫标记为COX2、NLRP3和IL-1β的数量显著增加。结论:这些结果表明,在雌激素缺乏和糖尿病的骨重塑过程中,ANXA1/FPR2通路可能作为一种微调/抗炎调节剂,抵消骨细胞中COX2/NLRP3/IL-1β活化的加剧。
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引用次数: 0
Association of environmental polycyclic aromatic hydrocarbons exposure with periodontitis in NHANES 2009–2014: A mixtures approach NHANES 2009-2014中环境多环芳烃暴露与牙周炎的关系:混合方法。
IF 4.2 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-21 DOI: 10.1002/JPER.23-0428
Jinqiu Sun, Feifei Guo, Lin Wang, Fulei Han, Jia Yang, Shengli Gao

Background

Polycyclic aromatic hydrocarbons (PAHs) can invade and cause harm to the human body through various pathways, but there is currently little research on the relationship between mixed-PAHs exposure and periodontitis. The purpose of this study was to examine the effects of mixed-urinary PAHs exposure on periodontitis in adults in the United States.

Methods

The cross-sectional study included 2749 subjects selected from the National Health and Nutrition Examination Survey (NHANES) 2009–2014 cycles. A professional examination of the periodontal status was conducted to distinguish between periodontitis and non-periodontitis based on the Centers for Disease Control and Prevention/American Academy of Periodontology (CDC/AAP) case definition. Laboratory testing of urine samples was performed to obtain the levels of urinary PAHs. Pearson correlation coefficients were utilized to determine the degree of correlation between urinary PAHs, while weighted binary logistic regression and Bayesian kernel machine regression (BKMR) were employed to evaluate the relationship between urinary PAHs and periodontitis.

Results

In a single-exposure model, 3-hydroxyfluorene (OH-3F), 2-hydroxyfluorene (OH-2F), 1-hydroxyphenanthrene (OH-1Ph), and 2-hydroxyphenanthrene and 3-hydroxyphenanthrene (OH-2,3Ph) were positively associated with periodontitis risk. In the mixed-exposure model, BKMR analysis demonstrated that mixed exposure to urinary PAHs was positively associated with periodontitis, with OH-2F being the most critical factor for the overall mixed effects (posterior inclusion probability [PIP] = 0.98). Univariate exposure–response function and univariate effects analysis revealed a positive correlation between urinary OH-2F levels and periodontitis.

Conclusions

The study reveals a significant positive correlation between exposure to mixed PAHs and periodontitis, with a particular emphasis on the pivotal role of OH-2F. Mitigating PAHs in the environment may serve as a preventive measure against periodontitis and alleviate its global public health burden.

背景:多环芳烃(Polycyclic aromatic hydrocarbons, PAHs)可通过多种途径侵入人体并对其造成危害,但目前关于混合PAHs暴露与牙周炎之间关系的研究很少。本研究的目的是检查混合尿多环芳烃暴露对美国成人牙周炎的影响。方法:横断面研究纳入2009-2014年全国健康与营养检查调查(NHANES)周期的2749名受试者。根据疾病控制和预防中心/美国牙周病学会(CDC/AAP)的病例定义,对牙周状况进行专业检查,以区分牙周炎和非牙周炎。对尿液样本进行了实验室检测,以获得尿液中多环芳烃的水平。采用Pearson相关系数确定尿中多环芳烃与牙周炎的相关程度,采用加权二元logistic回归和贝叶斯核机回归(BKMR)评估尿中多环芳烃与牙周炎的关系。结果:在单次暴露模型中,3 -羟基芴(OH-3F)、2-羟基芴(OH-2F)、1-羟基菲(OH-1Ph)、2-羟基菲和3-羟基菲(oh - 2,3ph)与牙周炎风险呈正相关。在混合暴露模型中,BKMR分析表明,混合暴露于尿液多环芳烃与牙周炎呈正相关,OH-2F是整体混合效应的最关键因素(后验包含概率[PIP] = 0.98)。单因素暴露-反应函数和单因素效应分析显示尿OH-2F水平与牙周炎呈正相关。结论:本研究揭示了混合多环芳烃暴露与牙周炎之间的显著正相关,并特别强调了OH-2F的关键作用。减少环境中的多环芳烃可作为预防牙周炎和减轻其全球公共卫生负担的措施。
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引用次数: 0
Mediating role of systemic inflammation in the association between heavy metals exposure and periodontitis risk 全身炎症在重金属暴露与牙周炎风险之间的中介作用。
IF 4.3 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-21 DOI: 10.1002/JPER.23-0079
Mi Du, Ke Deng, Qingqing Cai, Shixian Hu, Yuntao Chen, Shulan Xu, Geerten-Has E. Tjakkes, Shaohua Ge, Minghua Ge, An Li

Background

This study evaluated the mediating role of systemic inflammation in the association between exposure to heavy metals and periodontitis in a nationwide sample of adults.

Methods

Pooled cross-sectional data from the National Health and Nutrition Examination Survey (NHANES 2009-2014) were used (n = 8993). Periodontitis was defined by a full-mouth examination and classified as no/mild and moderate/severe (mod/sev) groups. Blood and urinary heavy metal levels were investigated, including cadmium (Cd), lead (Pb), and mercury (Hg). In addition, systemic inflammation was assessed using circulatory leukocyte counts and C-reactive protein (CRP) levels.

Results

Multivariable logistic regression analysis revealed the positive associations of blood and urinary levels of Cd and Pb with mod/sev periodontitis. In contrast,blood Hg levels did not show a significant association. The odds of having periodontitis were 1.233 and 1.311 times higher for each one-unit increment in Ln-transformed blood Cd (95% confidence interval [CI]: 1.109–1.371) and Pb (95% CI: 1.170-1.470), respectively. Mediation analysis suggested a 6.3% to 11.5% contribution of leucocyte counts in the association of blood Cd and Pb levels with periodontitis. Sensitivity analyses for urinary Cd levels yielded consistent mediating effects. However, no significant mediating effect of CRP was detected.

Conclusion

Higher exposures to Cd and Pb were positively associated with periodontitis risk. These associations might be partially mediated by the elevated levels of leukocytes rather than CRP. Further longitudinal studies are needed to elucidate the discordant results of the systemic inflammatory biomarkers.

背景:本研究在全国成人样本中评估了全身炎症在重金属暴露和牙周炎之间的中介作用。方法:采用国家健康与营养检查调查(NHANES 2009-2014)的汇总横截面数据(n = 8993)。通过全口检查确定牙周炎,并将其分为无/轻度和中度/重度(mod/sev)组。研究了血液和尿液中的重金属水平,包括镉(Cd)、铅(Pb)和汞(Hg)。此外,使用循环白细胞计数和c反应蛋白(CRP)水平评估全身炎症。结果:多变量logistic回归分析显示血、尿Cd、Pb水平与modv /sev牙周炎呈正相关。相比之下,血液中汞含量没有显示出显著的关联。ln转化血Cd(95%可信区间[CI]: 1.109-1.371)和Pb(95%可信区间:1.170-1.470)每增加一个单位,患牙周炎的几率分别高出1.233倍和1.311倍。中介分析表明,白细胞计数在血液Cd和Pb水平与牙周炎的关系中起6.3%至11.5%的作用。尿中Cd水平的敏感性分析得出了一致的中介效应。而CRP未见明显的介导作用。结论:较高的镉、铅暴露与牙周炎风险呈正相关。这些关联可能部分是由白细胞水平升高介导的,而不是CRP。需要进一步的纵向研究来阐明系统性炎症生物标志物的不一致结果。
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引用次数: 0
Association between sequelae of COVID-19 with periodontal disease and obesity: A cross-sectional study COVID-19后遗症与牙周病和肥胖之间的关系:一项横断面研究
IF 4.2 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-21 DOI: 10.1002/JPER.23-0412
Maísa Casarin, Francisco Hecktheuer Silva, Ana Flávia Leite Pontes, Betina Dutra Lima, Flavia Q. Pirih, Francisco Wilker Mustafa Gomes Muniz

Background

To assess the sequelae of coronavirus disease 2019 (COVID-19) and associated factors, such as obesity and periodontitis in adults.

Methods

The study included 128 individuals aged ≥35 years with a history of a diagnosis of COVID-19 through real-time polymerase chain reaction (RT-PCR), from Pelotas, Brazil. Self-report sequelae from COVID-19 were defined as the primary outcome. A questionnaire containing sociodemographic, medical, behavioral and self-report of sequelae of COVID-19 was applied. A complete periodontal clinical examination was performed. Weight and height were assessed. Uni-, bi- and multivariate analyses were performed using Poisson regression with robust variance. Additional analyses were performed considering obesity as a subgroup.

Results

When considering the whole sample, no statistically significant associations between sequelae of COVID-19 with periodontitis (prevalence ratio [PR]:1.14;95% confidence interval [95%CI]: 0.80–1.61) and obesity (0.93 [0.68–1.26]) were identified. In the subgroup analysis, considering only individuals with obesity, those diagnosed with generalized periodontitis had 86% higher probability to have sequelae of COVID-19 when compared to individuals with periodontal health or localized periodontitis. However, when only those without obesity were considered, no significant association with periodontal status was detected (0.82 [0.55–1.23). No significant association with periodontal status were observed when the severity of sequelae (no sequelae, 1 sequela, and >1 sequela) were considered (p > 0.05).

Conclusions

Individuals diagnosed with obesity and periodontitis have a higher PR of reporting sequelae from COVID-19 compared to individuals with only obesity.

背景:评估成人冠状病毒病2019 (COVID-19)的后遗症及其相关因素,如肥胖和牙周炎。方法:该研究纳入了来自巴西佩洛塔斯的128名年龄≥35岁且通过实时聚合酶链反应(RT-PCR)诊断为COVID-19的个体。自我报告的COVID-19后遗症被定义为主要结局。采用新型冠状病毒肺炎后遗症社会人口学、医学、行为和自我报告问卷。进行了完整的牙周临床检查。评估了体重和身高。单、双、多变量分析采用泊松回归进行稳健方差分析。将肥胖作为一个亚组进行额外的分析。结果:在整个样本中,COVID-19的后遗症与牙周炎(患病率[PR]:1.14;95%可信区间[95% ci]: 0.80-1.61)和肥胖(0.93[0.68-1.26])之间没有统计学意义上的相关性。在亚组分析中,仅考虑肥胖个体,与牙周健康或局部牙周炎个体相比,被诊断为广泛性牙周炎的患者患COVID-19后遗症的可能性高86%。然而,当只考虑那些没有肥胖的人时,没有发现与牙周状态有显著关联(0.82[0.55-1.23])。当考虑到后遗症的严重程度(无后遗症、1后遗症和>1后遗症)时,未观察到与牙周状况的显著相关性(p > 0.05)。结论:与仅肥胖的个体相比,诊断为肥胖和牙周炎的个体报告COVID-19后遗症的概率更高。
{"title":"Association between sequelae of COVID-19 with periodontal disease and obesity: A cross-sectional study","authors":"Maísa Casarin,&nbsp;Francisco Hecktheuer Silva,&nbsp;Ana Flávia Leite Pontes,&nbsp;Betina Dutra Lima,&nbsp;Flavia Q. Pirih,&nbsp;Francisco Wilker Mustafa Gomes Muniz","doi":"10.1002/JPER.23-0412","DOIUrl":"10.1002/JPER.23-0412","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background</h3>\u0000 \u0000 <p>To assess the sequelae of coronavirus disease 2019 (COVID-19) and associated factors, such as obesity and periodontitis in adults.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Methods</h3>\u0000 \u0000 <p>The study included 128 individuals aged ≥35 years with a history of a diagnosis of COVID-19 through real-time polymerase chain reaction (RT-PCR), from Pelotas, Brazil. Self-report sequelae from COVID-19 were defined as the primary outcome. A questionnaire containing sociodemographic, medical, behavioral and self-report of sequelae of COVID-19 was applied. A complete periodontal clinical examination was performed. Weight and height were assessed. Uni-, bi- and multivariate analyses were performed using Poisson regression with robust variance. Additional analyses were performed considering obesity as a subgroup.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>When considering the whole sample, no statistically significant associations between sequelae of COVID-19 with periodontitis (prevalence ratio [PR]:1.14;95% confidence interval [95%CI]: 0.80–1.61) and obesity (0.93 [0.68–1.26]) were identified. In the subgroup analysis, considering only individuals with obesity, those diagnosed with generalized periodontitis had 86% higher probability to have sequelae of COVID-19 when compared to individuals with periodontal health or localized periodontitis. However, when only those without obesity were considered, no significant association with periodontal status was detected (0.82 [0.55–1.23). No significant association with periodontal status were observed when the severity of sequelae (no sequelae, 1 sequela, and &gt;1 sequela) were considered (<i>p</i> &gt; 0.05).</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusions</h3>\u0000 \u0000 <p>Individuals diagnosed with obesity and periodontitis have a higher PR of reporting sequelae from COVID-19 compared to individuals with only obesity.</p>\u0000 </section>\u0000 </div>","PeriodicalId":16716,"journal":{"name":"Journal of periodontology","volume":"95 7","pages":"688-698"},"PeriodicalIF":4.2,"publicationDate":"2023-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138176400","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Clinical and radiographic evaluation of the use of PRF, CGF, and autogenous bone in the treatment of periodontal intrabony defects: Treatment of periodontal defect by using autologous products 使用PRF、CGF和自体骨治疗牙周骨内缺损的临床和影像学评价:使用自体产品治疗牙周缺损
IF 4.2 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-20 DOI: 10.1002/JPER.23-0481
Basem Alshujaa, Ahmet Cemil Talmac, Dicle Altindal, Anas Alsafadi, Abdullah Seckin Ertugrul

Background

The purpose of this randomized clinical study was to clinically evaluate and compare the efficiencies of platelet-rich fibrin (PRF), concentrated growth factor (CGF) and autogenous bone graft (ABG) in the treatment of intrabony pockets and to assess the alveolar bone gain (AB gain) radiographically (panoramic and CBCT images).

Methods

Eighty intrabony pockets were divided into four groups: ojnly open flap debridement (OFD), OFD+PRF, OFD+CGF and OFD+ABG; each group consisted of 20 defects. Plaque index (PI), gingival index (GI), probing depth (PD), clinical attachment level (CAL), and tooth mobility (TM) by using Periotest M device were evaluated. Radiographic images were also taken to evaluate the AB gain. PRF was produced using a protocol of 2,700 RPM for 12 min and the relative centrifugal force (RCF) was evaluated. CGF was prepared as follows: 2 min 2700 rpm, 4 min 2400 rpm, 4 min 2700 rpm, 3 min 3000 rpm.

Results

The study results revealed a similar improvement in PI and GI values in all groups (p > 0.05). There was a statistically significant decrease in PD and CAL in favor of ABG group at day 180 in comparison with other groups (p = 0.001). There was also a statistically significant decrease in TM and alveolar bone height loss (ABHL), whereby the AB gain gradually increased among the groups with the best group being ABG, followed by CGF, PRF, and control groups, respectively (p = 0.001).

Conclusions

The study results support the treatment of periodontal intrabony pockets using OFD in combination with ABG, CGF, and PRF, as ABG showed the best results followed by CGF and PRF.

背景:本随机临床研究的目的是临床评价和比较富血小板纤维蛋白(PRF)、浓缩生长因子(CGF)和自体骨移植(ABG)治疗骨内袋的效果,并评估牙槽骨增重(AB增重)x线摄影(全景和CBCT图像)。方法:将80个骨内袋分为4组:单纯开瓣清创(OFD)组、OFD+PRF组、OFD+CGF组和OFD+ABG组;每组有20个缺陷。采用Periotest M器械评估牙菌斑指数(PI)、牙龈指数(GI)、探探深度(PD)、临床附着水平(CAL)和牙齿活动度(TM)。x线图像也被用来评估AB增益。在2700转/分(RPM) 12分钟的转速下产生PRF,并评估相对离心力(RCF)。CGF的制备方法为:2 min 2700 rpm, 4 min 2400 rpm, 4 min 2700 rpm, 3 min 3000 rpm。结果:研究结果显示,各组PI和GI值的改善相似(p < 0.05)。与其他组相比,ABG组在180天PD和CAL下降有统计学意义(p = 0.001)。TM和牙槽骨高度损失(ABHL)也有统计学意义的降低,其中AB增加在各组间逐渐增加,ABG组最好,CGF组次之,PRF组次之,对照组次之(p = 0.001)。结论:本研究结果支持OFD联合ABG、CGF和PRF治疗牙周骨内袋,ABG效果最好,CGF和PRF效果次之。
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引用次数: 0
Extracellular adenosine triphosphate regulates inflammatory responses of periodontal ligament cells 细胞外三磷酸腺苷调节牙周膜细胞的炎症反应。
IF 4.3 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-06 DOI: 10.1002/JPER.23-0389
Maythwe Kyawsoewin, Jeeranan Manokawinchoke, Chutimon Termkwanchareon, Hiroshi Egusa, Thanaphum Osathanon, Phoonsuk Limraksasin

Background

Various stimuli, that is, mechanical stresses or inflammation, induce the release of adenosine triphosphate (ATP) by human periodontal ligament cells (HPDLCs). Extracellular adenosine triphosphate (eATP) affects HPDLCs’ functions such as immunosuppressive action and inflammatory responses. Lipopolysaccharide (LPS) is the key factor involved in periodontal inflammation. However, the possible correlation and detailed mechanism of inflammation-mediated eATP by LPS and inflammatory cascade formation in HPDLCs is unclarified. This study aims to examine the role of eATP on the HPDLCs’ responses concerning inflammatory actions after LPS treatment.

Methods

HPDLCs were stimulated with Porphyromonas gingivalis LPS and polyinosinic:polycytidylic acid (poly I:C). The amount of ATP release was measured at different time points using a bioluminescence assay. HPDLCs were treated with eATP. The expression of pro-inflammatory and anti-inflammatory genes was determined. Specific P2X purinoreceptor 7 (P2X7) inhibitors (brilliant blue G [BBG] and KN62), a specific P2Y purinoreceptor 1 (P2Y1) inhibitors (MRS2179), calcium chelator (EGTA), protein kinase C (PKC) inhibitors, nuclear factor kappa-light-chain-enhancer of activated B cells (NF𝜅B) activation inhibitors, and cyclic adenosine monophosphate (cAMP)-dependent protein kinase A (PKA) inhibitors (H89 dihydrochloride) and activators (forskolin) were used to dissect the mechanism of eATP-induced HPDLCs’ inflammatory responses.

Results

LPS and poly I:C induced ATP release. A low concentration of eATP (50 µM) increased pro-inflammatory genes (COX2, IL1B, IL6, IL8, IL12, and TNFA), while a high concentration (500 µM) enhanced anti-inflammatory genes (IL4 and IL10). BBG, KN62, and NF𝜅B activation inhibitors impeded eATP-induced pro-inflammatory genes. MRS2179 and H89 markedly suppressed eATP-induced anti-inflammatory genes. Forskolin induced IL4 and IL10.

Conclusion

HPDLCs respond to LPS by releasing ATP. eATP has dose-dependent dual functions on HPDLCs’ inflammatory responses via different pathways. As regulation of inflammation is important in regeneration, eATP may help to limit inflammation and trigger periodontal regeneration.

{"title":"Extracellular adenosine triphosphate regulates inflammatory responses of periodontal ligament cells","authors":"Maythwe Kyawsoewin,&nbsp;Jeeranan Manokawinchoke,&nbsp;Chutimon Termkwanchareon,&nbsp;Hiroshi Egusa,&nbsp;Thanaphum Osathanon,&nbsp;Phoonsuk Limraksasin","doi":"10.1002/JPER.23-0389","DOIUrl":"10.1002/JPER.23-0389","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background</h3>\u0000 \u0000 <p>Various stimuli, that is, mechanical stresses or inflammation, induce the release of adenosine triphosphate (ATP) by human periodontal ligament cells (HPDLCs). Extracellular adenosine triphosphate (eATP) affects HPDLCs’ functions such as immunosuppressive action and inflammatory responses. Lipopolysaccharide (LPS) is the key factor involved in periodontal inflammation. However, the possible correlation and detailed mechanism of inflammation-mediated eATP by LPS and inflammatory cascade formation in HPDLCs is unclarified. This study aims to examine the role of eATP on the HPDLCs’ responses concerning inflammatory actions after LPS treatment.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Methods</h3>\u0000 \u0000 <p>HPDLCs were stimulated with <i>Porphyromonas gingivalis</i> LPS and polyinosinic:polycytidylic acid (poly I:C). The amount of ATP release was measured at different time points using a bioluminescence assay. HPDLCs were treated with eATP. The expression of pro-inflammatory and anti-inflammatory genes was determined. Specific P<sub>2</sub>X purinoreceptor 7 (P<sub>2</sub>X<sub>7</sub>) inhibitors (brilliant blue G [BBG] and KN62), a specific P<sub>2</sub>Y purinoreceptor 1 (P<sub>2</sub>Y<sub>1</sub>) inhibitors (MRS2179), calcium chelator (EGTA), protein kinase C (PKC) inhibitors, nuclear factor kappa-light-chain-enhancer of activated B cells (NF𝜅B) activation inhibitors, and cyclic adenosine monophosphate (cAMP)-dependent protein kinase A (PKA) inhibitors (H89 dihydrochloride) and activators (forskolin) were used to dissect the mechanism of eATP-induced HPDLCs’ inflammatory responses.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>LPS and poly I:C induced ATP release. A low concentration of eATP (50 µM) increased pro-inflammatory genes (<i>COX2, IL1B, IL6, IL8, IL12</i>, and <i>TNFA</i>), while a high concentration (500 µM) enhanced anti-inflammatory genes (<i>IL4</i> and <i>IL10</i>). BBG, KN62, and NF𝜅B activation inhibitors impeded eATP-induced pro-inflammatory genes. MRS2179 and H89 markedly suppressed eATP-induced anti-inflammatory genes. Forskolin induced <i>IL4</i> and <i>IL10</i>.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusion</h3>\u0000 \u0000 <p>HPDLCs respond to LPS by releasing ATP. eATP has dose-dependent dual functions on HPDLCs’ inflammatory responses via different pathways. As regulation of inflammation is important in regeneration, eATP may help to limit inflammation and trigger periodontal regeneration.</p>\u0000 </section>\u0000 </div>","PeriodicalId":16716,"journal":{"name":"Journal of periodontology","volume":"95 3","pages":"281-295"},"PeriodicalIF":4.3,"publicationDate":"2023-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71482682","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Superoxide dismutase 2 scavenges ROS to promote osteogenic differentiation of human periodontal ligament stem cells by regulating Smad3 in alveolar bone-defective rats 超氧化物歧化酶2清除ROS,通过调节牙槽骨缺损大鼠的Smad3促进人牙周膜干细胞的成骨分化。
IF 4.3 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-03 DOI: 10.1002/JPER.23-0469
Wei Qiu, Qian Sun, Na Li, Zehao Chen, Hongle Wu, Zhao Chen, Xiaolan Guo, Fuchun Fang

Background

Osteogenic differentiation of human periodontal ligament stem cells (hPDLSCs) is an essential event in alveolar bone regeneration. Oxidative stress may be the main inhibiting factor of hPDLSC osteogenesis. Superoxide dismutase 2 (SOD2) is a key antioxidant enzyme, but its effect on hPDLSC osteogenic differentiation is unclear.

Methods

Several surface markers were detected by flow cytometry, and the differentiation potential of hPDLSCs was validated by alkaline phosphatase (ALP), Alizarin Red S, and Oil Red O staining. Osteogenic indicators of hPDLSCs were detected by real-time quantitative polymerase chain reaction (RT-qPCR), Western blotting, and ALP staining. Furthermore, alveolar bone defect rat models were analyzed through micro-CT, hematoxylin and eosin, and Masson staining. The intracellular reactive oxygen species (ROS) level was evaluated by a ROS assay kit. Finally, the expression of SOD2, Smad3, and p-Smad3 in hPDLSCs was detected by RT-qPCR and Western blotting (WB).

Results

SOD2 positively regulated the gene and protein expressions of ALP, BMP6, and RUNX2 in hPDLSCs (p < 0.05). Ideal bone formation and continuous cortical bone were obtained by transplanting LV-SOD2 hPDLSCs (lentivirus vector for overexpressing SOD2 in hPDLSCs) in vivo. Exogenous H2O2 downregulated osteogenic indicators (ALP, BMP6, RUNX2) in hPDLSCs (p < 0.05); this was reversed by overexpression of SOD2. WB results showed that the Smad3 and p-Smad3 signaling pathways participated in the osteogenic process of SOD2 in hPDLSCs.

Conclusion

SOD2 positively regulated hPDLSC osteogenic differentiation in vitro and in vivo. Mechanistically, SOD2 promotes hPDLSC osteogenic differentiation by regulating the phosphorylation of Smad3 to scavenge ROS. This work provides a theoretical basis for the treatment of alveolar bone regeneration.

背景:人牙周膜干细胞(hPDLSCs)的成骨分化是牙槽骨再生中的一个重要事件。氧化应激可能是hPDLSC成骨的主要抑制因子。超氧化物歧化酶2(SOD2)是一种关键的抗氧化酶,但其对hPDLSC成骨分化的影响尚不清楚。方法:用流式细胞仪检测几种表面标志物,并用碱性磷酸酶(ALP)、茜素红S和油红O染色验证hPDLSCs的分化潜力。通过实时定量聚合酶链反应(RT-qPCR)、蛋白质印迹和ALP染色检测hPDLSCs的成骨指标。此外,通过显微CT、苏木精和伊红以及Masson染色对大鼠牙槽骨缺损模型进行分析。通过ROS测定试剂盒评估细胞内活性氧(ROS)水平。最后,通过RT-qPCR和蛋白质印迹(WB)检测hPDLSCs中SOD2、Smad3和p-Smad3的表达。结果:SOD2对ALP、BMP6、BMP5的基因和蛋白表达具有正调控作用,和hPDLSCs中的RUNX2(p2 O2下调hPDLSCs中的成骨指标(ALP、BMP6、RUNX2)(p结论:SOD2在体内外均对hPDLSC的成骨分化具有正向调控作用。从机制上讲,SOD2通过调节Smad3的磷酸化清除ROS来促进hPDLSC的成骨细胞分化。本研究为治疗牙槽骨再生提供了理论依据。
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引用次数: 0
Suppression of subgingival bacteria by antimicrobial photodynamic therapy using transgingival irradiation: A randomized clinical trial 抗微生物光动力疗法经牙龈照射抑制龈下细菌:一项随机临床试验。
IF 4.2 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-01 DOI: 10.1002/JPER.23-0328
Jun-ichiro Hayashi, Kohta Ono, Yuki Iwamura, Yasuyuki Sasaki, Tasuku Ohno, Ryoma Goto, Eisaku Nishida, Genta Yamamoto, Takeshi Kikuchi, Naoya Higuchi, Akio Mitani, Mitsuo Fukuda

Background

Antimicrobial photodynamic therapy (aPDT) is an effective method for eradicating bacteria in periodontal therapy. Standard aPDT requires the insertion of a laser tip into a periodontal pocket, in which the direction of irradiation is limited. Therefore, we devised an aPDT method that uses a transgingival near-infrared wavelength and indocyanine green-encapsulated and chitosan-coated nanoparticles as a photosensitizer.

Methods

Forty patients undergoing supportive periodontal therapy, who had a single root tooth with a pocket of 5 mm or deeper, were used as subjects. In the test group, aPDT was performed by laser irradiation from outside the gingiva using photosensitizer nanoparticles. In the control group, pseudo aPDT without photosensitizer was performed by transgingival irradiation. Subgingival plaque was sampled from inside the pocket before, immediately after, and 1 week after treatment, and evaluated by colony counting and real-time polymerase chain reaction.

Results

There were no significant differences in age, sex, periodontal pocket depth, and bleeding on probing between the test and control groups. Compared with the colony count before treatment, the count in the test group was significantly reduced immediately after treatment. The number of patients with colony reduction to ≤50% and ≤10% was significantly higher in the test group than in the control group. None of the participants reported pain, although one participant reported discomfort.

Conclusion

As a bacterial control method for residual pockets in patients undergoing supportive periodontal therapy, transgingival aPDT is a promising treatment strategy that is not generally accompanied by pain or discomfort.

背景:抗菌光动力疗法(aPDT)是牙周治疗中一种有效的除菌方法。标准aPDT需要将激光尖端插入牙周袋中,其中照射方向受到限制。因此,我们设计了一种aPDT方法,该方法使用跨牙龈近红外波长和吲哚菁绿包裹和壳聚糖包裹的纳米颗粒作为光敏剂。方法:选择40名接受支持性牙周治疗的患者作为受试者,他们的单根牙的窝深为5毫米或5毫米。在试验组中,通过使用光敏剂纳米颗粒从牙龈外进行激光照射来进行aPDT。在对照组中,通过经牙龈照射进行不含光敏剂的伪aPDT。在治疗前、治疗后立即和治疗后1周从袋内取样龈下菌斑,并通过菌落计数和实时聚合酶链式反应进行评估。结果:试验组和对照组在年龄、性别、牙周袋深度和探查出血方面没有显著差异。与治疗前的菌落计数相比,试验组的菌落计数在治疗后立即显著减少。试验组菌落减少至≤50%和≤10%的患者数量显著高于对照组。没有一名参与者报告疼痛,但有一名参与者表示不适。结论:作为一种治疗支持性牙周治疗患者残留菌袋的细菌控制方法,经牙龈aPDT是一种很有前途的治疗策略,通常不会伴随疼痛或不适。
{"title":"Suppression of subgingival bacteria by antimicrobial photodynamic therapy using transgingival irradiation: A randomized clinical trial","authors":"Jun-ichiro Hayashi,&nbsp;Kohta Ono,&nbsp;Yuki Iwamura,&nbsp;Yasuyuki Sasaki,&nbsp;Tasuku Ohno,&nbsp;Ryoma Goto,&nbsp;Eisaku Nishida,&nbsp;Genta Yamamoto,&nbsp;Takeshi Kikuchi,&nbsp;Naoya Higuchi,&nbsp;Akio Mitani,&nbsp;Mitsuo Fukuda","doi":"10.1002/JPER.23-0328","DOIUrl":"10.1002/JPER.23-0328","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background</h3>\u0000 \u0000 <p>Antimicrobial photodynamic therapy (aPDT) is an effective method for eradicating bacteria in periodontal therapy. Standard aPDT requires the insertion of a laser tip into a periodontal pocket, in which the direction of irradiation is limited. Therefore, we devised an aPDT method that uses a transgingival near-infrared wavelength and indocyanine green-encapsulated and chitosan-coated nanoparticles as a photosensitizer.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Methods</h3>\u0000 \u0000 <p>Forty patients undergoing supportive periodontal therapy, who had a single root tooth with a pocket of 5 mm or deeper, were used as subjects. In the test group, aPDT was performed by laser irradiation from outside the gingiva using photosensitizer nanoparticles. In the control group, pseudo aPDT without photosensitizer was performed by transgingival irradiation. Subgingival plaque was sampled from inside the pocket before, immediately after, and 1 week after treatment, and evaluated by colony counting and real-time polymerase chain reaction.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>There were no significant differences in age, sex, periodontal pocket depth, and bleeding on probing between the test and control groups. Compared with the colony count before treatment, the count in the test group was significantly reduced immediately after treatment. The number of patients with colony reduction to ≤50% and ≤10% was significantly higher in the test group than in the control group. None of the participants reported pain, although one participant reported discomfort.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusion</h3>\u0000 \u0000 <p>As a bacterial control method for residual pockets in patients undergoing supportive periodontal therapy, transgingival aPDT is a promising treatment strategy that is not generally accompanied by pain or discomfort.</p>\u0000 </section>\u0000 </div>","PeriodicalId":16716,"journal":{"name":"Journal of periodontology","volume":"95 8","pages":"718-728"},"PeriodicalIF":4.2,"publicationDate":"2023-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/JPER.23-0328","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71424436","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Aggressive periodontitis in southwestern American Indian adolescents 美国西南部印度青少年的侵袭性牙周炎。
IF 4.2 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-11-01 DOI: 10.1002/JPER.23-0410
Thomas E. Rams, Adolfo Contreras, Jørgen Slots

Background

This study determined the prevalence of aggressive (molar-incisor pattern) (Ag/MI) periodontitis and assessed the associated subgingival bacterial-herpesvirus microbiota in Pueblo Indian adolescents in the southwestern United States.

Methods

The study included 240 Pueblo Indian adolescents, aged 13–20 years old, residing in three Rio Grande River villages in New Mexico and the Hopi Pueblo reservation in Arizona. Adolescents with Ag/MI periodontitis or periodontal health provided subgingival samples for culture of bacterial pathogens and for polymerase chain reaction detection of periodontal herpesviruses.

Results

Ag/MI periodontitis was detected in 22 (9.2%) Pueblo Indian adolescents, with 21 exhibiting a localized molar-incisor breakdown pattern. Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, and other red/orange complex bacterial pathogens predominated in Ag/MI periodontitis, whereas periodontal health yielded mainly viridans streptococci and Actinomyces species. Periodontal herpesviruses demonstrated a 3.5 odds ratio relationship with Ag/MI periodontitis. The only adolescent with generalized Ag/MI periodontitis harbored viral co-infection by cytomegalovirus plus Epstein–Barr virus Type 1, in addition to A. actinomycetemcomitans, P. gingivalis, and several other periodontopathic bacteria.

Conclusions

Pueblo Indian adolescents showed an unusually high prevalence of early-age Ag/MI periodontitis predominated by periodontopathic bacteria and herpesviruses suspected to be major etiologic agents of the disease.

背景:本研究确定了美国西南部普韦布洛印第安人青少年侵袭性(臼齿-切牙型)(Ag/MI)牙周炎的患病率,并评估了相关的龈下细菌疱疹病毒微生物群,居住在新墨西哥州的三个格兰德河村庄和亚利桑那州的霍皮普韦布洛保留地。患有Ag/MI牙周炎或牙周健康的青少年提供了龈下样本,用于细菌病原体的培养和牙周疱疹病毒的聚合酶链式反应检测。结果:在22名(9.2%)普韦布洛印第安人青少年中检测到Ag/MI牙周炎,其中21人表现出局部磨牙-门牙破坏模式。Ag/MI牙周炎主要由聚合放线菌、牙龈卟啉单胞菌和其他红色/橙色复合细菌病原体引起,而牙周健康主要由绿色链球菌和放线菌引起。牙周疱疹病毒与Ag/MI牙周炎的比值比为3.5。唯一一名患有全身性Ag/MI牙周炎的青少年携带巨细胞病毒加1型EB病毒,以及共放线菌、牙龈卟啉单胞菌和其他几种牙周病细菌的病毒共同感染。结论:普韦布洛-印度青少年早期Ag/MI牙周炎的患病率异常高,主要由牙周病细菌和疱疹病毒引起,怀疑它们是该疾病的主要病因。
{"title":"Aggressive periodontitis in southwestern American Indian adolescents","authors":"Thomas E. Rams,&nbsp;Adolfo Contreras,&nbsp;Jørgen Slots","doi":"10.1002/JPER.23-0410","DOIUrl":"10.1002/JPER.23-0410","url":null,"abstract":"<div>\u0000 \u0000 \u0000 <section>\u0000 \u0000 <h3> Background</h3>\u0000 \u0000 <p>This study determined the prevalence of aggressive (molar-incisor pattern) (Ag/MI) periodontitis and assessed the associated subgingival bacterial-herpesvirus microbiota in Pueblo Indian adolescents in the southwestern United States.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Methods</h3>\u0000 \u0000 <p>The study included 240 Pueblo Indian adolescents, aged 13–20 years old, residing in three Rio Grande River villages in New Mexico and the Hopi Pueblo reservation in Arizona. Adolescents with Ag/MI periodontitis or periodontal health provided subgingival samples for culture of bacterial pathogens and for polymerase chain reaction detection of periodontal herpesviruses.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Results</h3>\u0000 \u0000 <p>Ag/MI periodontitis was detected in 22 (9.2%) Pueblo Indian adolescents, with 21 exhibiting a localized molar-incisor breakdown pattern. <i>Aggregatibacter actinomycetemcomitans</i>, <i>Porphyromonas gingivalis</i>, and other red/orange complex bacterial pathogens predominated in Ag/MI periodontitis, whereas periodontal health yielded mainly viridans streptococci and <i>Actinomyces</i> species. Periodontal herpesviruses demonstrated a 3.5 odds ratio relationship with Ag/MI periodontitis. The only adolescent with generalized Ag/MI periodontitis harbored viral co-infection by cytomegalovirus plus Epstein–Barr virus Type 1, in addition to <i>A</i>. <i>actinomycetemcomitans</i>, <i>P</i>. <i>gingivalis</i>, and several other periodontopathic bacteria.</p>\u0000 </section>\u0000 \u0000 <section>\u0000 \u0000 <h3> Conclusions</h3>\u0000 \u0000 <p>Pueblo Indian adolescents showed an unusually high prevalence of early-age Ag/MI periodontitis predominated by periodontopathic bacteria and herpesviruses suspected to be major etiologic agents of the disease.</p>\u0000 </section>\u0000 </div>","PeriodicalId":16716,"journal":{"name":"Journal of periodontology","volume":"95 6","pages":"594-602"},"PeriodicalIF":4.2,"publicationDate":"2023-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71424425","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
引用次数: 0
Effects of a stabilized stannous fluoride dentifrice on clinical, immunomodulatory, and microbial outcomes in a human experimental gingivitis model 在人类实验性牙龈炎模型中,稳定的氟化亚锡洁牙剂对临床、免疫调节和微生物结果的影响。
IF 4.3 2区 医学 Q1 DENTISTRY, ORAL SURGERY & MEDICINE Pub Date : 2023-10-27 DOI: 10.1002/JPER.22-0710
Noah Fine, Abdelahhad Barbour, Kamini Kaura, Kristopher A. Kerns, Dandan Chen, Harsh M. Trivedi, Juliana Gomez, Amarpreet Sabharwal, Jeffrey S. McLean, Richard P. Darveau, Michael Glogauer

Background

Stannous fluoride dentifrice is well established for its beneficial clinical effects. In this study, we evaluated the effects of stannous fluoride on inflammation and oral microbiome.

Methods

In this randomized, parallel-arm, double-blind, controlled clinical trial, we compared clinical resolution of experimental gingivitis by evaluating bleeding on probing, gingival index, and plaque index between stannous fluoride stabilized with zinc phosphate (test) and sodium fluoride (control) dentifrices. Further, these groups were compared for oral neutrophil counts, systemic priming of neutrophils, gingival crevicular fluid (GCF) expression of inflammatory markers, and the oral microbiome.

Results

We found significant reduction in bleeding on probing in the test group compared to the control group in experimental gingivitis when participants used the test dentifrice prior to induction of experimental gingivitis. The test group also showed significant reductions in GCF levels of inflammatory markers (matrix metalloproteinase 8 [MMP8], receptor activator of nuclear factor kappa-Β ligand [RANKL]), oral polymorphonuclear neutrophil (PMN) counts, and systemic neutrophil priming (CD11b expression) during experimental gingivitis. Further, significant reductions in the gram-negative genera Porphyromonas, Tannerella, and Treponema were noted in the test group.

Conclusion

The stannous fluoride stabilized with zinc phosphate dentifrice formulation demonstrated clinical reduction in gingival inflammation and a beneficial effect on microbiome and immune markers. This intervention should be explored as a preventive aid in the progression of plaque-induced gingivitis to periodontitis.

背景:氟化亚锡洁牙剂具有良好的临床疗效。在这项研究中,我们评估了氟化亚锡对炎症和口腔微生物组的影响。方法:在这项随机、平行、双盲、对照的临床试验中,我们通过评估磷酸锌稳定的氟化亚锡(试验)和氟化钠(对照)洁牙剂的探针出血、牙龈指数和牙菌斑指数,比较了实验性牙龈炎的临床解决方案。此外,比较了这些组的口腔中性粒细胞计数、中性粒细胞的全身启动、炎症标志物的龈沟液(GCF)表达和口腔微生物组。结果:我们发现,与对照组相比,当参与者在诱发实验性牙龈炎之前使用测试洁牙剂时,测试组在实验性牙髓炎中的探查出血显著减少。试验组还显示,在实验性牙龈炎期间,炎症标志物(基质金属蛋白酶8[MMP8]、核因子κ-β配体受体激活剂[RANKL])、口腔中性粒细胞(PMN)计数和全身中性粒细胞启动(CD11b表达)的GCF水平显著降低。此外,在试验组中,革兰氏阴性属卟啉单胞菌属、单核菌属和密螺旋体属显著减少。结论:磷酸锌稳定的氟化亚锡洁牙剂在临床上减少了牙龈炎症,并对微生物组和免疫标志物产生了有益影响。这种干预措施应被探索为预防牙菌斑诱导的牙龈炎发展为牙周炎的辅助措施。
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引用次数: 0
期刊
Journal of periodontology
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