International Urology and Nephrology

, Volume 51, Issue 4, pp 691–698 | Cite as

Biomarkers and risk factors for sepsis in stage 5 chronic kidney disease: a retrospective case–control study

  • Lijuan Jiang
  • Xiaonan Shao
  • Wei Xing
  • Yanbei SunEmail author
Nephrology - Original Paper



To assess the predictive value of procalcitonin (PCT) in the risk of sepsis in patients with stage 5 chronic kidney disease (CKD).


A total of 373 inpatients with stage 5 CKD were retrospectively analyzed. The patients were divided into non-infection group, local infection group, and sepsis group. The clinical characteristics and inflammatory parameters including PCT, C-reactive protein (CRP), white blood cell count (WBC), and neutrophil percentage (NEU%) were compared and the receiver operating characteristic (ROC) curves to predict sepsis were plotted. Related risk factors of sepsis were analyzed by logistic regression analysis.


(1) The hemodialysis ratio of sepsis group was the highest at 92.3%. PCT, CRP, and NEU% were significantly different among the three subgroups (P < 0.05 for all). Total cholesterol and low density lipoprotein (LDL) levels in sepsis group were significantly lower than that in local infection group (P < 0.05 for both). (2) CRP and WBC were unable to predict sepsis (P > 0.05 for all), while PCT and NEU% could predict sepsis with areas under the curve (AUC) of 0.838 and 0.691, respectively (P < 0.05 for all). (3) Multivariate logistic regression analysis showed that PCT > 1.650 ng/mL was a risk factor (OR = 6.926, P = 0.002) while LDL was probably a protective factor (OR = 0.336, P = 0.040) of sepsis in patients with stage 5 CKD.


At stage 5 CKD, the predictive value of PCT for sepsis is best among inflammatory markers, and PCT and LDL levels are independent factors of sepsis.


Chronic kidney disease Procalcitonin Low density lipoprotein Sepsis Risk factors 



Chronic kidney disease




C-reactive protein


White blood cell count


Neutrophil percentage


Alanine aminotransferase


Aspartate aminotransferase


Receiver operating characteristic


Areas under the curve


End-stage renal diseases


Renal replacement therapy


Systemic inflammatory response syndrome


Glomerular filtration rate


Estimated glomerular filtration rate


Serum creatinine


Blood urea nitrogen


Total cholesterol




High density lipoprotein


Low density lipoprotein


Peritoneal dialysis




Coronary atherosclerotic disease


Author contributions

YS and XS conceived of the study, and drafted the manuscript. LJ carried out the Lab testing. XS participated in the design of the study and performed the statistical analysis.


This work was supported by Natural Science Foundation of China (No. 81771798).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

The study has been approved by the Ethics Committee of Soochow University.


  1. 1.
    Mills KT, Xu Y, Zhang W, Bundy JD, Chen CS, Kelly TN, Chen J, He J (2015) A systematic analysis of worldwide population-based data on the global burden of chronic kidney disease in 2010. Kidney Int 88(5):950–957. Google Scholar
  2. 2.
    Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS (2007) Prevalence of chronic kidney disease in the United States. JAMA 298(17):2038–2047. Google Scholar
  3. 3.
    Perner A, Rhodes A, Venkatesh B, Angus DC, Martin-Loeches I, Preiser JC, Vincent JL, Marshall J, Reinhart K, Joannidis M, Opal SM (2017) Sepsis: frontiers in supportive care, organisation and research. Intensive Care Med 43(4):496–508. Google Scholar
  4. 4.
    Girndt M, Sester M, Sester U, Kaul H, Kohler H (2001) Molecular aspects of T- and B-cell function in uremia. Kidney Int Suppl 78:S206–S211. Google Scholar
  5. 5.
    McDonald HI, Thomas SL, Nitsch D (2014) Chronic kidney disease as a risk factor for acute community-acquired infections in high-income countries: a systematic review. BMJ Open 4(4):e004100. Google Scholar
  6. 6.
    Collins AJ, Foley R, Herzog C, Chavers B, Gilbertson D, Ishani A, Kasiske B, Liu J, Mau LW, McBean M, Murray A, St Peter W, Xue J, Fan Q, Guo H, Li Q, Li S, Li S, Peng Y, Qiu Y, Roberts T, Skeans M, Snyder J, Solid C, Wang C, Weinhandl E, Zaun D, Zhang R, Arko C, Chen SC, Dalleska F, Daniels F, Dunning S, Ebben J, Frazier E, Hanzlik C, Johnson R, Sheets D, Wang X, Forrest B, Constantini E, Everson S, Eggers P, Agodoa L (2008) Excerpts from the United States Renal Data System 2007 annual data report. Am J Kidney Dis 51(1 Suppl 1):S1–S320. Google Scholar
  7. 7.
    Sarnak MJ, Jaber BL (2000) Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney Int 58(4):1758–1764. Google Scholar
  8. 8.
    Wang HE, Shapiro NI, Griffin R, Safford MM, Judd S, Howard G (2012) Chronic medical conditions and risk of sepsis. PLoS ONE 7(10):e48307. Google Scholar
  9. 9.
    Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111(12):1805–1812. Google Scholar
  10. 10.
    Sager R, Kutz A, Mueller B, Schuetz P (2017) Procalcitonin-guided diagnosis and antibiotic stewardship revisited. BMC Med 15(1):15. Google Scholar
  11. 11.
    Herget-Rosenthal S, Marggraf G, Pietruck F, Husing J, Strupat M, Philipp T, Kribben A (2001) Procalcitonin for accurate detection of infection in haemodialysis. Nephrol Dial Transplant 16(5):975–979Google Scholar
  12. 12.
    Sitter T, Schmidt M, Schneider S, Schiffl H (2002) Differential diagnosis of bacterial infection and inflammatory response in kidney diseases using procalcitonin. J Nephrol 15(3):297–301Google Scholar
  13. 13.
    Dahaba AA, Rehak PH, List WF (2003) Procalcitonin and C-reactive protein plasma concentrations in nonseptic uremic patients undergoing hemodialysis. Intensive Care Med 29(4):579–583. Google Scholar
  14. 14.
    Dumea R, Siriopol D, Hogas S, Mititiuc I, Covic A (2014) Procalcitonin: diagnostic value in systemic infections in chronic kidney disease or renal transplant patients. Int Urol Nephrol 46(2):461–468. Google Scholar
  15. 15.
    Grace E, Turner RM (2014) Use of procalcitonin in patients with various degrees of chronic kidney disease including renal replacement therapy. Clin Infect Dis 59(12):1761–1767. Google Scholar
  16. 16.
    Schmidt M, Burchardi C, Sitter T, Held E, Schiffl H (2000) Procalcitonin in patients undergoing chronic hemodialysis. Nephron 84(2):187–188Google Scholar
  17. 17.
    Meisner M, Schmidt J, Huttner H, Tschaikowsky K (2000) The natural elimination rate of procalcitonin in patients with normal and impaired renal function. Intensive Care Med 26(Suppl 2):S212–S216. Google Scholar
  18. 18.
    Opatrna S, Klaboch J, Opatrny K Jr, Holubec L, Tomsu M, Sefrna F, Topolcan O (2005) Procalcitonin levels in peritoneal dialysis patients. Perit Dial Int 25(5):470–472Google Scholar
  19. 19.
    Herget-Rosenthal S, Klein T, Marggraf G, Hirsch T, Jakob HG, Philipp T, Kribben A (2005) Modulation and source of procalcitonin in reduced renal function and renal replacement therapy. Scand J Immunol 61(2):180–186. Google Scholar
  20. 20.
    Steinbach G, Bolke E, Grunert A, Storck M, Orth K (2004) Procalcitonin in patients with acute and chronic renal insufficiency. Wien Klin Wochenschr 116(24):849–853Google Scholar
  21. 21.
    Yilmaz FM, Yilmaz G, Akay H, Duranay M, Yucel D (2007) Evaluation of a card test for procalcitonin in continuous ambulatory peritoneal dialysis peritonitis. Ann Clin Biochem 44(Pt 5):482–484. Google Scholar
  22. 22.
    Guz G, Colak B, Hizel K, Reis KA, Erten Y, Bali M, Sindel S (2006) Procalcitonin and conventional markers of inflammation in peritoneal dialysis patients and peritonitis. Perit Dial Int 26(2):240–248Google Scholar
  23. 23.
    Lam MF, Leung JC, Lam CW, Tse KC, Lo WK, Lui SL, Chan TM, Tam S, Lai KN (2008) Procalcitonin fails to differentiate inflammatory status or predict long-term outcomes in peritoneal dialysis-associated peritonitis. Perit Dial Int 28(4):377–384Google Scholar
  24. 24.
    Amour J, Birenbaum A, Langeron O, Le Manach Y, Bertrand M, Coriat P, Riou B, Bernard M, Hausfater P (2008) Influence of renal dysfunction on the accuracy of procalcitonin for the diagnosis of postoperative infection after vascular surgery. Crit Care Med 36(4):1147–1154. Google Scholar
  25. 25.
    Levey AS, Coresh J, Bolton K, Culleton B, Harvey KS, Ikizler TA, Johnson CA, Kausz A, Kimmel PL, Kusek J, Levin A (2002) K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 39(2 Suppl 1):S1–S266Google Scholar
  26. 26.
    Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF III, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612Google Scholar
  27. 27.
    Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, Sevransky JE, Sprung CL, Douglas IS, Jaeschke R, Osborn TM, Nunnally ME, Townsend SR, Reinhart K, Kleinpell RM, Angus DC, Deutschman CS, Machado FR, Rubenfeld GD, Webb SA, Beale RJ, Vincent JL, Moreno R (2013) Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit Care Med 41(2):580–637. Google Scholar
  28. 28.
    James MT, Quan H, Tonelli M, Manns BJ, Faris P, Laupland KB, Hemmelgarn BR (2009) CKD and risk of hospitalization and death with pneumonia. Am J Kidney Dis 54(1):24–32. Google Scholar
  29. 29.
    Davenport A (2009) Peritonitis remains the major clinical complication of peritoneal dialysis: the London, UK, peritonitis audit 2002–2003. Perit Dial Int 29(3):297–302Google Scholar
  30. 30.
    Mactier R (2009) Peritonitis is still the achilles’ heel of peritoneal dialysis. Perit Dial Int 29(3):262–266Google Scholar
  31. 31.
    Hildebrand A, Komenda P, Miller L, Rigatto C, Verrelli M, Sood AR, Sathianathan C, Reslerova M, Eng L, Eng A, Sood MM (2010) Peritonitis and exit site infections in First Nations patients on peritoneal dialysis. Clin J Am Soc Nephrol 5(11):1988–1995. Google Scholar
  32. 32.
    James MT, Laupland KB, Tonelli M, Manns BJ, Culleton BF, Hemmelgarn BR (2008) Risk of bloodstream infection in patients with chronic kidney disease not treated with dialysis. Arch Intern Med 168(21):2333–2339. Google Scholar
  33. 33.
    Orasan OH, Sava M, Iancu M, Cozma A, Saplontai-Pop A, Sarlea Tarmure S, Lungoci C, Orasan RA, Patiu IM, Dumitrascu DL (2015) Serum hyaluronic acid in chronic viral hepatitis B and C: a biomarker for assessing liver fibrosis in chronic hemodialysis patients. Int Urol Nephrol 47(7):1209–1217. Google Scholar
  34. 34.
    Orasan OH, Iancu M, Sava M, Saplontai-Pop A, Cozma A, Sarlea ST, Lungoci C, Ungureanu MI, Negrean V, Sampelean D, Dumitrascu DL (2015) Non-invasive assessment of liver fibrosis in chronic viral hepatitis. Eur J Clin Invest 45(12):1243–1251. Google Scholar
  35. 35.
    Trimarchi H, Dicugno M, Muryan A, Lombi F, Iturbe L, Rana MS, Young P, Nau K, Iriarte R, Pomeranz V, Forrester M, Karl A, Alonso M (2013) Pro-calcitonin and inflammation in chronic hemodialysis. Medicina 73(5):411–416Google Scholar
  36. 36.
    Luzzani A, Polati E, Dorizzi R, Rungatscher A, Pavan R, Merlini A (2003) Comparison of procalcitonin and C-reactive protein as markers of sepsis. Crit Care Med 31(6):1737–1741. Google Scholar
  37. 37.
    Castelli GP, Pognani C, Meisner M, Stuani A, Bellomi D, Sgarbi L (2004) Procalcitonin and C-reactive protein during systemic inflammatory response syndrome, sepsis and organ dysfunction. Crit Care 8(4):R234–R242. Google Scholar
  38. 38.
    Schuetz P, Albrich W, Christ-Crain M, Chastre J, Mueller B (2010) Procalcitonin for guidance of antibiotic therapy. Expert Rev Anti-infect Ther 8(5):575–587. Google Scholar
  39. 39.
    Lee SH, Chan RC, Wu JY, Chen HW, Chang SS, Lee CC (2013) Diagnostic value of procalcitonin for bacterial infection in elderly patients—a systemic review and meta-analysis. Int J Clin Pract 67(12):1350–1357. Google Scholar
  40. 40.
    Lu XL, Xiao ZH, Yang MY, Zhu YM (2013) Diagnostic value of serum procalcitonin in patients with chronic renal insufficiency: a systematic review and meta-analysis. Nephrol Dial Transplant 28(1):122–129. Google Scholar
  41. 41.
    Park JH, Kim DH, Jang HR, Kim MJ, Jung SH, Lee JE, Huh W, Kim YG, Kim DJ, Oh HY (2014) Clinical relevance of procalcitonin and C-reactive protein as infection markers in renal impairment: a cross-sectional study. Crit Care 18(6):640. Google Scholar
  42. 42.
    Lee SH, Park MS, Park BH, Jung WJ, Lee IS, Kim SY, Kim EY, Jung JY, Kang YA, Kim YS, Kim SK, Chang J, Chung KS (2015) Prognostic implications of serum lipid metabolism over time during sepsis. BioMed Res Int 2015:789298. PubMedCentralGoogle Scholar
  43. 43.
    Guirgis FW, Donnelly JP, Dodani S, Howard G, Safford MM, Levitan EB, Wang HE (2016) Cholesterol levels and long-term rates of community-acquired sepsis. Crit Care 20(1):408. PubMedCentralGoogle Scholar
  44. 44.
    Lagrost L, Girard C, Grosjean S, Masson D, Deckert V, Gautier T, Debomy F, Vinault S, Jeannin A, Labbe J, Bonithon-Kopp C (2014) Low preoperative cholesterol level is a risk factor of sepsis and poor clinical outcome in patients undergoing cardiac surgery with cardiopulmonary bypass. Crit Care Med 42(5):1065–1073. Google Scholar
  45. 45.
    Feingold KR, Grunfeld C (1997) Lipoproteins: are they important components of host defense? Hepatology 26(6):1685–1686. Google Scholar
  46. 46.
    Hakeem A, Bhatti S, Chang SM (2014) Screening and risk stratification of coronary artery disease in end-stage renal disease. JACC Cardiovasc Imaging 7(7):715–728. Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Lijuan Jiang
    • 1
  • Xiaonan Shao
    • 2
  • Wei Xing
    • 3
  • Yanbei Sun
    • 4
    Email author
  1. 1.Department of Clinical LaboratoryThe Third Affiliated Hospital of Soochow UniversityChangzhouChina
  2. 2.Department of Nuclear MedicineThe Third Affiliated Hospital of Soochow UniversityChangzhouChina
  3. 3.Department of RadiologyThe Third Affiliated Hospital of Soochow UniversityChangzhouChina
  4. 4.Department of NephrologyThe Third Affiliated Hospital of Soochow UniversityChangzhouChina

Personalised recommendations