Skip to main content

Clinical and microbiological characteristics of peritoneal dialysis-related peritonitis caused by Escherichia coli in southern Taiwan

European Journal of Clinical Microbiology & Infectious Diseases volume 37, pages 1699–1707 (2018)Cite this article

Abstract

Peritonitis is a serious complication and major cause of treatment failure in patients undergoing peritoneal dialysis (PD). Escherichia coli is the major pathogen in extraintestinal Gram-negative infections, including PD-related peritonitis. The outcomes of E. coli peritonitis in PD varied from relatively favorable outcomes to a higher incidence of treatment failure. The aim of this study was to investigate the impact of bacterial virulence and host characteristics on the outcomes of PD-related peritonitis caused by E. coli. From January 2000 to June 2016, a total of 47 episodes of monomicrobial and 10 episodes of polymicrobial E. coli PD-related peritonitis, as well as 89 episodes of monomicrobial Gram-positive (56 Staphylococcus spp. and 33 Streptococcus spp.) PD-related peritonitis cases, were retrospectively enrolled. Clinical features, E. coli bacterial virulence, and outcomes were analyzed. Compared to Streptococcus spp. peritonitis, E. coli peritonitis had a higher peritoneal catheter removal rate (38 versus 12%; P = 0.0115). Compared to the monomicrobial group, patients in polymicrobial group were older and had higher peritoneal catheter removal rate (80 versus 38%; P = 0.0324). Treatment failure of E. coli peritonitis was associated with more polymicrobial peritonitis and immunocompromised comorbidity, longer duration of PD therapy, and more antimicrobial resistance. E. coli isolates with more iron-related genes had higher prevalence of phylogenetic group B2 and papG II, iha, ompT, and usp genes. This study demonstrates the important roles of clinical and bacterial characteristics in the outcomes of monomicrobial and polymicrobial E. coli PD-related peritonitis.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Oreopoulos DG, Tzamaloukas AH (2000) Peritoneal dialysis in the next millennium. Adv Ren Replace Ther 7(4):338–346

    Article  PubMed  CAS  Google Scholar 

  2. Li PK, Szeto CC, Piraino B, de Arteaga J, Fan S, Figueiredo AE, Fish DN, Goffin E, Kim YL, Salzer W, Struijk DG, Teitelbaum I, Johnson DW (2016) ISPD peritonitis recommendations: 2016 update on prevention and treatment. Perit Dial Int 36(5):481–508

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bernardini J, Holley JL, Johnston JR, Perlmutter JA, Piraino B (1991) An analysis of ten-year trends in infections in adults on continuous ambulatory peritoneal dialysis (CAPD). Clin Nephrol 36(1):29–34

    PubMed  CAS  Google Scholar 

  4. Zelenitsky S, Barns L, Findlay I, Alfa M, Ariano R, Fine A, Harding G (2000) Analysis of microbiological trends in peritoneal dialysis-related peritonitis from 1991 to 1998. Am J Kidney Dis 36(5):1009–1013

    Article  PubMed  CAS  Google Scholar 

  5. Huang ST, Chuang YW, Cheng CH, Wu MJ, Chen CH, Yu TM, Shu KH (2011) Evolution of microbiological trends and treatment outcomes in peritoneal dialysis-related peritonitis. Clin Nephrol 75(5):416–425

    Article  PubMed  Google Scholar 

  6. Russo TA, Johnson JR (2003) Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5(5):449–456

    Article  PubMed  Google Scholar 

  7. Szeto CC, Chow VC, Chow KM, Lai RW, Chung KY, Leung CB, Kwan BC, Li PK (2006) Enterobacteriaceae peritonitis complicating peritoneal dialysis: a review of 210 consecutive cases. Kidney Int 69(7):1245–1252

    Article  PubMed  Google Scholar 

  8. Jarvis EM, Hawley CM, McDonald SP, Brown FG, Rosman JB, Wiggins KJ, Bannister KM, Johnson DW (2010) Predictors, treatment, and outcomes of non-pseudomonas gram-negative peritonitis. Kidney Int 78(4):408–414

    Article  PubMed  CAS  Google Scholar 

  9. Wang MC, Tseng CC, Chen CY, Wu JJ, Huang JJ (2002) The role of bacterial virulence and host factors in patients with Escherichia coli bacteremia who have acute cholangitis or upper urinary tract infection. Clin Infect Dis 35(10):1161–1166

    Article  PubMed  Google Scholar 

  10. Barretti P, Moraes TM, Camargo CH, Caramori JC, Mondelli AL, Montelli AC, da Cunha Mde L (2012) Peritoneal dialysis-related peritonitis due to Staphylococcus aureus: a single-center experience over 15 years. PLoS One 7:e31780

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. de Lourdes Ribeiro de Souza da Cunha M, Montelli AC, Fioravante AM, Neves Batalha JE, Teixeira Caramori JC, Barretti P (2005) Predictive factors of outcome following staphylococcal peritonitis in continuous ambulatory peritoneal dialysis. Clin Nephrol 64(5):378–382

  12. Szeto CC, Kwan BC, Chow KM, Lau MF, Law MC, Chung KY, Leung CB, Li PK (2008) Coagulase negative staphylococcal peritonitis in peritoneal dialysis patients: review of 232 consecutive cases. Clin J Am Soc Nephrol 3(1):91–97

    Article  PubMed  PubMed Central  Google Scholar 

  13. Camargo CH, Cunha Mde L, Caramori JC, Mondelli AL, Montelli AC, Barretti P (2014) Peritoneal dialysis-related peritonitis due to coagulase-negative Staphylococcus: a review of 115 cases in a Brazilian center. Clin J Am Soc Nephrol 9(6):1074–1081

    Article  PubMed  PubMed Central  Google Scholar 

  14. O’Shea S, Hawley CM, McDonald SP, Brown FG, Rosman JB, Wiggins KJ, Bannister KM, Johnson DW (2009) Streptococcal peritonitis in Australian peritoneal dialysis patients: predictors, treatment and outcomes in 287 cases. BMC Nephrol 10:19

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shukla A, Abreu Z, Bargman JM (2006) Streptococcal PD peritonitis--a 10-year review of one centre's experience. Nephrol Dial Transplant 21(12):3545–3549

    Article  PubMed  Google Scholar 

  16. Kiernan L, Finkelstein FO, Kliger AS, Gorban-Brennan N, Juergensen P, Mooraki A, Brown E (1995) Outcome of polymicrobial peritonitis in continuous ambulatory peritoneal dialysis patients. Am J Kidney Dis 25(3):461–464

    Article  PubMed  CAS  Google Scholar 

  17. Barraclough K, Hawley CM, McDonald SP, Brown FG, Rosman JB, Wiggins KJ, Bannister KM, Johnson DW (2010) Polymicrobial peritonitis in peritoneal dialysis patients in Australia: predictors, treatment, and outcomes. Am J Kidney Dis 55(1):121–131

    Article  PubMed  Google Scholar 

  18. Bunke CM, Brier ME, Golper TA (1997) Outcomes of single organism peritonitis in peritoneal dialysis: gram negatives versus gram positives in the network 9 peritonitis study. Kidney Int 52(2):524–529

    Article  PubMed  CAS  Google Scholar 

  19. Valdés-Sotomayor J, Cirugeda A, Bajo MA, del Peso G, Escudero E, Sánchez-Tomero JA, Selgas R, Grupo de Estudios Peritoneales de Madrid (2003) Increased severity of Escherichia coli peritonitis in peritoneal dialysis patients independent of changes in in vitro antimicrobial susceptibility testing. Perit Dial Int 23(5):450–455

    PubMed  Google Scholar 

  20. Pérez-Fontán M, Lueiro F (2006) Escherichia coli peritonitis in patients undergoing peritoneal dialysis: a serious problem that may get worse. Perit Dial Int 26(2):174–177

    PubMed  Google Scholar 

  21. Feng X, Yang X, Yi C, Guo Q, Mao H, Jiang Z, Li Z, Chen D, Cui Y, Yu X (2014) Escherichia coli peritonitis in peritoneal dialysis: the prevalence, antibiotic resistance and clinical outcomes in a South China dialysis center. Perit Dial Int 34(3):308–316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Yip T, Tse KC, Ng F, Hung I, Lam MF, Tang S, Lui SL, Lai KN, Chan TM, Lo WK (2011) Clinical course and outcomes of single-organism Enterococcus peritonitis in peritoneal dialysis patients. Perit Dial Int 31(5):522–528

    Article  PubMed  Google Scholar 

  23. Li YF, Su N, Chen SY, Hu WX, Li FF, Jiang ZP, Yu XQ (2016) Genetic background of Escherichia coli isolates from peritoneal dialysis patients with peritonitis and uninfected control subjects. Genet Mol Res 15(1). https://doi.org/10.4238/gmr.15017341

  24. Wang MC, Lin WH, Tseng CC, Wu AB, Teng CH, Yan JJ, Wu JJ (2013) Role of K1 capsule antigen in cirrhotic patients with Escherichia coli spontaneous bacterial peritonitis in southern Taiwan. Eur J Clin Microbiol Infect Dis 32(3):407–412

    Article  PubMed  CAS  Google Scholar 

  25. Mao BH, Chang YF, Scaria J, Chang CC, Chou LW, Tien N, Wu JJ, Tseng CC, Wang MC, Chang CC, Hsu YM, Teng CH (2012) Identification of Escherichia coli genes associated with urinary tract infections. J Clin Microbiol 50(2):449–456

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Kao CY, Sheu BS, Sheu SM, Yang HB, Chang WL, Cheng HC, Wu JJ (2012) Higher motility enhances bacterial density and inflammatory response in dyspeptic patients infected with Helicobacter pylori. Helicobacter 17(6):411–416

    Article  PubMed  Google Scholar 

  28. Jain AK, Blake PG (2006) Non-Pseudomonas Gram-negative peritonitis. Kidney Int 69(7):1107–1109

    Article  PubMed  CAS  Google Scholar 

  29. Lin WH, Tseng CC, Wu AB, Yang DC, Cheng SW, Wang MC, Wu JJ (2015) Clinical and microbiological characteristics of peritoneal dialysis-related peritonitis caused by Klebsiella pneumoniae in southern Taiwan. J Microbiol Immunol Infect 48(3):276–283

    Article  PubMed  Google Scholar 

  30. Prasad KN, Singh K, Rizwan A, Mishra P, Tiwari D, Prasad N, Gupta A (2014) Microbiology and outcomes of peritonitis in northern India. Perit Dial Int 34(2):188–194

    Article  PubMed  PubMed Central  Google Scholar 

  31. Holley JL, Bernardini J, Piraino B (1992) Polymicrobial peritonitis in patients on continuous peritoneal dialysis. Am J Kidney Dis 19(2):162–166

    Article  PubMed  CAS  Google Scholar 

  32. Kim GC, Korbet SM (2000) Polymicrobial peritonitis in continuous ambulatory peritoneal dialysis patients. Am J Kidney Dis 36(5):1000–1008

    Article  PubMed  CAS  Google Scholar 

  33. Szeto CC, Chow KM, Wong TY, Leung CB, Li PK (2002) Conservative management of polymicrobial peritonitis complicating peritoneal dialysis--a series of 140 consecutive cases. Am J Med 113(9):728–733

    Article  PubMed  Google Scholar 

  34. D'Souza AL (2007) Ageing and the gut. Postgrad Med J 83(975):44–53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Lau CK, Krewulak KD, Vogel HJ (2016) Bacterial ferrous iron transport: the Feo system. FEMS Microbiol Rev 40(2):273–298

    Article  PubMed  CAS  Google Scholar 

  36. Watts RE, Totsika M, Challinor VL, Mabbett AN, Ulett GC, De Voss JJ, Schembri MA (2012) Contribution of siderophore systems to growth and urinary tract colonization of asymptomatic bacteriuria Escherichia coli. Infect Immun 80(1):333–344

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Le Gall T, Clermont O, Gouriou S, Picard B, Nassif X, Denamur E, Tenaillon O (2007) Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol Biol Evol 24(11):2373–2384

    Article  PubMed  CAS  Google Scholar 

  38. Luo Y, Ma Y, Zhao Q, Wang L, Guo L, Ye L, Zhang Y, Yang J (2012) Similarity and divergence of phylogenies, antimicrobial susceptibilities, and virulence factor profiles of Escherichia coli isolates causing recurrent urinary tract infections that persist or result from reinfection. J Clin Microbiol 50(12):4002–4007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Russo TA, McFadden CD, Carlino-MacDonald UB, Beanan JM, Barnard TJ, Johnson JR (2002) IroN functions as a siderophore receptor and is a urovirulence factor in an extraintestinal pathogenic isolate of Escherichia coli. Infect Immun 70(12):7156–7160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Russo TA, McFadden CD, Carlino-MacDonald UB, Beanan JM, Olson R, Wilding GE (2003) The Siderophore receptor IroN of extraintestinal pathogenic Escherichia coli is a potential vaccine candidate. Infect Immun 71(12):7164–7169

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Feldmann F, Sorsa LJ, Hildinger K, Schubert S (2007) The salmochelin siderophore receptor IroN contributes to invasion of urothelial cells by extraintestinal pathogenic Escherichia coli in vitro. Infect Immun 75(6):3183–3187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Gao Q, Wang X, Xu H, Xu Y, Ling J, Zhang D, Gao S, Liu X (2012) Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol 12:143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Koga VL, Tomazetto G, Cyoia PS, Neves MS, Vidotto MC, Nakazato G, Kobayashi RK (2014) Molecular screening of virulence genes in extraintestinal pathogenic Escherichia coli isolated from human blood culture in Brazil. Biomed Res Int 2014:465054

  44. Cusumano CK, Hung CS, Chen SL, Hultgren SJ (2010) Virulence plasmid harbored by uropathogenic Escherichia coli functions in acute stages of pathogenesis. Infect Immun 78(4):1457–1467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Smajs D, Weinstock GM (2001) The iron- and temperature-regulated cjrBC genes of Shigella and enteroinvasive Escherichia coli strains code for colicin Js uptake. J Bacteriol 183(13):3958–3966

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Parham NJ, Pollard SJ, Chaudhuri RR, Beatson SA, Desvaux M, Russell MA, Ruiz J, Fivian A, Vila J, Henderson IR (2005) Prevalence of pathogenicity island IICFT073 genes among extraintestinal clinical isolates of Escherichia coli. J Clin Microbiol 43(5):2425–2434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Wang MC, Tseng CC, Wu AB, Huang JJ, Sheu BS, Wu JJ (2009) Different roles of host and bacterial factors in Escherichia coli extra-intestinal infections. Clin Microbiol Infect 15(4):372–379

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank all the technical staff at the Division of Nephrology at the National Cheng Kung University Hospital.

Funding

This work was supported partially by grants from NCKUH-10702019 and Ministry of Science and Technology, Taiwan (MOST) (102-2314-B-006-015).

Author information

Author notes

  1. Wei-Hung Lin and Chin-Chung Tseng contributed equally to this work.

Affiliations

  1. Department of Internal Medicine, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan

    Wei-Hung Lin

  2. Institute of Clinical Medicine, College of Medicine, National Cheng Kung University, Tainan, Taiwan

    Wei-Hung Lin

  3. Division of Nephrology, Department of Internal Medicine, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, No. 138, Sheng-Li Road, Tainan, 70428, Taiwan

    Chin-Chung Tseng, An-Bang Wu, Yu-Tzu Chang, Te-Hui Kuo, Jo-Yen Chao & Ming-Cheng Wang

  4. Institute of Clinical Pharmacy and Pharmaceutical Sciences, College of Medicine, National Cheng Kung University, Tainan, Taiwan

    Ming-Cheng Wang

  5. Department of Biotechnology and Laboratory Science in Medicine, School of Biomedical Science and Engineering, National Yang Ming University, No. 155, Section 2, Li-Nong Street, Taipei, 11221, Taiwan

    Jiunn-Jong Wu

Authors
  1. Wei-Hung Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chin-Chung Tseng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. An-Bang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu-Tzu Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Te-Hui Kuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jo-Yen Chao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ming-Cheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jiunn-Jong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ming-Cheng Wang or Jiunn-Jong Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

For this type of study, formal consent is not required.

Informed consent

No identifying information is included.

Electronic supplementary material

ESM 1

(DOCX 19 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lin, WH., Tseng, CC., Wu, AB. et al. Clinical and microbiological characteristics of peritoneal dialysis-related peritonitis caused by Escherichia coli in southern Taiwan. Eur J Clin Microbiol Infect Dis 37, 1699–1707 (2018). https://doi.org/10.1007/s10096-018-3302-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-018-3302-y

Keywords

  • Escherichia coli
  • Peritoneal dialysis
  • Peritonitis
  • Virulence