Skip to main content

Advertisement

SpringerLink
Log in

The relation between hemoglobin variability and carotid intima-media thickness in chronic hemodialysis patients

  • Nephrology – Original Paper
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Purpose

Hemoglobin variability is a common problem among hemodialysis patients. We have previously demonstrated an association between Hb variability and left ventricular mass index. In this study, we investigated a possible relation between Hb variability and carotid intima-media thickness (CIMT).

Methods

Twelve-month hemoglobin (Hb) values of 135 patients on maintenance hemodialysis were examined retrospectively. The range of 11–12 gr/dl was accepted as normal according to the KDOQI guidelines. Hemoglobin levels were classified as: Hb < 11 gr/dl:Low, Hb = 11–12 gr/dl:Normal and Hb > 12 gr/dl:High. According to 12-month Hb trajectory, the patients were divided into three groups: low–normal (LN), normal–high (NH) and low–high (LH). The CIMT measurements were taken on common carotid arteries bilaterally, and the average of these measurements were taken. The groups were compared in terms of CIMT measurements, demographic and laboratory features.

Results

The LN, NH and LH groups were similar in terms of age, gender, incidence of diabetes mellitus, hypertension and cardiovascular diseases. Duration of hemodialysis, hemodialysis adequacy, serum lipids and CaxP products were also similar among the groups. The mean CIMT value was 0.601 ± 0.107, 0.744 ± 0.139 and 0.604 ± 0.134 mm in the LN, LH and NH groups, respectively (p < 0.001). CIMT was significantly higher in LH than in the other two groups.

Conclusions

In our study, when the three groups with similar risk factors for atherosclerosis were examined, we found that the LH group with the highest hemoglobin variability has the highest CIMT. This study is the first study to demonstrate that Hb variability is associated with an increase in CIMT in HD 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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Regidor DL, Kopple JD, Kovesdy CP, Kilpatrick RD, McAllister CJ, Aronovitz J, Greenland S, Kalantar-Zadeh K (2006) Associations between changes in hemoglobin and administered erythropoiesis-stimulating agent and survival in hemodialysis patients. J Am Soc Nephrol 17:1181–1191. doi:10.1681/ASN.2005090997

    Article  CAS  PubMed  Google Scholar 

  2. Yang W, Israni RK, Brunelli SM, Joffe MM, Fishbane S, Feldman HI (2007) Hemoglobin variability and mortality in ESRD. J Am Soc Nephrol 18:3164–3170. doi:10.1681/ASN.2007010058

    Article  CAS  PubMed  Google Scholar 

  3. Brunelli SM, Joffe MM, Israni RK, Yang W, Fishbane S, Berns JS, Harold I, Feldman HI (2008) Adjusted marginal structural analysis of the association between hemoglobin variability and mortality among chronic hemodialysis patients. Clin J Am Soc Nephrol 3:777–782. doi:10.2215/CJN.04281007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Brunelli SM, Lynch KE, Ankers ED, Joffe MM, Yang W, Thadhani RI, Feldman HI (2008) Association of hemoglobin variability and mortality among contemporary incident hemodialysis patients. Clin J Am Soc Nephrol 3:1733–1740. doi:10.2215/CJN.02390508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Gilbertson DT, Ebben JP, Foley RN, Weinhandl ED, Bradbury BD, Collins AJ (2008) Hemoglobin level variability: associations with mortality. Clin J Am Soc Nephrol 3:133–138. doi:10.2215/CJN.01610407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Boudville NC, Djurdjev O, Macdougall IC, de Francisco AL, Deray G, Besarab A, Stevens PE, Walker RG, Ureña P et al (2009) Hemoglobin variability in nondialysis chronic kidney disease: examining the association with mortality. Clin J Am Soc Nephrol 4:1176–1182. doi:10.2215/CJN.04920908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Eckardt KU, Kim J, Kronenberg F, Aljama P, Anker SD, Canaud B, Molemans B, Stenvinkel P et al (2010) Hemoglobin variability does not predict mortality in European hemodialysis patients. J Am Soc Nephrol 21:1765–1775. doi:10.1681/ASN.2009101017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Lau JH, Gangji AS, Rabbat CG, Brimble KS (2010) Impact of haemoglobin and erythropoietin dose changes on mortality: a secondary analysis of results from a randomized anaemia management trial. Nephrol Dial Transplant 25:4002–4009. doi:10.1093/ndt/gfq330

    Article  CAS  PubMed  Google Scholar 

  9. Weinhandl ED, Peng Y, Gilbertson DT, Bradbury BD, Collins AJ (2011) Hemoglobin Variability and mortality: confounding by disease severity. Am J Kidney Dis 57:255–265. doi:10.1053/j.ajkd.2010.06.013

    Article  CAS  PubMed  Google Scholar 

  10. Altunoren O, Dogan E, Sayarlioglu H, Acar G, Yavuz YC, Aydın N, Sahin M, Akkoyun M, Isik IO, Altunoren Ö (2013) Effect of hemoglobin variability on mortality and some cardiovascular parameters in hemodialysis patients. Ren Fail 35(6):819–824. doi:10.3109/0886022X.2013.801270

    Article  CAS  PubMed  Google Scholar 

  11. Mukherjee D, Yadav JS (2002) Carotid artery intimal-medial thickness: indicator of atherosclerotic burden and response to risk factor modification. Am Heart J 144:753–759. doi:10.1067/mhj.2002.124865

    Article  PubMed  Google Scholar 

  12. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115:459–467. doi:10.1161/CIRCULATIONAHA.106.628875

    Article  PubMed  Google Scholar 

  13. Simon A, Gariepy J, Chironi G, Megnien JL, Levenson J (2002) Intima–media thickness: a new tool for diagnosis and treatment of cardiovascular risk. J Hypertens 20:159–169

    Article  CAS  PubMed  Google Scholar 

  14. Rahn KH, Barenbrock M, Hausberg M, Kosch M, Suwelack B, Witta J (2000) Vessel wall alterations in patients with renal failure. Hypertens Res 23:3–6

    Article  CAS  PubMed  Google Scholar 

  15. Ishimura E, Taniwaki H, Tabata T, Tsujimoto Y, Jono S, Emoto M, Shoji T, Inaba M, Inoue T, Nishizawa Y (2005) Cross-sectional association of serum phosphate with carotid intima-medial thickness in hemodialysis patients. Am J Kidney Dis 45:859–865

    Article  CAS  PubMed  Google Scholar 

  16. Kuang D, You H, Ding F, Xue J, Chen J, Ronco C, Gu Y (2009) Intima-media thickness of the carotid artery and its correlation factors in maintenance hemodialysis patients: a cross-sectional study. Blood Purif 28:181–186. doi:10.1159/000227787

    Article  PubMed  Google Scholar 

  17. Li X, Jiang W, Xu Y (2015) Carotid artery intima-media thickness and influencing factors in hemodialysis patients. Clin Lab 61:1865–1870

    CAS  PubMed  Google Scholar 

  18. National Kidney Foundation (2007) KDOQI clinical practice guideline and clinical practice recommendations for anemia in chronic kidney disease: 2007 update of hemoglobin target. Am J Kidney Dis 50:471–530

    Article  Google Scholar 

  19. Ossareh S, Alaei A, Saedi D (2011) Carotid intima-media thickness in maintenance hemodialysis patients: role of cardiovascular risk factor. Iran J Kidney Dis 5:169–174

    PubMed  Google Scholar 

  20. Patel ML, Radheyshyam Verma A, Sachan R, Kamal R (2015) Impact of carotid intima-media thickness on long-term outcome in hemodialysis patients. N Am J Med Sci 7:281–287. doi:10.4103/1947-2714.159339

    Article  PubMed  PubMed Central  Google Scholar 

  21. Kato A, Takita T, Maruyama Y, Kumagai H, Hishida A (2003) Impact of carotid atherosclerosis on long-term mortality in chronic hemodialysis patients. Kidney Int 64:1472–1479. doi:10.1046/j.1523-1755.2003.00205.x

    Article  PubMed  Google Scholar 

  22. Polak JF, O’Leary DH (2016) Carotid intima-media thickness as surrogate for and predictor of CVD. Glob Heart 11:295–312. doi:10.1016/j.gheart.2016.08.006

    Article  PubMed  Google Scholar 

  23. Boulanger CM, Amabile N, Guérin AP, Pannier B, Leroyer AS, Mallat CN, Tedgui A, London GM (2007) In vivo shear stress determines circulating levels of endothelial microparticles in end-stage renal disease. Hypertension 49:902–908. doi:10.1161/01.HYP.0000259667.22309.df

    Article  CAS  PubMed  Google Scholar 

  24. Davignon J, Ganz P (2004) Role of endothelial dysfunction in atherosclerosis. Circulation 109(23 Suppl 1):27–32

    Google Scholar 

  25. Malyszko J (2010) Mechanism of endothelial dysfunction in chronic kidney disease. Clin Chim Acta 411:1412–1420. doi:10.1016/j.cca.2010.06.019

    Article  CAS  PubMed  Google Scholar 

  26. Eckardt KU (2001) Anaemia in end-stage renal disease: pathophysiological considerations. Nephrol Dial Transplant 16:2–8

    Article  CAS  PubMed  Google Scholar 

  27. Martin W, Villani GM, Jothianandan D, Furchgott RF (1985) Selective blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation by hemoglobin and by methylene blue in the rabbit aorta. J Pharmacol Exp Ther 232(3):708–716

    CAS  PubMed  Google Scholar 

  28. Martin W, Smith JA, White DG (1986) The mechanisms by which haemoglobin inhibits the relaxation of rabbit aorta induced by nitrovasodilators, nitric oxide, or bovine retractor penis inhibitory factor. Br J Pharmacol 89:563–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Meyer C, Heiss C, Drexhage C, Kehmeier ES, Balzer J, Mühlfeld A, Merx MW, Lauer T, Kühl H, Floege J, Kelm M, Rassaf T (2010) Hemodialysis-induced release of hemoglobin limits nitric oxide bioavailability and impairs vascular function. J Am Coll Cardiol 55:454–459

    Article  CAS  PubMed  Google Scholar 

  30. Anand IS, Chandrashekhar Y, Wander GS, Chawla LS (1995) Endothelium-derived relaxing factor is important in mediating the high output state in chronic severe anemia. J Am Coll Cardiol 25:1402–1407

    Article  CAS  PubMed  Google Scholar 

  31. Abbasi MR, Abbaszadeh SH, Rokni-Yazdi H, Lessan-Pezeshki M, Khatami MR, Mahdavi-Mazdeh M, Ahmadi F, Seifi S, Gatmiri SM (2016) Carotid intima-media thickness as a marker of atherosclerosis in hemodialysis patients. Indian J Nephrol 26:97–101. doi:10.4103/0971-4065.161544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Pignoli P, Tremoli E, Poli A, Oreste P, Paoletti R (1986) Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation 74:1399–1406

    Article  CAS  PubMed  Google Scholar 

  33. Poyrazoğlu HM, Düşünsel R, Yikilmaz A, Narin N, Anarat R, Gündüz Z, Coşkun A, Baykan A, Oztürk A (2007) Carotid artery thickness in children and young adults with end stage renal disease. Pediatr Nephrol 22:109–116. doi:10.1007/s00467-006-0268-2

    Article  PubMed  Google Scholar 

  34. Janda K, Krzanowski M, Gajda M, Dumnicka P, Fedak D, Lis GJ, Jaśkowski P, Pietrzycka A, Litwin JA, Sułowicz W (2015) Cardiovascular risk in chronic kidney disease patients: intima-media thickness predicts the incidence and severity of histologically assessed medial calcification in radial arteries. BMC Nephrol 16:78. doi:10.1186/s12882-015-0067-8

    Article  PubMed  PubMed Central  Google Scholar 

  35. London GM, Marchais SJ, Guerin AP, Metivier F, Adda H (2002) Arterial structure and function in end-stage renal disease. Nephrol Dial Transplant 17:1713–1724

    Article  PubMed  Google Scholar 

  36. Guérin AP, Pannier B, Marchais SJ, London GM (2008) Arterial structure and function in end-stage renal disease. Curr Hypertens Rep 10:107–111

    Article  PubMed  Google Scholar 

  37. Metivier F, Marchais SJ, Guerin AP, Pannier B, London GM (2000) Pathophysiology of anaemia: focus on the heart and blood vessels. Nephrol Dial Transplant 15:14–18

    Article  PubMed  Google Scholar 

  38. London GM, Guerin AP, Marchais SJ, Pannier B, Safar ME, Day M, Metivier F (1996) Cardiac and arterial interactions in end-stage renal disease. Kidney Int 50:600–608

    Article  CAS  PubMed  Google Scholar 

  39. Barenbrock M, Spieker C, Laske V, Heidenreich S, Hohage H, Bachmann J, Hoeks AP, Rahn KH (1994) Studies of the vessel wall properties in hemodialysis patients. Kidney Int 45:1397–1400

    Article  CAS  PubMed  Google Scholar 

  40. Patsalas S, Eleftheriadis T, Spaia S, Theodoroglou H, Panou E, Liakopoulos V, Antoniadi G, Passadakis P, Vayonas G, Kanakis E, Vargemezis V (2005) The value of computed tomography-derived coronary artery calcification score in coronary artery disease detection in asymptomatic hemodialysis patients. Ren Fail 27:683–688

    Article  PubMed  Google Scholar 

  41. Dogan M, Citak EC (2012) The evaluation of carotid intima-media thickness in children with beta-thalassaemia major. Cardiol Young 22:79–83

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Medicine, Internal Medicine Department, Kahramanmaras Sutcu Imam University, Kahramanmaraş, Turkey

    Safa Ersen Ganidagli & Berivan Ganidagli

  2. Faculty of Medicine, Nephrology Department, Kahramanmaras Sutcu Imam University, Kahramanmaraş, Turkey

    Orcun Altunoren, Ertuğrul Erken & Ozkan Gungor

  3. FMC Kahramanmaras Dialysis Center, Internalist, Kahramanmaraş, Turkey

    Ismet Onder Isık

  4. Faculty of Medicine, Nephrology Department, Kocaeli University, Izmit, Turkey

    Necmi Eren

  5. Nephrology Department, Erzurum Training and Research Hospital, Erzurum, Turkey

    Yasemin Coskun Yavuz

Authors
  1. Safa Ersen Ganidagli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Orcun Altunoren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ertuğrul Erken
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ismet Onder Isık
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Berivan Ganidagli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Necmi Eren
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yasemin Coskun Yavuz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ozkan Gungor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Orcun Altunoren.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ganidagli, S.E., Altunoren, O., Erken, E. et al. The relation between hemoglobin variability and carotid intima-media thickness in chronic hemodialysis patients. Int Urol Nephrol 49, 1859–1866 (2017). https://doi.org/10.1007/s11255-017-1651-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11255-017-1651-6

Keywords

Search

Navigation