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Thorac Cardiovasc Surg 2018; 66(01): 083-090
DOI: 10.1055/s-0035-1564689
Original Basic Science
Georg Thieme Verlag KG Stuttgart · New York

Periodontal Bacterial DNA and Their Link to Human Cardiac Tissue: Findings of a Pilot Study

Dirk Ziebolz
1   Department of Cariology, Endodontology and Periodontology, University of Leipzig, Leipzig, Germany
,
Christoph Rost
2   Department of Preventive Dentistry, Periodontology and Cariology, University Medical Center of Göttingen, Göttingen, Germany
,
Julia Schmidt
2   Department of Preventive Dentistry, Periodontology and Cariology, University Medical Center of Göttingen, Göttingen, Germany
,
Regina Waldmann-Beushausen
3   Department of Thoracic and Cardiovascular Surgery, University Medical Center of Göttingen, Göttingen, Germany
,
Friedrich A. Schöndube
3   Department of Thoracic and Cardiovascular Surgery, University Medical Center of Göttingen, Göttingen, Germany
,
Rainer F. Mausberg
2   Department of Preventive Dentistry, Periodontology and Cariology, University Medical Center of Göttingen, Göttingen, Germany
,
Bernhard C. Danner
3   Department of Thoracic and Cardiovascular Surgery, University Medical Center of Göttingen, Göttingen, Germany
› Author Affiliations
Further Information

Publication History

22 May 2015

17 August 2015

Publication Date:
05 October 2015 (online)

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Abstract

Background The aim of this pilot study was to detect correlations of microbiological DNA, inflammatory proteins, and infection parameters in patients with periodontal disease (PD) and valvular heart disease (VHD).

Methods A perioperative comprehensive dental examination for the investigation of periodontal status, including sampling of specific subgingival bacteria, was performed in 10 patients with indication for surgery of aortic valve stenosis with or without concomitant myocardial revascularization. Standard protocol biopsies were taken from right atrium (A), left septal myocardium (M), and aortic valve (V). Eleven periodontal pathogens DNA in oral and cardiac tissue samples (A/M/V) were analyzed using polymerase chain reaction. For cardiac tissue samples, Western blot analysis of LPS-binding protein (LBP), immunohistochemical (IHC) detection of LBP-big42, LPS-binding protein receptor (CD14), and macrophages (CD68), as well as inflammation scoring measurement were performed.

Results Periodontitis was present in all patients with severe intensity in 7, moderate in 2 and mild in one patient. Same bacterial DNA was detected in A, M, and V in different distribution, and detection was more often in atrium than in myocardium or valve tissue. Morphological investigation revealed increased extracellular inflammatory cell migration. In IHC markers of LBP, CD68 and CD14 showed positive findings for all patients in atrium and myocardium.

Conclusion Our results demonstrate the presence of oral bacterial DNA in human cardiac tissue, as well as inflammatory markers potentially indicating connection of PD and VHD. Further investigation is necessary to confirm these preliminary data.

Keywords

heart valve surgery - systemic inflammation - microbiology - periodontal disease

Funding

This research received no grant from any funding agency in the public, commercial, or not-for-profit sectors.


 

  • References

  • 1 Holtfreter B, Demmer RT, Bernhardt O. , et al. A comparison of periodontal status in the two regional, population-based studies of SHIP and INVEST. J Clin Periodontol 2012; 39 (12) 1115-1124
    CrossrefPubMedSearch in Google Scholar
  • 2 Haffajee AD, Socransky SS. Microbiology of periodontal diseases: introduction. Periodontol 2000 2005; 38: 9-12
    CrossrefPubMedSearch in Google Scholar
  • 3 Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent Jr RL. Microbial complexes in subgingival plaque. J Clin Periodontol 1998; 25 (02) 134-144
    CrossrefPubMedSearch in Google Scholar
  • 4 Dye BA, Choudhary K, Shea S, Papapanou PN. Serum antibodies to periodontal pathogens and markers of systemic inflammation. J Clin Periodontol 2005; 32 (12) 1189-1199
    CrossrefPubMedSearch in Google Scholar
  • 5 Lockhart PB, Bolger AF, Papapanou PN. , et al; American Heart Association Rheumatic Fever, Endocarditis, and Kawasaki Disease Committee of the Council on Cardiovascular Disease in the Young, Council on Epidemiology and Prevention, Council on Peripheral Vascular Disease, and Council on Clinical Cardiology. Periodontal disease and atherosclerotic vascular disease: does the evidence support an independent association? A scientific statement from the American Heart Association. Circulation 2012; 125 (20) 2520-2544
    CrossrefPubMedSearch in Google Scholar
  • 6 Blaizot A, Vergnes JN, Nuwwareh S, Amar J, Sixou M. Periodontal diseases and cardiovascular events: meta-analysis of observational studies. Int Dent J 2009; 59 (04) 197-209
    PubMedSearch in Google Scholar
  • 7 Desvarieux M, Demmer RT, Rundek T. , et al. Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Circulation 2005; 111 (05) 576-582
    CrossrefPubMedSearch in Google Scholar
  • 8 Aimetti M, Romano F, Nessi F. Microbiologic analysis of periodontal pockets and carotid atheromatous plaques in advanced chronic periodontitis patients. J Periodontol 2007; 78 (09) 1718-1723
    CrossrefPubMedSearch in Google Scholar
  • 9 Bratel J, Kennergren C, Dernevik L, Hakeberg M. Treatment of oral infections prior to heart valve surgery does not improve long-term survival. Swed Dent J 2011; 35 (02) 49-55
    PubMedSearch in Google Scholar
  • 10 Nishimura RA, Otto CM, Bonow RO. , et al; ACC/AHA Task Force Members. 2014 AHA/ACC guideline for the management of patients with valvular heart disease: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 2014; 129 (23) 2440-2492
    CrossrefPubMedSearch in Google Scholar
  • 11 Nakamura Y, Tagusari O, Seike Y. , et al. Prevalence of periodontitis and optimal timing of dental treatment in patients undergoing heart valve surgery. Interact Cardiovasc Thorac Surg 2011; 12 (05) 696-700
    CrossrefPubMedSearch in Google Scholar
  • 12 Smith MM, Barbara DW, Mauermann WJ, Viozzi CF, Dearani JA, Grim KJ. Morbidity and mortality associated with dental extraction before cardiac operation. Ann Thorac Surg 2014; 97 (03) 838-844
    CrossrefPubMedSearch in Google Scholar
  • 13 Wilson W, Taubert KA, Gewitz M. , et al; American Heart Association Rheumatic Fever, Endocarditis, and Kawasaki Disease Committee; American Heart Association Council on Cardiovascular Disease in the Young; American Heart Association Council on Clinical Cardiology; American Heart Association Council on Cardiovascular Surgery and Anesthesia; Quality of Care and Outcomes Research Interdisciplinary Working Group. Prevention of infective endocarditis: guidelines from the American Heart Association: a guideline from the American Heart Association Rheumatic Fever, Endocarditis, and Kawasaki Disease Committee, Council on Cardiovascular Disease in the Young, and the Council on Clinical Cardiology, Council on Cardiovascular Surgery and Anesthesia, and the Quality of Care and Outcomes Research Interdisciplinary Working Group. Circulation 2007; 116 (15) 1736-1754
    CrossrefPubMedSearch in Google Scholar
  • 14 Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol 2007; 78 (7, Suppl): 1387-1399
    CrossrefPubMedSearch in Google Scholar
  • 15 Nakano K, Nemoto H, Nomura R. , et al. Detection of oral bacteria in cardiovascular specimens. Oral Microbiol Immunol 2009; 24 (01) 64-68
    CrossrefPubMedSearch in Google Scholar
  • 16 Chiang CY, Fu E, Shen EC, Chiu HC. Effects of CD14 receptors on tissue reactions induced by local injection of two gram-negative bacterial lipopolysaccharides. J Periodontal Res 2003; 38 (01) 36-43
    CrossrefPubMedSearch in Google Scholar
  • 17 Parolari A, Loardi C, Mussoni L. , et al. Nonrheumatic calcific aortic stenosis: an overview from basic science to pharmacological prevention. Eur J Cardiothorac Surg 2009; 35 (03) 493-504
    CrossrefPubMedSearch in Google Scholar
  • 18 Baumgarten G, Knuefermann P, Kalra D. , et al. Load-dependent and -independent regulation of proinflammatory cytokine and cytokine receptor gene expression in the adult mammalian heart. Circulation 2002; 105 (18) 2192-2197
    CrossrefPubMedSearch in Google Scholar
  • 19 Nemoto S, Vallejo JG, Knuefermann P. , et al. Escherichia coli LPS-induced LV dysfunction: role of toll-like receptor-4 in the adult heart. Am J Physiol Heart Circ Physiol 2002; 282 (06) H2316-H2323
    CrossrefPubMedSearch in Google Scholar
  • 20 Niederbichler AD, Hoesel LM, Ipaktchi K. , et al. Burn-induced heart failure: lipopolysaccharide binding protein improves burn and endotoxin-induced cardiac contractility deficits. J Surg Res 2011; 165 (01) 128-135
    CrossrefPubMedSearch in Google Scholar
  • 21 Comstock KL, Krown KA, Page MT. , et al. LPS-induced TNF-alpha release from and apoptosis in rat cardiomyocytes: obligatory role for CD14 in mediating the LPS response. J Mol Cell Cardiol 1998; 30 (12) 2761-2775
    CrossrefPubMedSearch in Google Scholar
  • 22 Knuefermann P, Nemoto S, Misra A. , et al. CD14-deficient mice are protected against lipopolysaccharide-induced cardiac inflammation and left ventricular dysfunction. Circulation 2002; 106 (20) 2608-2615
    CrossrefPubMedSearch in Google Scholar
  • 23 Cowan DB, Poutias DN, Del Nido PJ, McGowan Jr FX. CD14-independent activation of cardiomyocyte signal transduction by bacterial endotoxin. Am J Physiol Heart Circ Physiol 2000; 279 (02) H619-H629
    CrossrefPubMedSearch in Google Scholar
  • 24 Conraads VM, Bosmans JM, Schuerwegh AJ. , et al. Intracellular monocyte cytokine production and CD 14 expression are up-regulated in severe vs mild chronic heart failure. J Heart Lung Transplant 2005; 24 (07) 854-859
    CrossrefPubMedSearch in Google Scholar
  • 25 Devaux B, Scholz D, Hirche A, Klövekorn WP, Schaper J. Upregulation of cell adhesion molecules and the presence of low grade inflammation in human chronic heart failure. Eur Heart J 1997; 18 (03) 470-479
    CrossrefPubMedSearch in Google Scholar
  • 26 Wijesurendra RS, Casadei B. Atrial fibrillation: effects beyond the atrium?. Cardiovasc Res 2015; 105 (03) 238-247
    CrossrefPubMedSearch in Google Scholar
  • 27 Guo Y, Lip GY, Apostolakis S. Inflammation in atrial fibrillation. J Am Coll Cardiol 2012; 60 (22) 2263-2270
    CrossrefPubMedSearch in Google Scholar