Skip to main content

Advertisement

SpringerLink
Log in

Markers of Chlamydia pneumoniae and human cytomegalovirus infection in patients with chronic peripheral vascular disease and their relation to inflammation, endothelial dysfunction and changes in lipid metabolism

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Our aim was to detect markers of Chlamydia pneumoniae (CPN) and human cytomegalovirus (HCMV) infection in patients with peripheral vascular occlusive disease and to follow markers of inflammation, endothelial dysfunction and lipid metabolism alteration in patients with active infection. CPN genome was detected in 9 (47.4 %) patients by at least one PCR method. Serological markers of acute CPN infection were found in 5 (26.3 %) subjects; each of them showed also positivity in at least one of the PCR methods. HCMV DNA were detected in 2 (10.5 %) patients; HCMV-specific antibodies were detected in 14 (73.7 %) subjects, however only in IgG subclass. Subjects with HCMV PCR positivity thus showed no serological markers of active HCMV infection. Laboratory findings of acute CPN infection were associated with increased plasma levels of Lp(a), triacylglycerols, atherogenic index of plasma and E-selectin (p < 0.05). No significant differences were found in the other markers, including plasma levels of total cholesterol, ferritin, homocysteine, oxidized LDL, IL-6, IL-8, IL-18, TNF-α, soluble forms of VCAM-1 and ICAM-1, von Willebrand factor, C-reactive protein, and plasma nitrites & nitrates. Frequent presence of chlamydial DNA in atheromatous plaques from patients with peripheral vascular disease was confirmed. HCMV DNA was detected only sporadically and with positivity in anamnestic anti-HCMV antibodies (IgG) only, indicating a rare presence of latent virus rather than active replication. Patients with laboratory markers of acute CPN infection exhibited more pronounced alterations in lipid metabolism and endothelial dysfunction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ABI:

ankle-brachial index

AIP:

atherogenic index of plasma

ALT:

alanine aminotransferase

AST:

aspartate aminotransferase

CHS:

cholesterol

CPN:

Chlamydia pneumoniae

DSA:

digital subtraction angiography

HCMV:

human cytomegalovirus

HDL:

high density lipoprotein

HOMA-IR:

homeostatic model assessment

hsCRP:

high sensitivity C-reactive protein

ICAM:

intercellular adhesion molecule

IL:

interleukin

LDL:

low density lipoprotein

LPS:

lipopolysaccharide

MIF:

microimmunofluorescence

MOMP:

major outer membrane protein

PCR:

polymerase chain reaction

TGs:

triacylglycerols

TNF-α:

tumor necrosis factor α

VCAM:

vascular cell adhesion molecule-1

vWf:

von Willebrand factor

References

  • Apfalter P., Blasi F., Boman J., Gaydos C.A., Kundi M., Maass M., Makristathis A., Meijer A., Nadrchal R., Persson K., Rotter M.L., Tong C.Y.W., Stanek G., Hirschl A.M.: Multicenter comparison trial of DNA extraction methods and PCR assays for detection of Chlamydia pneumoniae in endarterectomy specimens. J.Clin.Microbiol. 39, 519–524 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Apfalter P., Assidian O., Blasi F., Boman J., Gaydosh C., Kundi M., Makristathis A., Nehr M., Rotter M.L., Hirschl A.M.: Reliability of nested PCR for detection of Chlamydia pneumoniae in atheromas: results from multicenter study applying standardized protocols. J.Clin.Microbiol. 40, 4428–4434 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Bastard J.P., Maachi M., Lagathu C., Kim M.J., Caron M., Vidal H., Capeau J., Feve B.: Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur.Cytokine Netw. 17, 4–12 (2006).

    PubMed  CAS  Google Scholar 

  • Bulvas M., Urbanová R., Klezlová R., Vítková I.: Markedly eccentric peripheral vascular stenoses: percutaneous atherectomy with an endomyocardial biopsy device. Radiology 217, 587–592 (2000).

    PubMed  CAS  Google Scholar 

  • Campbell L.A., O’Brien E.R., Cappuccio A.L., Kuo C.C., Wang S.P., Stewart D., Patton D.L., Cummings P.K., Grayston J.T.: Detection of Chlamydia pneumoniae (TWAR) in human coronary artherectomy tissues. J.Infect.Dis. 172, 858–588 (1995).

    Google Scholar 

  • Cochrane M., Pospischil A., Walker P., Gibbs H., Timms P.: Distribution of Chlamydia pneumoniae DNA in atherosclerotic carotid arteries: significance for sampling procedures. J.Clin.Microbiol. 41, 1454–1457 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Crkovská J., Štípek S.: Factors influencing the determination of serum nitrite and nitrate using nitrate reductase and Griess reagent. Klin.Biochem.Metab. 6, 82–87 (1998).

    Google Scholar 

  • Dahlén G.H.: Lipoprotein(a) as a risk factor atherosclerotic diseases. Arctic Med.Res. 47(Suppl. I), 458–641 (1988).

    PubMed  Google Scholar 

  • Danesh J., Collins R., Peto R.: Chronic infections and coronary heart disease: is there a link? Lancet 350, 430–436 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Davidson M., Kuo C.C., Middaugh J.P., Campbell L.A., Wang S.P., Newman W.P. 3rd, Finley J.C., Grayston J.T.: Confirmed previous infection with Chlamydia pneumoniae (TWAR) and its presence in early coronary atherosclerosis. Circulation 98, 628–633 (1998).

    PubMed  CAS  Google Scholar 

  • Dobiášova M., Frohlich J.: The plasma parameter log (TG/HDL-C) as an atherogenic index: correlation with lipoprotein particle size and esterification rate in apoB lipoprotein-depleted plasma (FER/HDL). Clin.Biochem. 34, 583–588 (2001).

    Article  PubMed  Google Scholar 

  • Dowell S.F., Peeling R.W., Boman J., Carlone G.M., Fields B.S., Guarner J., Hammerschlag M.R., Jackson L.A., Kuo C.C., Maass M., Messmer T.O., Talkington D.F., Tondella M.L., Zaki S.R.: Standardizing Chlamydia pneumoniae assays: recomendations from the centers for disease control and prevention (USA) and the laboratory centre for disease control (Canada). Clin.Infect.Dis. 33, 492–450 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-real J.M., Vayreda M., Richart C., Gutierrez C., Broch M., Vendrell J., Ricart W.: Circulating interleukin-6 levels, blood pressure, and insulin sensitivity in apparently healthy men and women. J.Clin.Endocrinol.Metab. 86, 1154–1159 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Gieffers J., Durling L., Ouellette S.P., Rupp J., Maass M., Byrne G.I., Caldwell H.D., Belland R.J.: Genotypic differences in the Chlamydia pneumoniae tyrP locus related to vascular tropism and pathogenicity. J.Infect.Dis. 188, 1085–1093 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Glader C.A., Boman J., Saikku P., Stenlund H., Weinehall L., Hallmanns G., Dahlén G.H.: The proatherogenic properties of lipoprotein(a) may be enhanced through the formation of circulating immune complexes containing Chlamydia pneumoniaespecific IgG antibodies. Eur.Heart J. 21, 639–646 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Grayston T.: Background of current knowledge of Chlamydia pneumoniae and atherosclerosis. J.Infect.Dis. 181(Suppl. 3), S402–S410 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Heinsohn S., Golta S., Kabisch H., Zur Stadt U.: Standardized detection of Simian virus 40 by real-time quantitative polymerase chain reaction in pediatric malignancies. Haematologica 90, 94–98 (2005).

    PubMed  CAS  Google Scholar 

  • Hrubá D., Roubalová K., Kraml P., Anděl M.: Examination of the manifastation of Chlamydia pneumoniae active infection at patients with heart ischemia. (In Czech) Čas.Lék.Čes. 143, 830–835 (2004).

    Google Scholar 

  • Ibrahim A.I., Obeid M.T., Jouma M.J., Moasis G.A., Al-richane W.L., Kindermann I., Boehm M., Roemer K., Muellerlantzsch N., Gärtner B.C.: Detection of herpes simplex virus, cytomegalovirus and Epstein-Barr virus DNA in atherosclerotic plaques and in unaffected bypass grafts. J.Clin.Virol. 32, 29–32 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Jackson L.A., Campbell L.A., Schmidt R.A., Kuo C.C., Cappuccio A.L., Lee M.J., Grayston J.T.: Specificity of detection of Chlamydia pneumoniae in cardiovascular artheroma: evaluation of inocent bystader hypothesis. Am.J.Pathol. 150, 1785–1790 (1997).

    PubMed  CAS  Google Scholar 

  • Kaukoranta-Tolvanen S.S., Ronni T., Leinonen M.: Expression of adhesion molecules on endothelial cells stimulated by Chlamydia pneumoniae. Microb.Pathog. 21, 407–411 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Kostner G.M., Avogaro P., Cazzolato G., Marth E., Bittolo-Bon G., Quinici G.B.: Lipoprotein Lp(a) and the risk for myocardial infarction. Atherosclerosis 38, 51–61 (1981).

    Article  PubMed  CAS  Google Scholar 

  • Kuo C.C., Gown A., Benditt E., Grayston T.: Detection of Chlamydia pneumoniae in aortic lesions of atherosclerosis by immunocytochemical stain. Arteioscler.Tromb. 13, 1501–1504 (1993a).

    CAS  Google Scholar 

  • Kuo C.C., Shor A., Campbell L.A., Fukushi H., Patton D.L., Grayston J.T.: Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J.Infect.Dis. 167, 841–849 (1993b).

    PubMed  CAS  Google Scholar 

  • Kuo C.C., Grayston J.T., Campbell L.A., Goo Y.A., Wissler R.W., Benditt E.P.: Chlamydia pnumoniae (TWAR) in coronary arteries of young adults (15 to 35 years old). Proc.Soc.Acad.Sci.USA 92, 6911–6914 (1995).

    Article  CAS  Google Scholar 

  • Kuo C.C., Coulson A.S., Campbell L.A., Cappuccio A.L., Wang S.P., Grayston J.T.: Detection of Chlamydia pneumoniae in atherosclerotic plaques in walls of arteries of lower extremities from patients undergoing bypass operation for arterial obstruction. J.Vasc.Surg. 26, 29–31 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Kuo C.C., Campbell L.A.: Detection of Chlamydia pneumoniae in arterial tissues. J.Infect.Dis. 181(Suppl. 3), S432–S436 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Laurila A., Bloigu A., Näyhä S., Hassi J., Leinonen M., Saikku P.: Chronic Chlamydia pneumoniae infection is associated with a serum lipid profile known to be a risk factor for atherosclerosis. Arter.Thromb.Vasc.Biol. 17, 2910–2913 (1997).

    CAS  Google Scholar 

  • Levy J.C., Matthews D.R., Hermans M.P.: Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 21, 2191–2192 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Liu R., Moroi M., Yamamoto M., Kubota T., Ono T., Funatsu A., Komatsu H., Tsuji T., Hara H., Nakamura M., Hirai H., Yamaguchi T.: Presence and severity of Chlamydia pneumoniae and cytomegalovirus infection in coronary plaques are associated with acute coronary syndromes. Internat.Heart J. 47, 511–519 (2006).

    Article  Google Scholar 

  • Maraha B., Berg H., Kerver M., Kranendonk S., Hamming J., Kluytmans J., Peeters M., Van Der Zee A.: Is the perceived association between Chlamydia pneumoniae and vascular diseases biased by methodology? J.Clin.Microbiol. 42, 3937–3941 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Ramirez J.A.: Chlamydia pneumoniae/atherosclerosis study group. Isolation of Chlamydia pneumoniae from the coronary artery of a patient with coronary atherosclerosis. Ann.Intern.Med. 125, 979–982 (1996).

    PubMed  CAS  Google Scholar 

  • Rhoads G.G., Dahlén G., Berg K., Morton N.E., Dannenberg A.L.: Lp(a) lipoprotein as a risk factor for myocardial infarction. JAMA 256, 2540–2544 (1986).

    Article  PubMed  CAS  Google Scholar 

  • Roubalová K.: Concomitant detection of DNA Chlamydia pneumoniae and Chlamydia trachomatis using real-time PCR. Epidemiol. Microbiol.Immunol. 4, 166–176 (2007).

    Google Scholar 

  • Schäfer P., Braun R.W., Möhring K., Henco K., Kang J., Wendland T., Kühn J.E.: Quantitative determination of human cytomegalovirus target sequences in peripheral blood leukocytes by nested polymerase chain reaction and temperature gradient gel electrophoresis. J.Gen.Virol. 74, 2699–2707 (1993).

    Article  PubMed  Google Scholar 

  • Schumacher A., Seljeflot I., Lerkerød A.B., Sommervoll L., Otterstad J.E., Arnesen H.: Does infection with Chlamydia pneumoniae and/or Helicobacter pylori increase the expression of endothelial cell adhesion molecules in humans? Clin. Microbiol.Infect. 8, 654–661 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Shor A., Kuo C.C., Patton D.: Detection of Chlamydia pneumoniae in coronary arterial fatty streaks and atheromatous plaques. South Afr.Med.J. 82, 158–161 (1992).

    CAS  Google Scholar 

  • Tong C.Y.W., Sillis M.: Detection of Chlamydia pneumoniae and Chlamydia psitacii in sputum samples by PCR. J.Clin.Pathol. 46, 313–317 (1993).

    Article  PubMed  CAS  Google Scholar 

  • Vielma S.A., Mironova M., Ku J.R., Lopes Virella M.F.: Oxidized LDL further enhances expression of adhesion molecules in Chlamydophila pneumoniae-infected endothelial cells. J.Lipid Res. 45, 873–880 (2004).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. 2nd Department of Internal Medicine, Charles University in Prague and Královské Vinohrady University Hospital, 100 34, Prague, Czechia

    P. J. Kraml, M. Bulvas, Z. Sommerová, J. PotoČková & M. Anděl

  2. Department of Pathology, 3rd Faculty of Medicine, Charles University in Prague and Královské Vinohrady University Hospital, 100 34, Prague, Czechia

    V. Mandys

  3. Center of Epidemiology and Microbiology, National Institute of Public Health, Prague, Czechia

    K. Roubalová

Authors
  1. P. J. Kraml
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Roubalová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Bulvas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Z. Sommerová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. PotoČková
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Mandys
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Anděl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. J. Kraml.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kraml, P.J., Roubalová, K., Bulvas, M. et al. Markers of Chlamydia pneumoniae and human cytomegalovirus infection in patients with chronic peripheral vascular disease and their relation to inflammation, endothelial dysfunction and changes in lipid metabolism. Folia Microbiol 53, 551–557 (2008). https://doi.org/10.1007/s12223-008-0088-9

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-008-0088-9

Keywords

Search

Navigation