New therapeutic approaches for treatment of tularaemia: A review

Frontiers in Cellular and Infection Microbiology

Volumn 5, Issue MAR, 2014, Pages

  Boisset, Sandrine ^a,b,c   Caspar, Yvan ^a,b,c   Sutera, Vivien ^a,b,c   Maurin, Max ^a,b,c  

^a GRENOBLE UNIVERSITY HOSPITAL   (France)

^b UNIV GRENOBLE ALPES   (France)

^c CNRS   (France)

Author keywords

Antibiotics; Antibodie; Immunotherapy; Treatment; Tularaemia

Indexed keywords

ANTISERUM; CEFTRIAXONE; CIPROFLOXACIN; CPG OLIGODEOXYNUCLEOTIDE; DOXYCYCLINE; GALANTAMINE; GATIFLOXACIN; GENTAMICIN; GREPAFLOXACIN; IMMUNOGLOBULIN; INTERLEUKIN 12; KETOLIDE; LEVOFLOXACIN; LINEZOLID; MONOCLONAL ANTIBODY; OROSOMUCOID; POLYINOSINIC POLYCYTIDYLIC ACID; POLYPEPTIDE ANTIBIOTIC AGENT; POLYSACCHARIDE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SPARFLOXACIN; STREPTOMYCIN; TIGECYCLINE; TROVAFLOXACIN; AMINOGLYCOSIDE ANTIBIOTIC AGENT; AZITHROMYCIN; BETA LACTAM ANTIBIOTIC; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CEPHALOSPORIN; CETHROMYCIN; CHLORAMPHENICOL; ERYTHROMYCIN; GLYCYLCYCLINE DERIVATIVE; MACROLIDE; MOXIFLOXACIN; TELITHROMYCIN; TETRACYCLINE; UNINDEXED DRUG; ANTIBIOTIC AGENT; ANTIBODY; ANTIINFECTIVE AGENT;

CPG ISLAND; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG DELIVERY SYSTEM; DRUG MECHANISM; FRANCISELLA TULARENSIS; IMMUNE RESPONSE; IMMUNOMODULATION; LYMPHADENOPATHY; NATURAL KILLER CELL; NONHUMAN; RECURRENCE RISK; REVIEW; SYSTEMIC DISEASE; TULAREMIA; APOPTOSIS; GEOGRAPHIC DISTRIBUTION; HUMAN; IMMUNIZATION; IMMUNOTHERAPY; INNATE IMMUNITY; MINIMUM INHIBITORY CONCENTRATION; MORTALITY; SIGNAL TRANSDUCTION; ANIMAL; ANTIBIOTIC PROPHYLAXIS; DRUG DEVELOPMENT; DRUG EFFECT; METHODOLOGY; TREATMENT;

ANTIBIOTICS; ANTIBODIES; IMMUNOTHERAPY; TREATMENT; TULARAEMIA;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBIOTIC PROPHYLAXIS; DRUG DISCOVERY; FRANCISELLA TULARENSIS; HUMANS; IMMUNOTHERAPY; TULAREMIA;

EID: 84898046808     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2014.00040     Document Type: Review

References (70)

1. Antunes, N. T., Frase, H., Toth, M., and Vakulenko, S. B. (2012). The class A beta-lactamase FTU-1 is native to Francisella tularensis. Antimicrob. Agents Chemother. 56, 666-671. doi: 10.1128/AAC.05305-11
2. Aranda, E. A. (2001). Treatment of tularemia with levofloxacin. Clin. Microbiol. Infect. 7, 167-168. doi: 10.1046/j.1469-0691.2001.00234.x
3. Barlow, P. G., Svoboda, P., Mackellar, A., Nash, A. A., York, I. A., Pohl, J., et al. (2011). Antiviral activity and increased host defense against influenza infection elicited by the human cathelicidin LL-37. PLoS ONE 6:e25333. doi: 10.1371/journal.pone.0025333
4. Bosio, C. M., Bielefeldt-Ohmann, H., and Belisle, J. T. (2007). Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J. Immunol. 178, 4538-4547.
5. Celebi, G., Baruonu, F., Ayoglu, F., Cinar, F., Karadenizli, A., Ugur, M. B., et al. (2006). Tularemia, a reemerging disease in northwest Turkey: epidemiological investigation and evaluation of treatment responses. Jpn. J. Infect. Dis. 59, 229-234.
6. Chitadze, N., Kuchuloria, T., Clark, D. V., Tsertsvadze, E., Chokheli, M., Tsertsvadze, N., et al. (2009). Water-borne outbreak of oropharyngeal and glandular tularemia in Georgia: investigation and follow-up. Infection 37, 514-521. doi: 10.1007/s15010-009-8193-5
7. Conley, J., Yang, H., Wilson, T., Blasetti, K., Di Ninno, V., Schnell, G., et al. (1997). Aerosol delivery of liposome-encapsulated ciprofloxacin: aerosol characterization and efficacy against Francisella tularensis infection in mice. Antimicrob. Agents Chemother. 41, 1288-1292.
8. Cowley, S. C., and Elkins, K. L. (2011). Immunity to francisella. Front. Microbiol. 2:26. doi: 10.3389/fmicb.2011.00026
9. Cross, J. T., and Jacobs, R. F. (1993). Tularemia: treatment failures with outpatient use of ceftriaxone. Clin. Infect. Dis. 17, 976-980. doi: 10.1093/clinids/17.6.976
10. Crown, J., Jakubowski, A., Kemeny, N., Gordon, M., Gasparetto, C., Wong, G., et al. (1991). A phase I trial of recombinant human interleukin-1 beta alone and in combination with myelosuppressive doses of 5-fluorouracil in patients with gastrointestinal cancer. Blood 78, 1420-1427.
11. D'Elia, R. V., Harrison, K., Oyston, P. C., Lukaszewski, R. A., and Clark, G. C. (2013). Targeting the "cytokine storm" for therapeutic benefit. Clin. Vaccine Immunol. 20, 319-327. doi: 10.1128/CVI.00636-12
12. Dentan, C., Pavese, P., Pelloux, I., Boisset, S., Brion, J. P., Stahl, J. P., et al. (2013). Treatment of tularemia in pregnant woman, France. Emerging Infect. Dis. 19, 996-998. doi: 10.3201/eid1906.130138
13. Elkins, K. L., Colombini, S. M., Krieg, A. M., and De Pascalis, R. (2009). NK cells activated in vivo by bacterial DNA control the intracellular growth of Francisella tularensis LVS. Microbes Infect. 11, 49-56. doi: 10.1016/j.micinf.2008.10.005
14. Elkins, K. L., Cowley, S. C., and Bosio, C. M. (2007). Innate and adaptive immunity to Francisella. Ann. N.Y. Acad. Sci. 1105, 284-324. doi: 10.1196/annals.1409.014
15. Elkins, K. L., Rhinehart-Jones, T. R., Stibitz, S., Conover, J. S., and Klinman, D. M. (1999). Bacterial DNA containing CpG motifs stimulates lymphocyte-dependent protection of mice against lethal infection with intracellular bacteria. J. Immunol. 162, 2291-2298.
16. Ellis, J., Oyston, P. C., Green, M., and Titball, R. W. (2002). Tularemia. Clin. Microbiol. Rev. 15, 631-646. doi: 10.1128/CMR.15.4.631-646.2002
17. Enderlin, G., Morales, L., Jacobs, R. F., and Cross, J. T. (1994). Streptomycin and alternative agents for the treatment of tularemia: review of the literature. Clin. Infect. Dis. 19, 42-47. doi: 10.1093/clinids/19.1.42
18. Evans, M. E., Gregory, D. W., Schaffner, W., and McGee, Z. A. (1985). Tularemia: a 30-year experience with 88 cases. Medicine (Baltimore) 64, 251-269. doi: 10.1097/00005792-198507000-00006
19. Flick-Smith, H. C., Fox, M. A., Hamblin, K. A., Richards, M. I., Jenner, D. C., Laws, T. R., et al. (2013). Assessment of antimicrobial peptide LL-37 as a post-exposure therapy to protect against respiratory tularemia in mice. Peptides 43, 96-101. doi: 10.1016/j.peptides.2013.02.024
20. Garcia del Blanco, N., Gutierrez Martin, C. B., de la Puente Redondo, V. A., and Rodriguez Ferri, E. F. (2004). In vitro susceptibility of field isolates of Francisella tularensis subsp. holarctica recovered in Spain to several antimicrobial agents. Res. Vet. Sci. 76, 195-198. doi: 10.1016/j.rvsc.2003.12.002
21. Georgi, E., Schacht, E., Scholz, H. C., and Splettstoesser, W. D. (2012). Standardized broth microdilution antimicrobial susceptibility testing of Francisella tularensis subsp. holarctica strains from Europe and rare Francisella species. J. Antimicrob. Chemother. 67, 2429-2433. doi: 10.1093/jac/dks238
22. Gestin, B., Valade, E., Thibault, F., Schneider, D., and Maurin, M. (2010). Phenotypic and genetic characterization of macrolide resistance in Francisella tularensis subsp. holarctica biovar I. J. Antimicrob. Chemother. 65, 2359-2367. doi: 10.1093/jac/dkq315
23. Gill, V., and Cunha, B. A. (1997). Tularemia pneumonia. Semin. Respir. Infect. 12, 61-67.
24. Kirimanjeswara, G. S., Golden, J. M., Bakshi, C. S., and Metzger, D. W. (2007). Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J. Immunol. 179, 532-539.
25. Hallaj-Nezhadi, S., and Hassan, M. (2013). Nanoliposome-based antibacterial drug delivery. Drug Deliv. doi: 10.3109/10717544.2013.863409. [Epub ahead of print].
26. Hammerschlag, M. R., and Sharma, R. (2008). Use of cethromycin, a new ketolide, for treatment of community-acquired respiratory infections. Expert Opin. Investig. Drugs 17, 387-400. doi: 10.1517/13543784.17.3.387
27. Hauri, A. M., Hofstetter, I., Seibold, E., Kaysser, P., Eckert, J., Neubauer, H., et al. (2010). Investigating an airborne tularemia outbreak, Germany. Emerging Infect. Dis. 16, 238-243. doi: 10.3201/eid1602.081727
28. Hepburn, M. J., and Simpson, A. J. (2008). Tularemia: current diagnosis and treatment options. Expert Rev. Anti Infect. Ther. 6, 231-240. doi: 10.1586/14787210.6.2.231
29. Ikaheimo, I., Syrjala, H., Karhukorpi, J., Schildt, R., and Koskela, M. (2000). In vitro antibiotic susceptibility of Francisella tularensis isolated from humans and animals. J. Antimicrob. Chemother. 46, 287-290. doi: 10.1093/jac/46.2.287
30. Into, T., Inomata, M., Shibata, K., and Murakami, Y. (2010). Effect of the antimicrobial peptide LL-37 on Toll-like receptors 2-, 3-and 4-triggered expression of IL-6, IL-8 and CXCL10 in human gingival fibroblasts. Cell. Immunol. 264, 104-109. doi: 10.1016/j.cellimm.2010.05.005
31. Johansson, A., Urich, S. K., Chu, M. C., Sjostedt, A., and Tarnvik, A. (2002). In vitro susceptibility to quinolones of Francisella tularensis subspecies tularensis. Scand. J. Infect. Dis. 34, 327-330. doi: 10.1080/00365540110080773
32. Kirimanjeswara, G. S., Olmos, S., Bakshi, C. S., and Metzger, D. W. (2008). Humoral and cell-mediated immunity to the intracellular pathogen Francisella tularensis. Immunol. Rev. 225, 244-255. doi: 10.1111/j.1600-065X.2008.00689.x
33. Klimpel, G. R., Eaves-Pyles, T., Moen, S. T., Taormina, J., Peterson, J. W., Chopra, A. K., et al. (2008). Levofloxacin rescues mice from lethal intra-nasal infections with virulent Francisella tularensis and induces immunity and production of protective antibody. Vaccine 26, 6874-6882. doi: 10.1016/j.vaccine.2008.09.077
34. Kosker, M., Sener, D., Kilic, O., Akil, F., Yilmaz, M., Ozturk, O., et al. (2013). A case of oculoglandular tularemia resistant to medical treatment. Scand. J. Infect. Dis. 45, 725-727. doi: 10.3109/00365548.2013.796089
35. Kreizinger, Z., Hornok, S., Dan, A., Hresko, S., Makrai, L., Magyar, T., et al. (2013a). Prevalence of Francisella tularensis and francisella-like endosymbionts in the tick population of hungary and the genetic variability of francisella-like agents. Vector Borne Zoonotic Dis. 13, 160-163. doi: 10.1089/vbz.2012.1065
36. Kreizinger, Z., Makrai, L., Helyes, G., Magyar, T., Erdelyi, K., and Gyuranecz, M. (2013b). Antimicrobial susceptibility of Francisella tularensis subsp. holarctica strains from Hungary, Central Europe. J. Antimicrob. Chemother. 68, 370-373. doi: 10.1093/jac/dks399
37. Kudelina, R. I., and Olsufiev, N. G. (1980). Sensitivity to macrolide antibiotics and lincomycin in Francisella tularensis holarctica. J. Hyg. Epidemiol. Microbiol. Immunol. 24, 84-91.
38. KuoLee, R., and Chen, W. (2007). Vaccines and therapeutic agents for tularemia. Expert Opin. Ther. Patents 17, 267-275. doi: 10.1517/13543776.17.3.267
39. Larsson, P., Oyston, P. C., Chain, P., Chu, M. C., Duffield, M., Fuxelius, H. H., et al. (2005). The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat. Genet. 37, 153-159. doi: 10.1038/ng1499
40. Lembo, A., Pelletier, M., Iyer, R., Timko, M., Dudda, J. C., West, T. E., et al. (2008). Administration of a synthetic TLR4 agonist protects mice from pneumonic tularemia. J. Immunol. 180, 7574-7581.
41. Li, J., Lv, C., Sun, W., Li, Z., Han, X., Li, Y., and Shen, Y. (2013). Cytosporone B, an inhibitor of the type III secretion system of Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother. 57, 2191-2198. doi: 10.1128/AAC.02421-12
42. Limaye, A. P., and Hooper, C. J. (1999). Treatment of tularemia with fluoroquinolones: two cases and review. Clin. Infect. Dis. 29, 922-924. doi: 10.1086/520458
43. Liu, Z. H., Ma, Y. F., Wu, J. S., Gan, J. X., Xu, S. W., and Jiang, G. Y. (2010). Effect of cholinesterase inhibitor galanthamine on circulating tumor necrosis factor alpha in rats with lipopolysaccharide-induced peritonitis. Chin. Med. J. 123, 1727-1730.
44. Lu, Z., Roche, M. I., Hui, J. H., Unal, B., Felgner, P. L., Gulati, S., et al. (2007). Generation and characterization of hybridoma antibodies for immunotherapy of tularemia. Immunol. Lett. 112, 92-103. doi: 10.1016/j.imlet.2007.07.006
45. Maurin, M., Mersali, N. F., and Raoult, D. (2000). Bactericidal activities of antibiotics against intracellular Francisella tularensis. Antimicrob. Agents Chemother. 44, 3428-3431. doi: 10.1128/AAC.44.12.3428-3431.2000
46. Maurin, M., Pelloux, I., Brion, J. P., Del Bano, J. N., and Picard, A. (2011). Human tularemia in France, 2006-2010. Clin. Infect. Dis. 53, e133-e141. doi: 10.1093/cid/cir612
47. Meric, M., Willke, A., Finke, E. J., Grunow, R., Sayan, M., Erdogan, S., et al. (2008). Evaluation of clinical, laboratory, and therapeutic features of 145 tularemia cases: the role of quinolones in oropharyngeal tularemia. APMIS 116, 66-73. doi: 10.1111/j.1600-0463.2008.00901.x
48. Nelson, M., Lever, M. S., Dean, R. E., Pearce, P. C., Stevens, D. J., and Simpson, A. J. (2010). Bioavailability and efficacy of levofloxacin against Francisella tularensis in the common marmoset (Callithrix jacchus). Antimicrob Agents Chemother 54, 3922-3926. doi: 10.1128/AAC.00390-10
49. Scott, M. G., Davidson, D. J., Gold, M. R., Bowdish, D., and Hancock, R. E. (2002). The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol. 169, 3883-3891.
50. Pammit, M. A., Budhavarapu, V. N., Raulie, E. K., Klose, K. E., Teale, J. M., and Arulanandam, B. P. (2004). Intranasal interleukin-12 treatment promotes antimicrobial clearance and survival in pulmonary Francisella tularensis subsp. novicida infection. Antimicrob. Agents Chemother. 48, 4513-4519. doi: 10.1128/AAC.48.12.4513-4519.2004
51. Pankey, G. A. (2005). Tigecycline. J. Antimicrob. Chemother. 56, 470-480. doi: 10.1093/jac/dki248
52. Penn, R. L., and Kinasewitz, G. T. (1987). Factors associated with a poor outcome in tularemia. Arch. Intern. Med. 147, 265-268. doi: 10.1001/archinte.1987.00370020083041
53. Perez-Castrillon, J. L., Bachiller-Luque, P., Martin-Luquero, M., Mena-Martin, F. J., and Herreros, V. (2001). Tularemia epidemic in northwestern Spain: clinical description and therapeutic response. Clin. Infect. Dis. 33, 573-576. doi: 10.1086/322601
54. Piercy, T., Steward, J., Lever, M. S., and Brooks, T. J. (2005). In vivo efficacy of fluoroquinolones against systemic tularemia infection in mice. J. Antimicrob. Chemother. 56, 1069-1073. doi: 10.1093/jac/dki359
55. Pohanka, M., Pavlis, O., and Pikula, J. (2012). Galantamine effect on tularemia pathogenesis in a BALB/c mouse model. Iran. Biomed. J. 16, 156-161.
56. Pyles, R. B., Jezek, G. E., and Eaves-Pyles, T. D. (2010). Toll-like receptor 3 agonist protection against experimental Francisella tularensis respiratory tract infection. Infect. Immun. 78, 1700-1710. doi: 10.1128/IAI.00736-09
57. Rozak, D. A., Gelhaus, H. C., Smith, M., Zadeh, M., Huzella, L., Waag, D., et al. (2010). CpG oligodeoxyribonucleotides protect mice from Burkholderia pseudomallei but not Francisella tularensis Schu S4 aerosols. J. Immune Based Ther. Vaccines 8:2. doi: 10.1186/1476-8518-8-2
58. Savitt, A. G., Mena-Taboada, P., Monsalve, G., and Benach, J. L. (2009). Francisella tularensis infection-derived monoclonal antibodies provide detection, protection, and therapy. Clin. Vaccine Immunol. 16, 414-422. doi: 10.1128/CVI.00362-08
59. Scheel, O., Hoel, T., Sandvik, T., and Berdal, B. P. (1993). Susceptibility pattern of Scandinavian Francisella tularensis isolates with regard to oral and parenteral antimicrobial agents. APMIS 101, 33-36. doi: 10.1111/j.1699-0463.1993.tb00077.x
60. Skyberg, J. A. (2013). Immunotherapy for tularemia. Virulence 4, 859-870. doi: 10.1371/journal.ppat.1002587
61. Skyberg, J. A., Rollins, M. F., Holderness, J. S., Marlenee, N. L., Schepetkin, I. A., Goodyear, A., et al. (2012). Nasal Acai polysaccharides potentiate innate immunity to protect against pulmonary Francisella tularensis and Burkholderia pseudomallei Infections. PLoS Pathog. 8:e1002587. doi: 10.1371/journal.ppat.1002587
62. Steward, J., Piercy, T., Lever, M. S., Simpson, A. J., and Brooks, T. J. (2006). Treatment of murine pneumonic Francisella tularensis infection with gatifloxacin, moxifloxacin or ciprofloxacin. Int. J. Antimicrob. Agents 27, 439-443. doi: 10.1016/j.ijantimicag.2006.02.006
63. Sutera, V., Levert, M., Burmeister, W. P., Schneider, D., and Maurin, M. (2014). Evolution toward high-level fluoroquinolone resistance in Francisella species. J. Antimicrob. Chemother. 69, 101-110. doi: 10.1093/jac/dkt321
64. Sutherland, M. D., Goodyear, A. W., Troyer, R. M., Chandler, J. C., Dow, S. W., and Belisle, J. T. (2012). Post-exposure immunization against Francisella tularensis membrane proteins augments protective efficacy of gentamicin in a mouse model of pneumonic tularemia. Vaccine 30, 4977-4982. doi: 10.1016/j.vaccine.2012.05.037
65. Syrjala, H., Schildt, R., and Raisainen, S. (1991). In vitro susceptibility of Francisella tularensis to fluoroquinolones and treatment of tularemia with norfloxacin and ciprofloxacin. Eur. J. Clin. Microbiol. Infect. Dis. 10, 68-70. doi: 10.1007/BF01964409
66. Tarnvik, A., and Chu, M. C. (2007). New approaches to diagnosis and therapy of tularemia. Ann. N.Y. Acad. Sci. 1105, 378-404. doi: 10.1196/annals.1409.017
67. Tomaso, H., Al Dahouk, S., Hofer, E., Splettstoesser, W. D., Treu, T. M., Dierich, M. P., et al. (2005). Antimicrobial susceptibilities of Austrian Francisella tularensis holarctica biovar II strains. Int. J. Antimicrob. Agents 26, 279-284. doi: 10.1016/j.ijantimicag.2005.07.003
68. Wong, J. P., Yang, H., Blasetti, K. L., Schnell, G., Conley, J., and Schofield, L. N. (2003). Liposome delivery of ciprofloxacin against intracellular Francisella tularensis infection. J. Control. Release 92, 265-273. doi: 10.1016/S0168-3659(03)00358-4
69. World Health Organisation. (2007). WHO Guidelines on Tularaemia. Geneva: World Health Organization.
70. Yesilyurt, M., Kilic, S., Celebi, B., Celik, M., Gul, S., Erdogan, F., et al. (2011). Antimicrobial susceptibilities of Francisella tularensis subsp. holarctica strains isolated from humans in the Central Anatolia region of Turkey. J. Antimicrob. Chemother. 66, 2588-2592. doi: 10.1093/jac/dkr338