Biofilm formation caused by clinical acinetobacter baumannii isolates is associated with overexpression of the AdeFGH efflux pump

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 8, 2015, Pages 4817-4825

  He, Xinlong ^a   Lu, Feng ^b   Yuan, Fenglai ^a   Jiang, Donglin ^a   Zhao, Peng ^a   Zhu, Jie ^a   Cheng, Huali ^a   Cao, Jun ^b,c   Lu, Guozhong ^a  

^a WUXI PEOPLE S HOSPITAL AFFILIATED TO NANJING MEDICAL UNIVERSITY   (China)

^b JIANGSU INSTITUTE OF PARASITIC DISEASES   (China)

^c JIANGNAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ABAI PROTEIN; ADEB PROTEIN; ADEFGH EFFLUX PUMP; ADEG PROTEIN; AMIKACIN; BACTERIAL PROTEIN; CARO PROTEIN; CEFTAZIDIME; GENTAMICIN; LEVOFLOXACIN; MEROPENEM; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN A; TETRACYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CARRIER PROTEIN;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTION; ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ARTICLE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BIOFILM; BURN INFECTION; BURN PATIENT; CHRONIC WOUND; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUORUM SENSING; WOUND INFECTION; ACINETOBACTER INFECTIONS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; PROCEDURES; UPREGULATION;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOFILMS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; QUORUM SENSING; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84939839310     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00877-15     Document Type: Article

References (49)

1. Fournier PE, Richet H. 2006. The epidemiology and control of Acinetobacter baumannii in health care facilities. Clin Infect Dis 42:692-699. http://dx.doi.org/10.1086/500202.
2. Mezzatesta ML, D'Andrea MM, Migliavacca R, Giani T, Gona F, Nucleo E, Fugazza G, Pagani L, Rossolini GM, Stefani S. 2012. Epidemiological characterization and distribution of carbapenem-resistant Acinetobacter baumannii clinical isolates in Italy. Clin Microbiol Infect 18:160-166. http://dx.doi.org/10.1111/j.1469-0691.2011.03527.x.
3. Cisneros JM, Reyes MJ, Pachon J, Becerril B, Caballero FJ, Garcia-Garmendia JL, Ortiz C, Cobacho AR. 1996. Bacteremia due to Acinetobacter baumannii: epidemiology, clinical findings, and prognostic features. Clin Infect Dis 22:1026-1032.
4. Chaari A, Mnif B, Bahloul M, Mahjoubi F, Chtara K, Turki O, Gharbi N, Chelly H, Hammami A, Bouaziz M. 2013. Acinetobacter baumannii ventilator-associated pneumonia: epidemiology, clinical characteristics, and prognosis factors. Int J Infect Dis 17:1225-1228. http://dx.doi.org/10.1016/j.ijid.2013.07.014.
5. Yang M, Hu Z, Hu F. 2012. Nosocomial meningitis caused by Acinetobacter baumannii: risk factors and their impact on patient outcomes and treatments. Future Microbiol 7:787-793. http://dx.doi.org/10.2217/fmb.12.42.
6. Gaynes R, Edwards JR, National Nosocomial Infections Surveillance System. 2005. Overview of nosocomial infections caused by Gramnegative bacilli. Clin Infect Dis 41:848-854. http://dx.doi.org/10.1086/432803.
7. Guerrero DM, Perez F, Conger NG, Solomkin JS, Adams MD, Rather PN, Bonomo RA. 2010. Acinetobacter baumannii-associated skin and soft tissue infections: recognizing a broadening spectrum of disease. Surg Infect (Larchmt) 11:49-57. http://dx.doi.org/10.1089/sur.2009.022.
8. Maragakis LL, Perl TM. 2008. Acinetobacter baumannii: epidemiology, antimicrobial resistance, and treatment options. Clin Infect Dis 46:1254-1263. http://dx.doi.org/10.1086/529198.
9. Durante-Mangoni E, Zarrilli R. 2011. Global spread of drug-resistant Acinetobacter baumannii: molecular epidemiology and management of antimicrobial resistance. Future Microbiol 6:407-422. http://dx.doi.org/10.2217/fmb.11.23.
10. Jain R, Danziger LH. 2004. Multidrug-resistant Acinetobacter infections: an emerging challenge to clinicians. Ann Pharmacother 38:1449-1459. http://dx.doi.org/10.1086/652759.
11. Dijkshoorn L, Nemec A, Seifert H. 2007. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol 5:939-951. http://dx.doi.org/10.1038/nrmicro1789.
12. Rodríguez-Baño J, Martí S, Soto S, Fernandez-Cuenca F, Cisneros JM, Pachon J, Pascual A, Martínez-Martínez L, McQueary C, Actis LA, Vila J, Spanish Group for the Study of Nosocomial Infections (GEIH). 2008. Biofilm formation in Acinetobacter baumannii: associated features and clinical implications. Clin Microbiol Infect 14:276-278. http://dx.doi.org/10.1111/j.1469-0691.2007.01916.x.
13. von Eiff C, Jansen B, Kohnen W, Becker K. 2005. Infections associated with medical devices: pathogenesis, management and prophylaxis. Drugs 65:179-214. http://dx.doi.org/10.2165/00003495-200565020-00003.
14. Kennedy P, Brammah S, Wills E. 2010. Burns, biofilm and a new appraisal of burn wound sepsis. Burns 36:49-56. http://dx.doi.org/10.1016/j.burns.2009.02.017.
15. Kaplan JB. 2011. Antibiotic-induced biofilm formation. Int J Artif Organs 34:737-751. http://dx.doi.org/10.5301/ijao.5000027.
16. Anbazhagan D, Mansor M, Yan GO, Md Yusof MY, Hassan H, Sekaran SD. 2012. Detection of quorum sensing signal molecules and identification of an autoinducer synthase gene among biofilm forming clinical isolates of Acinetobacter spp. PLoS One 7:e36696. http://dx.doi.org/10.1371/journal.pone.0036696.
17. Bhargava N, Sharma P, Capalash N. 2010. Quorum sensing in Acinetobacter: an emerging pathogen. Crit Rev Microbiol 36:349-360. http://dx.doi.org/10.3109/1040841X.2010.512269.
18. Smith MG, Gianoulis TA, Pukatzki S, Mekalanos JJ, Ornston LN, Gerstein M, Snyder M. 2007. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev 21:601-614. http://dx.doi.org/10.1101/gad.1510307.
19. Varga ZG, Armada A, Cerca P, Amaral L, Mior Ahmad Subki MA, Savka MA, Szegedi E, Kawase M, Motohashi N, Molnar J. 2012. Inhibition of quorum sensing and efflux pump system by trifluoromethyl ketone proton pump inhibitors. In Vivo 26:277-285.
20. Amaral L, Udwadia Z, Abbate E, van Soolingen D. 2012. The added effect of thioridazine in the treatment of drug-resistant tuberculosis. Int J Tuberc Lung Dis 16:1706-1708; author reply, 1708-1709. http://dx.doi.org/10.5588/ijtld.12.0616.
21. Chu YW, Chau SL, Houang ET. 2006. Presence of active efflux systems AdeABC, AdeDE and AdeXYZ in different Acinetobacter genomic DNA groups. J Med Microbiol 55:477-478. http://dx.doi.org/10.1099/jmm.0.46433-0.
22. Nemec A, Maixnerova M, van der Reijden TJ, van den Broek PJ, Dijkshoorn L. 2007. Relationship between the AdeABC efflux system gene content, netilmicin susceptibility and multidrug resistance in a genotypically diverse collection of Acinetobacter baumannii strains. J Antimicrob Chemother 60:483-489. http://dx.doi.org/10.1093/jac/dkm231.
23. Yoon EJ, Courvalin P, Grillot-Courvalin C. 2013. RND-type efflux pumps in multidrug-resistant clinical isolates of Acinetobacter baumannii: major role for AdeABC overexpression and AdeRS mutations. Antimicrob Agents Chemother 57:2989-2995. http://dx.doi.org/10.1128/AAC.02556-12.
24. Yap PS, Krishnan T, Yiap BC, Hu CP, Chan KG, Lim SH. 2014. Membrane disruption and anti-quorum sensing effects of synergistic interaction between Lavandula angustifolia (lavender oil) in combination with antibiotic against plasmid-conferred multi-drug-resistant Escherichia coli. J Appl Microbiol 116:1119-1128. http://dx.doi.org/10.1111/jam.12444.
25. Walzer G, Rosenberg E, Ron EZ. 2006. The Acinetobacter outer membrane protein A (OmpA) is a secreted emulsifier. Environ Microbiol 8:1026-1032. http://dx.doi.org/10.1111/j.1462-2920.2006.00994.x.
26. Versalovic J, Koeuth T, Lupski JR. 1991. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823-6831. http://dx.doi.org/10.1093/nar/19.24.6823.
27. Nei M, Li WH. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A76:5269-5273. http://dx.doi.org/10.1073/pnas.76.10.5269.
28. Clinical and Laboratory Standards Institute. 2007. Performance standards for antimicrobial susceptibility testing; approved standard. CLSI document M100-S15. Clinical and Laboratory Standards Institute, Wayne, PA.
29. Hawkey PM, Jones AM. 2009. The changing epidemiology of resistance. J Antimicrob Chemother 64(Suppl 1):i3-i10. http://dx.doi.org/10.1093/jac/dkp256.
30. Jamulitrat S, Arunpan P, Phainuphong P. 2009. Attributable mortality of imipenem-resistant nosocomial Acinetobacter baumannii blood stream infection. J Med Assoc Thai 92:413-419.
31. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
32. Stewart PS. 2002. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107-113. http://dx.doi.org/10.1078/1438-4221-00196.
33. Perez LR. 2014. Acinetobacter baumannii displays inverse relationship between meropenem resistance and biofilm production. J Chemother 27:13-16. http://dx.doi.org/10.1179/1973947813Y.0000000159.
34. Nucleo E, Steffanoni L, Fugazza G, Migliavacca R, Giacobone E, Navarra A, Pagani L, Landini P. 2009. Growth in glucose-based medium and exposure to subinhibitory concentrations of imipenem induce biofilm formation in a multidrug-resistant clinical isolate of Acinetobacter baumannii. BMC Microbiol 9:270. http://dx.doi.org/10.1186/1471-2180-9.270.
35. Linares JF, Gustafsson I, Baquero F, Martinez JL. 2006. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA103:19484-19489. http://dx.doi.org/10.1073/pnas.0608949103.
36. Boehm A, Steiner S, Zaehringer F, Casanova A, Hamburger F, Ritz D, Keck W, Ackermann M, Schirmer T, Jenal U. 2009. Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol 72:1500-1516. http://dx.doi.org/10.1111/j.1365-2958.2009.06739.x.
37. Sanchez CJ, Jr, Mende K, Beckius ML, Akers KS, Romano DR, Wenke JC, Murray CK. 2013. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 13:47. http://dx.doi.org/10.1186/1471-2334-13-47.
38. Espinal P, Marti S, Vila J. 2012. Effect of biofilm formation on the survival of Acinetobacter baumannii on dry surfaces. J Hosp Infect 80:56-60. http://dx.doi.org/10.1016/j.jhin.2011.08.013.
39. Kvist M, Hancock V, Klemm P. 2008. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl Environ Microbiol 74:7376-7382. http://dx.doi.org/10.1128/AEM.01310-08.
40. Mukherji R, Prabhune A. 2014. Novel glycolipids synthesized using plant essential oils and their application in quorum sensing inhibition and as antibiofilm agents. Sci World J 2014:890709. http://dx.doi.org/10.1155/2014/890709.
41. Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. 2007. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 51:3471-3484. http://dx.doi.org/10.1128/AAC.01464-06.
42. Rumbo C, Gato E, Lopez M, Ruiz de Alegria C, Fernandez-Cuenca F, Martinez-Martinez L, Vila J, Pachon J, Cisneros JM, Rodriguez-Bano J, Pascual A, Bou G, Tomas M, Spanish Group of Nosocomial Infections and Mehcanisms of Action and Resistance to Antimicrobials (GEIH-GEMARA), Spanish Society of Clinical Microbiology and Infectious Diseases (SEIMC), Spanish Network for Research in Infectious Diseases (REIPI). 2013. Contribution of efflux pumps, porins, and β-lactamases to multidrug resistance in clinical isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 57:5247-5257. http://dx.doi.org/10.1128/AAC.00730-13.
43. Damier-Piolle L, Magnet S, Bremont S, Lambert T, Courvalin P. 2008. AdeIJK, a resistance-nodulation-cell division pump effluxing multiple antibiotics in Acinetobacter baumannii. Antimicrob Agents Chemother 52:557-562. http://dx.doi.org/10.1128/AAC.00732-07.
44. Sugawara E, Nikaido H. 2012. OmpA is the principal nonspecific slow porin of Acinetobacter baumannii. J Bacteriol 194:4089-4096. http://dx.doi.org/10.1128/JB.00435-12.
45. Coyne S, Guigon G, Courvalin P, Perichon B. 2010. Screening and quantification of the expression of antibiotic resistance genes in Acinetobacter baumannii with a microarray. Antimicrob Agents Chemother 54:333-340. http://dx.doi.org/10.1128/AAC.01037-09.
46. Coyne S, Rosenfeld N, Lambert T, Courvalin P, Perichon B. 2010. Over-expression of resistance-nodulation-cell division pump AdeFGH confers multidrug resistance in Acinetobacter baumannii. Antimicrob Agents Chemother 54:4389-4393. http://dx.doi.org/10.1128/AAC.00155-10.
47. Fonseca EL, Scheidegger E, Freitas FS, Cipriano R, Vicente AC. 2013. Carbapenem-resistant Acinetobacter baumannii from Brazil: role of carO alleles expression and blaOXA-23 gene. BMC Microbiol 13:245. http://dx.doi.org/10.1186/1471-2180-13-245.
48. Beceiro A, Maharjan S, Gaulton T, Doumith M, Soares NC, Dhanji H, Warner M, Doyle M, Hickey M, Downie G, Bou G, Livermore DM, Woodford N. 2011. False extended-spectrum {beta}-lactamase phenotype in clinical isolates of Escherichia coli associated with increased expression of OXA-1 or TEM-1 penicillinases and loss of porins. J Antimicrob Chemother 66:2006-2010. http://dx.doi.org/10.1093/jac/dkr265.
49. th ed. Clinical and Laboratory Standards Institute, Wayne, PA.