Sources of bacterial penetration into the kidney (review - part II)


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Abstract

Kidney and upper urinary tract infections are a serious general medical problem that is the subject of ongoing experimental and clinical research. However, etiological factors and the pathophysiological mechanisms of acute infectious renal inflammation are poorly understood. This also applies to the problem of sources of bacterial penetration into the kidney. The existing hypotheses on this score have «blank spots». This review comprehensively examines the pathways of invasion of microorganisms into the kidney, causing the development of acute inflammation in it. The proofs in favour of the existing views and their criticism are presented. Also, weaknesses in the inference system are determined.

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About the authors

M. I Kogan

Rostov State Medical University

Email: dept_kogan@mail.ru
Honored Scientist of the Russian Federation, M.D., Dr. Sc. (M), Full Prof.; Head, Dept. of Urology and Human Reproductive Health (with the Pediatric Urology and Andrology course)

Y. L Naboka

Rostov State Medical University

Email: nagu22@mail.ru
M.D., Dr. Sc. (M), Full Prof.; Head, Dept. of Microbiology and Virology №1

References

  1. Jameson J.L., Loscalzo J. Harrison’s Nephrology and Acid-Base Disorders (Harrison’s Medical Guides). 1st Edition. McGraw-Hill Professional; 2010.
  2. Grossman S., Porth C.M., Conelius J., Gerard S.O., Moriber N, O’Shea E.R., Wheeler K., Bautista C. Porth’s Pathophysiology: Concepts of Altered Health States-9th edition. Nursing and Health Studies Faculty Book Gallery; 2014.
  3. Lange D., Scotland K.B. (Eds.). The Role of Bacteria in Urology. Springer Nature Switzerland AG; 2019.
  4. Belyayeva M., Jeong J.M. Acute Pyelonephritis. [Updated 2019 Feb 28]. In: Stat Pearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2020. Available from: https://www.ncbi.nlm.nih.gov/books/NBK519537/
  5. Sintsova A., Frick-Cheng A.E., Smith S., Pirani A., Subashchandrabose S., Snitkin E.S., Mobley H. Genetically diverse uropathogenic Escherichia coli adopt a common transcriptional program in patients with UTIs. Elife. 2019;8:e49748. doi: 10.7554/eLife.49748.
  6. Ejrnxs K. Bacterial characteristics ofimportance for recurrent urinary tract infections caused by Escherichia coli. Dan Med Bull. 2011;58(4):B4187. PMID: 21466767.
  7. Ragnarsdottir B., Svanborg C. Susceptibility to acute pyelonephritis or asymptomatic bacteriuria: host-pathogen interaction in urinary tract infections. Pediatr Nephrol. 2012;27(11):2017-2029. Doi: 10.1007/ s00467-011-2089-1.
  8. Choong F.X., Antypas H., Richter-Dahlfors A. Integrated Pathophysiology of Pyelonephritis. Microbiol Spectr. 2015;3(5). doi: 10.1128/microbiolspec. UTI-0014-2012.
  9. Ejrn&s K., Stegger M., Reisner A., Ferry S., Monsen T., Holm S.E., Lundgren B., Frimodt-M0llerN. Characteristics of Escherichia coli causing persistence or relapse of urinary tract infections: phylogenetic groups, virulence factors and biofilm formation. Virulence. 2011;2(6):528-537. doi: 10.4161/viru.2.6.18189.
  10. Turck M., Petersdorf R.G. The epidemiology of nonenteric Escherichia coli infections: prevalence of serological groups. J Clin Invest. 1962;41(9):1760-1765. doi: 10.1172/JCI104635.
  11. Yamamoto S., Tsukamoto T., Terai A., Kurazono H., Takeda Y., Yoshida O. Genetic evidence supporting the fecal-perineal-urethral hypothesis in cystitis caused by Escherichia coli. J Urol. 1997; 157(3): 1127- 1129. PMID: 9072556.
  12. Vysakh A., Raji N.R., Suma D., Jayesh K., Jyothis M., Latha M.S. Role of antioxidant defence, renal toxicity markers and inflammatory cascade in disease progression of acute pyelonephritis in experimental rat model. Microb Pathog. 2017;109:189-194. doi: 10.1016/j.micpath.2017.05.047.
  13. Li K., Wu K.Y., Wu W, Wang N, Zhang T., Choudhry N, Song Y., Farrar C.A., Ma L, Wei L.L., Duan Z.Y., Dong X., Liu E.Q., Li Z.F., Sacks S.H., Zhou W. C5aR1 promotes acute pyelonephritis induced by uropathogenic E.coli. JCI Insight. 2017;2(24):e97626. doi: 10.1172/jci.insight.97626.
  14. McLellan L.K., Hunstad D.A. Urinary Tract Infection: Pathogenesis and Outlook. Trends Mol Med. 2016;22(11):946-957. Doi: 10.1016/j. molmed.2016.09.003.
  15. Shields J., Maxwell A.P. Acute pyelonephritis can have serious complications. Practitioner. 2010;254(1728):19, 21, 23-24, 2. PMID: 20486480.
  16. Lane M.C., Alteri C.J., Smith S.N., Mobley H.L. Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci USA. 2007;104(42):16669-16674. doi: 10.1073/pnas.0607898104.
  17. Ragnarsdottir B., Fischer H., Godaly G., Gronberg-Hernandez J., Gustafsson M., Karpman D., Lundstedt A.C., Lutay N., Ramisch S., Svensson M.L., Wullt B., Yadav M., Svanborg C. TLR- and CXCR1-dependent innate immunity: insights into the genetics of urinary tract infections. Eur J Clin Invest. 2008;38(2):12-20. doi: 10.1111/j.1365-2362.2008.02004.x.
  18. Hvidberg H., Struve C., Krogfelt K.A., Christensen N., Rasmussen S.N., Frimodt-M0ller N. Development of a long-term ascending urinary tract infection mouse model for antibiotic treatment studies. Antimicrob Agents Chemother. 2000;44( 1): 156-163. doi: 10.1128/aac.44.1.156-163.2000.
  19. Hagberg L., Engberg I., Freter R., Lam J., Olling S., Svanborg Eden C. Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect Immun. 1983;40(1):273-283. PMID: 6339403; PMCID: PMC264845.
  20. Johnson D.E., Russell R.G., Lockatell C.V., Zulty J.C., Warren J.W., Mobley H.L. Contribution of Proteus mirabilis urease to persistence, urolithiasis, and acute pyelonephritis in a mouse model of ascending urinary tract infection. Infect Immun. 1993;61(7):2748-2754. PMID: 8514376; PMCID: PMC280917.
  21. Carey A.J., Tan C.K., Ipe D.S., Sullivan M.J., Cripps A.W., Schembri M.A., Ulett G.C. Urinary tract infection of mice to model human disease: Practicalities, implications and limitations. Crit Rev Microbiol. 2016;42(5):780-799. doi: 10.3109/1040841X.2015.1028885.
  22. LiB., Haridas B., Jackson A.R., Cortado H., Mayne N., Kohnken R., Bolon B., McHugh K.M., Schwaderer A.L., Spencer J.D., Ching C.B., Hains D.S., Justice S.S., Partida-Sanchez S., Becknell B. Inflammation drives renal scarring in experimental pyelonephritis. Am J. Physiol Renal Physiol. 2017;312(1):F43-F53. doi: 10.1152/ajprenal.00471.2016.
  23. Kudinha T., Kong F., Johnson J.R., Andrew S.D., Anderson P., Gilbert G.L. Multiplex PCR-based reverse line blot assay for simultaneous detection of 22 virulence genes in uropathogenic Escherichia coli. Appl Environ Microbiol. 2012;78(4):1198-1202. doi: 10.1128/AEM.06921-11.
  24. Measley R.E., Levison M.E. Host defense mechanisms in the pathogenesis of urinary tract infection. Med Clin North Am. 1991;75(2):275-286. doi: 10.1016/s0025-7125(16)30453-9.
  25. Gorrill R.H., Denavasquez S.J. Experimental pyelonephritis in the mouse produced by Escherichia coli, Pseudomonas aeruginosa and Proteus mirabilis. J. Pathol Bacteriol. 1964;87:79-87. Doi: 10.1002/ path.1700870112.
  26. Sullivan M.J., Ulett G.C. Evaluation of hematogenous spread and ascending infection in the pathogenesis of acute pyelonephritis due to group B. streptococcus in mice. Microb Pathog. 2020;138:103796. doi: 10.1016/j.micpath.2019.103796.
  27. Коган М.И., Пасечник Д.Г., Набока Ю.Л., Ибишев Х.С., Газаев З.И., Гудима И.А. Могут ли неклостридиально-анаэробные бактерии вызывать острый пиелонефрит? (экспериментальная модель). Урология. 2012;(2):8-13.
  28. Пасечник Д.Г., Набока Ю.Л., Митусова Е.В., Ибишев Х.С., Газаев З.И. Сравнительный анализ течения экспериментального острого обструктивного пиелонефрита, вызванного различными неклостридиально-анаэробными бактериями. Вестник урологии. 2013;(1):8-20
  29. Pasechnik D.G., Gudima I.A., Kogan M.I., Mitusova E.V., Ibishev K.S., Bejanyan S.K., Gazayev Z.I., Naboka Y.L. Do non-clostridial anaerobic bacteria cause of acute pyelonephritis in ureter obstruction? Medical news of North Caucasus. 2016; 11(2):207-210. Doi: 10.14300/ mnnc.2016.11038.
  30. Smith W., Hale J.H., Smith M.M. The role of coagulase in staphylococcal infections. Br J. Exp Pathol. 1947;28(1):57-67. PMID: 20290308; PMCID: PMC2073007.
  31. Pytel A., Ryabinsky V., Rodoman V. On morphological peculiarities of the urinary leucocytes in inflammatory diseases of kidneys and urinary tract. Urol Int. 1968;23(5):377-387. doi: 10.1159/000279574. PMID: 5703943.
  32. Blanco J.D., Gibbs R.S., Castaneda Y.S. Bacteremia in obstetrics: clinical course. Obstet Gynecol. 1981;58(5):621-625. PMID: 7301239.
  33. Chen C.H. Staphylococcus saprophyticus bacteremia with pyelonephritis cured by gentamicin. J. Formos Med Assoc. 2014;113(7):483-484. doi: 10.1016/j.jfma.2012.11.003.
  34. Uno S., Hase R., Toguchi A., Otsuka Y., Hosokawa N. Pyelonephritis with bacteremia caused by Listeria monocytogenes: A case report. J. Infect Chemother. 2017;23(2):111-113. doi: 10.1016/j.jiac.2016.08.006.
  35. Non L.R., Nazinitsky A., Gonzalez M.D., Burnham C.A., Patel R. Actinobaculum schaalii bacteremia: A report of two cases. Anaerobe. 2015;34:84-85. doi: 10.1016/j.anaerobe.2015.04.006.
  36. Ahmad N.M., Ahmad K.M. Corynebacterium minutissimum pyelonephritis with associated bacteraemia: a case report and review of literature. J. Infect. 2005;51(5):e299-303. doi: 10.1016/j.jinf.2005.02.026.
  37. Chazan B., Raz R., Shental Y., Sprecher H., Colodner R. Bacteremia and pyelonephritis caused by Lactobacillus jensenii in a patient with urolithiasis. Isr Med Assoc J. 2008;10(2):164-165. PMID: 18432039.
  38. Owrangi B.,Masters N., Kuballa A., O’Dea C., Vollmerhausen T.L., Katouli M. Invasion and translocation of uropathogenic Escherichia coli isolated from urosepsis and patients with community-acquired urinary tract infection. Eur J. Clin Microbiol Infect Dis. 2018;37(5):833- 839. doi: 10.1007/s10096-017-3176-4.
  39. Ljungdahl M., Lundholm M., Katouli M., Rasmussen I., Engstrand L., Haglund U. Bacterial translocation in experimental shock is dependent on the strains in the intestinal flora. Scand J. Gastroenterol. 2000;35(4):389- 397. doi: 10.1080/003655200750023958.
  40. MacFie J., O’Boyle C., Mitchell C.J., Buckley P.M., Johnstone D., Sudworth P. Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity. Gut. 1999;45(2):223-228. doi: 10.1136/gut.45.2.223.
  41. Reddy B.S., MacFie J., Gatt M., Macfarlane-Smith L., Bitzopoulou K., Snelling A.M. Commensal bacteria do translocate across the intestinal barrier in surgical patients. Clin Nutr. 2007;26(2):208-215. doi: 10.1016/j.clnu.2006.10.006.
  42. Ramos N.L., Saayman M.L., Chapman T.A., Tucker J.R., Smith H.V., Faoagali J., Chin J.C., Brauner A., Katouli M. Genetic relatedness and virulence gene profiles of Escherichia coli strains isolated from septicaemic and uroseptic patients. Eur J. Clin Microbiol Infect Dis. 2010;29(1):15-23. doi: 10.1007/s10096-009-0809-2.
  43. McNally A., Alhashash F., Collins M., Alqasim A., Paszckiewicz K., Weston V., Diggle M. Genomic analysis of extra-intestinal pathogenic Escherichia coli urosepsis. Clin Microbiol Infect. 2013;19(8):E328-334. doi: 10.1111/1469-0691.12202.
  44. Berg R.D., Garlington A.W. Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun. 1979;23(2):403- 411. PMID: 154474; PMCID: PMC414179.
  45. Deitch E.A., Berg R. Bacterial translocation from the gut: a mechanism of infection. J. Burn Care Rehabil. 1987;8(6):475-482. PMID: 3125184.
  46. Olofsson P., Nylander G., Olsson P. Endotoxin: routes of transport in experimental peritonitis. Am J. Surg. 1986; 151(4) :443-446. doi: 10.1016/0002-9610(86)90098-x.
  47. Wells C.L., Maddaus M.A., Erlandsen S.L., Simmons R.L. Evidence for the phagocytic transport of intestinal particles in dogs and rats. Infect Immun. 1988;56(1):278-282. PMID: 3335406; PMCID: PMC259271.
  48. Steffen E.K., Berg R.D., Deitch E.A. Comparison of translocation rates of various indigenous bacteria from the gastrointestinal tract to the mesenteric lymph node. J. Infect Dis. 1988; 157(5): 1032-1038. doi: 10.1093/infdis/157.5.1032.
  49. Cruz N., Lu Q., Alvarez X., Deitch E.A. Bacterial translocation is bacterial species dependent: results using the human Caco-2 intestinal cell line. J. Trauma. 1994;36(5):612-616. PMID: 8189459.
  50. Deitch E.A. Role of bacterial translocation in necrotizing enterocolitis. Acta Paediatr Suppl. 1994;396:33-36. Doi: 10.1111/j. 1651-2227.1994. tb13239.x.
  51. Hilali F., Ruimy R., Saulnier P., Barnabe C., Lebouguenec C., Tibayrenc M., Andremont A. Prevalence of virulence genes and clonality in Escherichia coli strains that cause bacteremia in cancer patients. Infect Immun. 2000;68(7):3983-3989. doi: 10.1128/iai.68.7.3983-3989.2000.
  52. Katouli M., Brauner A., Haghighi L.K., Kaijser B., Muratov V., Mollby R. Virulence characteristics of Escherichia coli strains causing acute cystitis in young adults in Iran. J. Infect. 2005;50(4):312-321. Doi: 10.1016/j. jinf.2004.05.021.
  53. Macutkiewicz C., Carlson G., Clark E., Dobrindt U., Roberts I., Warhurst G. Characterisation of Escherichia coli strains involved in transcytosis across gut epithelial cells exposed to metabolic and inflammatory stress. Microbes Infect. 2008;10(4):424-431. doi: 10.1016/j.micinf.2008.01.001.
  54. Ljungdahl M., Lundholm M., Katouli M., Rasmussen I., Engstrand L., Haglund U. Bacterial translocation in experimental shock is dependent on the strains in the intestinal flora. Scand J. Gastroenterol. 2000;35(4):389- 397. doi: 10.1080/003655200750023958.
  55. Nettelbladt C.G., Katouli M., Bark T., Svenberg T., Mollby R., Ljungqvist O. Evidence of bacterial translocation in fatal hemorrhagic pancreatitis. J. Trauma. 2000;48(2):314-315. doi: 10.1097/00005373-200002000 00021.
  56. Katouli M., Nettebladt C.G., Muratov V., Ljungqvist O., Bark T., Svenberg T., Mollby R. Selective translocation of coliform bacteria adhering to caecal epithelium of rats during catabolic stress. J. Med Microbiol. 1997;46(7):571-578. doi: 10.1099/00222615-46-7-571.
  57. Nettelbladt C.G., Katouli M., Bark T., Svenberg T., Mollby R., Ljungqvist O. Orally inoculated Escherichia coli strains colonize the gut and increase bacterial translocation after stress in rats. Shock. 2003;20(3):251-256. doi: 10.1097/01.shk.0000068324.41183.c2.
  58. Katouli M., Nettebladt C.G., Muratov V., Ljungqvist O., Bark T., Svenberg T., Mollby R. Selective translocation of coliform bacteria adhering to caecal epithelium of rats during catabolic stress. J. Med Microbiol. 1997;46(7):571-578. doi: 10.1099/00222615-46-7-571.
  59. Ramos N.L., Saayman M.L., Chapman T.A., Tucker J.R., Smith H.V., Faoagali J., Chin J.C., Brauner A., Katouli M. Genetic relatedness and virulence gene profiles of Escherichia coli strains isolated from septicaemic and uroseptic patients. Eur J. Clin Microbiol Infect Dis. 2010;29(1):15-23. doi: 10.1007/s10096-009-0809-2.
  60. Tullus K., KUhn I., Orskov I., Orskov F., Mollby R. The importance of P. and type 1 fimbriae for the persistence of Escherichia coli in the human gut. Epidemiol Infect. 1992; 108(3):415-421. doi: 10.1017/s095026880004992x.
  61. Brauner A., Kaijser B., Wretlind B., Kuhn I. Characterization of Escherichia coli isolated in blood, urine and faeces from bacteraemic patients and possible spread of infection. APMIS. 1991;99(4):381-386. PMID: 2036220.
  62. McNally A., Alhashash F., Collins M., Alqasim A., Paszckiewicz K., Weston V., Diggle M. Genomic analysis of extra-intestinal pathogenic Escherichia coli urosepsis. Clin Microbiol Infect. 2013;19(8):E328-334. doi: 10.1111/1469-0691.12202.
  63. Vollmerhausen T.L., Woods J.L., Faoagali J., Katouli M. Interactions of uroseptic Escherichia coli with renal (A-498) and gastrointestinal (HT-29) cell lines. J Med Microbiol. 2014;63(12):1575-1583. Doi: 10.1099/ jmm.0.076562-0.
  64. Aguilar-Duran S., Horcajada J.P., SorliL., Montero M., Salvado M., Grau S., Gomez J., Knobel H. Community-onset healthcare-related urinary tract infections: comparison with community and hospital-acquired urinary tract infections. J Infect. 2012;64(5):478-483. Doi: 10.1016/j. jinf.2012.01.010.
  65. Marschall J., Fraser V.J., Doherty J., Warren D.K. Between community and hospital: healthcare-associated gram-negative bacteremia among hospitalized patients. Infect Control Hosp Epidemiol. 2009;30(11):1050- 1056. doi: 10.1086/606165.
  66. Moreno E., Andreu A., Pigrau C., Kuskowski M.A., Johnson J.R., Prats G. Relationship between Escherichia coli strains causing acute cystitis in women and the fecal E.coli population of the host. J Clin Microbiol. 2008;46(8):2529-2534. doi: 10.1128/JCM.00813-08.

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