Treatment of Highly Virulent Extraintestinal Pathogenic Escherichia coli Pneumonia with Bacteriophages

Critical Care Medicine

Volumn 43, Issue 6, 2015, Pages e190-e198

  Dufour, Nicolas ^a,b,c,d   Debarbieux, Laurent ^a   Fromentin, Mélanie ^b   Ricard, Jean Damien ^b,c,d  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HÔPITAL LOUIS MOURIER   (France)

Author keywords

bacteriophage; Escherichia coli; lung infection; nosocomial infections; phage therapy; ventilator associated pneumonia

Indexed keywords

CEFTRIAXONE; LACTATE DEHYDROGENASE; PROBIOTIC AGENT; ANTIINFECTIVE AGENT;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COUNT; BACTERIAL VIRULENCE; BACTERIOLYSIS; BACTERIOPHAGE; BIOLUMINESCENCE; BODY WEIGHT; COLONY FORMING UNIT; COMPARATIVE STUDY; CONTROLLED STUDY; ESCHERICHIA COLI PNEUMONIA; EXTRAINTESTINAL PATHOGENIC ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; LACTATE DEHYDROGENASE BLOOD LEVEL; LUNG HOMOGENATE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECORDING; VENTILATOR ASSOCIATED PNEUMONIA; VIRUS STRAIN; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; LUNG; LUNG LAVAGE; MICROBIOLOGY; PNEUMONIA, BACTERIAL; PNEUMONIA, VENTILATOR-ASSOCIATED; VIROLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOPHAGES; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; LUNG; MALE; MICE; MICE, INBRED BALB C; PNEUMONIA, BACTERIAL; PNEUMONIA, VENTILATOR-ASSOCIATED;

EID: 84937556720     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0000000000000968     Document Type: Article

References (59)

1. World Health Organization: The 10 leading causes of death by broad income group. 2008. Available at: http://www.who.int/mediacentre/factsheets/fs310/en/index.html. Accessed March 15, 2014
2. Fagon JY, Chastre J, Hance AJ, et al: Nosocomial pneumonia in ventilated patients: A cohort study evaluating attributable mortality and hospital stay. Am J Med 1993; 94:281-288
3. Heyland DK, Cook DJ, Griffth L, et al: The attributable morbidity and mortality of ventilator-associated pneumonia in the critically ill patient. The Canadian Critical Trials Group. Am J Respir Crit Care Med 1999; 159:1249-1256
4. Kollef MH: Ventilator-associated pneumonia. A multivariate analysis. JAMA 1993; 270:1965-1970
5. Torres A, Aznar R, Gatell JM, et al: Incidence, risk, and prognosis factors of nosocomial pneumonia in mechanically ventilated patients. Am Rev Respir Dis 1990; 142:523-528
6. Center for Disease Control: Antibiotic resistance threats in the United States. 2013. Available at: http://www.cdc.gov/drugresistance/threat-report-2013. Accessed March 15, 2014
7. Vincent JL, Rello J, Marshall J, et al; EPIC II Group of Investigators: International study of the prevalence and outcomes of infection in intensive care units. JAMA 2009; 302:2323-2329
8. Hamet M, Pavon A, Dalle F, et al: Candida spp. airway colonization could promote antibiotic-resistant bacteria selection in patients with suspected ventilator-associated pneumonia. Intensive Care Med 2012; 38:1272-1279
9. Messika J, Magdoud F, Clermont O, et al: Pathophysiology of Escherichia coli ventilator-associated pneumonia: Implication of highly virulent extraintestinal pathogenic strains. Intensive Care Med 2012; 38:2007-2016
10. Brzuszkiewicz E, Brüggemann H, Liesegang H, et al: How to become a uropathogen: Comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci USA 2006; 103:12879-12884
11. Lynch JP3rd, Clark NM, Zhanel GG: Evolution of antimicrobial resistance among Enterobacteriaceae (focus on extended spectrum p-lactamases and carbapenemases). Expert Opin Pharmacother 2013; 14:199-210
12. Ricard JD: New therapies for pneumonia. Curr Opin Pulm Med2012; 18:181-186
13. Roux D, Ricard JD: Novel therapies for Pseudomonas aeruginosa pneumonia. Infect Disord Drug Targets 2011; 11:389-394
14. Fauci AS, Marston HD: The perpetual challenge of antimicrobial resistance. JAMA 2014; 311:1853-1854
15. Brüssow H: What is needed for phage therapy to become a reality in Western medicine? Virology 2012; 434:138-142
16. Matsuzaki S, Uchiyama J, Takemura-Uchiyama I, et al: Perspective: The age of the phage. Nature 2014; 509:S9
17. Carmody LA, Gill JJ, Summer EJ, et al: Effcacy of bacteriophage therapy in a model of Burkholderia cenocepacia pulmonary infection. J Infect Dis 2010; 201:264-271
18. Chhibber S, Kaur S, Kumari S: Therapeutic potential of bacteriophage in treating Klebsiella pneumoniae B5055-mediated lobar pneumonia in mice. J Med Microbiol 2008; 57:1508-1513
19. Chhibber S, Kaur T, Sandeep Kaur: Co-therapy using lytic bacteriophage and linezolid: Effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS One 2013; 8:e56022
20. Debarbieux L, Leduc D, Maura D, et al: Bacteriophages can treat and prevent Pseudomonas aeruginosa lung infections. J Infect Dis 2010; 201:1096-1104
21. Clermont O, Bonacorsi S, Bingen E: Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66:4555-4558
22. Morin CE, Kaper JB: Use of stabilized luciferase-expressing plasmids to examine in vivo-induced promoters in the Vibrio cholerae vaccine strain CVD 103-HgR. FEMS Immunol Med Microbiol 2009; 57:69-79
23. Rhee KJ, Cheng H, Harris A, et al: Determination of spatial and temporal colonization of enteropathogenic E. coli and enterohem-orrhagic E. coli in mice using bioluminescent in vivo imaging. Gut Microbes 2011; 2:34-41
24. Van Twest R, Kropinski AM: Bacteriophage enrichment from water and soil. Methods Mol Biol 2009; 501:15-21
25. d'Herelle F: Sur un microbe invisible antagoniste des bacilles dysen-tériques. C R Acad Sci Paris 1917; 165:373-375
26. Boulanger P: Purifcation of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol Biol 2009; 502:227-238
27. Pickard DJ: Preparation of bacteriophage lysates and pure DNA. Methods Mol Biol 2009; 502:3-9
28. Tsonos J, Adriaenssens EM, Klumpp J, et al: Complete genome sequence of the novel Escherichia coli phage phAPEC8. J Virol 2012; 86:13117-13118
29. Kwiatkowski B, Boschek B, Thiele H, et al: Substrate specificity of two bacteriophage-associated endo-N-acetylneuraminidases. J Virol 1983; 45:367-374
30. Johanson WG, Pierce AK, Sanford JP: Changing pharyngeal bacterial fora of hospitalized patients. Emergence of gram-negative bacilli. N Engl J Med 1969; 281:1137-1140
31. Johanson WG Jr, Pierce AK, Sanford JP, et al: Nosocomial respiratory infections with gram-negative bacilli. The signifcance of colonization of the respiratory tract. Ann Intern Med 1972; 77:701-706
32. Ricard JD, Roux D: Candida colonization in ventilated ICU patients: No longer a bystander! Intensive Care Med 2012; 38:1243-1245
33. Ho WS, Gan HM, Yap KP, et al: Genome sequence of multidrug-resistant Escherichia coli EC302/04, isolated from a human tracheal aspirate. J Bacteriol 2012; 194:6691-6692
34. Köhler CD, Dobrindt U: What defines extraintestinal pathogenic Escherichia coli? Int J Med Microbiol 2011; 301:642-647
35. Herold S, Tabar TS, Janssen H, et al: Exudate macrophages attenuate lung injury by the release of IL-1 receptor antagonist in gram-negative pneumonia. Am J Respir Crit Care Med 2011; 183:1380-1390
36. Greenwood D: In vitro veritas? Antimicrobial susceptibility tests and their clinical relevance. J Infect Dis 1981; 144:380-385
37. Henry M, Lavigne R, Debarbieux L: Predicting in vivo effcacy of therapeutic bacteriophages used to treat pulmonary infections. Antimicrob Agents Chemother 2013; 57:5961-5968
38. Bull JJ, Otto G, Molineux IJ: In vivo growth rates are poorly correlated with phage therapy success in a mouse infection model. Antimicrob Agents Chemother 2012; 56:949-954
39. Duplessis M, Lévesque CM, Moineau S: Characterization of Streptococcus thermophilus host range phage mutants. Appl Environ Microbiol 2006; 72:3036-3041
40. Qimron U, Marintcheva B, Tabor S, et al: Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage. Proc Natl Acad Sci USA 2006; 103:19039-19044
41. Ravin V, Räisänen L, Alatossava T: A conserved C-terminal region in Gp71 of the small isometric-head phage LL-H and ORF474 of the prolate-head phage JCL1032 is implicated in specificity of adsorption of phage to its host, Lactobacillus delbrueckii. J Bacteriol 2002; 184:2455-2459
42. Uchiyama J, Takemura I, Satoh M, et al: Improved adsorption of an Enterococcus faecalis bacteriophage JEF24C with a spontaneous point mutation. PLoS One 2011; 6:e26648
43. Nguyen HM, Kang C: Lysis delay and burst shrinkage of coliphage T7 by deletion of terminator Tcp reversed by deletion of early genes. J Virol 2014; 88:2107-2115
44. Bondy-Denomy J, Pawluk A, Maxwell KL, et al: Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 2013; 493:429-432
45. Seed KD, Lazinski DW, Calderwood SB, et al: A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 2013; 494:489-491
46. Sauve C, Azoulay-Dupuis E, Moine P, et al: Efficacies of cefotaxime and ceftriaxone in a mouse model of pneumonia induced by two penicillin-and cephalosporin-resistant strains of Streptococcus pneumoniae. Antimicrob Agents Chemother 1996; 40:2829-2834
47. Domínguez-Herrera J, Velasco C, Docobo-Pérez F, et al: Impact of qnrA1, qnrB1 and qnrS1 on the effcacy of ciprofoxacin and levo-foxacin in an experimental pneumonia model caused by Escherichia coli with or without the GyrA mutation Ser83Leu. J Antimicrob Chemother 2013; 68:1609-1615
48. Docobo-Pérez F, Nordmann P, Domínguez-Herrera J, et al: Effcacies of colistin and tigecycline in mice with experimental pneumonia due to N DM-1-producing strains of Klebsiella pneumoniae and Escherichia coli. Int J Antimicrob Agents 2012; 39:251-254
49. Knudsen JD, Fuursted K, Frimodt-Møller N, et al: Comparison of the effect of cefepime with four cephalosporins against pneumococci with various susceptibilities to penicillin, in vitro and in the mouse peritonitis model. J Antimicrob Chemother 1997; 40:679-686
50. Chan BK, Abedon ST: Phage therapy pharmacology phage cocktails. Adv Appl Microbiol 2012; 78:1-23
51. Craven DE, Steger KA: Epidemiology of nosocomial pneumonia. New perspectives on an old disease. Chest 1995; 108:1S-16S
52. Letarov A, Kulikov E: The bacteriophages in human-and animal body-associated microbial communities. J Appl Microbiol 2009; 107:1-13
53. Méndez J, Audicana A, Cancer M, et al: Assessment of drinking water quality using indicator bacteria and bacteriophages. J Water Health 2004; 2:201-214
54. Miernikiewicz P, Dbrowska K, Piotrowicz A, et al: T4 phage and its head surface proteins do not stimulate infammatory mediator production. PLoS One 2013; 8:e71036
55. Dbrowska K, Miernikiewicz P, Piotrowicz A, et al: Immunogenicity studies of proteins forming the T4 phage head surface. J Virol 2014; 88:12551-12557
56. Loc-Carrillo C, Abedon ST: Pros and cons of phage therapy. Bacteriophage 2011; 1:111-114
57. Abedon ST, Kuhl SJ, Blasdel BG, et al: Phage treatment of human infections. Bacteriophage 2011; 1:66-85
58. Morello E, Saussereau E, Maura D, et al: Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fbrosis strains: First steps towards treatment and prevention. PLoS One 2011; 6:e16963
59. Alemayehu D, Casey PG, McAuliffe O, et al: Bacteriophages cpMR299-2 and cpNH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fbrosis lung airway cells. MBio 2012; 3:e00029-e00012