Peroral ciprofloxacin therapy impairs the generation of a protective immune response in a mouse model for Salmonella enterica serovar typhimurium diarrhea, while parenteral ceftriaxone therapy does not

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 5, 2012, Pages 2295-2304

  Endt, Kathrin ^a   Maier, Lisa ^a   Käppeli, Rina ^a   Barthel, Manja ^a   Misselwitz, Benjamin ^a   Kremer, Marcus ^b   Hardt, Wolf Dietrich ^a  

^a ETH ZURICH   (Switzerland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CEFTRIAXONE; CIPROFLOXACIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL SHEDDING; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLOSIS;

ADAPTIVE IMMUNITY; ADMINISTRATION, ORAL; ANIMALS; ANTI-BACTERIAL AGENTS; CEFTRIAXONE; CIPROFLOXACIN; COLONY COUNT, MICROBIAL; DIARRHEA; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; FECES; INFUSIONS, PARENTERAL; MICE; MICE, INBRED C57BL; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SEVERITY OF ILLNESS INDEX;

EID: 84860110061     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05819-11     Document Type: Article

References (58)

1. Ambrose NS, Johnson M, Burdon DW, Keighley MR. 1985. The influence of single dose intravenous antibiotics on faecal flora and emergence of Clostridium difficile. J. Antimicrob. Chemother. 15:319 -326.
2. Balfour AE, Lewis R, Ahmed S. 1999. Convalescent excretion of Salmonella enteritidis in infants. J. Infect. 38:24 -25.
3. Bergan T, et al. 1986. Pharmacokinetics of ciprofloxacin and effect of repeated dosage on salivary and fecal microflora. Antimicrob. Agents Chemother. 29:298 -302.
4. Boyd JF. 1985. Pathology of the alimentary tract in Salmonella typhimurium food poisoning. Gut 26:935-944. (Pubitemid 15229644)
5. Brumfitt W, Franklin I, Grady D, Hamilton-Miller JM, Iliffe A. 1984. Changes in the pharmacokinetics of ciprofloxacin and fecal flora during administration of a 7-day course to human volunteers. Antimicrob. Agents Chemother. 26:757-761. (Pubitemid 15211676)
6. Buchwald DS, Blaser MJ. 1984. A review of human salmonellosis. II. Duration of excretion following infection with nontyphi Salmonella. Rev. Infect. Dis. 6:345-356.
7. Cash HL, Whitham CV, Behrendt CL, Hooper LV. 2006. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126-1130. (Pubitemid 44300239)
8. Chang HR, Vladoianu IR, Pechere JC. 1990. Effects of ampicillin, ceftriaxone, chloramphenicol, pefloxacin and trimethoprim-sulphamethoxazole on Salmonella typhi within human monocyte-derived macrophages. J. Antimicrob. Chemother. 26:689-694.
9. Coombes BK, et al. 2005. Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect. Immun. 73:7161-7169. (Pubitemid 41587613)
10. Dethlefsen L, Huse S, Sogin ML, Relman DA. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6:e280.
11. Dethlefsen L, Relman DA. 2011. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl. 1):4554-4561.
12. Eckburg PB, et al. 2005. Diversity of the human intestinal microbial flora. Science 308:1635-1638. (Pubitemid 40807514)
13. Endt K, et al. 2010. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog. 6:e1001097.
14. Enzensberger R, Shah PM, Knothe H. 1985. Impact of oral ciprofloxacin on the faecal flora of healthy volunteers. Infection 13:273-275. (Pubitemid 16194042)
15. Fey PD, et al. 2000. Ceftriaxone-resistant Salmonella infection acquired by a child from cattle. N. Engl. J. Med. 342:1242-1249. (Pubitemid 30235953)
16. Giraud E, Baucheron S, Cloeckaert A. 2006. Resistance to fluoroquinolones in Salmonella: emerging mechanisms and resistance prevention strategies. Microbes Infect. 8:1937-1944. (Pubitemid 44144556)
17. Giuliano M, Barza M, Jacobus NV, Gorbach SL. 1987. Effect of broadspectrum parenteral antibiotics on composition of intestinal microflora of humans. Antimicrob. Agents Chemother. 31:202-206. (Pubitemid 17011238)
18. Glynn MK, et al. 2004. Prior antimicrobial agent use increases the risk of sporadic infections with multidrug-resistant Salmonella enterica serotype Typhimurium: a FoodNet case-control study, 1996-1997. Clin. Infect. Dis. 38(Suppl. 3):S227-S236. (Pubitemid 38553329)
19. Gomez HF, Cleary TG. 1998. Salmonella, p 1321-1334. In Feigin RD, Cherry JD (ed), Textbook of pediatric infectious diseases, 4th ed. W. B. Saunders Company, Philadelphia, PA.
20. Gorbach SL. 1993. Perturbation of intestinal microflora. Vet. Hum. Toxicol. 35(Suppl 1):15-23. (Pubitemid 23261032)
21. Greig JD, Todd EC, Bartleson CA, Michaels BS. 2007. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 1. Description of the problem, methods, and agents involved. J. Food Prot. 70:1752-1761. (Pubitemid 47076119)
22. Hapfelmeier S, et al. 2004. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72:795- 809.
23. Hapfelmeier S, et al. 2008. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step inΔinvG S. Typhimurium colitis. J. Exp. Med. 205:437- 450.
24. Hapfelmeier S, et al. 2005. The Salmonella pathogenicity island (SPI)-1 and SPI-2 type III secretion systems allow Salmonella serovar Typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174:1675-1685.
25. Hohmann E. 2011. Approach to the patient in nontyphoidal Salmonella in a stool culture. In Calderwood SB, Baron EL (ed), UpToDate, the clinical information service on the web and mobile devices. UpToDate, Inc., Waltham, MA.
26. Iankov ID, et al. 2001. Monoclonal antibodies of IgA isotype specific for lipopolysaccharide of Salmonella enteritidis: production, purification, characterization and application as serotyping reagents. FEMS Microbiol. Lett. 196:215-221. (Pubitemid 32232263)
27. Iankov ID, et al. 2002. Production and characterization of monoclonal immunoglobulin A antibodies directed against Salmonella H:g,m flagellar antigen. FEMS Immunol. Med. Microbiol. 33:107-113. (Pubitemid 34607527)
28. Jimenez-Valera M, Gonzalez-Torres C, Moreno E, Ruiz-Bravo A. 1998. Comparison of ceftriaxone, amikacin, and ciprofloxacin in treatment of experimental Yersinia enterocolitica O9 infection in mice. Antimicrob. Agents Chemother. 42:3009 -3011.
29. Kaiser P, Diard M, Stecher B, Hardt WD. 2012. The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen's virulence factors, and the host's mucosal immune response. Immunol. Rev. 245:56-83.
30. Kazemi M, Gumpert TG, Marks MI. 1973. A controlled trial comparing sulfamethoxazole-trimethoprim, ampicillin, and no therapy in the treatment of Salmonella gastroenteritis in children. J. Pediatr. 83:646-650.
31. Kelly CP, Pothoulakis C, LaMont JT. 1994. Clostridium difficile colitis. N. Engl. J. Med. 330:257-262. (Pubitemid 24034138)
32. Kingsley RA, Baumler AJ. 2000. Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol. Microbiol. 36:1006-1014. (Pubitemid 30330672)
33. Lahdevirta J. 1989. Ciprofloxacin in the elimination of enteric Salmonella carriage stage. Scand. J. Infect. Dis. Suppl. 60:112-115. (Pubitemid 19163358)
34. Ljungberg B, Nilsson-Ehle I, Edlund C, Nord CE. 1990. Influence of ciprofloxacin on the colonic microflora in young and elderly volunteers: no impact of the altered drug absorption. Scand. J. Infect. Dis. 22:205-208. (Pubitemid 20169934)
35. Lolekha S, Patanachareon S, Thanangkul B, Vibulbandhitkit S. 1988. Norfloxacin versus co-trimoxazole in the treatment of acute bacterial diarrhoea: a placebo controlled study. Scand. J. Infect. Dis. Suppl. 56:35- 45.
36. Maaser C, et al. 2004. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72:3315-3324. (Pubitemid 38697754)
37. MacLennan CA, et al. 2010. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 328:508 -512.
38. Martinoli C, Chiavelli A, Rescigno M. 2007. Entry route of Salmonella typhimurium directs the type of induced immune response. Immunity 27:975-984. (Pubitemid 50013977)
39. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122:107-118. (Pubitemid 40977944)
40. Michetti P, Mahan MJ, Slauch JM, Mekalanos JJ, Neutra MR. 1992. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60:1786 -1792.
41. Nelson JD, Kusmiesz H, Jackson LH, Woodman E. 1980. Treatment of Salmonella gastroenteritis with ampicillin, amoxicillin, or placebo. Pediatrics 65:1125-1130. (Pubitemid 10068747)
42. Perrin-Guyomard A, et al. 2005. Impact of residual and therapeutic doses of ciprofloxacin in the human-flora-associated mice model. Regul. Toxicol. Pharmacol. 42:151-160. (Pubitemid 40826560)
43. Santos RL, et al. 2001. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect. 3:1335-1344. (Pubitemid 34033770)
44. Singh SP, Williams YU, Klebba PE, Macchia P, Miller S. 2000. Immune recognition of porin and lipopolysaccharide epitopes of Salmonella typhimurium in mice. Microb. Pathog. 28:157-167.
45. Sirinavin S, Garner P. 2000. Antibiotics for treating salmonella gut infections. Cochrane Database Syst. Rev. 2:CD001167.
46. Sirinavin S, Jayanetra P, Lolekha S, Layangkul T. 1988. Predictors for extraintestinal infection in Salmonella enteritis in Thailand. Pediatr. Infect. Dis. J. 7:44-48. (Pubitemid 18040768)
47. Slack E, et al. 2009. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 325:617- 620.
48. Smith ER, Badley BW. 1971. Treatment of Salmonella enteritis and its effect on the carrier state. Can. Med. Assoc. J. 104:1004 -1006.
49. Sperber SJ, Schleupner CJ. 1987. Salmonellosis during infection with human immunodeficiency virus. Rev. Infect. Dis. 9:925-934.
50. Stecher B, et al. 2008. Motility allows S. Typhimurium to benefit from the mucosal defence. Cell. Microbiol. 10:1166 -1180.
51. Stecher B, et al. 2010. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog. 6:e1000711.
52. Stecher B, Hardt WD. 2008. The role of microbiota in infectious disease. Trends Microbiol. 16:107-114.
53. Stecher B, et al. 2007. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5:e244.
54. Su H, et al. 1999. The effect of doxycycline treatment on the development of protective immunity in a murine model of chlamydial genital infection. J. Infect. Dis. 180:1252-1258. (Pubitemid 30070211)
55. Suar M, et al. 2006. Virulence of broad- and narrow-host-range Salmonella enterica serovars in the streptomycin-pretreated mouse model. Infect. Immun. 74:632- 644.
56. Uren TK, et al. 2005. Vaccine-induced protection against gastrointestinal bacterial infections in the absence of secretory antibodies. Eur. J. Immunol. 35:180 -188.
57. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk Lekkerkerk V. 1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (Lond.) 69:405- 411.
58. Wijburg OL, et al. 2006. Innate secretory antibodies protect against natural Salmonella typhimurium infection. J. Exp. Med. 203:21-26. (Pubitemid 43139640)