Yersinia enterocolitica Infection in Patients Undergoing Intermittent Hemodialysis

Main Article Content

Chueh lin Hsu
Dr. Leszek Niepolski


end stage renal disease, hemodialysis, yersinia enterocolitica, enteric yersiniosis


End-stage renal disease is the last stage of chronic kidney disease and affects more than 2 million patients worldwide. The infection-related hospitalization is an important cause of excess morbidity and mortality in this group of patients. Yersinia enterocolitica (YE) is one of the bacteria that hemodialysis (HD) patients can occasionally be infected with. The most common symptoms are fever and mild diarrhea, which is self-limited. However, in HD patients, especially in iron overloaded cases, severe watery or bloody diarrhea can occur. The consumption of undercooked food by patients should sensitize the physician to the possibility of YE infection. Clinically, YE is difficult to diagnose due to nonspecific symptoms and the relatively low prevalence of yersiniosis, compared to other causative pathogens in dialysis patients. There is little information about yersiniosis in HD patients. For this reason, this review aims to summarize the current knowledge on YE infection in HD patients, with the main objective of expounding the problems in identifying, diagnosing, and treating yersiniosis in HD patients.


Download data is not yet available.
Abstract 470 | PDF Downloads 123 HTML Downloads 7 XML Downloads 10


1. Aziz M, Yelamanchili VS. Yersinia enterocolitica. [Updated 2020 Jul 6]. In: StatPearls. Treasure Island, FL: StatPearls Publishing; 2020 Jan.
2. European Centre for Disease Prevention and Control. Annual epidemiological report 2016—Yersiniosis. Stockholm: ECDC; 2016.
3. R V Tauxe. Epidemiology of yersiniosis. [UpToDate. Jul 1 2019]
4. Rahman A, Bonny TS, Stonsaovapak S, Ananchaipattana C. Yersinia enterocolitica: Epidemiological studies and out-breaks. J Pathog. 2011;2011:239391.
5. Le Guern AS, Martin L, Savin C, Carniel E. Yersiniosis in France: Overview and potential sources of infection. Int J Infect Dis. 2016 May;46:1–7. ijid.2016.03.008
6. Stoffel MP, Pollok M, Seifert H, Baldamus CA. Systemic infection with Yersinia enterocolitica in a hemodialysis patient. Zentralbl Bakteriol. 1998 May;287(4):485–7. http://dx.doi. org/10.1016/S0934-8840(98)80188-6
7. Eleftheriadis T, Antoniadi G, Liakopoulos V, Kartsios C, Stefanidis I. Basic science and dialysis: Disturbances of acquired immunity in hemodialysis patients. Semin Dialysis. 2007 Jul;20(5): 440-451.
8. Fabrega A, Vila J. Yersinia enterocolitica: Pathogenesis, virulence and antimicrobial resistance. Enferm Infecc Microbiol Clin. 2012 Jan;30(1):24–32.
9. Griveas I, Visvardis G, Fleva A, Papadopoulou D, Mitsopoulos E, Kyriklidou P et al. Comparative analysis of immunophenotypic abnormalities in cellular immunity of ure-mic patients undergoing either hemodialysis or continuous ambulatory peritoneal dialysis. Ren Fail. 2005;27(3);279–82.
10. March DS, Graham-Brown MPM, Stover CM, Bishop NC, Burton JO. Intestinal barrier disturbances in hemodialysis patients: Mechanisms, consequences, and therapeutic options. Biomed Res Int. 2017;2017:5765417. http://dx.doi. org/10.1155/2017/5765417
11. Robins-Browne RM, Prpic JK. Iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun. 1985 Mar; 47(3):774–9.
12. Abcarian PW, Demas BE. Systemic Yersinia enterocolitica infection associated with iron overload and deferoxamine therapy. AJR Am J Roentgenol. 1991 Oct;157(4):773–5. http://dx.doi. org/10.2214/ajr.157.4.1892033
13. Gallent T, Freedman MH, Vellend H, Francombe WH. Yersinia sepsis in patients with iron overload treated with deferoxamine. N Engl J Med. 1986 Jun;314(25):1643. NEJM198606193142514
14. Adeolu M, Alnajar S, Naushad S, Gupta RS. Genome-based phylogeny and taxonomy of the “Enterobacteriales”: Proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol. 2016;66(12):5575–99. ijsem.0.001485
15. Leon-Velarde CG, Happonen L, Pajunen M, Leskinen K, Kropinski AM, Mattinen L. Yersinia enterocolitica-specific infection by bacteriophages TG1 and ?R1-RT is dependent on temperature-regulated expression of the phage host receptor OmpF. Appl Environ Microbiol. 2016;82(17):5340–53. http://
16. Marceau M. Transcriptional regulation in Yersinia: An update. Curr Issues Mol Biol. 2005 Jul;7(2):151–77.
17. Straley SC, Perry RD. Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol. 1995 Aug;3(8):310–17. S0966-842X(00)88960-X
18. Kapatral V, Olson JW, Pepe JC, Miller VL, Minnich SA. Temperature-dependent regulation of Yersinia enterocolitica Class III flagellar genes. Mol. 1996 Mar;19(5): 1061-1071. http://
19. Bengoechea JA. Regulation of O-antigen biosynthesis in Yersinia enterocolitica. Adv Exp Med Biol. 2003;529:267–74.
20. Bengoechea JA, Zhang L, Toivanen P, Skurnik M. Regulatory network of lipopolysaccharide O-antigen biosynthesis in Yersinia enterocolitica includes cell envelope-dependent sig-nals. Mol Microbiol. 2002 May;44(4):1045–62. http://dx.doi. org/10.1046/j.1365-2958.2002.02940.x
21. Ratnam S, Mercer E, Picco B, Parsons S, Butler R. A nosocomial outbreak of diarrheal disease due to Yersinia enterocolitica Serotype 0:5, Biotype 1. J Infect. 1982 Feb;145(2):242–7. http://
22. Stolk-Engelaar VM, Hoogkamp-Korstanje JA. Clinical presentation and diagnosis of gastrointestinal infections by Yersinia enterocolitica in 261 Dutch patients. Scand J Infect Dis. 1996;28(6):571–5.
23. Skurnik M, Nurmi T, Granfors K, Koskela M, Tiilikainen AS. Plasmid associated antibody production against Yersinia enterocolitica in man. Scand J Infect Dis. 1983;15(2):173–7. http://dx.
24. Grahek-Ogden D, Schimmer B, Cudjoe KS, Nygard K, Kapperud G. Outbreak of Yersinia enterocolitica serogroup O:9 infection and processed pork, Norway. Emerg Infect Dis. 2007 May;13(5):754–6.
25. Rosner BM, Stark K, Werber D. Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001–2008. BMC Public Health. 2010 Jun;2010;10:337. http://dx.doi. org/10.1186/1471-2458-10-337
26. Sakai T, Nakayama A, Hashida M, Yamamoto Y, Takebe H, Imai S. Outbreak of food poisoning by Yersinia enterocolitica serotype O8 in Nara prefecture: the first case report in Japan. Jpn Infect Dis. 2005Aug;58(4):257–8. http://dx.doi. org/10.1186/1471-2458-10-337
27. Butler T, Islam M, Islam MR, Azad AK, Huq MI, Speelman P et al. Isolation of Yersinia enterocolitica and Y. intermedia from fatal cases of diarrhoeal illness in Bangladesh. Trans R Soc Trop Med Hyg. 1984;78(4):449–50. http://dx.doi. org/10.1016/0035-9203(84)90057-9
28. Asakawa Y, Akahane S, Shiozawa K, Honma T. Investigations of source and route of Yersinia enterocolitica infection. Contrib Microbiol Immunol. 1979;5;115–21.
29. Kishore P, Devivilla S, Minimol VA, Thakur A, Uchoi D, Nayak BB. Effect of washing on the adhesion of Yersinia enterocolitica on fish and shrimp muscle surface. Fishery Technol. 2017;54:202–8.
30. Hauser AB, Stinghen AEM, Kato S, Bucharles S, Aita C, Yuzawa Y et al. Characteristics and causes of immune dysfunction related to uremia and dialysis. Perit Dial Int. 2008 Jun;28(Suppl. 3):S183–7.
31. Tamadon MR. Immunity and chronic kidney disease. Immunopathol Persa. 2016 May;2(2):e16.
32. Sharif MR, Chitsazian Z, Moosavian M, Raygan F, Nikoueinejad H, Sharif AR et al. Immune disorders in hemodialysis patients. IJKD. 2015;9(2):84-96.
33. Sardenberg C, Suassuna P, Andreoli MC, Watanabe R, Dalboni MA, Manfredi SR et al. Effects of uremia and dialysis modality on polymorphonuclear cell apoptosis and function. Nephrol Dial Transplant. 2006 Jan;21(1):160–5. http://dx.doi. org/10.1093/ndt/gfi095
34. Verhaegen J, Vanrenterghem Y, Vandepitte J. Generalized yersinia enterocolitica infection in a renal transplant patient. Infection. 1981;9:208–9.
35. Eschbach JW, Egrie JC, Downing MR, Browne JK, Adamson JW. Correction of the anemia of end- stage renal disease with recombinant human erythropoietin. Results of a combined phase I and II clinical trial. N Engl J Med. 1987 Jan;316(2):73–8.
36. Kalantar ZK, Rodriguez RA, Humphreys MH. Association between serum ferritin and measures of inflammation, nutrition and iron in hemodialysis patients. Nephrol Dial Transplant. 2004 Jan;19(1):141–9.
37. Cartar RA, Hawkins JB, Robinson BH. Iron metabolism in the anemia of chronic renal failure. Effects of dialysis and of parenteral iron. Br Med J. 1969 Jul 26;3(5664):206–10. http://dx.doi. org/10.1136/bmj.3.5664.206
38. Ali M, Fayemi AO, Rigolosi R, Frascino J, Marsden T, Malcolm D. Hemosiderosis in hemodialysis patients. An autopsy study of 50 cases. JAMA. 1980 Jul;244(4):343–5. http://
39. Gokal R, Millard PR, Weatherall DJ, Callender ST, Ledingham JG, Oliver DO. Iron metabolism in hemodialysis patients. A study of the management of iron therapy and over-load. Q J Med.1979 Jul;48(191):369–91.
40. Hakim RM, Stivelman JC, Schulman G, Fosburg M, Wolfe L, Imber MJ et al. Iron overload and mobilization in long-term hemodialysis patients. Am J Kidney Dis. 1987 Oct;10(4):249–9.
41. Kalantar-Zadeh K. Controversies Conference on Iron Management in CKD. Mar 27-30, 2014. wp-content/uploads/2017/02/5.-KalantarZadeh_Iron-Overload-in-CKD-and-Effects-on-Various-Tissues.pdf
42. Patruta SI, Edlinger R, Sunder-Plassmann G, Horl WH. Neutrophil impairment associated with iron therapy in hemodialysis patients with functional iron deficiency. J Am Soc Nephrol. 1998 Apr;9(4):655–63.
43. Flament J, Goldman M, Waterlot Y, Dupont E, Wybran J, Vanherweghem JL. Impairment of phagocyte oxidative metabolism in hemodialyzed patients with iron overloaded. Clin Nephrol. 1986 May;25(5):227–30.
44. Hoen B, Paul-Dauphin A, Hestin D, Kessler M. EPIBACDIAL: A multicenter prospective study of risk factors for bacteremia in chronic hemodialysis patients. J Am Soc Nephrol. 1998 May;9(5):869–76.
45. Cantinieaux B, Boelaert J, Hariga C, Fondu P. Impaired neutrophil defense against Yersinia enterocolitica in patients with iron overload who are undergoing dialysis. J Lab Clin Med. 1988 May;111(5):524–8.
46. Sritharan M. Iron and bacterial virulence. Indian J Med Microbiol. 2006 Jul;24(3):163–4.
47. Griffiths E. Iron and bacterial virulence—A brief overview. Biol Met. 1991;4(1):7–13.
48. Zughaier SM, Cornelis P. Editorial: Role of Iron in bacterial pathogenesis. Front Cell Infect Microbiol. 2018 Oct 16;8:344.
49. Rakin A, Schneider L, Podladchikova O. Hunger for iron: The alternative siderophore iron scavenging systems in highly virulent Yersinia. Front Cell Infect Microbiol. 2012;2:151. http://
50. Berman S. Infections in Patients Undergoing Chronic Dialysis. Antimicrobe.
51. Eleftheriadis T, Liakopoulos V, Leivaditis K, Antoniadi G, Stefanidis I. Infections in hemodialysis: A concise review—Part 1: Bacteremia and respiratory infections. Hippokratia. 2011 Jan–Mar;15(1):12–17.
52. Mergenhagen KA, Telesz AL. Yersinia enterocolitica bacteremia in a chronic, mildly iron overloaded dialysis patient. Ann Phamacother. 2011 Feb;45(2):e14. aph.1P603
53. Fakir M, Salson C, Wong T, Matta B, Hardin JM. Septicemia due to Yersinia enterocolitica in a hemodialyzed, iron-depleted patient receiving omeprazole and oral iron supplementation. Am J Kidney Dis. 1992 Mar;19(3):282–4. S0272-6386(13)80010-8
54. Gaughan WJ, Beserab A, Stein HD, Sirota RA, Yudis M. Serum bactericidal activity for Yersinia enterocolitica in hemodialysis patients: Effects of iron overload and deferoxamine. Am J Kidney Dis. 1992 Feb;19(2):144–8. S0272-6386(12)70123-3
55. Hoen B, Kessier M. Infectious risks in patients with renal failure on hemodialysis. Importance of iron overload and deferoxamine. Presse Med. 1991Apr;20(15):681–2.
56. Intra J, Auricchio S, Roberta M, Brambilla SP. A rare case of enteric and systemic Yersinia enterocolitica infection in a chronic, not iron-overloaded dialysis patient. Microbiologia Medica. 2017 Mar;32(1).
57. Eschbach JW, Adamson JW. Iron overload in renal failure patients: Changes since the introduction of erythropoietin therapy. Kidney Int. 1999;55(69):35–43. http://dx.doi. org/10.1046/j.1523-1755.1999.055Suppl.69035.x
58. Vecchio D, Francesco L. Erythropoietin and iron therapy in patients with renal failure. Transfus Altern Transfus Med. 2010;11:20–9.
59. Boelaert JR, Cantinieaux BF, Hariga CF, Fondu PG. Recombinant erythropoietin reverses polymorphonuclear granulocyte dysfunction in iron-overloaded dialysis patients. Nephrol Dial Transplant. 1990;5(7):504–17.
60. Hoen B, Renoult E, Jonon B, Kessler M. Septicemia due to Yersinia enterocolitica in a long-term hemodialysis patient after a single desferrioxamine administration. Nephron. 1988;50(4):378–9.
61. Boyce N, Wood C, Holdsworth S, Thomson NM, Atkins RC. Life-threatening sepsis complicating heavy metal chelation therapy with desferrioxamine. Aust N Z J Med. 1985 Oct;15(5):654–5.
62. Waterlot Y, Vanherweghem JL. Desferrioxamine in hemodialysis as the cause of Yersinia enterocolitica septicemia. Presse Med. 1985 Mar;14(12):699.
63. De Albuquerque SE, De Souza Cavalcante R, Ponce D, Fortaleza CMCB. Epidemiology of healthcare-associated infections among patients from a hemodialysis unit in southeastern Brazil. Braz J Infect Dis. 2014;18(3); 327-330. http://dx.doi. org/10.1016/j.bjid.2013.10.001
64. Karkar A, Bouhaha BM, Dammang ML. Infection control in hemodialysis units: A quick access to essential elements. Saudi J Kidney Dis Transpl. 2014;25:496–519. http://dx.doi. org/10.4103/1319-2442.132150
65. Khan YH. Hamzah AA, Azhar K, Azreen A, Amer K, Tauqeer K et al. Nosocomial infections in hemodialysis patient: What health care professionals neglect? World J Med Sci. 2014 Jan;11(2):265–7.
66. Kist M, Langmaack H, Just M. Spread of Yersinia enterocolitica infection within a hospital. Dtsh Med Wochenschr. 1980 Feb;105(6):185–9.
67. Cannon CG, Linnemann CC. Yersinia enterocolitica infections in hospitalized patients: The problem of hospital-acquired infections. Infect Control Hosp Epidemiol. 1992 Mar;13(3):139–43.
68. William R, Jarvis MD. Bennett & Brachman’s Hospital infections. Philadelphia, PA: Wolters Kluwer; 2013.
69. Finelli L, Miller JT, Tokars JI, Alter MJ, Arduino J. National surveillance of dialysis-associated diseases in the United States, 2002. Semin Dial. 2005;18(1):52–61. http://dx.doi. org/10.1111/j.1525-139X.2005.18108.x
70. D’Agata EM. Antimicrobial- resistant, gram- positive bacteria among patients undergoing chronic hemodialysis. Clin Infect Dis. 2002 Nov;35(10):1212–18. 344282
71. Wares JR, Lawson B, Shemin D, D’Agata EMC. Evaluating infection prevention strategies in out-patient dialysis units using agent-based modeling. PLoS One. 2016;11(5):e0153820. http://
72. Garner J. Guideline for isolation precautions in hospitals. Infect Control Hosp Epidemiol. 1996;17(1):54–80. http://dx.doi. org/10.1017/S0195941700006123
73. Vonberg RP, Gastmeier P. Hospital-acquired infections related to contaminated substances. J Hosp Infect. 2007 Jan;65(1):15– 23.
74. Ducel G, Fabry J, Nicolle L. Prevention of hospital-acquired infections, a practical guide. Malta: WHO; 2002.
75. Gould LH, Walsh KA, Vieira AR, Herman K, Williams IT, Hall AJ et al. Surveillance for foodborne disease outbreaks—United States, 1998–2008. Atlanta, GA: Center for Disease Control and Prevention; 2013.
76. Boyce JM, Pittet D. Guideline for hand hygiene in health-care settings. Center Dis Control Prevent. 2002 Oct;51(RR16):1–44.
77. Cover TL, Aber RC. Yersinia enterocolitica. N Engl J Med. 1989;321:16–24.
78. Rabson AR, Hallett AF, Koornhof HJ, Generalized Yersinia enterocolitica infection. J Infect. 1975;131(4):447–51.
79. Delicou S, Petrocheilou A, Pougiouka M, Maragkos K. Systemic Yersinia enterocolitica in an iron overloaded and immunocompromised thalassemic patients. Microbiol Med. 2017;32:6873.
80. Ahvonen P, Sievers K, Aho K. Arthritis associated with Yersinia enterocolitica infection. Acta Rheumatol Scand. 1969;15(1– 4):232–53.
81. Chlebicz A, Slizewska K. Campylobacteriosis, samonellosis, yersiniosis, and listeriosis as zoonotic foodborne diseases: A review. Int J Environ Res Public Health. 2018;15(5);863 http://
82. Aepfelbacher M, Wolters M. Acting on actin: Rac and Rho played by Yersinia. Curr Top Microbiol Immunol. 2017;399:201–220.
83. Zheng H, Wang J, Sun Y, Jiang B. Clinical isolation and characterization of Yersinia enterocolitica in China using real-time PCR and culture method. Digestion. 2007;76(4):199–204. http://
84. Savin C, Lecleroq A, Carniel E. Evaluation of a single procedure allowing the isolation of enteropathogenic Yersinia along with other bacterial enteropathogens from human stools. PLoS One. 2012;7(7):e41176.
85. Hewison C, Heath CH, Ingram PR. Stool culture. Aust Fam. 2012;41:775–9.
86. Rand KH, Tremblay EE, Hoidal M, Fisher LB, Grau KR, Karst SM. Multiplex gastrointestinal pathogen panels: Implications for infection control. Diagn Microbiol Infect Dis. 2015;82(2):154–7. 01.007
87. Bottone EJ. Yersinia enterocolitica: The charisma contin-ues. Clin Microbiol Rev. 1997;10(2):257–76. http://dx.doi. org/10.1128/CMR.10.2.257
88. Bottone EJ, Sheehan DJ. Yersinia enterocolitica: Guidelines for serologic diagnosis of human infections. Rev Infect. 1983;5(5):898–906.
89. Garo-Falides B, Wainwright TW. Pseudoappendicitis: Abdominal pain arising from thoracic spine dysfunction-a forgotten entity and a reminder of an important clinical les-son. BMJ Case Rep. 2016;2016:bcr2016216490. http://dx.doi. org/10.1136/bcr-2016-216490
90. Pai CH, Gillis F, Tuomanen E, Marks MI. Placebo-controlled double-blind evaluation of trimethoprim-sulfamethoxazole treatment of Yersinia enterocolitica gastroenteritis. J Pediatr. 1984;104(2):308–11.
91. Ostroff MS, Kapperud G, Lassen J, Aasen S, Tauxe RV. Clinical features of sporadic Yersinia enterocolitica infections in Norway. J Infect Dis. 1992;166(4):812–17. infdis/166.4.812
92. Gayraud M, Scavizzi MR, Mollaret HH, Guillevin L, Hornstein MJ. Antibiotic treatment of Yersinia enterocolitica septicemia: A retrospective review of 43 cases. Clin Infect Dis. 1993;17(3):405– 10.
93. Tauxe RV. Treatment and prevention of Yersinia enterocolitica and Yersinia pseudotuberculosis infection. UpToDate. Mar 24, 2019.