Abstract
Background
Inflammatory process in hemodialysis patients involves hematopoiesis. The aim of the study was to determine the relationship between serum C-reactive protein (CRP) as a marker of inflammation with hemoglobin in patients under hemodialysis.
Methods
Patients under maintenance hemodialysis for more than 3 months were studied. Serum high-sensitive CRP (hs-CRP) was measured by immunoturbidimetric method and hemoglobin <11 g/dl was considered as anemia. Iron deficiency anemia was confirmed by percent transferrin saturation <20 %. Correlation coefficient, linear regression and odds ratio (OR) were used to determine the relationship.
Results
A total of 73 patients aged 50 ± 16.9 years with median hemodialysis duration of 24 (3–280) months entered the study. High serum hs-CRP (>5 mg/l) was found in 42 (57.5 %) and anemia in 32 (43.8 %) patients. High CRP was significantly associated with anemia OR = 20.8 (95 % CI 5.35–81, p = 0.001). After adjustment for age, dialysis duration, blood indices and serum albumin, the odds of anemia in the high CRP group remained at a significant level of 16.7 (95 % CI 3.7–75, p = 0.001). Hemoglobin levels conversely correlated with serum hs-CRP (r = −0.607, r 2 = 0.36, p = 0.001). In linear regression analysis for each 1 mg/l increase in serum hs-CRP, hemoglobin value increased by 12.4 % (p = 0.002). Serum iron at cutoff level of 54 µg/dl discriminated patients with and without iron deficiency anemia with sensitivity of 93.3 %, specificity of 84 % and accuracy of 90 % (AUC ± SE = 0.901 ± 0.04 (95 % CI, 0.805–0.998, p = 0.001).
Conclusion
These findings indicate that in hemodialysis patients, the inflammatory process alters hemoglobin level in converse correlation with CRP concentration with a linear relationship pattern. Serum iron <54 µg/dl indicates iron deficiency anemia with high accuracy.
Similar content being viewed by others
References
Heidari B. C-reactive protein and other markers of inflammation in hemodialysis patients. Caspian J Intern Med. 2013;4(1):611–6.
Owen WF, Lowrie EG. C-reactive protein as an outcome predictor for maintenance hemodialysis patients. Kidney Int. 1998;54:627–36.
Collado S. Anemia in chronic kidney disease and its cardiovascular implications. Med Clin. 2009;132:38–42. doi:10.1016/S0025.
Yeun JY, Kaysen GA. C-reactive protein predicts all-cause and cardiovascular mortality in hemodialysis patients. Am J Kidney Dis. 2000;35:469–76.
Chawla LS, Krishnan M. Causes and consequences of inflammation on anemia management in hemodialysis patients. Hemodial Int. 2009;13:222–34. doi:10.1111/j.1542-4758.2009.00352.x.
Al Saran K, Sabry A, Al Sherbeiny S, Abdelkader M. Level of C-reactive protein in chronic hemodialysis patients: a comparative study between patients with non-infected catheters and arteriovenous fistula in a large Saudi hemodialysis center. Ther Apher Dial. 2013;17:35–9.
Hung A, Pupim L, Yu C, et al. Determinants of C-reactive protein in chronic hemodialysis patients: relevance of dialysis catheter utilization. Hemodial Int. 2008;12:236–43. doi:10.1111/j.1542-4758.2008.00260.x.
Kaygin MA, Halici U, Aydin A, Dag O, Binici DN, Limandal HK, et al. The relationship between arteriovenous fistula success and inflammation. Ren Fail. 2013;35:1085-8. doi:10.3109/0886022X.2013.815100.
Kadiroglu AK, Kadiroglu ET, Sit D, Dag A, Yilmaz ME. Periodontitis is an important and occult source of inflammation in hemodialysis patients. Blood Purif. 2006;24(4):400–4.
Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol. 2001;72(9):1221–7.
Zoccali C, Benedetto FA, Mallamaci F, et al. Inflammation is associated with carotid atherosclerosis in dialysis patients. Creed Investigators. Cardiovascular risk extended evaluation in dialysis patients. J Hypertens. 2000;18(9):1207–13.
Madore F, Lowrie EG, Brugnara C, et al. Anemia in hemodialysis patients: variables affecting this outcome predictor. J Am Soc Nephrol. 1997;8(12):1921–9.
Panichi V, Rosati A, Bigazzi R, et al. Anaemia and resistance to erythropoiesis-stimulating agents as prognostic factors in haemodialysis patients: results from the RISCAVID study. Nephrol Dial Transpl. 2011;26:2641–8. doi:10.1093/ndt/gfq802.
Mukhopadhyay P, Sinha U, Banerjee J, Choudhury AR, Philips CA. The effects in correction of anaemia in chronic kidney disease with erythropoietin therapy–preference to cardiovascular, neurologic and general well-being of patients from a tertiary care centre. J Indian Med Assoc. 2012;110(12):885–8.
Stenvinkel P. Anaemia and inflammation: what are the implications for the nephrologist? Nephrol Dial Transpl. 2003;18:17–22.
Collins AJ, Ma JZ, Ebben J. Impact of hematocrit on morbidity and mortality. Semin Nephrol. 2000;20:345–9.
Stojceva-Taneva O, et al. Inflammation and anaemia as predictors of cardiovascular mortality in hemodialysis patients. Hippokratia. 2007;11:39–43.
Selim G, Stojceva-Taneva O, Sikole A, et al. Association between haemoglobin level and all-cause mortality in haemodialysis patients: the link with inflammation and malnutrition. Prilozi. 2007;28:81–95.
Lee CT, Lee CH, Su Y, Chuang YC, Tsai TL, Cheni JB. The relationship between inflammatory markers, leptin, adiponectin in chronic hemodialysis patients. Int J Artif Organs. 2004;27:833–41.
Panichi V, Migliori M, De Pietro S, et al. Plasma C-reactive protein in hemodialysis patients: a cross-sectional, longitu dinal clinical survey. Blood Purif. 2000;18:30–6.
Panichi V, Migliori M, De Pietro S, et al. C reactive protein in patients with chronic renal diseases. Ren Fail. 2001;23:551–62.
Lee CT, Lam KK, Lin CR, Chen JB. Inflammatory markers and hepatocyte growth factor in sustained hemodialysis hypotension. Artif Organs. 2005;29:980–3.
Firouzjahi A, Monadi M, Karimpoor F, Heidari B, Dankoob Y, Hajian-Tilaki K, Firozjahi MG. Serum C-reactive protein level and distribution in chronic obstructive pulmonary disease versus healthy controls: a case-control study from Iran. Inflammation. 2013;36:1122–8. doi:10.1007/s10753-013-9646-7.
Heidari B, Heidari P, Tayebi ME. The value of changes in CRP and ESR for predicting treatment response in rheumatoid arthritis. APLAR Journal of Rheumatology. 2007;10:23–8.
Bran P. Inflammation and, serum C-reactive protein and erythropoietin resistance. Nephrol Dial Transpl. 2001;16:224–7.
Rattanasompattikul M, Molnar MZ, Zaritsky JJ, et al. Association of malnutrition-inflammation complex and responsiveness to erythropoiesis-stimulating agents in long-term hemodialysis patients. Nephrol Dial Transpl. 2013;28:1936–45. doi:10.1093/ndt/gfs368.
Gunnell J, Yeun JY, Depner TA, Kaysen GA. Acute-phase response predicts erythropoietin resistance in hemodialysis and peritoneal dialysis. Am J Kidney Dis. 1999;3:63–72.
Barany P, Filho JD, Bergstrom J. High C-reactive protein is a strong predictor of resistance to erythropoietin in hemodialysis patients. Am J Kidney Dis. 1997; 565–568.
Teruel JL, Marcen R, Ocaña J, et al. Clinical significance of C-reactive protein in patients on hemodialysis: a longitudinal study. Nephron Clin Pract. 2005;100:140–5.
Wang AY, Woo J, Lam CW, et al. Is a single time point C-reactive protein predictive of outcome in peritoneal dialysis patients? J Am Soc Nephrol. 2003;14:871–9.
Chonchol M, Lippi G, Montagnana M, Muggeo M, Targher G. Association of inflammation with anaemia in patients with chronic kidney disease not requiring chronic dialysis. Nephrol Dial Transpl. 2008;23:2879–83. doi:10.1093/ndt/gfn109.
Iseki K, Kohagura K. Anemia as a risk factor for chronic kidney disease. Kidney Int Suppl. 2007;107:S4–9.
Dowling TC. Prevalence, etiology, and consequences of anemia and clinical and economic benefits of anemia correction in patients with chronic kidney disease: an overview. Am J Health Syst Pharm. 2007; 64(13 Suppl 8): S3–7; quiz S23-5.
Kalantar-Zadeh K, Höffken B, Wünsch H, Fink H, Kleiner M, Luft FC. Diagnosis of iron deficiency anemia in renal failure patients during the post-erythropoietin era. Am J Kidney Dis. 1995;26:292–9.
Makhlough A, Kosaryan M, Roshan P.Credibility of the measurement of serum ferritin and transferrin receptor as indicators of iron deficiency anemia in hemodialysis patients. Eur Rev Med Pharmacol Sci. 2011; 15: 1158–62.
Stenvinkel P. Anaemia and inflammation: what are the implications for the nephrologist? Nephrol Dial Transpl. 2003; 18(Suppl 8): viii17-22.
Valenti L, Messa P, Plusi S, Capostrinei N, Girelli D. Hepcidin levels in chronic hemodialysis patients: a critical evaluation. Clin Chem Lab Med. 2013; 14: 1–7.
Kalantar-Zadeh K, Rodriguez RA, Humphreys MH. Association between serum ferritin and measures of inflammation, nutrition and iron in haemodialysis patients. Nephrol Dial Transpl. 2004; 19(91): 141–9.
Gonçalves SM, Dal Lago EA, de Moraes TP, et al. Lack of adequate predialyis care and previous hemodialysis, but not hemoglobin variability, are independent predictors of anemia-associated mortality in incident Brazilian peritoneal dialysis patients: results from the BRAZPD study. Blood Purif. 2012;34:298–305. doi:10.1159/000342618.
Brattich M. Relationships between hemoglobin and hematocrit levels and hospitalization and survival rates in dialysis patients. Nephrol Nurs J. 2003;30:231–4.
Snaedal S, Heimbürger O, Qureshi AR, et al. Comorbidity and acute clinical events as determinants of C-reactive protein variation in hemodialysis patients: implications for patient survival. Am J Kidney Dis. 2009;53:1024–33. doi:10.1053/j.ajkd.2009.02.008.
Siribamrungwong M, Puangpanngam K. Treatment of periodontal diseases reduces chronic systemic inflammation in maintenance hemodialysis patients. Ren Fail. 2012;34:171–5. doi:10.3109/0886022X.2011.643351.
Conflict of interest
There is no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Heidari, B., Fazli, M.R., Misaeid, M.A.G. et al. A linear relationship between serum high-sensitive C-reactive protein and hemoglobin in hemodialysis patients. Clin Exp Nephrol 19, 725–731 (2015). https://doi.org/10.1007/s10157-014-1048-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10157-014-1048-0