AbstractPeriodontitis is a chronic inflammatory disease initiated by biofilm microorganisms and mediated by host immune imbalance. Uncontrolled periodontal infections are the leading cause of tooth loss in adults. Thrombotic diseases can lead to partial or complete obstruction of blood flow in the circulatory system, manifesting as organ or tissue ischemia and necrosis in patients with arterial thrombosis, and local edema, pain and circulatory instability in patients with venous thrombosis, which may lead to mortality or fatality in severe case.

摘要牙周炎是由生物膜微生物引发并由宿主免疫失衡介导的慢性炎症性疾病。不受控制的牙周感染是成人牙齿脱落的主要原因。血栓性疾病可导致循环系统血流部分或完全阻塞，表现为动脉血栓形成患者的器官或组织缺血和坏死，静脉血栓形成患者的局部水肿，疼痛和循环不稳定，严重时可能导致死亡或死亡。

Recent studies found that periodontitis might enhance thrombosis through bacterial transmission or systemic inflammation by affecting platelet-immune cell interactions, as well as the coagulation, and periodontal therapy could have a prophylactic effect on patients with thrombotic diseases. In this review, we summarized clinical findings on the association between periodontitis and thrombotic diseases and discussed several novel prothrombotic periodontitis-related agents, and presented a perspective to emphasize the necessity of oral health management for people at high risk of thrombosis..

最近的研究发现，牙周炎可能通过影响血小板-免疫细胞相互作用以及凝血来通过细菌传播或全身炎症增强血栓形成，牙周治疗可能对血栓性疾病患者具有预防作用。在这篇综述中，我们总结了牙周炎与血栓性疾病之间关系的临床发现，并讨论了几种新型促血栓形成性牙周炎相关药物，并提出了一个观点，以强调对血栓形成高危人群进行口腔健康管理的必要性。。

IntroductionPeriodontitis is a chronic inflammatory disease initiated by biofilm microorganisms and mediated by host immune imbalance,1 which is characterized by the destruction of tooth-supporting tissues, including the gingiva, alveolar bone, periodontal ligament, and cementum,2 and it is the leading cause of tooth loss in adults.3,4,5 The overall prevalence of periodontitis is as high as 45%-50% globally, with the most severe cases affecting 11.2% of the world’s population, ranking it the sixth most prevalent disease in humans.6 Extensive evidence suggests a strong association between periodontitis and various systemic diseases such as atherosclerosis,7 rheumatoid arthritis,8 inflammatory bowel disease,9 diabetes mellitus (DM),10,11,12 and chronic obstructive pulmonary disease.13 The keystone pathogens in periodontitis, represented by Porphyromonas gingivalis (P.

简介牙周炎是一种由生物膜微生物引发并由宿主免疫失衡介导的慢性炎症性疾病，1其特征是牙齿支持组织的破坏，包括牙龈，牙槽骨，牙周韧带和牙骨质，2它是成人牙齿脱落的主要原因。3,4,5全球牙周炎的总体患病率高达45%〜50%，最严重的病例影响了世界人口的11.2%，是人类第六大最常见的疾病。广泛的证据表明，牙周炎与各种全身性疾病之间有很强的关联，如动脉粥样硬化，7类风湿性关节炎，8炎症性肠病，9糖尿病（DM），10,11,12和慢性阻塞性肺病[13]。牙周炎的主要病原体，以牙龈卟啉单胞菌（P。

gingivalis), can invade the blood circulation directly through ulcers in the periodontal pockets and colonize distal organs to produce toxins that trigger inflammation.14 Periodontal pathogen can also invade the intestinal mucosal barrier via the oral-gut axis, causing gut dysbiosis.15 In addition, the release of damage-associated molecular patterns (DAMPs) due to localized periodontal tissue destruction and subsequent systemic immune responses also contribute to an increased inflammatory burden in other organs.16 The high prevalence of periodontitis worldwide necessitates the management of oral cavity infection and inflammation as an inevitable health concern for patients with systemic diseases.

牙龈），可以通过牙周袋中的溃疡直接侵入血液循环，并在远端器官定植，产生引发炎症的毒素[14]。牙周病原体也可以通过口腔-肠道轴侵入肠粘膜屏障，导致肠道生态失调[15]。此外，由于局部牙周组织破坏和随后的全身免疫反应导致的损伤相关分子模式（DAMPs）的释放也导致其他器官的炎症负担增加[16]。全球牙周炎的高发病率需要管理口腔感染和炎症，这是全身性疾病患者不可避免的健康问题。

Therefore, it is crucial to focus on prevention or treatment of periodontitis in order to effectively control this risk factor. The association between periodontitis and cardiovascular disease (CVD) has been extensi.

因此，重点预防或治疗牙周炎以有效控制这一危险因素至关重要。牙周炎与心血管疾病（CVD）之间的关联已经广泛。

Thromboangiitis obliterans (TAO)

血栓闭塞性脉管炎（TAO）

TAO, also known as Buerger disease or von Winiwarter-Buerger syndrome, is a chronic, nonatherosclerotic, segmental, obliterative, inflammatory vasculopathy characterized by the presence of a highly cellular arterial thrombus and extensive intimal inflammation.56 While the etiology of TAO remains unknown, immune-mediated vascular injury has been proposed as a possible mechanism.56 Previous studies have identified smoking as a significant risk factor for TAO,57,58 yet there are still some patients with TAO who have never used tobacco.

TAO也称为Buerger病或von Winiwarter-Buerger综合征，是一种慢性，非动脉粥样硬化，节段性，闭塞性，炎性血管病变，其特征是存在高度细胞性动脉血栓和广泛的内膜炎症[56]。虽然TAO的病因尚不清楚，但已提出免疫介导的血管损伤是一种可能的机制[56]。先前的研究已经确定吸烟是TAO的重要危险因素[57,58]，但仍有一些TAO患者从未使用过烟草。

It is worth emphasizing that poor oral hygiene and a high prevalence of periodontitis are common among TAO patients. In 2005, researchers identified causative organisms of oral origin from TAO lesions.59 A retrospective study involving 58 patients with TAO reported that periodontitis corresponding to moderate grade in 31% of cases, while severe grade and edentulous patients was revealed in 56% and 13%, respectively.60 In addition, compared to healthy individuals, patients with TAO not only had a higher prevalence of periodontitis, but also higher serum levels of antibodies related to periodontal pathogens,61 and a positive correlation with the percentage of sites with clinical attachment loss ≥ 4 mm.62 Consequently, it has been postulated that TAO may be an infectious disease, with periodontitis being the most probable source of infection in these patients.63.

值得强调的是，不良的口腔卫生和牙周炎的高患病率在TAO患者中很常见。2005年，研究人员从TAO病变中发现了口腔来源的致病微生物[59]。一项涉及58例TAO患者的回顾性研究报道，31%的患者牙周炎相当于中度，而重度和无牙颌患者分别为56%和13%[60]。此外，与健康人相比，TAO患者不仅牙周炎患病率较高，而且与牙周病原体相关的抗体血清水平也较高[61]，与临床附着丧失≥4mm的部位百分比呈正相关[62]。因此，据推测，TAO可能是一种传染病，牙周炎是这些患者最可能的感染源。

Atrial fibrillation-related thrombosis

心房颤动相关血栓形成

Atrial fibrillation (AF) is a chaotic, rapid (300-500 bpm), and irregular atrial rhythm, which is the result of either electrophysiological abnormalities that underlie impulse generation and/or structural abnormalities of cellular connections that typically facilitate rapid and uniform impulse conduction.64 Dislodgment of an attached thrombus due to AF can result in acute embolization, and secondary thrombosis around the emboli makes thrombolysis and reperfusion more difficult.

心房颤动（AF）是一种混乱，快速（300-500 bpm）和不规则的心房节律，这是脉冲产生的电生理异常和/或细胞连接的结构异常的结果，通常有助于快速和均匀的脉冲传导.64由于房颤引起的附着血栓的脱落可导致急性栓塞，并且栓子周围的继发性血栓形成使溶栓和再灌注更加困难。

Periodontitis is a risk factor for the occurrence of atrial fibrillation. Chen et al. evaluated 393,745 patients with periodontitis as well as 393 745 non-periodontitis subjects using the 1999-2010 Taiwanese National Health Insurance Research Database and found a higher risk of AF in the periodontitis group compared with the non-periodontitis group after adjusting for potential confounders (HR = 1.31; 95% confidence interval, 1.25-1.36).26 Interestingly, the higher risk of AF in the periodontitis group remained significant in all disease subgroups (except hyperthyroidism and sleep apnea).

牙周炎是心房颤动发生的危险因素。陈等人使用1999-2010年台湾国民健康保险研究数据库评估了393745名牙周炎患者和393745名非牙周炎患者，发现在调整潜在混杂因素后，牙周炎组的房颤风险高于非牙周炎组（HR=1.31；95%置信区间，1.25-1.36）[26]。有趣的是，牙周炎组房颤的高风险在所有疾病亚组（甲状腺功能亢进和睡眠呼吸暂停除外）中仍然显着。

Miyauchi et al. conducted a study on 596 patients with AF who underwent a first session of radiofrequency catheter ablation for recurrence with a mean follow-up period of 17.1 ± 14.5 months and tested the serum IgG antibody titers against P. gingivalis (types I-IV). Multivariate Cox proportional analysis demonstrated that high-value serum antibody titer against P.

Miyauchi等人对596例房颤患者进行了一项研究，这些患者接受了第一次射频导管消融治疗复发，平均随访时间为17.1±14.5个月，并测试了针对牙龈卟啉单胞菌（I-IV型）的血清IgG抗体滴度。多变量Cox比例分析表明，针对P的高值血清抗体滴度。

gingivalis type IV independently predicted late AF recurrence, providing further evidence of the association between periodontitis and AF.65 In addition, Miyauchi et al. categorized left atrial appendage spontaneous echo contrast (LAA-SEC), a thrombosis indicator, into nondense SEC and dense SEC based on echocardiography images and found out that high-.

IV型牙龈炎独立预测晚期房颤复发，为牙周炎与房颤之间的关联提供了进一步的证据。此外，Miyauchi等人根据超声心动图图像将血栓形成指标左心耳自发回声对比（LAA-SEC）分为非致密SEC和致密SEC，并发现高。

Arterial dissection-related thrombosis

动脉夹层相关血栓形成

Secondary thrombosis from arterial dissection can lead to serious ischemic cardiovascular events or increase the risk of arterial dissection rupture, which can lead directly to death.69 Delgado et al. reported a case of severe carotid artery dissection caused by periodontal infection of the second inferior molar and cervical cellulitis, suggesting that severe periodontal infection may be a contributing factor in the development of arterial dissection.70.

动脉夹层继发性血栓形成可导致严重的缺血性心血管事件或增加动脉夹层破裂的风险，从而直接导致死亡.69 Delgado等报道了一例由第二下磨牙牙周感染引起的严重颈动脉夹层和颈蜂窝织炎，提示严重的牙周感染可能是动脉夹层发展的一个因素.70。

Marfan syndrome (MFS) is an autosomal dominant connective tissue disorder caused by missense mutations in fibronectin-1 (FBN-1), a component of extracellular microfibrils. Cardiovascular complications including aortic root dilatation, coarctation, and rupture are the primary contributor to MFS mortality.71 Umezawa et al.

。心血管并发症包括主动脉根部扩张，缩窄和破裂是MFS死亡率的主要原因.71 Umezawa等。

conducted an 8-month follow-up evaluation of periodontal parameters and cardiac function markers in 3 pre-surgery MFS patients, 4 post-surgery MFS patients, and 7 healthy volunteers. During this period, all patients underwent supportive periodontal therapy (SPT). The study revealed that the BOP and periodontal inflamed surface area (PISA) of MFS preoperative patients were higher at baseline compared with the control group.

对3名术前MFS患者，4名术后MFS患者和7名健康志愿者进行了为期8个月的牙周参数和心脏功能标志物随访评估。在此期间，所有患者均接受了支持性牙周治疗（SPT）。研究表明，与对照组相比，MFS术前患者的BOP和牙周发炎表面积（PISA）在基线时更高。

Even more interestingly, cardiac function indicators, such as left ventricular end-diastolic diameter (LVDd) and ejection fraction (EF) values, were significantly improved in the pre-surgery MFS patient group after SPT.72 This study showed that MFS patients exhibit a deteriorated periodontal condition, while periodontal treatment exerts a positive impact on the cardiovascular function of MFS patients.

。

Not only that, both LVDd and EF are important indicators for predicting the occurrence of thrombosis,73,74 suggesting a potential relationship between periodontitis or periodontal therapy and thrombosis induced by arterial dissection..

不仅如此，LVDd和EF都是预测血栓形成发生的重要指标[73,74]，提示牙周炎或牙周治疗与动脉夹层引起的血栓形成之间存在潜在关系。。

Periodontitis and venous thromboembolismVenous thromboembolism (VTE), which encompasses deep venous thrombosis (DVT) and pulmonary embolism (PE), are the most common preventable cause of hospital death and a source of substantial long-term morbidity. A study conducted in 2007 proposed oral bacteria as a risk factor for valvular incompetence in primary varicose veins.75 Subsequently, a cross-sectional study involving 197 individuals found that a high prevalence of periodontal disease was detected in patients with thromboembolic disease.

牙周炎和静脉血栓栓塞包括深静脉血栓形成（DVT）和肺栓塞（PE）的静脉血栓栓塞（VTE）是最常见的可预防的医院死亡原因，也是长期发病率的来源。2007年进行的一项研究提出口腔细菌是原发性静脉曲张瓣膜功能不全的危险因素[75]。随后，一项涉及197人的横断面研究发现，血栓栓塞性疾病患者的牙周病患病率很高。

Various periodontal parameters, including bleeding index, gingival index, simplified oral hygiene index, clinical attachment level, and probing pocket depth, were found to be significantly higher in VTE disease patients than healthy control group.76 The same research team also observed a relationship between the presence of periodontitis and elevated D-dimer levels in another cross-sectional, case‑control study that enrolled 142 patients, which suggested that patients with VTE disease and periodontal disease may face an increased risk of experiencing a new episode of thromboembolism.77 Furthermore, results from a prospective cohort study comprising 8 092 participants indicated that the VTE incidence rate of 4.53/1 000 person in periodontal disease compared to 2.79/1 000 person without periodontal disease.78 Meanwhile, a state-of-the-art systematic review evaluating and including 15 articles drew firm conclusions about the association between periodontal disease and the incidence of VTE.79 Last but not least, although DVT mainly occurs in lower extremity, several researches reported that periodontal bacteria can be involved in venous thrombosis within the whole body.

VTE疾病患者的各种牙周参数，包括出血指数、牙龈指数、简化口腔卫生指数、临床附着水平和探测袋深度，均显着高于健康对照组。76同一研究小组还观察到牙周炎的存在与D-二聚体水平升高之间的关系，另一项横断面病例对照研究招募了142名患者，这表明VTE疾病和牙周病患者可能面临新发血栓栓塞的风险增加。77此外，一项由8092名参与者组成的前瞻性队列研究结果表明，牙周病VTE发病率为4.53/1000人，而2.79/1000人1000人没有牙周疾病。78与此同时，一项最新的系统评价评估并包括15篇文章，得出了关于牙周病与VTE发病率之间关系的确切结论.79最后但并非最不重要的是，尽管DVT主要发生在下肢，但一些研究报道牙周细菌可能参与全身静脉血栓形成。

Hiral et al. reported a case of Lemierre syndrome (right internal jugular.

Hiral等人报道了一例Lemierre综合征（右颈内静脉）。

1.

1.

Can the periodontal health condition serve as a potential classification method for thrombotic diseases?

牙周健康状况能否作为血栓性疾病的潜在分类方法？

2.

2.

Does periodontal therapy effectively reduce the incidence of thrombosis or disease progression in high-risk patients?

牙周治疗能否有效降低高危患者血栓形成或疾病进展的发生率？

3.

3.

Is routine periodontal care essential for thrombotic diseases patients who require surgery intervention?

常规牙周护理对需要手术干预的血栓性疾病患者至关重要吗？

4.

4.

To what extent does periodontal treatment impact the prognosis of patients with thrombotic diseases?

牙周治疗在多大程度上影响血栓性疾病患者的预后？

5.

5.

Through which key signal pathway or biomarkers periodontitis poses its influence on thrombotic diseases and is it possible to develop targeted therapeutic options?

牙周炎通过哪些关键信号通路或生物标志物对血栓性疾病产生影响，是否有可能开发有针对性的治疗选择？

Nevertheless, the exploration and transformation of thrombotic diseases treatment extend beyond conventional medication and surgical approaches, emphasizing the urgent need to elucidate the potential role and effect of periodontal therapy on thrombosis as well as the underlying mechanism linking periodontitis and thrombotic diseases, thereby shaping the future landscape of multidisciplinary treatment (MDT) for such conditions and providing better outcome and new therapeutic options for these patients (Fig.

然而，血栓性疾病治疗的探索和转变超出了传统的药物治疗和手术方法，强调迫切需要阐明牙周治疗对血栓形成的潜在作用和影响，以及牙周炎和血栓性疾病之间的潜在机制，从而塑造未来多学科治疗（MDT）的前景，为这些患者提供更好的结果和新的治疗选择（图）。

5).Fig. 5Future perspective regarding the potential role of oral health management in the treatment of thrombotic diseases. Numerous studies have consistently demonstrated the impact of periodontitis on thrombotic diseases across various stages, ranging from pre-clinical to post-operative. Moreover, it has been observed that periodontal treatment positively influences the prognosis of patients with thrombotic diseases.

5） 。图5口腔健康管理在血栓性疾病治疗中的潜在作用的未来前景。许多研究一致证明了牙周炎对血栓性疾病的影响，从临床前到手术后的各个阶段。此外，已经观察到牙周治疗对血栓性疾病患者的预后有积极影响。

However, current therapeutic approaches for thrombotic conditions primarily revolve around lifestyle modifications, medications, and surgical interventions. The significance of oral health management in preventing and treating thrombotic diseases is currently underappreciated, while the underlying key molecules and pathways through which periodontitis exacerbates these conditions remain elusive.

然而，目前血栓性疾病的治疗方法主要围绕生活方式改变，药物治疗和手术干预。口腔健康管理在预防和治疗血栓性疾病方面的重要性目前尚未得到充分认识，而牙周炎加剧这些疾病的潜在关键分子和途径仍然难以捉摸。

It is essential to integrate oral health surveillance and management into the overall treatment plan for individuals with thrombotic diseases. Additionally, further exploration of the intricate mechanisms by which periodontitis impacts thrombosis can pave the way for potential targeted therapeutic strategies aimed at improving patient outcomes.

将口腔健康监测和管理纳入血栓性疾病患者的总体治疗计划至关重要。此外，进一步探索牙周炎影响血栓形成的复杂机制可以为旨在改善患者预后的潜在靶向治疗策略铺平道路。

The illustration was created by C.WFull size imageSummaryThe high prevalence of periodontitis and the potential systemi.

该图由C.WFull size ImageSummary创建，牙周炎和潜在系统的高患病率。

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Download referencesAcknowledgementsThis study was supported by the National Natural Science Foundation of China grant 82170970 (YW), 81970944 (LZ), 82300452 (CW), Sichuan Science and Technology Program 2023NSFSC0553 (LZ), 2019JDRC0104 (JG), 2022YFS0359, 2024YFFK0238 (TW), 2022YFS0187 (DY), 24QYCX0412 (JZ), 2024YFFK0239 (JG), 2024YFFK0237 (CW) and Post-Doctor Research Project of West China Hospital, Sichuan University 2023HXBH108 (JG).

。

The funding bodies played no role in the design of the study, the collection, analysis, and interpretation of the data, and the writing of the manuscript. The authors would like to thank Hanyao Huang, DDS, PhD for his assistance in the process of preparation, submission and revision of this manuscript.Author informationAuthor notesThese authors contributed equally: Jinting Ge, Xuanzhi ZhuAuthors and AffiliationsDivision of Vascular Surgery, Department of General Surgery, West China Hospital, Sichuan University, Chengdu, ChinaJinting Ge, Chengxin Weng, Ding Yuan, Jichun Zhao & Tiehao WangState Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases & West China Hospital of Stomatology, Sichuan University, Chengdu, ChinaXuanzhi Zhu, Lei Zhao & Yafei WuDepartment of Periodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, ChinaXuanzhi Zhu, Lei Zhao & Yafei WuAuthorsJinting GeView author publicationsYou can also search for this author in.

资助机构在研究的设计，数据的收集，分析和解释以及手稿的撰写中没有发挥任何作用。作者要感谢DDS博士Hanyao Huang在编写，提交和修订本手稿过程中的帮助。作者信息作者注：这些作者做出了同样的贡献：葛金亭，朱宣志作者和附属机构四川大学华西医院普外科血管外科，中国成都葛金亭，翁成新，丁元，赵吉春和王铁浩。口腔疾病国家重点实验室，国家口腔医学中心，国家口腔疾病临床研究中心，四川大学华西口腔医院，中国成都朱宣志，赵磊和吴亚飞四川大学华西口腔医院牙周病学系，中国成都朱宣志，赵磊和吴亚飞作者Jinting GeView作者出版物在中搜索此作者。

PubMed Google ScholarXuanzhi ZhuView author publicationsYou can also search for this author in

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PubMed Google ScholarContributionsJ.G. and X.Z. contributed to the conception and design of the work; J.G., X.Z. and C.W. performed data acquisition, analysis, and interpretation; X.Z. and C.W. were responsible for visualization; J.G., C.W., D.Y., J.Z., L.Z., T.W. and Y.W. were responsible for funding acquisition; J.G., X.Z.

。G、 X.Z.为作品的构思和设计做出了贡献；J、 G.，X.Z.和C.W.进行了数据采集，分析和解释；十、 Z.和C.W.负责可视化；J、 G.，C.W.，D.Y.，J.Z.，L.Z.，T.W.和Y.W.负责资金收购；J、 G.，X.Z。

and C.W. drafted initial manuscript, D.Y., J.Z., L.Z., T.W. and Y.W. performed writing—review and editing, J.G., X.Z., C.W., D.Y., J.Z., L.Z., T.W. and Y.W. critically revised the paper. All authors contributed to the article and approved the submitted version.Corresponding authorsCorrespondence to.

和C.W.起草的初稿，D.Y.，J.Z.，L.Z.，T.W.和Y.W.进行了写作审查和编辑，J.G.，X.Z.，C.W.，D.Y.，J.Z.，L.Z.，T.W.和Y.W.对论文进行了批判性修改。。通讯作者通讯。

Tiehao Wang or Yafei Wu.Ethics declarations

王铁浩或吴亚飞。道德宣言

Competing interests

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The authors declare no competing interests.

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Reprints and permissionsAbout this articleCite this articleGe, J., Zhu, X., Weng, C. et al. Periodontitis impacts on thrombotic diseases: from clinical aspect to future therapeutic approaches.

转载和许可本文引用本文Ge，J.，Zhu，X.，Weng，C。等人。牙周炎对血栓性疾病的影响：从临床角度到未来的治疗方法。

Int J Oral Sci 16, 58 (2024). https://doi.org/10.1038/s41368-024-00325-9Download citationReceived: 27 January 2024Revised: 08 July 2024Accepted: 12 September 2024Published: 15 October 2024DOI: https://doi.org/10.1038/s41368-024-00325-9Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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