Infect Chemother.  2014 Dec;46(4):226-238. 10.3947/ic.2014.46.4.226.

Clinical Importance and Epidemiology of Quinolone Resistance

• Kim ES
• Hooper DC

• KMID: 2170491
• DOI: http://doi.org/10.3947/ic.2014.46.4.226

Abstract

The quinolone class of antimicrobial agents is one of most widely used classes of antimicrobial agents in outpatient and inpatient treatment. However, quinolone resistance in gram-positive and gram-negative bacteria has emerged and increased globally. This resistance limits the usefulness of quinolones in clinical practice. The review summarizes mechanisms of quinolone resistance and its epidemiology and implications in the most common clinical settings, urinary tract infections, respiratory tract infections, intraabdominal infections, skin and skin structure infections, and sexually transmitted diseases.

Keyword

Quinolones; Drug resistance; Epidemiology; Mechanism; Clinical implications

MeSH Terms

Anti-Infective Agents
Drug Resistance
Epidemiology*
Gram-Negative Bacteria
Humans
Inpatients
Intraabdominal Infections
Outpatients
Quinolones
Respiratory Tract Infections
Sexually Transmitted Diseases
Skin
Urinary Tract Infections
Anti-Infective Agents
Quinolones

Reference

1. Hawkey PM. Mechanisms of quinolone action and microbial response. J Antimicrob Chemother. 2003; 51(Suppl 1):29–35. PMID: 12702701.

2. Jacoby GA. Mechanisms of resistance to quinolones. Clin Infect Dis. 2005; 41(Suppl 2):S120–S126. PMID: 15942878.

3. Hiasa H, Shea ME. DNA gyrase-mediated wrapping of the DNA strand is required for the replication fork arrest by the DNA gyrase-quinolone-DNA ternary complex. J Biol Chem. 2000; 275:34780–34786. PMID: 11053451.

4. Freifeld AG, Bow EJ, Sepkowitz KA, Boeckh MJ, Ito JI, Mullen CA, Raad II, Rolston KV, Young JA, Wingard JR. Infectious Diseases Society of America. Clinical practice guideline for the use of antimicrobial agents in neutropenic patients with cancer: 2010 Update by the Infectious Diseases Society of America. Clin Infect Dis. 2011; 52:427–431. PMID: 21205990.

5. Bratzler DW, Dellinger EP, Olsen KM, Perl TM, Auwaerter PG, Bolon MK, Fish DN, Napolitano LM, Sawyer RG, Slain D, Steinberg JP, Weinstein RA. American Society of Health-System Pharmacists. Infectious Disease Society of America. Surgical Infection Society. Society for Healthcare Epidemiology of America. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm. 2013; 70:195–283. PMID: 23327981.

6. Neuhauser MM, Weinstein RA, Rydman R, Danziger LH, Karam G, Quinn JP. Antibiotic resistance among gram-negative bacilli in US intensive care units: implications for fluoroquinolone use. JAMA. 2003; 289:885–888. PMID: 12588273.

7. Jun KI, Koo HL, Kim MK, Kang CK, Kim MJ, Chun SH, Song JS, Kim HS, Kim NJ, Kim EC, Oh MD. Trends in antibiotic use in a single university hospital. Korean J Nosocomial Infect Control. 2013; 18:44–50.

8. Thauvin-Eliopoulos C, Eliopoulos GM. Activity in vitro of the quinolones. In : Hooper DC, Rubinstein E, editors. Quinolone Antimicrobial Agents. 3rd ed. Washington, DC: American Society for Microbiology Press;2003. p. 91–111.

9. Hooper DC. Mechanism of quinolone resistance. In : Hooper DC, Rubinstein E, editors. Quinolone Antimicrobial Agents. 3rd ed. Washington, DC: American Society for Microbiology Press;2003. p. 41–67.

10. Yoshida H, Bogaki M, Nakamura M, Nakamura S. Quinolone resistance-determining region in the DNA gyrase gyrA gene of Escherichia coli. Antimicrob Agents Chemother. 1990; 34:1271–1272. PMID: 2168148.

11. Friedman SM, Lu T, Drlica K. Mutation in the DNA gyrase A gene of Escherichia coli that expands the quinolone resistance-determining region. Antimicrob Agents Chemother. 2001; 45:2378–2380. PMID: 11451702.

12. Barnard FM, Maxwell A. Interaction between DNA gyrase and quinolones: effects of alanine mutations at GyrA subunit residues Ser(83) and Asp(87). Antimicrob Agents Chemother. 2001; 45:1994–2000. PMID: 11408214.

13. Willmott CJ, Maxwell A. A single point mutation in the DNA gyrase A protein greatly reduces binding of fluoroquinolones to the gyrase-DNA complex. Antimicrob Agents Chemother. 1993; 37:126–127. PMID: 8381633.

14. Ng EY, Trucksis M, Hooper DC. Quinolone resistance mutations in topoisomerase IV: relationship to the flqA locus and genetic evidence that topoisomerase IV is the primary target and DNA gyrase is the secondary target of fluoroquinolones in Staphylococcus aureus. Antimicrob Agents Chemother. 1996; 40:1881–1888. PMID: 8843298.

15. Eliopoulos GM. Quinolone resistance mechanisms in pneumococci. Clin Infect Dis. 2004; 38(Suppl 4):S350–S356. PMID: 15127369.

16. Poole K. Efflux-mediated antimicrobial resistance. J Antimicrob Chemother. 2005; 56:20–51. PMID: 15914491.

17. Wang H, Dzink-Fox JL, Chen M, Levy SB. Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: role of acrR mutations. Antimicrob Agents Chemother. 2001; 45:1515–1521. PMID: 11302820.

18. Alekshun MN, Levy SB. Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob Agents Chemother. 1997; 41:2067–2075. PMID: 9333027.

19. Cohen SP, McMurry LM, Hooper DC, Wolfson JS, Levy SB. Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob Agents Chemother. 1989; 33:1318–1325. PMID: 2679373.

20. Thanassi DG, Cheng LW, Nikaido H. Active efflux of bile salts by Escherichia coli. J Bacteriol. 1997; 179:2512–2518. PMID: 9098046.

21. Zhanel GG, Hoban DJ, Schurek K, Karlowsky JA. Role of efflux mechanisms on fluoroquinolone resistance in Streptococcus pneumoniae and Pseudomonas aeruginosa. Int J Antimicrob Agents. 2004; 24:529–535. PMID: 15555873.

22. Kosmidis C, Schindler BD, Jacinto PL, Patel D, Bains K, Seo SM, Kaatz GW. Expression of multidrug resistance efflux pump genes in clinical and environmental isolates of Staphylococcus aureus. Int J Antimicrob Agents. 2012; 40:204–209. PMID: 22766161.

23. Kwak YG, Truong-Bolduc QC, Kim HB, Song KH, Kim ES, Hooper DC. Association of norB overexpression and fluoroquinolone resistance in clinical isolates of Staphylococcus aureus from Korea. J Antimicrob Chemother. 2013; 68:2766–2772. PMID: 23928023.

24. Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet. 1998; 351:797–799. PMID: 9519952.

25. Rodríguez-Martínez JM, Pascual A, García I, Martínez-Martínez L. Detection of the plasmid-mediated quinolone resistance determinant qnr among clinical isolates of Klebsiella pneumoniae producing AmpC-type beta-lactamase. J Antimicrob Chemother. 2003; 52:703–706. PMID: 12951342.

26. Wang M, Sahm DF, Jacoby GA, Hooper DC. Emerging plasmid-mediated quinolone resistance associated with the qnr gene in Klebsiella pneumoniae clinical isolates in the United States. Antimicrob Agents Chemother. 2004; 48:1295–1299. PMID: 15047532.

27. Wang M, Tran JH, Jacoby GA, Zhang Y, Wang F, Hooper DC. Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob Agents Chemother. 2003; 47:2242–2248. PMID: 12821475.

28. Cheung TK, Chu YW, Chu MY, Ma CH, Yung RW, Kam KM. Plasmid-mediated resistance to ciprofloxacin and cefotaxime in clinical isolates of Salmonella enterica serotype Enteritidis in Hong Kong. J Antimicrob Chemother. 2005; 56:586–589. PMID: 16033804.

29. Hata M, Suzuki M, Matsumoto M, Takahashi M, Sato K, Ibe S, Sakae K. Cloning of a novel gene for quinolone resistance from a transferable plasmid in Shigella flexneri 2b. Antimicrob Agents Chemother. 2005; 49:801–803. PMID: 15673773.

30. Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A, Hooper DC. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother. 2006; 50:1178–1182. PMID: 16569827.

31. Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S, Hooper DC, Wang M. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother. 2009; 53:1892–1897. PMID: 19258263.

32. Cavaco LM, Hasman H, Xia S, Aarestrup FM. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother. 2009; 53:603–608. PMID: 19029321.

33. Xia R, Guo X, Zhang Y, Xu H. qnrVC-like gene located in a novel complex class 1 integron harboring the ISCR1 element in an Aeromonas punctata strain from an aquatic environment in Shandong Province, China. Antimicrob Agents Chemother. 2010; 54:3471–3474. PMID: 20516288.

34. Singh R, Rajpara N, Tak J, Patel A, Mohanty P, Vinothkumar K, Chowdhury G, Ramamurthy T, Ghosh A, Bhardwaj AK. Clinical isolates of Vibrio fluvialis from Kolkata, India, obtained during 2006: plasmids, the qnr gene and a mutation in gyrase A as mechanisms of multidrug resistance. J Med Microbiol. 2012; 61:369–374. PMID: 22034163.

35. Fonseca EL, Vicente AC. Epidemiology of qnrVC alleles and emergence out of the Vibrionaceae family. J Med Microbiol. 2013; 62:1628–1630. PMID: 23800600.

36. Kim HB, Wang M, Ahmed S, Park CH, LaRocque RC, Faruque AS, Salam MA, Khan WA, Qadri F, Calderwood SB, Jacoby GA, Hooper DC. Transferable quinolone resistance in Vibrio cholerae. Antimicrob Agents Chemother. 2010; 54:799–803. PMID: 19949057.

37. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, Bush K, Hooper DC. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med. 2006; 12:83–88. PMID: 16369542.

38. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev. 2009; 22:664–689. PMID: 19822894.

39. Hansen LH, Johannesen E, Burmølle M, Sørensen AH, Sørensen SJ. Plasmid-encoded multidrug efflux pump conferring resistance to olaquindox in Escherichia coli. Antimicrob Agents Chemother. 2004; 48:3332–3337. PMID: 15328093.

40. Yamane K, Wachino J, Suzuki S, Kimura K, Shibata N, Kato H, Shibayama K, Konda T, Arakawa Y. New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother. 2007; 51:3354–3360. PMID: 17548499.

41. Schito GC, Naber KG, Botto H, Palou J, Mazzei T, Gualco L, Marchese A. The ARESC study: an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections. Int J Antimicrob Agents. 2009; 34:407–413. PMID: 19505803.

42. Gupta K, Hooton TM, Naber KG, Wullt B, Colgan R, Miller LG, Moran GJ, Nicolle LE, Raz R, Schaeffer AJ, Soper DE. Infectious Diseases Society of America. European Society for Microbiology and Infectious Diseases. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: A 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis. 2011; 52:e103–e120. PMID: 21292654.

43. Hooton TM, Bradley SF, Cardenas DD, Colgan R, Geerlings SE, Rice JC, Saint S, Schaeffer AJ, Tambayh PA, Tenke P, Nicolle LE. Infectious Diseases Society of America. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin Infect Dis. 2010; 50:625–663. PMID: 20175247.

44. Zhanel GG, Hisanaga TL, Laing NM, DeCorby MR, Nichol KA, Weshnoweski B, Johnson J, Noreddin A, Low DE, Karlowsky JA; NAUTICA Group, Hoban DJ. Antibiotic resistance in Escherichia coli outpatient urinary isolates: final results from the North American Urinary Tract Infection Collaborative Alliance (NAUTICA). Int J Antimicrob Agents. 2006; 27:468–475. PMID: 16713191.

45. Lu PL, Liu YC, Toh HS, Lee YL, Liu YM, Ho CM, Huang CC, Liu CE, Ko WC, Wang JH, Tang HJ, Yu KW, Chen YS, Chuang YC, Xu Y, Ni Y, Chen YH, Hsueh PR. Epidemiology and antimicrobial susceptibility profiles of Gram-negative bacteria causing urinary tract infections in the Asia-Pacific region: 2009-2010 results from the Study for Monitoring Antimicrobial Resistance Trends (SMART). Int J Antimicrob Agents. 2012; 40(Suppl):S37–S43. PMID: 22749057.

46. Lee MY, Choi HJ, Choi JY, Song M, Song Y, Kim SW, Chang HH, Jung SI, Kim YS, Ki HK, Son JS, Kwon KT, Heo ST, Yeom JS, Shin SY, Chung DR, Peck KR, Song JH, Ko KS. Dissemination of ST131 and ST393 community-onset, ciprofloxacin-resistant Escherichia coli clones causing urinary tract infections in Korea. J Infect. 2010; 60:146–153. PMID: 19932131.

47. Kim Y, Wie SH, Chang UI, Kim J, Ki M, Cho YK, Lim SK, Lee JS, Kwon KT, Lee H, Cheong HJ, Park DW, Ryu SY, Chung MH, Pai H. Comparison of the clinical characteristics of diabetic and non-diabetic women with community-acquired acute pyelonephritis: a multicenter study. J Infect. 2014; 69:244–251. PMID: 24854421.

48. Park KH, Oh WS, Kim ES, Park SW, Hur JA, Kim YK, Moon C, Lee JH, Lee CS, Kim BN. Factors associated with ciprofloxacin-and cefotaxime-resistant Escherichia coli in women with acute pyelonephritis in the emergency department. Int J Infect Dis. 2014; 23:8–13. PMID: 24657271.

49. Chaniotaki S, Giakouppi P, Tzouvelekis LS, Panagiotakos D, Kozanitou M, Petrikkos G, Avlami A, Vatopoulos AC. WHO-NET Study Group. Quinolone resistance among Escherichia coli strains from community-acquired urinary tract infections in Greece. Clin Microbiol Infect. 2004; 10:75–78. PMID: 14706091.

50. Killgore KM, March KL, Guglielmo BJ. Risk factors for community-acquired ciprofloxacin-resistant Escherichia coli urinary tract infection. Ann Pharmacother. 2004; 38:1148–1152. PMID: 15150380.

51. Arslan H, Azap OK, Ergönül O, Timurkaynak F. Urinary Tract Infection Study Group. Risk factors for ciprofloxacin resistance among Escherichia coli strains isolated from community-acquired urinary tract infections in Turkey. J Antimicrob Chemother. 2005; 56:914–918. PMID: 16174685.

52. Johnson L, Sabel A, Burman WJ, Everhart RM, Rome M, MacKenzie TD, Rozwadowski J, Mehler PS, Price CS. Emergence of fluoroquinolone resistance in outpatient urinary Escherichia coli isolates. Am J Med. 2008; 121:876–884. PMID: 18823859.

53. van der Starre WE, van Nieuwkoop C, Paltansing S, van't Wout JW, Groeneveld GH, Becker MJ, Koster T, Wattel-Louis GH, Delfos NM, Ablij HC, Leyten EM, Blom JW, van Dissel JT. Risk factors for fluoroquinolone-resistant Escherichia coli in adults with community-onset febrile urinary tract infection. J Antimicrob Chemother. 2011; 66:650–656. PMID: 21123286.

54. Vellinga A, Tansey S, Hanahoe B, Bennett K, Murphy AW, Cormican M. Trimethoprim and ciprofloxacin resistance and prescribing in urinary tract infection associated with Escherichia coli: a multilevel model. J Antimicrob Chemother. 2012; 67:2523–2530. PMID: 22729920.

55. Colodner R, Kometiani I, Chazan B, Raz R. Risk factors for community-acquired urinary tract infection due to quinolone-resistant E. coli. Infection. 2008; 36:41–45. PMID: 18193386.

56. Cizman M, Orazem A, Krizan-Hergouth V, Kolman J. Correlation between increased consumption of fluoroquinolones in outpatients and resistance of Escherichia coli from urinary tract infections. J Antimicrob Chemother. 2001; 47:502. PMID: 11266434.

57. Zervos MJ, Hershberger E, Nicolau DP, Ritchie DJ, Blackner LK, Coyle EA, Donnelly AJ, Eckel SF, Eng RH, Hiltz A, Kuyumjian AG, Krebs W, McDaniel A, Hogan P, Lubowski TJ. Relationship between fluoroquinolone use and changes in susceptibility to fluoroquinolones of selected pathogens in 10 United States teaching hospitals, 1991-2000. Clin Infect Dis. 2003; 37:1643–1648. PMID: 14689346.

58. MacDougall C, Powell JP, Johnson CK, Edmond MB, Polk RE. Hospital and community fluoroquinolone use and resistance in Staphylococcus aureus and Escherichia coli in 17 US hospitals. Clin Infect Dis. 2005; 41:435–440. PMID: 16028149.

59. Mahamat A, Daurès JP, Sotto A. Evaluation of the relation between consumption of fluoroquinolones and emergence of resistance among Escherichia coli: contribution of observational and quasi-experimental studies. Med Mal Infect. 2005; 35:543–548. PMID: 16253458.

60. Gallini A, Degris E, Desplas M, Bourrel R, Archambaud M, Montastruc JL, Lapeyre-Mestre M, Sommet A. Influence of fluoroquinolone consumption in inpatients and outpatients on ciprofloxacin-resistant Escherichia coli in a university hospital. J Antimicrob Chemother. 2010; 65:2650–2657. PMID: 20876240.

61. Paterson DL, Mulazimoglu L, Casellas JM, Ko WC, Goossens H, Von GA, Mohapatra S, Trenholme GM, Klugman KP, McCormack JG, Yu VL. Epidemiology of ciprofloxacin resistance and its relationship to extended-spectrum beta-lactamase production in Klebsiella pneumoniae isolates causing bacteremia. Clin Infect Dis. 2000; 30:473–478. PMID: 10722430.

62. Hsueh PR, Hoban DJ, Carmeli Y, Chen SY, Desikan S, Alejandria M, Ko WC, Binh TQ. Consensus review of the epidemiology and appropriate antimicrobial therapy of complicated urinary tract infections in Asia-Pacific region. J Infect. 2011; 63:114–123. PMID: 21669223.

63. Lee SS, Kim Y, Chung DR. Impact of discordant empirical therapy on outcome of community-acquired bacteremic acute pyelonephritis. J Infect. 2011; 62:159–164. PMID: 21055417.

64. Jeon JH, Kim K, Han WD, Song SH, Park KU, Rhee JE, Song KH, Park WB, Kim ES, Park SW, Kim NJ, Oh MD, Kim HB. Empirical use of ciprofloxacin for acute uncomplicated pyelonephritis caused by Escherichia coli in communities where the prevalence of fluoroquinolone resistance is high. Antimicrob Agents Chemother. 2012; 56:3043–3046. PMID: 22391544.

65. Chen YH, Ko WC, Hsueh PR. The role of fluoroquinolones in the management of urinary tract infections in areas with high rates of fluoroquinolone-resistant uropathogens. Eur J Clin Microbiol Infect Dis. 2012; 31:1699–1704. PMID: 22052606.

66. 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. Infectious Diseases Society of America. American Thoracic Society. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis. 2007; 44(Suppl 2):S27–S72. PMID: 17278083.

67. Song JH, Kang MW, Kim DJ, Pai H, Suh JY, Shim TS, Ahn JH, Ahn CM, Woo JH, Lee NY, Lee DG, Lee MS, Lee SM, Lee YS, Lee H, Chung DR. a Joint committee for CAP Treatment Guideline. Treatment guidelines for community-acquired pneumonia in Korea: an evidence-based approach to appropriate antimicrobial therapy. Infect Chemother. 2009; 41:133–153.

68. Low DE. Quinolone resistance among pneumococci: therapeutic and diagnostic implications. Clin Infect Dis. 2004; 38(Suppl 4):S357–S362. PMID: 15127370.

69. Jenkins SG, Brown SD, Farrell DJ. Trends in antibacterial resistance among Streptococcus pneumoniae isolated in the USA: update from PROTEKT US years 1-4. Ann Clin Microbiol Antimicrob. 2008; 7:1. PMID: 18190701.

70. Patel SN, McGeer A, Melano R, Tyrrell GJ, Green K, Pillai DR, Low DE. Canadian Bacterial Surveillance Network. Susceptibility of Streptococcus pneumoniae to fluoroquinolones in Canada. Antimicrob Agents Chemother. 2011; 55:3703–3708. PMID: 21628545.

71. European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance surveillance in Europe 2012. Accessed 2 December 2014. Available at: http://ecdc.europa.eu/en/publications/Publications/antimicrobial-resistance-surveillance-europe-2012.pdf.

72. Jacobs E, Dalhoff A, Korfmann G. Susceptibility patterns of bacterial isolates from hospitalised patients with respiratory tract infections (MOXIAKTIV Study). Int J Antimicrob Agents. 2009; 33:52–57. PMID: 18835763.

73. Pletz MW, van der Linden M, von Baum H, Duesberg CB, Klugman KP, Welte T. CAPNETZ study group. Low prevalence of fluoroquinolone resistant strains and resistance precursor strains in Streptococcus pneumoniae from patients with community-acquired pneumonia despite high fluoroquinolone usage. Int J Med Microbiol. 2011; 301:53–57. PMID: 20692869.

74. Kim SH, Song JH, Chung DR, Thamlikitkul V, Yang Y, Wang H, Lu M, So TM, Hsueh PR, Yasin RM, Carlos CC, Pham HV, Lalitha MK, Shimono N, Perera J, Shibl AM, Baek JY, Kang CI, Ko KS, Peck KR. ANSORP Study Group.Changing trends in antimicrobial resistance and serotypes of Streptococcus pneumoniae isolates in Asian countries: an Asian Network for Surveillance of Resistant Pathogens (ANSORP) study. Antimicrob Agents Chemother. 2012; 56:1418–1426. PMID: 22232285.

75. Jiménez MR, Bellido JL, García Rodríguez JA. Risk factors associated with colonization by pneumococci with reduced susceptibility to fluoroquinolones in adult outpatients. J Clin Microbiol. 2005; 43:1193–1197. PMID: 15750082.

76. Ho PL, Tse WS, Tsang KW, Kwok TK, Ng TK, Cheng VC, Chan RM. Risk factors for acquisition of levofloxacin-resistant Streptococcus pneumoniae: a case-control study. Clin Infect Dis. 2001; 32:701–707. PMID: 11229837.

77. Kang CI, Song JH, Kim SH, Chung DR, Peck KR, So TM, Hsueh PR;. Risk factors for levofloxacin-nonsusceptible Streptococcus pneumoniae in community-acquired pneumococcal pneumonia: a nested case-control study. Eur J Clin Microbiol Infect Dis. 2014; 33:55–59. PMID: 24062235.

78. Kang CI, Song JH, Kim SH, Chung DR, Peck KR, Thamlikitkul V, Wang H, So TM, Hsueh PR, Yasin RM, Carlos CC, Van PH, Perera J. Asian Network for Surveillance of Resistant Pathogens (ANSORP) Study Group. Association of levofloxacin resistance with mortality in adult patients with invasive pneumococcal diseases: a post hoc analysis of a prospective cohort. Infection. 2013; 41:151–157. PMID: 22821428.

79. de Cueto M, Rodríguez JM, Soriano MJ, López-Cerero L, Venero J, Pascual A. Fatal levofloxacin failure in treatment of a bacteremic patient infected with Streptococcus pneumoniae with a preexisting parC mutation. J Clin Microbiol. 2008; 46:1558–1560. PMID: 18287316.

80. Pfaller MA, Farrell DJ, Sader HS, Jones RN. AWARE Ceftaroline Surveillance Program (2008-2010): trends in resistance patterns among Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis in the United States. Clin Infect Dis. 2012; 55(Suppl 3):S187–S193. PMID: 22903951.

81. Chung DR, Song JH, Kim SH, Thamlikitkul V, Huang SG, Wang H, So TM, Yasin RM, Hsueh PR, Carlos CC, Hsu LY, Buntaran L, Lalitha MK, Kim MJ, Choi JY, Kim SI, Ko KS, Kang CI, Peck KR. Asian Network for Surveillance of Resistant Pathogens Study Group. High prevalence of multidrug-resistant nonfermenters in hospital-acquired pneumonia in Asia. Am J Respir Crit Care Med. 2011; 184:1409–1417. PMID: 21920919.

82. Karlowsky JA, Draghi DC, Jones ME, Thornsberry C, Friedland IR, Sahm DF. Surveillance for antimicrobial susceptibility among clinical isolates of Pseudomonas aeruginosa and Acinetobacter baumannii from hospitalized patients in the United States, 1998 to 2001. Antimicrob Agents Chemother. 2003; 47:1681–1688. PMID: 12709340.

83. Jones ME, Draghi DC, Thornsberry C, Karlowsky JA, Sahm DF, Wenzel RP. Emerging resistance among bacterial pathogens in the intensive care unit-a European and North American surveillance study (2000-2002). Ann Clin Microbiol Antimicrob. 2004; 3:14. PMID: 15283864.

84. Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother. 2007; 51:3471–3484. PMID: 17646423.

85. Lagamayo EN. Antimicrobial resistance in major pathogens of hospital-acquired pneumonia in Asian countries. Am J Infect Control. 2008; 36(4 Suppl):S101–S108. PMID: 18468549.

86. Solomkin JS, Mazuski JE, Bradley JS, Rodvold KA, Goldstein EJ, Baron EJ, O'Neill PJ, Chow AW, Dellinger EP, Eachempati SR, Gorbach S, Hilfiker M, May AK, Nathens AB, Sawyer RG, Bartlett JG. Diagnosis and management of complicated intra-abdominal infection in adults and children: guidelines by the Surgical Infection Society and the Infectious Diseases Society of America. Clin Infect Dis. 2010; 50:133–164. PMID: 20034345.

87. Babinchak T, Badal R, Hoban D, Hackel M, Hawser S, Lob S, Bouchillon S. Trends in susceptibility of selected gram-negative bacilli isolated from intra-abdominal infections in North America: SMART 2005-2010. Diagn Microbiol Infect Dis. 2013; 76:379–381. PMID: 23541118.

88. Hawser SP, Bouchillon SK, Hoban DJ, Badal RE, Cantón R, Baquero F. Incidence and antimicrobial susceptibility of Escherichia coli and Klebsiella pneumoniae with extended-spectrum beta-lactamases in community- and hospital-associated intra-abdominal infections in Europe: results of the 2008 Study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother. 2010; 54:3043–3046. PMID: 20421398.

89. Bochicchio GV, Baquero F, Hsueh PR, Paterson DL, Rossi F, Snyder TA, McCarroll K, Satishchandran V, Dinubile MJ, Chow JW. In vitro susceptibilities of Escherichia coli isolated from patients with intra-abdominal infections worldwide in 2002-2004: results from SMART (Study for Monitoring Antimicrobial Resistance Trends). Surg Infect (Larchmt). 2006; 7:537–545. PMID: 17233571.

90. Ko WC, Hsueh PR. Increasing extended-spectrum beta-lactamase production and quinolone resistance among Gram-negative bacilli causing intra-abdominal infections in the Asia/Pacific region: data from the smart study 2002-2006. J Infect. 2009; 59:95–103. PMID: 19564044.

91. Yang Q, Wang H, Chen M, Ni Y, Yu Y, Hu B, Sun Z, Huang W, Hu Y, Ye H, Badal RE, Xu Y. Surveillance of antimicrobial susceptibility of aerobic and facultative Gram-negative bacilli isolated from patients with intra-abdominal infections in China: the 2002-2009 Study for Monitoring Antimicrobial Resistance Trends (SMART). Int J Antimicrob Agents. 2010; 36:507–512. PMID: 21036547.

92. Kang CI, Chung DR, Ko KS, Peck KR, Song JH. Korean Network for the Study of Infectious Diseases (KONSID). Risk factors for mortality and impact of broad-spectrum cephalosporin resistance on outcome in bacteraemic intra-abdominal infections caused by Gram-negative bacilli. Scand J Infect Dis. 2011; 43:202–208. PMID: 21142623.

93. Yagci D, Yoruk F, Azap A, Memikoglu O. Prevalence and risk factors for selection of quinolone-resistant Escherichia coli strains in fecal flora of patients receiving quinolone therapy. Antimicrob Agents Chemother. 2009; 53:1287–1289. PMID: 19064895.

94. Garau J, Xercavins M, Rodríguez-Carballeira M, Gómez-Vera JR, Coll I, Vidal D, Llovet T, Ruíz-Bremón A. Emergence and dissemination of quinolone-resistant Escherichia coli in the community. Antimicrob Agents Chemother. 1999; 43:2736–2741. PMID: 10543756.

95. Nagy E, Urbán E, Nord CE. ESCMID Study Group on Antimicrobial Resistance in Anaerobic Bacteria. Antimicrobial susceptibility of Bacteroides fragilis group isolates in Europe: 20 years of experience. Clin Microbiol Infect. 2011; 17:371–379. PMID: 20456453.

96. Low DE. Clinical Relevance of Quinolone Resistance. In : Hooper DC, Rubinstein E, editors. Quinolone Antimicrobial Agents. 3rd ed. Washington, DC: American Society for Microbiology Press;2003. p. 355–386.

97. Parry CM, Threlfall EJ. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis. 2008; 21:531–538. PMID: 18725804.

98. Gu B, Cao Y, Pan S, Zhuang L, Yu R, Peng Z, Qian H, Wei Y, Zhao L, Liu G, Tong M. Comparison of the prevalence and changing resistance to nalidixic acid and ciprofloxacin of Shigella between Europe-America and Asia-Africa from 1998 to 2009. Int J Antimicrob Agents. 2012; 40:9–17. PMID: 22483324.

99. Horiuchi S, Inagaki Y, Yamamoto N, Okamura N, Imagawa Y, Nakaya R. Reduced susceptibilities of Shigella sonnei strains isolated from patients with dysentery to fluoroquinolones. Antimicrob Agents Chemother. 1993; 37:2486–2489. PMID: 8285640.

100. Vinh H, Wain J, Chinh MT, Tam CT, Trang PT, Nga D, Echeverria P, Diep TS, White NJ, Parry CM. Treatment of bacillary dysentery in Vietnamese children: two doses of ofloxacin versus 5-days nalidixic acid. Trans R Soc Trop Med Hyg. 2000; 94:323–326. PMID: 10975012.

101. Khan WA, Seas C, Dhar U, Salam MA, Bennish ML. Treatment of shigellosis: V. Comparison of azithromycin and ciprofloxacin. A double-blind, randomized, controlled trial. Ann Intern Med. 1997; 126:697–703. PMID: 9139555.

102. Ge B, Wang F, Sjolund-Karlsson M, McDermott PF. Antimicrobial resistance in Campylobacter: susceptibility testing methods and resistance trends. J Microbiol Methods. 2013; 95:57–67. PMID: 23827324.

103. Shin E, Oh Y, Kim M, Jung J, Lee Y. Antimicrobial resistance patterns and corresponding multilocus sequence types of the Campylobacter jejuni isolates from human diarrheal samples. Microb Drug Resist. 2013; 19:110–116. PMID: 23098555.

104. Goodman LJ, Trenholme GM, Kaplan RL, Segreti J, Hines D, Petrak R, Nelson JA, Mayer KW, Landau W, Parkhurst GW, Levin S. Empiric antimicrobial therapy of domestically acquired acute diarrhea in urban adults. Arch Intern Med. 1990; 150:541–546. PMID: 2178582.

105. Kuschner RA, Trofa AF, Thomas RJ, Hoge CW, Pitarangsi C, Amato S, Olafson RP, Echeverria P, Sadoff JC, Taylor DN. Use of azithromycin for the treatment of Campylobacter enteritis in travelers to Thailand, an area where ciprofloxacin resistance is prevalent. Clin Infect Dis. 1995; 21:536–541. PMID: 8527539.

106. Karchmer AW. Treatment of skin and soft tissue infections. In : Hooper DC, Rubinstein E, editors. Quinolone Antimicrobial Agents. 3rd ed. Washington, DC: American Society for Microbiology Press;2003. p. 311–321.

107. Dalhoff A. Resistance surveillance studies: a multifaceted problem-the fluoroquinolone example. Infection. 2012; 40:239–262. PMID: 22460782.

108. Montes M, Tamayo E, Orden B, Larruskain J, Perez-Trallero E. Prevalence and clonal characterization of Streptococcus pyogenes clinical isolates with reduced fluoroquinolone susceptibility in Spain. Antimicrob Agents Chemother. 2010; 54:93–97. PMID: 19805559.

109. Van Heirstraeten L, Leten G, Lammens C, Goossens H, Malhotra-Kumar S. Increase in fluoroquinolone non-susceptibility among clinical Streptococcus pyogenes in Belgium during 2007-10. J Antimicrob Chemother. 2012; 67:2602–2605. PMID: 22815354.

110. Barry AL, Jones RN. In vitro activity of ciprofloxacin against gram-positive cocci. Am J Med. 1987; 82:27–32. PMID: 3578323.

111. Smith SM. In vitro comparison of A-56619, A-56620, amifloxacin, ciprofloxacin, enoxacin, norfloxacin, and ofloxacin against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 1986; 29:325–326. PMID: 2940966.

112. Flamm RK, Farrell DJ, Mendes RE, Ross JE, Sader HS, Jones RN. LEADER surveillance program results for 2010: an activity and spectrum analysis of linezolid using 6801 clinical isolates from the United States (61 medical centers). Diagn Microbiol Infect Dis. 2012; 74:54–61. PMID: 22704791.

113. Kim ES, Lee HJ, Chung GT, Lee YS, Shin DH, Jung SI, Song KH, Park WB, Kim NJ, Park KU, Kim EC, Oh MD, Kim HB. Molecular characterization of methicillin-resistant Staphylococcus aureus isolates in Korea. J Clin Microbiol. 2011; 49:1979–1982. PMID: 21411580.

114. Jones RN, Mendes RE, Sader HS. Ceftaroline activity against pathogens associated with complicated skin and skin structure infections: results from an international surveillance study. J Antimicrob Chemother. 2010; 65(Suppl 4):iv17–iv31. PMID: 21115451.

115. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, Johnson SK, Vandenesch F, Fridkin S, O'Boyle C, Danila RN, Lynfield R. Comparison of community-and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA. 2003; 290:2976–2984. PMID: 14665659.

116. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, Talan DA. EMERGEncy ID Net Study Group. Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med. 2006; 355:666–674. PMID: 16914702.

117. Mendes RE, Sader HS, Deshpande LM, Diep BA, Chambers HF, Jones RN. Characterization of baseline methicillin-resistant Staphylococcus aureus isolates recovered from phase IV clinical trial for linezolid. J Clin Microbiol. 2010; 48:568–574. PMID: 19940054.

118. Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ, Armstrong DG, Deery HG, Embil JM, Joseph WS, Karchmer AW, Pinzur MS, Senneville E. Infectious Diseases Society of America. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis. 2012; 54:e132–e173. PMID: 22619242.

119. Kim BN, Kim ES, Oh MD. Oral antibiotic treatment of staphylococcal bone and joint infections in adults. J Antimicrob Chemother. 2014; 69:309–322. PMID: 24072167.

120. Stevens DL, Bisno AL, Chambers HF, Dellinger EP, Goldstein EJ, Gorbach SL, Hirschmann JV, Kaplan SL, Montoya JG, Wade JC. Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the Infectious Diseases Society of America. Clin Infect Dis. 2014; 59:147–159. PMID: 24947530.

121. Centers for Disease Control and Prevention (CDC). Antibiotic-resistant gonorrhea basic information. Accessed 2 December 2014. Available at: http://www.cdc.gov/std/gonorrhea/arg/basic.htm.

122. Lee H, Hong SG, Soe Y, Yong D, Jeong SH, Lee K, Chong Y. Trends in antimicrobial resistance of Neisseria gonorrhoeae isolated from Korean patients from 2000 to 2006. Sex Transm Dis. 2011; 38:1082–1086. PMID: 21992988.

123. Rahman M, Alam A, Nessa K, Nahar S, Dutta DK, Yasmin L, Monira S, Sultan Z, Khan SA, Albert MJ. Treatment failure with the use of ciprofloxacin for gonorrhea correlates with the prevalence of fluoroquinolone-resistant Neisseria gonorrhoeae strains in Bangladesh. Clin Infect Dis. 2001; 32:884–889. PMID: 11247712.

124. Workowski KA, Berman S. Centers for Disease Control and Prevention (CDC). Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep. 2010; 59:1–110. PMID: 21160459.