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The Microbial Genetics of Antibiotic Cycling

Published online by Cambridge University Press:  02 January 2015

Joseph F. John Jr.  and
Louis B. Rice
Joseph F. John Jr.*
Affiliation:
Division of Allergy, Immunology, and Infectious Diseases, Robert Wood Johnson Medical School, New Brunswick, New Jersey
Louis B. Rice
Affiliation:
Division of Infectious Diseases, Department of Medicine, Case Western Reserve School of Medicine, Cleveland Department of Veterans' Affairs Medical Center, Cleveland, Ohio
*
1 RWJPl, 356 MEB, UMDNJ/RWJMS, New Brunswick, NJ 08903-0019
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Abstract

Cycling of currently available antibiotics to reduce resistance is an attractive concept. For cycling strategies to be successful, their implementation must have a demonstrable impact on the prevalence of resistance determinants already dispersed throughout the hospital and associated healthcare facilities. While antibiotic use in hospitals clearly constitutes a stimulus for the emergence of resistance, it is by no means the only important factor. The incorporation of resistance determinants into potentially stable genetic structures, including bacteriophages, plasmids, transposons, and the more newly discovered movable elements termed integrons and gene cassettes, forces some degree of skepticism about the potential for such strategies in institutions where resistance determinants are already prevalent. In particular, the expanding role of integrons may pose an ultimate threat to formulary manipulations such as cycling. Despite these concerns, the crisis posed by antimicrobial resistance warrants investigation of any strategy with the potential for reducing the prevalence of resistance. Over the next decade, new studies with carefully designed outcomes should determine the utility of antibiotic cycling as one control measure for nosocomial resistance.

Type
Review
Information
Infection Control & Hospital Epidemiology , Volume 21 , Issue S1 , January 2000 , pp. S22 - S31
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2000

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References

1.Davies, J, Webb, V. Antibiotic resistance in bacteria. In: Krause, RM, ed. Emerging Infections. San Diego, CA: Academic Press; 1998:239–273.Google Scholar
2.Shlaes, DM, Gerding, DN, John, JF Jr, Craig, WA, Bornstein, DL, Duncan, RA, et al. Society for Healthcare Epidemiology of America and Infectious Diseases Society of America Joint Committee on the Prevention of Antimicrobial Resistance: guidelines for the prevention of antimicrobial resistance in hospitals. Infect Control Hosp Epidemiol 1997;18:275–291.Google Scholar
3.McGowan, JE Jr, Gerding, DN. Does antibiotic restriction prevent resistance? New Horiz 1996;4:370–376.Google Scholar
4.Quintilliani, R, Sahm, DF, Courvalin, P. Antimicrobial resistance. In: Murray, R, Baron, MJ, Pfaller, MA, Tenover, FC, Yolken, RH, eds. Manual of Clinical Microbiology. Washington, DC: ASM Press; 1999:1505–1524.Google Scholar
5.Dyke, KG, Gregory, PResistance to β-lactam antibiotics. In: Crossley, KB, Archer, GL, eds. The Staphylococci in Human Disease. New York, NY: Livingstone Churchill; 1998:139–157.Google Scholar
6.Bennett, PM. Integrons and gene cassettes: a genetic construction kit for bacteria. J Antimkrob Chemother 1999;43:1–4.Google Scholar
7.Lyon, BR, Skurray, R. Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev 1987;51:88–134.Google Scholar
8.Rice, LB, Carias, LL, Donskey, CL, Rudin, SD. Transferable, plasmid mediated vanB-type glycopeptide resistance in Enterococcus faecium. Antimkrob Agents Chemother 1998;42:963–964.CrossRefGoogle ScholarPubMed
9.Dowson, CG, Hutchison, A, Brannigan, JA, George, RC, Hansman, D, Linares, J, et al. Horizontal transfer of penicillin-binding protein genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci USA 1989;86:8842–8846.CrossRefGoogle ScholarPubMed
10.Dowson, CG, Coffey, TJ, Spratt, BG. Origin and molecular epidemiology of penicillin-binding-protein-mediated resistance to beta-lactam antibiotics. Trends Microbiol 1994;2:361–366.Google Scholar
11.Pradier, C, Dunais, B, Carsenti-Etesse, H, Dellamonica, P. Pneumococcal resistance patterns in Europe. Eur J Clin Microbiol Infect Dis 1997;16:644–647.Google Scholar
12.Medeiros, AA, Cohenford, M, Jacoby, GA. Five novel plasmid-determined beta-lactamases. Antimkrob Agents Chemother 1985;27:715–719.CrossRefGoogle ScholarPubMed
13.Bush, K, Jacoby, GA, Medeiros, AA. A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimkrob Agents Chemother 1995;39:1211–1233.CrossRefGoogle ScholarPubMed
14.Chambers, HEMethicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 1997;10:781–791.CrossRefGoogle ScholarPubMed
15.Lowy, FD. Staphylococcus aureus infections. NEngl J Med 1998;339:520–532.CrossRefGoogle ScholarPubMed
16.Grayson, ML, Eliopoulos, GM, Wennersten, CB, Ruoff, KL, DeGirolami, PC, Ferrara, MJ, et al. Increasing resistance to beta-lactam antibiotics among clinical isolates of Enterococcus faecium: a 22-year review at one institution. Antimkrob Agents Chemother 1991;35:2180–2184.CrossRefGoogle ScholarPubMed
17.Chow, JW, Fine, MJ, Shlaes, DM, Quinn, JP, Hooper, DC, Johnson, MP, et al. Enterobacter bacteremia: clinical features and emergence of antibiotic resistance during therapy. Ann Intern Med 1991;115:585–590.CrossRefGoogle ScholarPubMed
18.Livermore, DM. Interplay of impermeability and chromosomal beta-lactamase activity in imipenem-resistant Pseudomonas aeruginosa. Antimkrob Agents Chemother 1992;36:2046–2048.CrossRefGoogle ScholarPubMed
19.Bradford, PA, Urban, C, Mariano, N, Projan, SJ, Ranal, JJ, Bush, K. Imipenem resistance in Klebsiella pneumoniae is associated with the combination of ACT-1, a plasmid-mediated AmpC beta-lactamase, and the foss of an outer membrane protein. Antimkrob Agents Chemother 1997;41:563–569.Google Scholar
20.Papanicolaou, GA, Medeiros, AA, Jacoby, GANovel plasmid-mediated beta-lactamase (MIR-1) conferring resistance to oxyimino- and alpha-methoxy beta-lactams in clinical isolates of Klebsiella pneumoniae. Antimkrob Agents Chemother 1990;34:2200–2209.CrossRefGoogle ScholarPubMed
21.Hooper, DC. Bacterial topoisomerases, antitopoisomerases, and anti-topoisomerase resistance. Clin Infect Dis 1998;27(suppl 1):S54–S63.CrossRefGoogle ScholarPubMed
22.Dubin, DT, Fitzgibbon, JE, Nahvi, MD, John, JF. Topoisomerase sequences of coagulase-negative staphylococcal isolates resistant to ciprofloxacin or trovafloxacin. Antimkrob Agents Chemother 1999;43:1631–1637.CrossRefGoogle ScholarPubMed
23.Huovinen, P, Sundstrom, L, Swedberg, G, Skold, O. Trimethoprim and sulfonamide resistance. Antimkrob Agents Chemother 1995;39:279–289.Google Scholar
24.Amyes, SG. Genes and spectrum: the theoretical limits. Clin Infect Dis 1998;27:S21–S28.Google Scholar
25.Hall, RM, Collis, CM. Antibiotic resistance in gram-negative bacteria: the role of gene cassettes and integrons. Drug Resistance Updates 1999;1:109–119.CrossRefGoogle Scholar
26.John, JF Jr, McNeill, WF. Characteristics of Serratia marcescens containing a plasmid coding for gentamicin resistance in nosocomial infections. J Infect Dis 1981;143:810–818.Google Scholar
27.Gerding, DN, Larson, TA. Aminoglycoside resistance in gram-negative bacilli during increased amikacin use. Comparison of experience in 14 United States hospitals with experience in the Minneapolis Veterans' Administration Medical Center. Am J Med 1985;79:1–7.CrossRefGoogle ScholarPubMed
28.Gerding, DN, Larson, TA, Hughes, RA, Weiler, M, Shanholtzer, C, Peterson, LR. Aminoglycoside resistance and aminoglycoside usage: ten years of experience in one hospital. Antimkrob Agents Chemother 1991;35:1284–1290.Google Scholar
29.Zervos, MJ, Kauffman, CA, Therasse, PM, Bergman, AG, Mikesell, TS, Schaberg, DR. Nosocomial infection by gentamicin-resistant Streptococcus faecalis. An epidemiologic study. Ann Intern Med 1987;106:687–691.Google Scholar
30.Paul, SM, Gursky, EAA statewide surveillance system for antibiotic-resistant bacteria: the New Jersey Department of Health. Infect Control Hosp Epidemiol 1996;17:345.CrossRefGoogle ScholarPubMed
31.Hospital Infections Program, Centers for Disease Control and Prevention. NNIS Antimicrobial Resistance Surveillance Report. Updated October 22, 1999. Atlanta, GA: CDC. http://www.cdc.gov/ncidod/hip/NNIS/AR_Survll98.htm.Google Scholar
32.Bartiett, JG, Chang, TW, Gurwith, M, Gorbach, SL, Onderdonk, AB. Antibiotic-associated pseudomembranous colitis due to toxin-producing Clostridia. N Engl J Med 1978;298:531–534.Google Scholar
33.Arthur, M, Reynolds, P, Courvalin, PGlycopeptide resistance in entero-cocci. Trends Microbiol 1996;4:401–407.Google Scholar
34.Pugliese, G, Weinstein, RA, eds. Issues and Controversies in Prevention and Control of VRE, Vancomycin-Resistant Enterococci. Chicago, IL: ETNA Communications; 1998.Google Scholar
35.Hall, RM, Brown, HJ, Brookes, DE, Stokes, HW. Integrons found in different locations have identical 5′ ends but variable 3′ ends. J Bacterid 1994;176:6286–6294.CrossRefGoogle ScholarPubMed
36.Martinez-Freijo, P, Fluit, AC, Schmitz, FJ, Verhoef, J, Jones, ME. Many class I integrons comprise distinct stable structures occurring in different species of Enterobacteriaceae isolated from widespread geographic regions in Europe. Antimkrob Agents Chemother 1999;43:686–689.Google Scholar
37.Foster, TJ, Hook, M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 1998;6:484–488.Google Scholar
38.Manning, PAClark, CA, Focareta, T. Gene capture in Vibrio cholerae. Trends Microbiol 1999;7:93–95.CrossRefGoogle ScholarPubMed
39.Clark, NC, Olsvik, O, Swenson, JM, Spiegel, CATenover, FC. Detection of a streptomycin/spectinomycin adenylyltransferase gene (aadA) in Enterococcus faecalis. Antimkrob Agents Chemother 1999;43:157–160.CrossRefGoogle ScholarPubMed
40.Archer, GL, Niemeyer, DM. Origin and evolution of DNA associated with resistance to methicillin in staphylococci. Trends Microbiol 1994;2:343–347.CrossRefGoogle ScholarPubMed
41.Clewell, DB. Movable genetic elements and antibiotic resistance in enterococci. Eur J Clin Microbiol Infect Dis 1990;9:90–102.Google Scholar
42.Rice, LB, Carias, LL. Transfer of Tn5385, a composite, multiresistance chromosomal element from Enterococcus faecalis. J Bacterial 1998;180:714–721.Google Scholar
43.Firth, N, Skurray, RThe staphylococci in human. Drug Resistance Updates 1997;1:49–58.CrossRefGoogle Scholar
44.Nahvi, MD. Structure of the mec Region of Staphylococcal Chromosome: Diversity, Evolution, and Instability. Piscataway, NJ: University of Medicine and Dentistry of New Jersey; 1997. Thesis.Google Scholar
45.Bonhoeffer, S, Lipsitch, M, Levin, BR. Evaluating treatment protocols to prevent antibiotic resistance. Proc Natl Acad Sci USA 1997;94:12106–12111.Google Scholar
46.Donskey, CJ, Hanrahan, JAHutton, RARice, LB. Effect of parenteral antibiotic administration on persistence of vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. J Infect Dis 1999;180:384–390.CrossRefGoogle ScholarPubMed
47.Trick, WE, Kuehnert, MJ, Quirk, SB, Arduino, MJ, Aguero, SM, Carson, LAet al. Regional dissemination of vancomycin-resistant enterococci resulting from interfacility transfer of colonized patients. J Infect Dis 1999;180:391–396.Google Scholar
48.Go, ES, Urban, C, Burns, J, Kreiswirth, B, Eisner, W, Mariano, N, et al. Clinical and molecular epidemiology of Acinetobacter infections sensitive only to polymyxin B and sulbactam. Lancet 1994;344:1329–1332.Google Scholar
49.Livermore, DM, Yuan, M. Antibiotic resistance and production of extended-spectrum beta-lactamases amongst Klebsiella species from intensive care units in Europe. J Antimkrob Chemother 1996;38:409–424.Google Scholar
50.Spencer, RC. The emergence of epidemic, multiple-antibiotic-resistant Stenotrophomonas (Xanthomonas) maltophilia and Burkholderia (Pseudomonas) cepacia. J Hosp Infect 1995;30(suppl):453–464.Google Scholar
51.Pallares, R, Pujol, M, Pena, C, Ariza, J, Martin, R, Gudiol, F. Cephalosporins as risk factor for nosocomial Enterococcus faecalis bacteremia. A matched case-control study. Arch Intern Med 1993;153:1581–1586.CrossRefGoogle ScholarPubMed
52.Rice, LB, Carias, LL, Bonomo, RAShlaes, DM. Molecular genetics of resistance to both ceftazidime and beta-lactam-beta-lactamase inhibitor combinations in Klebsiella pneumoniae and in vivo response to beta-lactam therapy. J Infect Dis 1996;173:151–158.Google Scholar
53.Burwen, DR, Banerjee, SN, Gaynes, RE Ceftazidime resistance among selected nosocomial gram-negative bacilli in the United States. National Nosocomial Infections Surveillance System. J Infect Dis 1994;170:1622–1625.Google Scholar
54.Carmeli, Y, Troillet, N, Eliopoulos, GM, Samore, MH. Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison of risks associated with different antipseudomonal agents. Antimkrob Agents Chemother 1999;43:1379–1382.Google Scholar
55.Levy, SB. Multidrug resistance: a sign of the times. N Engl J Med 1998;338:1376–1378.Google Scholar
56.Stapleton, PD, Shannon, KP, French, GL. Carbapenem resistance in Escherichia coli associated with plasmid-determined CMY-4 beta-lactamase production and loss of an outer membrane protein. Antimkrob Agents Chemother 1999;43:1206–1210.CrossRefGoogle ScholarPubMed
57.Meyer, KS, Urban, C, Eagan, JABerger, BJ, Rahal, JJ. Nosocomial outbreak of Klebsiella infection resistant to late-generation cephalosporins. Ann Intern Med 1993;119:353–358.Google Scholar
58.Pena, C, Pujol, M, Ardanuy, C, Ricart A Pallares, R, Linares, J, et al. Epidemiology and successful control of a large outbreak due to Klebsiella pneumoniae producing extended-spectrum beta-lactamases. Antimkrob Agents Chemother 1998;42:53–58.Google Scholar
59.Rice, LB, Eckstein, EC, DeVente, J, Shlaes, DM. Ceftazidime-resistant Klebsiella pneumoniae isolates recovered at the Cleveland Department of Veterans' Affairs Medical Center. Clin Infect Dis 1996;23:118–124.Google Scholar
60.Rahal, JJ, Urban, C, Horn, D, Freeman, K, Segal-Maurer, S, Maurer, J, et al. Class restriction of cephalosporin use to control total cephalosporin resistance in nosocomial Klebsiella. JAMA 1998;280:1233–1237.Google Scholar
61.Wiener, J, Quinn, JP, Bradford, PAGoering, RV, Nathan, C, Bush, K, et al. Multiple antibiotic-resistant Klebsiella and Escherichia coli in nursing homes. JAMA 1999;281:517–523.CrossRefGoogle ScholarPubMed
62.Fierer, J, Guiney, D. Extended-spectrum beta-lactamases: a plague of Plasmids. JAMA 1999;281:563–564.CrossRefGoogle ScholarPubMed
63.Shaw, WV. Chloramphenicol resistance in meningococci. N Engl J Med 1998;339:917–918.Google Scholar
64.Kobayashi, N, Urasawa, S, Uehara, N, Watanabe, N. Distribution of insertion sequence-like element IS1272 and its position relative to methicillin resistance genes in clinically important staphylococci. Antimkrob Agents Chemother 1999;43:2780–2782.CrossRefGoogle ScholarPubMed
65.Arthur, M, Molinas, C, Courvalin, P. The vanS-vanR two-component regulatory system controls synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacterial 1992;174:2582–2591.Google Scholar
66.Evers, S, Courvalin, P. Regulation of vanB-type vancomycin resistance gene expression by the vanS(B)-vanR (B) two-component regulatory system in Enterococcus faecalis V583. J Bacterial 1996;178:1302–1309.Google Scholar
67.Hackbarth, CJ, Chambers, HF. Wal and WaRl regulate beta-lactamase and PBP 2a production in methicillin-resistant Staphylococcus aureus. Antimkrob Agents Chemother 1993;37:1144–1149.Google Scholar
68.Low, DE, Kellner, JD, Wright, GD. Superbugs: how they evolve and minimize the cost of resistance. In: Mandeli, LA, ed. Current Infectious Disease Reports. Philadelphia, PACurrent Science. In press.Google Scholar
69.Berger-Bachi, B. Resistance not mediated by β-lactamase (methicillin resistance). In: Crossley, KB, Archer, GL, eds. The Staphylococci in Human Disease. New York, NY: Livingstone Churchill; 1998:159–174.Google Scholar
70.Jacoby, GAMedeiros, AAMore extended-spectrum beta-lactamases. Antimkrob Agents Chemother 1991;35:1697–1704.Google Scholar
71.Schiappa, DAHayden, MK, Matushek, MG, Hashemi, FN, Sullivan, J, Smith, KY, et al. Ceftazidime-resistant Klebsiella pneumoniae and Escherichia coli bloodstream infection: a case-control and molecular epidemiologic investigation. J Infect Dis 1996;174:529–536.CrossRefGoogle ScholarPubMed
72.Gerding, DN. Is there a relationship between vancomycin-resistant ente-rococcal infection and Clostridium difficile infection? Clin Infect Dis 1997;25(suppl 2):S206–S210.CrossRefGoogle Scholar
73.Morris, JG Jr, Shay, DK, Hebden, JN, McCarter, RJ Jr, Perdue, BE, Jarvis, W, et al. Enterococci resistant to multiple antimicrobial agents, including vancomycin. Establishment of endemicity in a university medical center. Ann Intern Med 1995;123:250–259.CrossRefGoogle Scholar
74.Moreno, F, Grota, P, Crisp, C, Magnon, K, Melcher, GP, Jorgensen, JH, et al. Clinical and molecular epidemiology of vancomycin-resistant Enterococcus faecium during its emergence in a city in southern Texas. Clin Infect Dis 1995;21:1234–1237.Google Scholar
75.Quale, J, Landman, D, Saurina, G, Atwood, E, DiTore, V, Patel, K. Manipulation of a hospital antimicrobial formulary to control an outbreak of vancomycin-resistant enterococci. Clin Infect Dis 1996;23:1020–1025.Google Scholar
76.Carias, LL, Rudin, SD, Donskey, CJ, Rice, LB. Genetic linkage and cotrans-fer of a novel, vanB-containing transposon (Tn5382) and a low-affinity penicillin-binding protein 5 gene in a clinical vancomycin-resistant Enterococcus faecium isolate. J Bacterial 1998;180:4426–4434.Google Scholar
77.Chirurgi, VA, Oster, SE, Goldberg, AA, McCabe, RE. Nosocomial acquisition of beta-lactamase—negative, ampicillin-resistant Enterococcus. Arch Intern Med 1992;152:1457–1461.CrossRefGoogle ScholarPubMed
78.Smith, KE, Besser, JM, Hedberg, CW, Leano, FT, Bender, JB, Wicklund, JH, et al. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. N Engl J Med 1999;340:1524–1532.Google Scholar
79.Low, DE, Wright, GD. Persistence of resistance genes. In: Ghanassia, JP, ed. Antibiotic Therapy and Control of Antimicrobials. Paris, France: Elsevier. In press.Google Scholar
80.Bisognano, C, Vaudaux, PE, Lew, DP, Ng, EY, Hooper, DC. Increased expression of fibronectm-binding proteins by fluoroquinolone-resistant Staphylococcus aureus exposed to subinhibitory levels of ciprofloxacin. Antimkrob Agents Chemother 1997;41:906–913.CrossRefGoogle ScholarPubMed
81.Roghmann, MC, Qaiyumi, S, Johnson, JA, Schwalbe, R, Morris, JG Jr. Recurrent vancomycin-resistant Enterococcus faecium bacteremia in a leukemia patient who was persistently colonized with vancomycin-resistant enterococci for two years. Clin Infect Dis 1997;24:514–515.CrossRefGoogle Scholar
82.Berchieri, A. Intestinal colonization of a human subject by vancomycin-resistant Enterococcus faecium. Clin Microbiol Infect 1999;5:97–100.Google Scholar
83.Bradly, SJ, Wilson, ALT, Allen, MC, Sher, HA, Goldstone, AH, Scott, GM. The control of hyperendemic glycopeptide-resistant Enterococcus spp. on a haematolgy unit by changing antibiotic usage. J Antimkrob Chemother 1999;43:261–266.Google Scholar
84.Martinez, E, de la Cruz, F. Genetic elements involved in Tn21 site-specific integration, a novel mechanism for the dissemination of antibiotic resistance genes. EMBO J 1990;9:1275–1281.Google Scholar
85.Dominguez, EA, Smith, TL, Reed, E, Sanders, CC, Sanders, WE Jr. A pilot study of antibiotic cycling in a hematology-oncology unit. Infect Control Hosp Epidemiol 1999;21(suppl):S4–S8.CrossRefGoogle Scholar
86.Gerding, DE. Antimicrobial cycling: lessons learned from the aminoglycoside experience. Infect Control Hosp Epidemiol 1999;21(suppl):S12–S17.Google Scholar
87.Baquero, F, Negri, MC, Morosini, MI, Blazquez, J. Antibiotic-selective environments. Clin Infect Dis 1998;27(suppl 1):S5–S11.Google Scholar
88.Johnson, AP, Livermore, DM. Quinupristin/dalfopristin, a new addition to the antibiotic arsenal. Lancet 1999;354:212–213.Google Scholar
89.Cockerill, FR III. Genetic methods for assessing antimicrobial resistance. Antimkrob Agents Chemother 1999;43:199–212.CrossRefGoogle ScholarPubMed