Efficacy of β-lactam-plus-macrolide combination therapy in a mouse model of lethal pneumococcal pneumonia

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 10, 2016, Pages 6146-6154

  Yoshioka, Daisuke ^a,b   Kajiwara, Chiaki ^a   Ishii, Yoshikazu ^a   Umeki, Kenji ^b   Hiramatsu, Kazufumi ^b   Kadota, Jun Ichi ^b   Tateda, Kazuhiro ^a  

^a TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b OITA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; CD86 ANTIGEN; CEFTRIAXONE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GLYCOPROTEIN P 15095; HLA ANTIGEN CLASS 2; PROGRAMMED DEATH 1 RECEPTOR; ANTIINFECTIVE AGENT; CD11B ANTIGEN; CD86 PROTEIN, MOUSE; PDCD1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL LOAD; BACTERIAL SURVIVAL; BRONCHOALVEOLAR LAVAGE FLUID; CONTROLLED STUDY; DENDRITIC CELL; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG RESEARCH; FEMALE; HELPER CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; LUNG BURDEN; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REGULATORY T LYMPHOCYTE; STREPTOCOCCUS PNEUMONIA; UPREGULATION; ANIMAL; CBA MOUSE; COMBINATION DRUG THERAPY; COMMUNITY ACQUIRED INFECTION; CYTOTOXIC T LYMPHOCYTE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; LUNG ALVEOLUS MACROPHAGE; MICROBIOLOGY; MORTALITY; PATHOGENICITY; PATHOLOGY; PNEUMONIA, PNEUMOCOCCAL; STREPTOCOCCUS PNEUMONIAE; SURVIVAL ANALYSIS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, CD11B; ANTIGENS, CD11C; ANTIGENS, CD86; AZITHROMYCIN; BACTERIAL LOAD; CEFTRIAXONE; COMMUNITY-ACQUIRED INFECTIONS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DRUG THERAPY, COMBINATION; FEMALE; GENE EXPRESSION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED CBA; NEUTROPHILS; PNEUMONIA, PNEUMOCOCCAL; PROGRAMMED CELL DEATH 1 RECEPTOR; STREPTOCOCCUS PNEUMONIAE; SURVIVAL ANALYSIS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84992752900     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01024-16     Document Type: Article

References (44)

1. Kovaleva A, Remmelts HH, Rijkers GT, Hoepelman AI, Biesma DH, Oosterheert JJ. 2012. Immunomodulatory effects of macrolides during community-acquired pneumonia: a literature review. J Antimicrob Chemother 67:530-540. http://dx.doi.org/10.1093/jac/dkr520.
2. Caballero J, Rello J. 2011. Combination antibiotic therapy for community- acquired pneumonia. Ann Intensive Care 1:48. http://dx.doi.org/10 .1186/2110-5820-1-48.
3. Mandell LA, Wunderink RG, Anzueto A, Bartlett JG, Campbell GD, Dean NC, Dowell SF, File TM, Jr, Musher DM, Niederman MS, Torres A, Whitney CG. 2007. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of communityacquired pneumonia in adults. Clin Infect Dis 44(Suppl):S27-S72. http: //dx.doi.org/10.1086/511159.
4. Miyashita N, Matsushima T, Oka M, Japanese Respiratory Society. 2006. The JRS guidelines for the management of community-acquired pneumonia in adults: an update and new recommendations. Intern Med 45:419-428. http://dx.doi.org/10.2169/internalmedicine.45.1691.
5. Woodhead M, Blasi F, Ewig S, Garau J, Huchon G, Ieven M, Ortqvist A, Schaberg T, Torres A, van der Heijden G, Read R, Verheij TJ. 2011. Guidelines for the management of adult lower respiratory tract infections- summary. Clin Microbiol Infect 17(Suppl):S1-S24. http://dx.doi .org/10.1111/j.1469-0691.2011.03602.x.
6. Rodrigo C, McKeever TM, Woodhead M, Lim WS. 2013. Single versus combination antibiotic therapy in adults hospitalised with community acquired pneumonia. Thorax 68:493-495. http://dx.doi.org/10.1136 /thoraxjnl-2012-202296.
7. Metersky ML, Ma A, Houck PM, Bratzler DW. 2007. Antibiotics for bacteremic pneumonia: improved outcomes with macrolides but not fluoroquinolones. Chest 131:466-473. http://dx.doi.org/10.1378/chest .06-1426.
8. Restrepo MI, Mortensen EM, Waterer GW, Wunderink RG, Coalson JJ, Anzueto A. 2009. Impact of macrolide therapy on mortality for patients with severe sepsis due to pneumonia. Eur Respir J 33:153-159. http://dx .doi.org/10.1183/09031936.00054108.
9. Martin-Loeches I, Lisboa T, Rodriguez A, Putensen C, Annane D, Garnacho-Montero J, Restrepo MI, Rello J. 2010. Combination antibiotic therapy with macrolides improves survival in intubated patients with community-acquired pneumonia. Intensive Care Med 36:612-620. http: //dx.doi.org/10.1007/s00134-009-1730-y.
10. Saiman L, Marshall BC, Mayer-Hamblett N, Burns JL, Quittner AL, Cibene DA, Coquillette S, Fieberg AY, Accurso FJ, Campbell PW, III. 2003. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA 290: 1749-1756. http://dx.doi.org/10.1001/jama.290.13.1749.
11. Hansen CR, Pressler T, Koch C, Høiby N. 2005. Long-term azitromycin treatment of cystic fibrosis patients with chronic Pseudomonas aeruginosa infection; an observational cohort study. J Cyst Fibros 4:35-40. http://dx .doi.org/10.1016/j.jcf.2004.09.001.
12. Fujii T, Kadota J, Kawakami K, Iida K, Shirai R, Kaseda M, Kawamoto S, Kohno S. 1995. Long term effect of erythromycin therapy in patients with chronic Pseudomonas aeruginosa infection. Thorax 50:1246-1252. http://dx.doi.org/10.1136/thx.50.12.1246.
13. Sharma P, Allison JP. 2015. The future of immune checkpoint therapy. Science 348:56-61. http://dx.doi.org/10.1126/science.aaa8172.
14. Weber J. 2010. Immune checkpoint proteins: a new therapeutic paradigm for cancer-preclinical background: CTLA-4 and PD-1 blockade. Semin Oncol 37:430-439. http://dx.doi.org/10.1053/j.seminoncol.2010.09.005.
15. Ceeraz S, Nowak EC, Noelle RJ. 2013. B7 family checkpoint regulators in immune regulation and disease. Trends Immunol 34:556-563. http://dx .doi.org/10.1016/j.it.2013.07.003.
16. Frazier WJ, Hall MW. 2008. Immunoparalysis and adverse outcomes from critical illness. Pediatr Clin NorthAm55:647-668. http://dx.doi.org /10.1016/j.pcl.2008.02.009.
17. Anas AA, Wiersinga WJ, de Vos AF, van der Poll T. 2010. Recent insights into the pathogenesis of bacterial sepsis. Neth J Med 68:147-152.
18. Tateda K, Takashima K, Miyazaki H, Matsumoto T, Hatori T, Yamaguchi K. 1996. Noncompromised penicillin-resistant pneumococcal pneumonia CBA/J mouse model and comparative efficacies of antibiotics in this model. Antimicrob Agents Chemother 40:1520-1525.
19. Takashima K, Tateda K, Matsumoto T, IIzawa Y, Nakao M, Yamaguchi K. 1997. Role of tumor necrosis factor alpha in pathogenesis of pneumococcal pneumonia in mice. Infect Immun 65:257-260.
20. Clinical and Laboratory Standards Institute. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically-9th ed. CLSI document M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
21. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 52:1. http://dx.doi.org/10.1093 /jac/dkg301.
22. Wang E, Bergeron Y, Bergeron MG. 2005. Ceftriaxone pharmacokinetics in interleukin-10-treated murine pneumococcal pneumonia. J Antimicrob Chemother 55:721-726. http://dx.doi.org/10.1093/jac/dki085.
23. Conte JE, Jr, Golden J, Duncan S, McKenna E, Lin E, Zurlinden E. 1996. Single-dose intrapulmonary pharmacokinetics of azithromycin, clarithromycin, ciprofloxacin, and cefuroxime in volunteer subjects. Antimicrob Agents Chemother 40:1617-1622.
24. Hoffmann N, Lee B, Hentzer M, Rasmussen TB, Song Z, Johansen HK, Givskov M, Høiby N. 2007. Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr(-/-) mice. Antimicrob Agents Chemother 51:3677-3687. http://dx.doi.org/10.1128/AAC .01011-06.
25. Zaynagetdinov R, Sherrill TP, Kendall PL, Segal BH, Weller KP, Tighe RM, Blackwell TS. 2013. Identification of myeloid cell subsets in murine lungs using flow cytometry. Am J Respir Cell Mol Biol 49:180-189. http: //dx.doi.org/10.1165/rcmb.2012-0366MA.
26. Hall JD, Woolard MD, Gunn BM, Craven RR, Taft-Benz S, Frelinger JA, Kawula TH. 2008. Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis Schu S4, LVS, or U112. Infect Immun 76:5843-5852. http://dx.doi.org/10.1128 /IAI.01176-08.
27. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83:64-70.
28. Condon TV, Sawyer RT, Fenton MJ, Riches DW. 2011. Lung dendritic cells at the innate-adaptive immune interface. J Leukoc Biol 90:883-895. http://dx.doi.org/10.1189/jlb.0311134.
29. Catalfamo M, Tai X, Karpova T, McNally J, Henkart PA. 2008. TcRinduced regulated secretion leads to surface expression of CTLA-4 in CD4 CD25 T cells. Immunology 125:70-79. http://dx.doi.org/10.1111 /j.1365-2567.2008.02822.x.
30. Lu Y, Schneider H, Rudd CE. 2012. Murine regulatory T cells differ from conventional T cells in resisting the CTLA-4 reversal of TCR stop-signal. Blood 120:4560-4570. http://dx.doi.org/10.1182/blood -2012-04-421420.
31. Drago L, Nicola L, Rodighiero V, Larosa M, Mattina R, De Vecchi E. 2011. Comparative evaluation of synergy of combinations of beta-lactams with fluoroquinolones or a macrolide in Streptococcus pneumoniae. J Antimicrob Chemother 66:845-849. http://dx.doi.org/10.1093/jac/dkr016.
32. Lin E, Stanek RJ, Mufson MA. 2003. Lack of synergy of erythromycin combined with penicillin or cefotaxime against Streptococcus pneumoniae in vitro. Antimicrob Agents Chemother 47:1151-1153. http://dx.doi.org /10.1128/AAC.47.3.1151-1153.2003.
33. Kirby AC, Raynes JG, Kaye PM. 2006. CD11b regulates recruitment of alveolar macrophages but not pulmonary dendritic cells after pneumococcal challenge. J Infect Dis 193:205-213. http://dx.doi.org/10.1086 /498874.
34. Poole JA, Gleason AM, Bauer C, West WW, Alexis N, van Rooijen N, Reynolds SJ, Romberger DJ, Kielian TL. 2012. CD11c/CD11b cells are critical for organic dust-elicited murine lung inflammation. Am J Respir Cell Mol Biol 47:652-659. http://dx.doi.org/10.1165/rcmb.2012-0095OC.
35. Arikawa T, Saita N, Oomizu S, Ueno M, Matsukawa A, Katoh S, Kojima K, Nagahara K, Miyake M, Yamauchi A, Kohrogi H, Hirashima M. 2010. Galectin-9 expands immunosuppressive macrophages to ameliorate T-cell-mediated lung inflammation. Eur J Immunol 40:548-558. http: //dx.doi.org/10.1002/eji.200939886.
36. GeurtsvanKessel CH, Willart MA, Bergen IM, van Rijt LS, Muskens F, Elewaut D, Osterhaus AD, Hendriks R, Rimmelzwaan GF, Lambrecht BN. 2009. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J Exp Med 206: 2339-2349. http://dx.doi.org/10.1084/jem.20090410
37. Osterholzer JJ, Curtis JL, Polak T, Ames T, Chen GH, McDonald R, Huffnagle GB, Toews GB. 2008. CCR2 mediates conventional dendritic cell recruitment and formation of bronchovascular mononuclear cell infiltrates in the lungs of mice infected with Cryptococcus neoformans. J Immunol 181:610-620. http://dx.doi.org/10.4049/jimmunol.181.1.610.
38. Nie W, Li B, Xiu Q. 2014. Beta-lactam/macrolide dual therapy versus beta-lactam monotherapy for the treatment of community-acquired pneumonia in adults: a systematic review and meta-analysis. J Antimicrob Chemother 69:1441-1446. http://dx.doi.org/10.1093/jac/dku033.
39. Lodise TP, Kwa A, Cosler L, Gupta R, Smith RP. 2007. Comparison of beta-lactam and macrolide combination therapy versus fluoroquinolone monotherapy in hospitalized Veterans Affairs patients with communityacquired pneumonia. Antimicrob Agents Chemother 51:3977-3982. http: //dx.doi.org/10.1128/AAC.00006-07.
40. Chang KC, Burnham CA, Compton SM, Rasche DP, Mazuski RJ, McDonough JS, Unsinger J, Korman AJ, Green JM, Hotchkiss RS. 2013. Blockade of the negative co-stimulatory molecules PD-1 and CTLA-4 improves survival in primary and secondary fungal sepsis. Crit Care 17:R85. http://dx.doi.org/10.1186/cc12711.
41. Risso K, Kumar G, Ticchioni M, Sanfiorenzo C, Dellamonica J, Guillouet-de Salvador F, Bernardin G, Marquette CH, Roger PM. 2015. Early infectious acute respiratory distress syndrome is characterized by activation and proliferation of alveolar T-cells. Eur J Clin Microbiol Infect Dis 34:1111-1118. http://dx.doi.org/10.1007/s10096-015-2333-x.
42. Guignant C, Lepape A, Huang X, Kherouf H, Denis L, Poitevin F, Malcus C, Cheron A, Allaouchiche B, Gueyffier F, Ayala A, Monneret G, Venet F. 2011. Programmed death-1 levels correlate with increased mortality, nosocomial infection and immune dysfunctions in septic shock patients. Crit Care 15:R99. http://dx.doi.org/10.1186/cc10112.
43. Brahmamdam P, Inoue S, Unsinger J, Chang KC, McDunn JE, Hotchkiss RS. 2010. Delayed administration of anti-PD-1 antibody reverses immune dysfunction and improves survival during sepsis. J Leukoc Biol 88:233-240. http://dx.doi.org/10.1189/jlb.0110037.
44. Fukuda Y, Yanagihara K, Higashiyama Y, Miyazaki Y, Hirakata Y, Mukae H, Tomono K, Mizuta Y, Tsukamoto K, Kohno S. 2006. Effects of macrolides on pneumolysin of macrolide-resistant Streptococcus pneumoniae. Eur Respir J 27:1020-1025.