Int J Angiol 2016; 25(01): 003-013
DOI: 10.1055/s-0035-1547385
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Association between Bacterial Infection and Peripheral Vascular Disease: A Review

Jacek Budzyński
1   Chair of Vascular and Internal Diseases, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Toruń, Poland
2   Department of Vascular and Internal Diseases, Jan Biziel Hospital No. 2, Bydgoszcz, Poland
,
Joanna Wiśniewska
2   Department of Vascular and Internal Diseases, Jan Biziel Hospital No. 2, Bydgoszcz, Poland
,
Marek Ciecierski
2   Department of Vascular and Internal Diseases, Jan Biziel Hospital No. 2, Bydgoszcz, Poland
,
Anna Kędzia
3   Department of Oral Microbiology, Chair of Microbiology, Medical University, Gdańsk, Poland
› Author Affiliations
Further Information

Publication History

Publication Date:
23 March 2015 (online)

Abstract

There are an increasing number of data showing a clinically important association between bacterial infection and peripheral artery disease (PAD). Bacteria suspected of being involved in PAD pathogenesis are: periodontal bacteria, gut microbiota, Helicobacter pylori, and Chlamydia pneumoniae. Infectious agents may be involved in the pathogenesis of atherosclerosis via activation of a systemic or local host immunological response to contamination of extravascular tissues or the vascular wall, respectively. A systemic immunological reaction may damage vascular walls in the course of autoimmunological cross-reactions between anti-pathogen antibodies and host vascular antigens (immunological mimicry), pathogen burden mechanisms (nonspecific activation of inflammatory processes in the vascular wall), and neuroendocrine-immune cross-talk. Besides activating the inflammatory pathway, bacterial infection may trigger PAD progression or exacerbation by enhancement of platelet reactivity, by a stimulatory effect on von Willebrand factor binding, factor VIII, fibrinogen, P-selectin activation, disturbances in plasma lipids, increase in oxidative stress, and resistance to insulin. Local inflammatory host reaction and induction of atherosclerotic plaque progression and/or instability result mainly from atherosclerotic plaque colonization by microorganisms. Despite these premises, the role of bacterial infection in PAD pathogenesis should still be recognized as controversial, and randomized, controlled trials are required to evaluate the outcome of periodontal or gut bacteria modification (through diet, prebiotics, and probiotics) or eradication (using antibiotics) in hard and surrogate cardiovascular endpoints.

 
  • References

  • 1 Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol 2012; 32 (9) 2045-2051
  • 2 Krintus M, Kozinski M, Stefanska A , et al. Value of C-reactive protein as a risk factor for acute coronary syndrome: a comparison with apolipoprotein concentrations and lipid profile. Mediators Inflamm 2012; 2012: 419804
  • 3 Koziński M, Krzewina-Kowalska A, Kubica J , et al. Percutaneous coronary intervention triggers a systemic inflammatory response in patients treated for in-stent restenosis — comparison with stable and unstable angina. Inflamm Res 2005; 54 (5) 187-193
  • 4 Kubica J, Koziński M, Krzewina-Kowalska A , et al. Combined periprocedural evaluation of CRP and TNF-alpha enhances the prediction of clinical restenosis and major adverse cardiac events in patients undergoing percutaneous coronary interventions. Int J Mol Med 2005; 16 (1) 173-180
  • 5 Budzyński J, Koziński M, Kłopocka M, Kubica JM, Kubica J. Clinical significance of Helicobacter pylori infection in patients with acute coronary syndromes: an overview of current evidence. Clin Res Cardiol 2014; 103 (11) 855-886
  • 6 Determann C, Hill AT, Monaghan H, Fraser SC. Atypical mycobacteria in a superficial femoral artery occlusion. BMJ Case Rep 2011; 2011 DOI: doi: 10.1136/bcr.02.2011..
  • 7 Sessa R, Pietro MD, Filardo S, Turriziani O. Infectious burden and atherosclerosis: a clinical issue. World J Clin Cases 2014; 2 (7) 240-249
  • 8 Chen BF, Xu X, Deng Y , et al. Relationship between Helicobacter pylori infection and serum interleukin-18 in patients with carotid atherosclerosis. Helicobacter 2013; 18 (2) 124-128
  • 9 Chen J, Zhu M, Ma G, Zhao Z, Sun Z. Chlamydia pneumoniae infection and cerebrovascular disease: a systematic review and meta-analysis. BMC Neurol 2013; 13: 183
  • 10 Chen YW, Umeda M, Nagasawa T , et al. Periodontitis may increase the risk of peripheral arterial disease. Eur J Vasc Endovasc Surg 2008; 35 (2) 153-158
  • 11 Krueger KD, Mitra AK, DelCore MG, Hunter III WJ, Agrawal DK. A comparison of stent-induced stenosis in coronary and peripheral arteries. J Clin Pathol 2006; 59 (6) 575-579
  • 12 Dietrich T, Sharma P, Walter C, Weston P, Beck J. The epidemiological evidence behind the association between periodontitis and incident atherosclerotic cardiovascular disease. J Periodontol 2013; 84 (4, Suppl): S70-S84
  • 13 Miao CY, Li ZY. The role of perivascular adipose tissue in vascular smooth muscle cell growth. Br J Pharmacol 2012; 165 (3) 643-658
  • 14 Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB. The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 2012; 95 (2) 194-204
  • 15 Zhang J, Wang H, Zhang L , et al. Chlamydia pneumoniae infection induces vascular smooth muscle cell migration via Rac1 activation. J Med Microbiol 2014; 63 (Pt 2) 155-161
  • 16 Chatterjee TK, Aronow BJ, Tong WS , et al. Human coronary artery perivascular adipocytes overexpress genes responsible for regulating vascular morphology, inflammation, and hemostasis. Physiol Genomics 2013; 45 (16) 697-709
  • 17 Tano JY, Schleifenbaum J, Gollasch M. Perivascular adipose tissue, potassium channels, and vascular dysfunction. Arterioscler Thromb Vasc Biol 2014; 34 (9) 1827-1830
  • 18 Ahmed U, Tanwir F. Association of periodontal pathogenesis and cardiovascular diseases: a literature review. Oral Health Prev Dent 2015; 13 (1) 21-27
  • 19 Tapashetti RP, Guvva S, Patil SR, Sharma S, Pushpalatha HM. C-reactive protein as predict of increased carotid intima media thickness in patients with chronic periodontitis. J Int Oral Health 2014; 6 (4) 47-52
  • 20 Caúla AL, Lira-Junior R, Tinoco EM, Fischer RG. The effect of periodontal therapy on cardiovascular risk markers: a 6-month randomized clinical trial. J Clin Periodontol 2014; 41 (9) 875-882
  • 21 Tanigawa T, Watanabe T, Nadatani Y , et al. Gastrointestinal bleeding after percutaneous coronary intervention. Digestion 2011; 83 (3) 153-160
  • 22 Bhatt DL, Scheiman J, Abraham NS , et al; American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents. ACCF/ACG/AHA 2008 expert consensus document on reducing the gastrointestinal risks of antiplatelet therapy and NSAID use: a report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents. J Am Coll Cardiol 2008; 52 (18) 1502-1517
  • 23 Abraham NS, Hlatky MA, Antman EM , et al; ACCF/ACG/AHA. ACCF/ACG/AHA 2010 expert consensus document on the concomitant use of proton pump inhibitors and thienopyridines: a focused update of the ACCF/ACG/AHA 2008 expert consensus document on reducing the gastrointestinal risks of antiplatelet therapy and NSAID use. A Report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol 2010; 56 (24) 2051-2066
  • 24 Gisbert JP, Khorrami S, Carballo F, Calvet X, Gene E, Dominguez-Muñoz E. Meta-analysis: Helicobacter pylori eradication therapy vs. antisecretory non-eradication therapy for the prevention of recurrent bleeding from peptic ulcer. Aliment Pharmacol Ther 2004; 19 (6) 617-629
  • 25 Holtfreter B, Empen K, Gläser S , et al. Periodontitis is associated with endothelial dysfunction in a general population: a cross-sectional study. PLoS ONE 2013; 8 (12) e84603
  • 26 Suzuki J, Aoyama N, Aoki M , et al. High incidence of periodontitis in Japanese patients with abdominal aortic aneurysm. Int Heart J 2014; 55 (3) 268-270
  • 27 Orlandi M, Suvan J, Petrie A , et al. Association between periodontal disease and its treatment, flow-mediated dilatation and carotid intima-media thickness: a systematic review and meta-analysis. Atherosclerosis 2014; 236 (1) 39-46
  • 28 Desvarieux M, Demmer RT, Jacobs DR, Papapanou PN, Sacco RL, Rundek T. Changes in clinical and microbiological periodontal profiles relate to progression of carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology study. J Am Heart Assoc 2013; 2 (6) e000254
  • 29 Jung YS, Shin MH, Kim IS , et al. Relationship between periodontal disease and subclinical atherosclerosis: the Dong-gu study. J Clin Periodontol 2014; 41 (3) 262-268
  • 30 Uyar IS, Akpinar MB, Sahin V , et al. Carotid and popliteal artery intima-media thickness in patients with poor oral hygiene and the association with acute-phase reactants. Cardiovasc J Afr 2013; 24 (8) 308-312
  • 31 Hayashida H, Saito T, Kawasaki K , et al. Association of periodontitis with carotid artery intima-media thickness and arterial stiffness in community-dwelling people in Japan: the Nagasaki Islands study. Atherosclerosis 2013; 229 (1) 186-191
  • 32 Yusuf S, Hawken S, Ounpuu S , et al; INTERHEART Study Investigators. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004; 364 (9438) 937-952
  • 33 Tonetti MS, Van Dyke TE. working group 1 of the joint EFP/AAP workshop. Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol 2013; 84 (4, Suppl): S24-S29
  • 34 Mete R, Oran M, Alpsoy S , et al. Carotid intima-media thickness and serum paraoxonase-1 activity in patients with Helicobacter pylori. Eur Rev Med Pharmacol Sci 2013; 17 (21) 2884-2889
  • 35 Gabrielli M, Santoliquido A, Cremonini F , et al. CagA-positive cytotoxic H. pylori strains as a link between plaque instability and atherosclerotic stroke. Eur Heart J 2004; 25 (1) 64-68
  • 36 Mayr M, Kiechl S, Mendall MA, Willeit J, Wick G, Xu Q. Increased risk of atherosclerosis is confined to CagA-positive Helicobacter pylori strains: prospective results from the Bruneck study. Stroke 2003; 34 (3) 610-615
  • 37 Diomedi M, Pietroiusti A, Silvestrini M , et al. CagA-positive Helicobacter pylori strains may influence the natural history of atherosclerotic stroke. Neurology 2004; 63 (5) 800-804
  • 38 Markus HS, Risley P, Mendall MA, Steinmetz H, Sitzer M. Helicobacter pylori infection, the cytotoxin gene A strain, and carotid artery intima-media thickness. J Cardiovasc Risk 2002; 9 (1) 1-6
  • 39 Izzotti A, Durando P, Ansaldi F, Gianiorio F, Pulliero A. Interaction between Helicobacter pylori, diet, and genetic polymorphisms as related to non-cancer diseases. Mutat Res 2009; 667 (1-2) 142-157
  • 40 Franceschi F, Niccoli G, Ferrante G , et al. CagA antigen of Helicobacter pylori and coronary instability: insight from a clinico-pathological study and a meta-analysis of 4241 cases. Atherosclerosis 2009; 202 (2) 535-542
  • 41 Lenzi C, Palazzuoli A, Giordano N , et al. H pylori infection and systemic antibodies to CagA and heat shock protein 60 in patients with coronary heart disease. World J Gastroenterol 2006; 12 (48) 7815-7820
  • 42 Rožanković PB, Huzjan AL, Cupić H, Benčić IJ, Bašić S, Demarin V. Influence of CagA-positive Helicobacter pylori strains on atherosclerotic carotid disease. J Neurol 2011; 258 (5) 753-761
  • 43 Kowalski M. Helicobacter pylori (H. pylori) infection in coronary artery disease: influence of H. pylori eradication on coronary artery lumen after percutaneous transluminal coronary angioplasty. The detection of H. pylori specific DNA in human coronary atherosclerotic plaque. J Physiol Pharmacol 2001; 52 (1) (Suppl. 01) 3-31
  • 44 Kowalski M, Konturek PC, Pieniążek P , et al. Prevalence of Helicobacter pylori infection in coronary artery disease and effect of its eradication on coronary lumen reduction after percutaneous coronary angioplasty. Dig Liver Dis 2001; 33 (3) 222-229
  • 45 Skowasch D, Jabs A, Andrié R , et al. Pathogen burden, inflammation, proliferation and apoptosis in human in-stent restenosis. Tissue characteristics compared to primary atherosclerosis. J Vasc Res 2004; 41 (6) 525-534
  • 46 Shanker J, Kakkar VV. Role of periodontal infection in cardiovascular disease: a current perspective. Arch Med Sci 2009; 5 (2) 125-134
  • 47 Ramdeen N, Aronow WS, Chugh S, Asija A. Patients undergoing coronary angiography because of chest pain with hepatitis C virus seropositivity have a higher prevalence of obstructive coronary artery disease than a control group. Arch Med Sci 2008; 4 (4) 452-454
  • 48 Chang L, Milton H, Eitzman DT, Chen YE. Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension. Circ J 2013; 77 (1) 11-18
  • 49 Azarkar Z, Jafarnejad M, Sharifzadeh G. The relationship between helicobacter pylori infection and myocardial infarction. Caspian J Intern Med 2011; 2 (2) 222-225
  • 50 Zhu J, Quyyumi AA, Norman JE , et al. Effects of total pathogen burden on coronary artery disease risk and C-reactive protein levels. Am J Cardiol 2000; 85 (2) 140-146
  • 51 Espinola-Klein C, Rupprecht HJ, Blankenberg S , et al. Impact of infectious burden on progression of carotid atherosclerosis. Stroke 2002; 33 (11) 2581-2586
  • 52 Elkind MS, Luna JM, Moon YP , et al. Infectious burden and carotid plaque thickness: the northern Manhattan study. Stroke 2010; 41 (3) e117-e122
  • 53 Corrado E, Rizzo M, Tantillo R , et al. Markers of inflammation and infection influence the outcome of patients with baseline asymptomatic carotid lesions: a 5-year follow-up study. Stroke 2006; 37 (2) 482-486
  • 54 Danesh J. Coronary heart disease, Helicobacter pylori, dental disease, Chlamydia pneumoniae, and cytomegalovirus: meta-analyses of prospective studies. Am Heart J 1999; 138 (5 Pt 2) S434-S437
  • 55 Danesh J, Peto R. Risk factors for coronary heart disease and infection with Helicobacter pylori: meta-analysis of 18 studies. BMJ 1998; 316 (7138) 1130-1132
  • 56 Celik T, Iyisoy A, Yuksel UC. Possible pathogenetic role of Helicobacter pylori infection in cardiac syndrome X. Int J Cardiol 2010; 142 (2) 193-194
  • 57 Budzyński J, Kłopocka M. Brain-gut axis in the pathogenesis of Helicobacter pylori infection. World J Gastroenterol 2014; 20 (18) 5212-5225
  • 58 Budzyński J, Kłopocka M, Bujak R, Świątkowski M, Pulkowski G, Sinkiewicz W. Autonomic nervous function in Helicobacter pylori-infected patients with atypical chest pain studied by analysis of heart rate variability. Eur J Gastroenterol Hepatol 2004; 16 (5) 451-457
  • 59 Grundy D, Al-Chaer ED, Aziz Q , et al. Fundamentals of neurogastroenterology: basic science. Gastroenterology 2006; 130 (5) 1391-1411
  • 60 Marques AH, Silverman MN, Sternberg EM. Evaluation of stress systems by applying noninvasive methodologies: measurements of neuroimmune biomarkers in the sweat, heart rate variability and salivary cortisol. Neuroimmunomodulation 2010; 17 (3) 205-208
  • 61 Wood JD. Neuropathophysiology of functional gastrointestinal disorders. World J Gastroenterol 2007; 13 (9) 1313-1332
  • 62 Ardila CM, Olarte-Sossa M, Ariza-Garcés AA. Association between the presence of Treponema denticola and reduced levels of antiatherogenic high density lipoprotein in periodontitis. Quintessence Int 2015; 46 (3) 207-215
  • 63 Kurita-Ochiai T, Yamamoto M. Periodontal pathogens and atherosclerosis: implications of inflammation and oxidative modification of LDL. Biomed Res Int 2014; 2014: 595981
  • 64 Huang B, Chen Y, Xie Q , et al. CagA-positive Helicobacter pylori strains enhanced coronary atherosclerosis by increasing serum OxLDL and HsCRP in patients with coronary heart disease. Dig Dis Sci 2011; 56 (1) 109-114
  • 65 Başyığıt S, Akbaş H, Süleymanlar İ, Kemaloğlu D, Koç S, Süleymanlar G. The assessment of carotid intima-media thickness, lipid profiles and oxidative stress markers in Helicobacter pylori-positive subjects. Turk J Gastroenterol 2012; 23 (6) 646-651
  • 66 Iwao Y, Takano T, Taneike I , et al. Anti-Helicobacter pylori actions of CV-6209, a platelet-activating factor receptor antagonist. J Gen Appl Microbiol 2013; 59 (2) 147-152
  • 67 Satoh K, Hirayama T, Takano K , et al. VacA, the vacuolating cytotoxin of Helicobacter pylori, binds to multimerin 1 on human platelets. Thromb J 2013; 11 (1) 23
  • 68 Kanbay M, Gür G, Yücel M, Yilmaz U, Boyacioğlu S. Does eradication of Helicobacter pylori infection help normalize serum lipid and CRP levels?. Dig Dis Sci 2005; 50 (7) 1228-1231
  • 69 Pellicano R. Lipid profile and Helicobacter Pylori infection. J Atheroscler Thromb 2010; 17 (11) 1199-1200
  • 70 Pellicano R, Mazzarello MG, Morelloni S , et al. Acute myocardial infarction and Helicobacter pylori seropositivity. Int J Clin Lab Res 1999; 29 (4) 141-144
  • 71 Pellicano R, Oliaro E, Fagoonee S , et al. Clinical and biochemical parameters related to cardiovascular disease after Helicobacter pylori eradication. Int Angiol 2009; 28 (6) 469-473
  • 72 Elizalde JI, Piqué JM, Moreno V , et al; Group of Study on Oesophageal and Gastric Diseases from The Spainish Gastroenterological Association. Influence of Helicobacter pylori infection and eradication on blood lipids and fibrinogen. Aliment Pharmacol Ther 2002; 16 (3) 577-586
  • 73 Deng L, Li C, Li Q, Zhang Y, Zhao H. Periodontal treatment for cardiovascular risk factors: a systematic review [in Chinese]. Hua Xi Kou Qiang Yi Xue Za Zhi 2013; 31 (5) 463-467
  • 74 Malfertheiner P, Megraud F, O'Morain CA , et al; European Helicobacter Study Group. Management of Helicobacter pylori infection—the Maastricht IV/ Florence Consensus Report. Gut 2012; 61 (5) 646-664
  • 75 Marietti M, Gasbarrini A, Saracco G, Pellicano R. Helicobacter pylori infection and diabetes mellitus: the 2013 state of art. Panminerva Med 2013; 55 (3) 277-281
  • 76 Whincup PH, Mendall MA, Perry IJ, Strachan DP, Walker M. Prospective relations between Helicobacter pylori infection, coronary heart disease, and stroke in middle aged men. Heart 1996; 75 (6) 568-572
  • 77 Whincup P, Danesh J, Walker M , et al. Prospective study of potentially virulent strains of Helicobacter pylori and coronary heart disease in middle-aged men. Circulation 2000; 101 (14) 1647-1652
  • 78 Gentile S, Turco S, Oliviero B, Torella R. The role of autonomic neuropathy as a risk factor of Helicobacter pylori infection in dyspeptic patients with type 2 diabetes mellitus. Diabetes Res Clin Pract 1998; 42 (1) 41-48
  • 79 Zhou X, Zhang C, Wu J, Zhang G. Association between Helicobacter pylori infection and diabetes mellitus: a meta-analysis of observational studies. Diabetes Res Clin Pract 2013; 99 (2) 200-208
  • 80 Ozaydin N, Turkyilmaz SA, Cali S. Prevalence and risk factors of Helicobacter pylori in Turkey: a nationally-representative, cross-sectional, screening with the 13C-Urea breath test. BMC Public Health 2013; 13: 1215
  • 81 Wang F, Liu J, Lv Z. Association of Helicobacter pylori infection with diabetes mellitus and diabetic nephropathy: a meta-analysis of 39 studies involving more than 20,000 participants. Scand J Infect Dis 2013; 45 (12) 930-938
  • 82 Strachan DP, Mendall MA, Carrington D , et al. Relation of Helicobacter pylori infection to 13-year mortality and incident ischemic heart disease in the caerphilly prospective heart disease study. Circulation 1998; 98 (13) 1286-1290
  • 83 Wang JY, Wang CY, Juang SY , et al. Low socioeconomic status increases short-term mortality of acute myocardial infarction despite universal health coverage. Int J Cardiol 2014; 172 (1) 82-87
  • 84 Jafri W, Yakoob J, Abid S , et al. Seroprevalence of hepatitis E and Helicobacter pylori in a low socioeconomic area of a metropolitan city in a developing country. Br J Biomed Sci 2013; 70 (1) 27-30
  • 85 Valliani A, Khan F, Chagani B , et al. Factors associated with Helicobacter pylori infection, results from a developing country - Pakistan. Asian Pac J Cancer Prev 2013; 14 (1) 53-56
  • 86 Murray LJ, Bamford KB, O'Reilly DP, McCrum EE, Evans AE. Helicobacter pylori infection: relation with cardiovascular risk factors, ischaemic heart disease, and social class. Br Heart J 1995; 74 (5) 497-501
  • 87 Eskandarian R, Ghorbani R, Shiyasi M, Momeni B, Hajifathalian K, Madani M. Prognostic role of Helicobacter pylori infection in acute coronary syndrome: a prospective cohort study. Cardiovasc J Afr 2012; 23 (3) 131-135
  • 88 Rogha M, Dadkhah D, Pourmoghaddas Z, Shirneshan K, Nikvarz M, Pourmoghaddas M. Association of helicobacter pylori infection with severity of coronary heart disease. ARYA Atheroscler 2012; 7 (4) 138-141
  • 89 Rogha M, Nikvarz M, Pourmoghaddas Z, Shirneshan K, Dadkhah D, Pourmoghaddas M. Is helicobacter pylori infection a risk factor for coronary heart disease?. ARYA Atheroscler 2012; 8 (1) 5-8
  • 90 Sheehan J, Kearney PM, Sullivan SO, Mongan C, Kelly E, Perry IJ. Acute coronary syndrome and chronic infection in the Cork coronary care case-control study. Heart 2005; 91 (1) 19-22
  • 91 Kosaka T, Kokubo Y, Ono T , et al. Salivary inflammatory cytokines may be novel markers of carotid atherosclerosis in a Japanese general population: the Suita study. Atherosclerosis 2014; 237 (1) 123-128
  • 92 de Boer SP, Cheng JM, Rangé H , et al. Antibodies to periodontal pathogens are associated with coronary plaque remodeling but not with vulnerability or burden. Atherosclerosis 2014; 237 (1) 84-91
  • 93 Serino M, Blasco-Baque V, Nicolas S, Burcelin R. Far from the eyes, close to the heart: dysbiosis of gut microbiota and cardiovascular consequences. Curr Cardiol Rep 2014; 16 (11) 540
  • 94 Stock J. Gut microbiota: an environmental risk factor for cardiovascular disease. Atherosclerosis 2013; 229 (2) 440-442
  • 95 Koren O, Spor A, Felin J , et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 2011; 108 (Suppl. 01) 4592-4598
  • 96 Karlsson F, Tremaroli V, Nielsen J, Bäckhed F. Assessing the human gut microbiota in metabolic diseases. Diabetes 2013; 62 (10) 3341-3349
  • 97 Chen D, Yang Z, Chen X , et al. The effect of Lactobacillus rhamnosus hsryfm 1301 on the intestinal microbiota of a hyperlipidemic rat model. BMC Complement Altern Med 2014; 14: 386
  • 98 Gan XT, Ettinger G, Huang CX , et al. Probiotic administration attenuates myocardial hypertrophy and heart failure after myocardial infarction in the rat. Circ Heart Fail 2014; 7 (3) 491-499
  • 99 Tang WH, Hazen SL. The contributory role of gut microbiota in cardiovascular disease. J Clin Invest 2014; 124 (10) 4204-4211
  • 100 Wang Z, Klipfell E, Bennett BJ , et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011; 472 (7341) 57-63
  • 101 Lee-Rueckert M, Blanco-Vaca F, Kovanen PT, Escola-Gil JC. The role of the gut in reverse cholesterol transport—focus on the enterocyte. Prog Lipid Res 2013; 52 (3) 317-328
  • 102 Loscalzo J. Lipid metabolism by gut microbes and atherosclerosis. Circ Res 2011; 109 (2) 127-129
  • 103 Ussher JR, Lopaschuk GD, Arduini A. Gut microbiota metabolism of L-carnitine and cardiovascular risk. Atherosclerosis 2013; 231 (2) 456-461
  • 104 Koeth RA, Wang Z, Levison BS , et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013; 19 (5) 576-585
  • 105 Tuohy KM, Fava F, Viola R. ‘The way to a man's heart is through his gut microbiota’—dietary pro- and prebiotics for the management of cardiovascular risk. Proc Nutr Soc 2014; 73 (2) 172-185
  • 106 Karlsson FH, Fåk F, Nookaew I , et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun 2012; 3: 1245
  • 107 Karlsson C, Ahrné S, Molin G , et al. Probiotic therapy to men with incipient arteriosclerosis initiates increased bacterial diversity in colon: a randomized controlled trial. Atherosclerosis 2010; 208 (1) 228-233
  • 108 Lam V, Su J, Koprowski S , et al. Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J 2012; 26 (4) 1727-1735
  • 109 Rajkumar H, Mahmood N, Kumar M, Varikuti SR, Challa HR, Myakala SP. Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized, controlled trial. Mediators Inflamm 2014; 2014: 348959
  • 110 Le MQ, Narins CR. Mycotic pseudoaneurysm of the left circumflex coronary artery: a fatal complication following drug-eluting stent implantation. Catheter Cardiovasc Interv 2007; 69 (4) 508-512
  • 111 Yan Y, Silvennoinen-Kassinen S, Leinonen M, Saikku P. Rapamycin can inhibit the development of Chlamydia pneumoniae, which might partly contribute to the prevention of in-stent restenosis. Cardiovasc Drugs Ther 2010; 24 (3) 189-195
  • 112 Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J 1999; 138 (5 Pt 2) S534-S536
  • 113 Rath SK, Mukherjee M, Kaushik R, Sen S, Kumar M. Periodontal pathogens in atheromatous plaque. Indian J Pathol Microbiol 2014; 57 (2) 259-264
  • 114 Iriz E, Cirak MY, Engin ED , et al. Detection of Helicobacter pylori DNA in aortic and left internal mammary artery biopsies. Tex Heart Inst J 2008; 35 (2) 130-135
  • 115 Vcev A, Nakić D, Mrden A , et al. Helicobacter pylori infection and coronary artery disease. Coll Antropol 2007; 31 (3) 757-760
  • 116 Kilic A, Onguru O, Tugcu H, Kilic S, Guney C, Bilge Y. Detection of cytomegalovirus and Helicobacter pylori DNA in arterial walls with grade III atherosclerosis by PCR. Pol J Microbiol 2006; 55 (4) 333-337
  • 117 Vijayvergiya R, Agarwal N, Bahl A , et al. Association of Chlamydia pneumoniae and Helicobacter pylori infection with angiographically demonstrated coronary artery disease. Int J Cardiol 2006; 107 (3) 428-429
  • 118 Kaplan M, Yavuz SS, Cinar B , et al. Detection of Chlamydia pneumoniae and Helicobacter pylori in atherosclerotic plaques of carotid artery by polymerase chain reaction. Int J Infect Dis 2006; 10 (2) 116-123
  • 119 Adiloglu AK, Ocal A, Can R, Duver H, Yavuz T, Aridogan BC. Detection of Helicobacter pylori and Chlamydia pneumoniae DNA in human coronary arteries and evaluation of the results with serologic evidence of inflammation. Saudi Med J 2005; 26 (7) 1068-1074
  • 120 Kinjo K, Sato H, Sato H , et al; Osaka Acute Coronary Insufficiency Study (OACIS) Group. Prevalence of Helicobacter pylori infection and its link to coronary risk factors in Japanese patients with acute myocardial infarction. Circ J 2002; 66 (9) 805-810
  • 121 Serra e Silva Filho W, Casarin RC, Nicolela Jr EL, Passos HM, Sallum AW, Gonçalves RB. Microbial diversity similarities in periodontal pockets and atheromatous plaques of cardiovascular disease patients. PLoS ONE 2014; 9 (10) e109761
  • 122 Figuero E, Lindahl C, Marín MJ , et al. Quantification of periodontal pathogens in vascular, blood, and subgingival samples from patients with peripheral arterial disease or abdominal aortic aneurysms. J Periodontol 2014; 85 (9) 1182-1193
  • 123 Kędzia A, Ciecierski M, Kufel A, Wierzbowska M, Kwapisz E. Izolacja bakterii beztlenowych z blaszek miażdżycowych występujących w tętnicach szyjnych. (Isolation of anaerobic bacteria from atherosclerotic plaques from carotid arteries.). Acta Angiol 2012; 18 (2) 59-67
  • 124 Rangé H, Labreuche J, Louedec L , et al. Periodontal bacteria in human carotid atherothrombosis as a potential trigger for neutrophil activation. Atherosclerosis 2014; 236 (2) 448-455
  • 125 Hokamura K, Umemura K. Roles of oral bacteria in cardiovascular diseases—from molecular mechanisms to clinical cases: Porphyromonas gingivalis is the important role of intimal hyperplasia in the aorta. J Pharmacol Sci 2010; 113 (2) 110-114
  • 126 Waghmare AS, Vhanmane PB, Savitha B, Chawla RL, Bagde HS. Bacteremia following scaling and root planing: a clinico-microbiological study. J Indian Soc Periodontol 2013; 17 (6) 725-730
  • 127 Ahmadnia H, Vossoughinia H, Mansourian E, Gaffarzadegan K. No detection of Helicobacter pylori in atherosclerotic plaques in end stage renal disease patients undergoing kidney transplantation. Indian J Nephrol 2013; 23 (4) 259-263
  • 128 Kędzia A, Ciecierski M, Wierzbowska M, Kufel A, Kwapisz E. Izolacja pałeczki Helicobacter pylori z blaszki miażdżycowej występującej w tętnicy udowej lub biodrowej. Acta Angiol 2010; 16 (3) 129-134
  • 129 Ameriso SF, Fridman EA, Leiguarda RC, Sevlever GE. Detection of Helicobacter pylori in human carotid atherosclerotic plaques. Stroke 2001; 32 (2) 385-391
  • 130 Rinaldi M, Perricone C, Ortega-Hernandez OD, Perricone R, Shoenfeld Y. Immune thrombocytopaenic purpura: an autoimmune cross-link between infections and vaccines. Lupus 2014; 23 (6) 554-567
  • 131 Gilden D, Nagel MA, Mahalingam R , et al. Clinical and molecular aspects of varicella zoster virus infection. Future Neurol 2009; 4 (1) 103-117
  • 132 Konin C, Anzouan-Kacou JB, Essam N'loo A. Arterial thrombosis in patients with human immunodeficiency virus: two-case reports and review of the literature. Case Rep Vasc Med 2011; 2011: 847241
  • 133 Goel SA, Guo LW, Liu B, Kent KC. Mechanisms of post-intervention arterial remodelling. Cardiovasc Res 2012; 96 (3) 363-371
  • 134 Schiele F, Batur MK, Seronde MF , et al. Cytomegalovirus, Chlamydia pneumoniae, and Helicobacter pylori IgG antibodies and restenosis after stent implantation: an angiographic and intravascular ultrasound study. Heart 2001; 85 (3) 304-311
  • 135 Han YW, Houcken W, Loos BG, Schenkein HA, Tezal M. Periodontal disease, atherosclerosis, adverse pregnancy outcomes, and head-and-neck cancer. Adv Dent Res 2014; 26 (1) 47-55
  • 136 Riffat F, Forer M, Wignall A, Veivers D, Patel N. Intracranial and internal jugular vein thrombosis secondary to ENT infections: a report of 3 cases. Ear Nose Throat J 2013; 92 (10-11) E25