Skip to main content

Advertisement

SpringerLink
Log in

Associations of serologic markers of infection and inflammation with vascular disease events and mortality in American dialysis patients

  • ORIGINAL ARTICLE
  • Published:
Clinical and Experimental Nephrology Aims and scope Submit manuscript

Abstract

Background

Inflammatory markers predict cardiovascular risk and mortality in endstage renal disease. The relationship of chronic infections to inflammation and vascular disease events has not been reported among American dialysis patients.

Methods

We performed a cross-sectional and prospective study of a multiracial cohort of 97 chronic hemodialysis patients in California. Anti-Chlamydia pneumoniae IgA and IgG antibodies (Cp-IgA and Cp-IgG), anti-Helicobacter pylori antibodies (Hp-IgG), and highly sensitive C-reactive protein (hsCRP) levels were measured at enrollment. We ascertained the prevalence of atherosclerotic vascular (coronary artery, cerebrovascular, and peripheral vascular) disease (AVD) events, and observed participants for at least 1 year for incident events and mortality. We defined statistical significance as P < 0.01.

Results

Elevated hsCRP levels (77%) and seropositivity to C. pneumoniae were common (Cp-IgA, 49%; Cp-IgG, 64%), whereas the seroprevalence of Hp-IgG was relatively low (25%). The hsCRP levels did not vary with infection status. In bivariate analysis, Cp-IgA and Cp-IgG were each associated with approximately fourfold higher odds of prevalent AVD (P < 0.01). Although anti-chlamydial antibodies maintained nearly significant associations with AVD after covariate adjustment (P < 0.05), antibodies did not predict outcomes over the period of observation. However, hsCRP was a nearly significant independent predictor of prevalent AVD (P = 0.02) and of mortality during follow-up (P = 0.01). We did not detect an association of Hp-IgG with any study outcome.

Conclusions

Our findings generalize a possible link between C. pneumoniae and prevalent atherosclerosis in American hemodialysis patients and confirm the importance of hsCRP as a prognostic indicator. Our work does not support H. pylori as an important mediator of cardiovascular risk in dialysis patients.

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

References

  1. P Stenvinkel O Heimburger F Paultre U Diczfalusy T Wang L Berglund et al. (1999) ArticleTitleStrong association between malnutrition, inflammation, and atherosclerosis in chronic renal failure Kidney Int 55 1899–911 Occurrence Handle10.1046/j.1523-1755.1999.00422.x Occurrence Handle1:STN:280:DyaK1M3ltV2msQ%3D%3D Occurrence Handle10231453

    Article  CAS  PubMed  Google Scholar 

  2. J Zimmermann S Herrlinger A Pruy T Metzger C Wanner (1999) ArticleTitleInflammation enhances cardiovascular risk and mortality in hemodialysis patients Kidney Int 55 648–58 Occurrence Handle10.1046/j.1523-1755.1999.00273.x Occurrence Handle1:STN:280:DyaK1M7ktFGlsA%3D%3D Occurrence Handle9987089

    Article  CAS  PubMed  Google Scholar 

  3. P Saikku M Leinonen K Mattila et al. (1988) ArticleTitleSerological evidence of an association of a novel Chlamydia, TWAR, with chronic coronary heart disease and acute myocardial infarction Lancet II 983–6

    Google Scholar 

  4. CC Kuo AS Coulson LA Campbell AL Cappuccio RD Lawrence SP Wang et al. (1997) ArticleTitleDetection of Chlamydia pneumoniae in atherosclerotic plaques in the walls of arteries of lower extremities from patients undergoing bypass operation for arterial obstruction J Vasc Surg 26 29–31 Occurrence Handle10.1016/S0741-5214(97)70143-5 Occurrence Handle1:STN:280:ByiA1cvmsFQ%3D Occurrence Handle9240318

    Article  CAS  PubMed  Google Scholar 

  5. TC Moazed LA Campbell ME Rosenfeld JT Grayston CC Kuo (1999) ArticleTitleChlamydia pneumoniae infection accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice J Infect Dis 180 238–41 Occurrence Handle10.1086/314855 Occurrence Handle1:STN:280:DyaK1M3ot1Kitw%3D%3D Occurrence Handle10353889

    Article  CAS  PubMed  Google Scholar 

  6. J Danesh L Youngman S Clark S Parish R Peto R Collins (1999) ArticleTitleHelicobacter pylori infection and early onset myocardial infarction: case-control and sibling pairs study BMJ 319 1157–62 Occurrence Handle1:STN:280:DC%2BD3c%2FgvFaksw%3D%3D Occurrence Handle10541503

    CAS  PubMed  Google Scholar 

  7. C Zoccali FA Benedetto F Mallamaci G Tripepi I Fermo A Foca et al. (2000) ArticleTitleInflammation is associated with carotid atherosclerosis in dialysis patients. CREED Investigators. Cardiovascular Risk Extended Evaluation in Dialysis Patients J Hypertens 18 1207–13 Occurrence Handle10.1097/00004872-200018090-00006 Occurrence Handle1:STN:280:DC%2BD3cvksVeksQ%3D%3D Occurrence Handle10994751

    Article  CAS  PubMed  Google Scholar 

  8. P Stenvinkel O Heimburger T Jogestrand (2002) ArticleTitleElevated interleukin-6 predicts progressive carotid artery atherosclerosis in dialysis patients: association with Chlamydia pneumoniae seropositivity Am J Kidney Dis 39 274–82 Occurrence Handle1:CAS:528:DC%2BD38XitVChs78%3D Occurrence Handle11840367

    CAS  PubMed  Google Scholar 

  9. C Zoccali (1998) ArticleTitleCREED Investigators. C-reactive protein and atherosclerosis in dialysis patients Nephrol Dial Transplant 13 2710–1

    Google Scholar 

  10. M Haubitz R Brunkhorst (2001) ArticleTitleC-reactive protein and chronic Chlamydia pneumoniae infection – long-term predictors for cardiovascular disease and survival in patients on peritoneal dialysis Nephrol Dial Transplant 16 809–15 Occurrence Handle1:STN:280:DC%2BD3M7osleltA%3D%3D Occurrence Handle11274279

    CAS  PubMed  Google Scholar 

  11. SC Wolf O Mayer S Jurgens R Vonthein G Schultze T Risler et al. (2003) ArticleTitleChlamydia pneumoniae IgA seropositivity is associated with increased risk for atherosclerotic vascular disease, myocardial infarction and stroke in dialysis patients Clin Nephrol 59 273–9 Occurrence Handle1:STN:280:DC%2BD3s7ovFaksQ%3D%3D Occurrence Handle12708567

    CAS  PubMed  Google Scholar 

  12. G Bellomo G Lippi P Saronio G Reboldi C Verdura F Timio et al. (2003) ArticleTitleInflammation, infection and cardiovascular events in chronic hemodialysis patients: a prospective study J Nephrol 16 245–51 Occurrence Handle12768072

    PubMed  Google Scholar 

  13. M Haubitz K Votsch A Woywodt B Nashan A Groh H Haller et al. (2004) ArticleTitleSerologic evidence of Chlamydia pneumoniae infection as a long-term predictor of cardiovascular death in renal transplant recipients Transplantation 77 1517–21 Occurrence Handle15239614

    PubMed  Google Scholar 

  14. C Zoccali F Mallamaci G Tripepi S Parlongo S Cutrupi FA Benedetto et al. (2003) ArticleTitleChlamydia pneumoniae, overall and cardiovascular mortality in end-stage renal disease (ESRD) Kidney Int 64 579–84 Occurrence Handle10.1046/j.1523-1755.2003.00095.x Occurrence Handle12846753

    Article  PubMed  Google Scholar 

  15. BR Naidu YF Ngeow T Pang (2003) ArticleTitleEthnic distribution of Chlamydophila pneumoniae antibodies in a Malaysian population and possible correlation with coronary heart disease Eur J Epidemiol 18 135–7 Occurrence Handle1:CAS:528:DC%2BD3sXislOqu7Y%3D Occurrence Handle12733835

    CAS  PubMed  Google Scholar 

  16. F Fabrizi P Martin V Dixit S Quan M Brezina H Abbey et al. (1999) ArticleTitleEpidemiology of Helicobacter pylori in chronic haemodialysis patients using the new RIBA H. pylori SIA Nephrol Dial Transplant 14 1929–33 Occurrence Handle1:STN:280:DyaK1MzovFeluw%3D%3D Occurrence Handle10462273

    CAS  PubMed  Google Scholar 

  17. SF Dowell RW Peeling J Boman GM Carlone BA Fileds J Guarner et al. (2001) ArticleTitleStandardizing Chlamydia pneumoniae assays: recommendations from the Centers for Disease Control and Prevention (USA) and the Laboratory Centre for Disease Control (Canada) Clin Infect Dis 33 492–503 Occurrence Handle1:CAS:528:DC%2BD3MXms1eht7w%3D Occurrence Handle11462186

    CAS  PubMed  Google Scholar 

  18. RP Verkooyen D Willemse SC Hiep-van Casteren SA Mousavi Joulandan RJ Shnijder JM Van Den Bosch et al. (1998) ArticleTitleEvaluation of PCR, culture, and serology for diagnosis of Chlamydia pneumoniae respiratory infections J Clin Microbiol 36 2301–7 Occurrence Handle1:CAS:528:DyaK1cXkvVWis70%3D Occurrence Handle9666010

    CAS  PubMed  Google Scholar 

  19. VY Hoymans JM Bosmans L Van Renterghem R Mak D Ursi F Wuyts et al. (2003) ArticleTitleImportance of methodology in determination of Chlamydia pneumoniae seropositivity in healthy subjects and in patients with coronary atherosclerosis J Clin Microbiol 41 4049–53 Occurrence Handle10.1128/JCM.41.9.4049-4053.2003 Occurrence Handle1:CAS:528:DC%2BD3sXnvFaqtr8%3D Occurrence Handle12958224

    Article  CAS  PubMed  Google Scholar 

  20. ML Replogle SL Glaser RA Hiatt J Parsonnet (1995) ArticleTitleBiologic sex as a risk factor for Helicobacter pylori infection in healthy young adults Am J Epidemiol 142 856–63 Occurrence Handle1:STN:280:BymD3MjktV0%3D Occurrence Handle7572962

    CAS  PubMed  Google Scholar 

  21. M Tozawa K Iseki C Iseki S Takishita (2002) ArticleTitlePulse pressure and risk of total mortality and cardiovascular events in patients on chronic hemodialysis Kidney Int 61 717–26 Occurrence Handle10.1046/j.1523-1755.2002.00173.x Occurrence Handle11849415

    Article  PubMed  Google Scholar 

  22. AW Haider PW Wilson MG Larson JC Evans EL Michelson PA Wolf et al. (2002) ArticleTitleThe association of seropositivity to Helicobacter pylori, Chlamydia pneumoniae, and cytomegalovirus with risk of cardiovascular disease: a prospective study J Am Coll Cardiol 40 1408–13 Occurrence Handle10.1016/S0735-1097(02)02272-6 Occurrence Handle12392829

    Article  PubMed  Google Scholar 

  23. A Kato M Odamaki T Takita Y Maruyama H Kumagai A Hishida (2002) ArticleTitleAssociation between interleukin-6 and carotid atherosclerosis in hemodialysis patients Kidney Int 61 1143–52 Occurrence Handle10.1046/j.1523-1755.2002.00215.x Occurrence Handle1:CAS:528:DC%2BD38Xit1ansrs%3D Occurrence Handle11849469

    Article  CAS  PubMed  Google Scholar 

  24. J Muller O Nyvad NA Larsen N Lokkegaard RS Pedersen J Solling et al. (2002) ArticleTitleChlamydia pneumoniae DNA in peripheral blood mononuclear cells in dialysis patients, renal transplant recipients and healthy controls Scand J Clin Lab Invest 62 503–9 Occurrence Handle1:STN:280:DC%2BD3s%2Fgs1OgsQ%3D%3D Occurrence Handle12512740

    CAS  PubMed  Google Scholar 

  25. F Nakajima M Sakaguchi H Oka Y Kawase N Shibahara T Inoue et al. (2004) ArticleTitlePrevalence of Helicobacter pylori antibodies in long-term dialysis patients Nephrology (Carlton) 9 73–6

    Google Scholar 

  26. D Jaspersen W Fassbinder P Heinkele H Kronsbein W Schorr C Raschka et al. (1995) ArticleTitleSignificantly lower prevalence of Helicobacter pylori in uremic patients than in patients with normal renal function J Gastroenterol 30 585–8 Occurrence Handle1:STN:280:BymC3cfntFc%3D Occurrence Handle8574329

    CAS  PubMed  Google Scholar 

  27. F Nakajima M Sakaguchi K Amemoto H Oka M Kubo N Shibahara et al. (2002) ArticleTitleHelicobacter pylori in patients receiving long-term dialysis Am J Nephrol 22 468–72 Occurrence Handle10.1159/000065278 Occurrence Handle12381945

    Article  PubMed  Google Scholar 

  28. A Gasbarrini F Cremonini A Armuzzi V Ojetti M Candelli C Di Campli et al. (1999) ArticleTitleThe role of Helicobacter pylori in cardiovascular and cerebrovascular diseases J Physiol Pharmacol 50 735–42 Occurrence Handle1:STN:280:DC%2BD3c7lvVWjsA%3D%3D Occurrence Handle10695555

    CAS  PubMed  Google Scholar 

  29. DW Jones LE Chambless AR Folsom G Heiss RG Hutchinson AR Sharrett et al. (2002) ArticleTitleRisk factors for coronary heart disease in African Americans: the Atherosclerosis Risk in Communities study, 1987–1997 Arch Intern Med 162 2565–71 Occurrence Handle10.1001/archinte.162.22.2565 Occurrence Handle12456228

    Article  PubMed  Google Scholar 

  30. E Duranti P Imperiali M Sasdelli (1996) ArticleTitleIs hypertension a mortality risk factor in dialysis? Kidney Int Suppl 55 S173–4 Occurrence Handle1:STN:280:BymA3snmsV0%3D Occurrence Handle8743547

    CAS  PubMed  Google Scholar 

  31. AK Cheung MJ Sarnak G Yan JT Dwyer RJ Heyka MV Rocco et al. (2000) ArticleTitleAtherosclerotic cardiovascular disease risks in chronic hemodialysis patients Kidney Int 58 353–62 Occurrence Handle10.1046/j.1523-1755.2000.00173.x Occurrence Handle1:STN:280:DC%2BD3cvgs1Sjuw%3D%3D Occurrence Handle10886582

    Article  CAS  PubMed  Google Scholar 

  32. RN Foley CA Herzog AJ Collins (2003) ArticleTitleSmoking and cardiovascular outcomes in dialysis patients: the United States Renal Data System Wave 2 study Kidney Int 63 1462–7 Occurrence Handle10.1046/j.1523-1755.2003.00860.x Occurrence Handle12631362

    Article  PubMed  Google Scholar 

  33. K Kalantar-Zadeh P Stenvinkel L Pillon JD Kopple (2003) ArticleTitleInflammation and nutrition in renal insufficiency Adv Ren Replace Ther 10 155–69 Occurrence Handle14708070

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Saint Louis University Center for Outcomes Research Salus Center, 2nd Floor, 3545 Lafayette Avenue, St. Louis, MO, 63104, USA

    Krista L. Lentine

  2. Division of Nephrology, Department of Medicine, Saint Louis University School of Medicine, St. Louis, MO, USA

    Krista L. Lentine

  3. Division of Infectious Diseases and Geographic Medicine, Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA

    Julie Parsonnet

  4. Division of Epidemiology, Department of Health Research and Policy, Stanford University School of Medicine, Stanford, CA, USA

    Julie Parsonnet

  5. Division of Nephrology, Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA

    Isabella Taylor & Richard A. Lafayette

  6. Diablo Nephrology Medical Group, Walnut Creek, CA, USA

    Elizabeth M. Wrone

Authors
  1. Krista L. Lentine
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julie Parsonnet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabella Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth M. Wrone
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Richard A. Lafayette
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Krista L. Lentine.

Additional information

The abstract for a portion of this work was presented at the American Society of Nephrology 36th Annual Meeting and Scientific Exposition, San Diego, CA, USA, November 2003

Institution at which work was performed: Stanford University Medical Center, Stanford, CA, USA

About this article

Cite this article

Lentine, K., Parsonnet, J., Taylor, I. et al. Associations of serologic markers of infection and inflammation with vascular disease events and mortality in American dialysis patients. Clin Exp Nephrol 10, 55–62 (2006). https://doi.org/10.1007/s10157-005-0392-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10157-005-0392-5

Key words

Search

Navigation