How to fight antimicrobial resistance
Cédric Foucault,
Philippe Brouqui,
Cédric Foucault
Service des Maladies Infectieuses et Tropicales, Hôpital Nord, Marseille, France
Search for more papers by this authorPhilippe Brouqui
Service des Maladies Infectieuses et Tropicales, Hôpital Nord, Marseille, France
Search for more papers by this authorCédric Foucault,
Philippe Brouqui,
Cédric Foucault
Service des Maladies Infectieuses et Tropicales, Hôpital Nord, Marseille, France
Search for more papers by this authorPhilippe Brouqui
Service des Maladies Infectieuses et Tropicales, Hôpital Nord, Marseille, France
Search for more papers by this authorCorrespondence: Philippe Brouqui, Service des Maladies Infectieuses et Tropicales, Hôpital Nord, Chemin des Bourrelys, 13915 Marseille Cedex 20, France. Tel.: +33 04 91 96 89 35; fax: +33 04 91 96 89 38; e-mail: [email protected]
Editor: Willem van Leeuwen
Abstract
Antimicrobial misuse results in the development of resistance and superbugs. Over recent decades, resistance has been increasing despite continuing efforts to control it, resulting in increased mortality and cost. Many authorities have proposed local, regional and national guidelines to fight against this phenomenon, and the usefulness of these programmes has been evaluated. Multifaceted intervention seems to be the most efficient method to control antimicrobial resistance. Monitoring of bacterial resistance and antibiotic use is essential, and the methodology has now been homogenized. The implementation of guidelines and infection control measures does not control antimicrobial resistance and needs to be reinforced by associated measures. Educational programmes and rotation policies have not been evaluated sufficiently in the literature. Combination antimicrobial therapy is inefficient in controlling antimicrobial resistance.
References
- Aarestrup FM (2000) Occurrence, selection and spread of resistance to antimicrobial agents used for growth promotion for food animals in Denmark. APMIS Suppl 101: 1–48.
- Al Eidan FA, McElnay JC, Scott MG, Kearney MP, Corrigan J & McConnell JB (2000) Use of a treatment protocol in the management of community-acquired lower respiratory tract infection. J Antimicrob Chemother 45: 387–394.
- Alanis AJ (2005) Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res 36: 697–705.
- Allegranzi B, Luzzati R, Luzzani A, Girardini F, Antozzi L, Raiteri R, Di Perri G & Concia E (2002) Impact of antibiotic changes in empirical therapy on antimicrobial resistance in intensive care unit-acquired infections. J Hosp Infect 52: 136–140.
- Austin DJ, Kristinsson KG & Anderson RM (1999) The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. Proc Natl Acad Sci USA 96: 1152–1156.
- Avorn J & Soumerai SB (1983) Improving drug-therapy decisions through educational outreach. A randomized controlled trial of academically based ‘detailing’. N Engl J Med 308: 1457–1463.
- Barrau K, Rovery C, Drancourt M & Brouqui P (2003) Hand antisepsis: evaluation of a sprayer system for alcohol distribution. Infect Control Hosp Epidemiol 24: 180–183.
- Barrett SP (2004) Debate-guidelines for GRE control–the case for optimism. J Hosp Infect 57: 285–289.
- Belongia EA, Sullivan BJ, Chyou PH, Madagame E, Reed KD & Schwartz B (2001) A community intervention trial to promote judicious antibiotic use and reduce penicillin-resistant Streptococcus pneumoniae carriage in children. Pediatrics 108: 575–583.
- Bergman M, Huikko S, Pihlajamaki M, Laippala P, Palva E, Huovinen P & Seppala H (2004) Effect of macrolide consumption on erythromycin resistance in Streptococcus pyogenes in Finland in 1997–2001. Clin Infect Dis 38: 1251–1256.
- Berk SL, Alvarez S, Ortega G, Verghese A & Holtsclaw-Berk SA (1986) Clinical and microbiologic consequences of amikacin use during a 42-month period. Arch Intern Med 146: 538–541.
- Betts RF, Valenti WM, Chapman SW, Chonmaitree T, Mowrer G, Pincus P, Messner M & Robertson R (1984) Five-year surveillance of aminoglycoside usage in a university hospital. Ann Intern Med 100: 219–222.
- Bradley SJ, Wilson AL, Allen MC, Sher HA, Goldstone AH & Scott GM (1999) The control of hyperendemic glycopeptide-resistant Enterococcus spp. on a haematology unit by changing antibiotic usage. J Antimicrob Chemother 43: 261–266.
- Bronzwaer SL, Goettsch W, Olsson-Liljequist B, Wale MC, Vatopoulos AC & Sprenger MJ (1999) European antimicrobial resistance surveillance system (EARSS): objectives and organisation. Euro Surveill 4: 41–44.
- Bronzwaer SL, Cars O, Buchholz U, Molstad S, Goettsch W, Veldhuijzen IK, Kool JL, Sprenger MJ & Degener JE (2002) A European study on the relationship between antimicrobial use and antimicrobial resistance. Emerg Infect Dis 8: 278–282.
- Burke JP (1998) Antibiotic resistance–squeezing the balloon? J Am Med Assoc 280: 1270–1271.
- Capelastegui A, Espana PP, Quintana JM, Gorordo I, Ortega M, Idoiaga I & Bilbao A (2004) Improvement of process-of-care and outcomes after implementing a guideline for the management of community-acquired pneumonia: a controlled before-and-after design study. Clin Infect Dis 39: 955–963.
- Carmeli Y, Troillet N, Eliopoulos GM & Samore MH (1999) Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison of risks associated with different antipseudomonal agents. Antimicrob Agents Chemother 43: 1379–1382.
- Chen DK, McGeer A, De Azavedo JC & Low DE (1999) Decreased susceptibility of Streptococcus pneumoniae to fluoroquinolones in Canada. Canadian Bacterial Surveillance Network. N Engl J Med 341: 233–239.
- Chow JW, Fine MJ, Shlaes DM, Quinn JP, Hooper DC, Johnson MP, Ramphal R, Wagener MM, Miyashiro DK & Yu VL (1991) Enterobacter bacteremia: clinical features and emergence of antibiotic resistance during therapy. Ann Intern Med 115: 585–590.
- Coenen S, Ferech M, Dvorakova K, Hendrickx E, Suetens C & Goossens H (2006a) European surveillance of antimicrobial consumption (ESAC): outpatient cephalosporin use in Europe. J Antimicrob Chemother 58: 413–417.
- Coenen S, Ferech M, Malhotra-Kumar S, Hendrickx E, Suetens C & Goossens H (2006b) European surveillance of antimicrobial consumption (ESAC): outpatient macrolide, lincosamide and streptogramin (MLS) use in Europe. J Antimicrob Chemother 58: 418–422.
- Cornaglia G, Hryniewicz W, Jarlier V, Kahlmeter G, Mittermayer H, Stratchounski L & Baquero F (2004) European recommendations for antimicrobial resistance surveillance. Clin Microbiol Infect 10: 349–383.
- Critchley IA & Karlowsky JA (2004) Optimal use of antibiotic resistance surveillance systems. Clin Microbiol Infect 10: 502–511.
- Curtis C, Marriott J & Langley C (2004) Development of a prescribing indicator for objective quantification of antibiotic usage in secondary care. J Antimicrob Chemother 54: 529–533.
- Dominguez EA, Smith TL, Reed E, Sanders CC & Sanders WE Jr (2000) A pilot study of antibiotic cycling in a hematology-oncology unit. Infect Control Hosp Epidemiol 21: S4–S8.
- Drancourt M, Stein A, Argenson JN, Zannier A, Curvale G & Raoult D (1993) Oral rifampin plus ofloxacin for treatment of Staphylococcus-infected orthopedic implants. Antimicrob Agents Chemother 37: 1214–1218.
- Drancourt M, Stein A, Argenson JN, Roiron R, Groulier P & Raoult D (1997) Oral treatment of Staphylococcus spp. infected orthopaedic implants with fusidic acid or ofloxacin in combination with rifampicin. J Antimicrob Chemother 39: 235–240.
- Ehrenkranz NJ (1992) Bland soap handwash or hand antisepsis? The pressing need for clarity. Infect Control Hosp Epidemiol 13: 299–301.
- Enne VI, Livermore DM, Stephens P & Hall LM (2001) Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 357: 1325–1328.
- Ferech M, Coenen S, Dvorakova K, Hendrickx E, Suetens C & Goossens H (2006a) European surveillance of antimicrobial consumption (ESAC): outpatient penicillin use in Europe. J Antimicrob Chemother 58: 408–412.
- Ferech M, Coenen S, Malhotra-Kumar S, Dvorakova K, Hendrickx E, Suetens C & Goossens H (2006b) European surveillance of antimicrobial consumption (ESAC): outpatient antibiotic use in Europe. J Antimicrob Chemother 58: 401–407.
- Finch R (2002) Bacterial resistance – the clinical challenge. Clin Microbiol Infect 8 (Suppl. 3), 21–32.
- Finch RG & Low DE (2002) A critical assessment of published guidelines and other decision-support systems for the antibiotic treatment of community-acquired respiratory tract infections. Clin Microbiol Infect 8 (Suppl. 2), 69–91.
- Finch RG, Metlay JP, Davey PG & Baker LJ (2004) Educational interventions to improve antibiotic use in the community: report from the International Forum on Antibiotic Resistance (IFAR) colloquium, 2002. Lancet Infect Dis 4: 44–53.
- Finkelstein JA, Davis RL, Dowell SF et al. (2001) Reducing antibiotic use in children: a randomized trial in 12 practices. Pediatrics 108: 1–7.
- Fish DN, Piscitelli SC & Danziger LH (1995) Development of resistance during antimicrobial therapy: a review of antibiotic classes and patient characteristics in 173 studies. Pharmacotherapy 15: 279–291.
- Frank MO, Batteiger BE, Sorensen SJ, Hartstein AI, Carr JA, McComb JS, Clark CD, Abel SR, Mikuta JM & Jones RB (1997) Decrease in expenditures and selected nosocomial infections following implementation of an antimicrobial-prescribing improvement program. Clin Perform Qual Health Care 5: 180–188.
- Fridkin SK (2003) Routine cycling of antimicrobial agents as an infection-control measure. Clin Infect Dis 36: 1438–1444.
- Frieden TR, Munsiff SS, Low DE, Willey BM, Williams G, Faur Y, Eisner W, Warren S & Kreiswirth B (1993) Emergence of vancomycin-resistant enterococci in New York City. Lancet 342: 76–79.
- Friedland IR, Funk E, Khoosal M & Klugman KP (1992) Increased resistance to amikacin in a neonatal unit following intensive amikacin usage. Antimicrob Agents Chemother 36: 1596–1600.
- Garner JS (1996) Guideline for isolation precautions in hospitals. The hospital infection control practices advisory committee. Infect Control Hosp Epidemiol 17: 53–80.
- Garner JS & Favero MS (1986) CDC guidelines for the prevention and control of nosocomial infections. Guideline for handwashing and hospital environmental control, 1985. Supersedes guideline for hospital environmental control published in 1981. Am J Infect Control 14: 110–129.
- Gerding DN, Larson TA, Hughes RA, Weiler M, Shanholtzer C & Peterson LR (1991) Aminoglycoside resistance and aminoglycoside usage: ten years of experience in one hospital. Antimicrob Agents Chemother 35: 1284–1290.
- Gonzales R, Steiner JF, Lum A & Barrett PH Jr (1999) Decreasing antibiotic use in ambulatory practice: impact of a multidimensional intervention on the treatment of uncomplicated acute bronchitis in adults. J Am Med Assoc 281: 1512–1519.
- Goossens H (2000) Antibiotic resistance and policy in Belgium. Verh K Acad Geneeskd Belg 62: 439–469.
- Gruson D, Hilbert G, Vargas F, Valentino R, Bebear C, Allery A, Bebear C, Gbikpi-Benissan G & Cardinaud JP (2000) Rotation and restricted use of antibiotics in a medical intensive care unit. Impact on the incidence of ventilator-associated pneumonia caused by antibiotic-resistant gram-negative bacteria. Am J Respir Crit Care Med 162: 837–843.
- Hammond JM, Potgieter PD, Forder AA & Plumb H (1990) Influence of amikacin as the primary aminoglycoside on bacterial isolates in the intensive care unit. Crit Care Med 18: 607–610.
- Harris AD, Perencevich E, Roghmann MC, Morris G, Kaye KS & Johnson JA (2002a) Risk factors for piperacillin–tazobactam-resistant Pseudomonas aeruginosa among hospitalized patients. Antimicrob Agents Chemother 46: 854–858.
- Harris AD, Smith D, Johnson JA, Bradham DD & Roghmann MC (2002b) Risk factors for imipenem-resistant Pseudomonas aeruginosa among hospitalized patients. Clin Infect Dis 34: 340–345.
- Hennessy TW, Petersen KM, Bruden D, Parkinson AJ, Hurlburt D, Getty M, Schwartz B & Butler JC (2002) Changes in antibiotic-prescribing practices and carriage of penicillin-resistant Streptococcus pneumoniae: a controlled intervention trial in rural Alaska. Clin Infect Dis 34: 1543–1550.
- John JF Jr. (2000) Antibiotic cycling: is it ready for prime time? Infect Control Hosp Epidemiol 21: 9–11.
- Johnson S, Gerding DN, Olson MM, Weiler MD, Hughes RA, Clabots CR & Peterson LR (1990) Prospective, controlled study of vinyl glove use to interrupt Clostridium difficile nosocomial transmission. Am J Med 88: 137–140.
- Kaye KS, Harris AD, Gold H & Carmeli Y (2000) Risk factors for recovery of ampicillin–sulbactam-resistant Escherichia coli in hospitalized patients. Antimicrob Agents Chemother 44: 1004–1009.
- Keuleyan E & Gould M (2001) Key issues in developing antibiotic policies: from an institutional level to Europe-wide. European Study Group on Antibiotic Policy (ESGAP), Subgroup III. Clin Microbiol Infect 7 (Suppl. 6), 16–21.
- Kollef MH, Vlasnik J, Sharpless L, Pasque C, Murphy D & Fraser V (1997) Scheduled change of antibiotic classes: a strategy to decrease the incidence of ventilator-associated pneumonia. Am J Respir Crit Care Med 156: 1040–1048.
- Larson E (1988) Guideline for use of topical antimicrobial agents. Am J Infect Control 16: 253–266.
- Larson EL (1995) APIC guideline for handwashing and hand antisepsis in health care settings. Am J Infect Control 23: 251–269.
- Larson E (1999) Skin hygiene and infection prevention: more of the same or different approaches? Clin Infect Dis 29: 1287–1294.
- Lautenbach E, Fishman NO, Bilker WB, Castiglioni A, Metlay JP, Edelstein PH & Strom BL (2002) Risk factors for fluoroquinolone resistance in nosocomial Escherichia coli and Klebsiella pneumoniae infections. Arch Intern Med 162: 2469–2477.
- Lautenbach E, Strom BL, Nachamkin I, Bilker WB, Marr AM, Larosa LA & Fishman NO (2004) Longitudinal trends in fluoroquinolone resistance among Enterobacteriaceae isolates from inpatients and outpatients, 1989–2000: differences in the emergence and epidemiology of resistance across organisms. Clin Infect Dis 38: 655–662.
- Lee SC, Fung CP, Liu PY, Wang TC, See LC, Lee N, Chen SC & Shieh WB (1999) Nosocomial infections with ceftazidime-resistant Pseudomonas aeruginosa: risk factors and outcome. Infect Control Hosp Epidemiol 20: 205–207.
- Lepper PM, Grusa E, Reichl H, Hogel J & Trautmann M (2002) Consumption of imipenem correlates with beta-lactam resistance in Pseudomonasaeruginosa. Antimicrob Agents Chemother 46: 2920–2925.
- Levine JF, Maslow MJ, Leibowitz RE, Pollock AA, Hanna BA, Schaefler S, Simberkoff MS & Rahal JJ Jr. (1985) Amikacin-resistant gram-negative bacilli: correlation of occurrence with amikacin use. J Infect Dis 151: 295–300.
- Levine OS, Farley M, Harrison LH, Lefkowitz L, McGeer A & Schwartz B (1999) Risk factors for invasive pneumococcal disease in children: a population-based case–control study in North America. Pediatrics 103: E28.
- Lopez-Lozano JM, Monnet DL, Yague A, Burgos A, Gonzalo N, Campillos P & Saez M (2000) Modelling and forecasting antimicrobial resistance and its dynamic relationship to antimicrobial use: a time series analysis. Int J Antimicrob Agents 14: 21–31.
- MacDougall C & Polk RE (2005) Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev 18: 638–656.
- Magee JT, Pritchard EL, Fitzgerald KA, Dunstan FD & Howard AJ (1999) Antibiotic prescribing and antibiotic resistance in community practice: retrospective study, 1996–8. Br Med J 319: 1239–1240.
- McGowan JE Jr (1994) Do intensive hospital antibiotic control programs prevent the spread of antibiotic resistance? Infect Control Hosp Epidemiol 15: 478–483.
- McGowan JE (2004) Debate-guidelines for control of glycopeptide-resistant enterococci (GRE) have not yet worked. J Hosp Infect 57: 281–284.
- Merz LR, Warren DK, Kollef MH & Fraser VJ (2004) Effects of an antibiotic cycling program on antibiotic prescribing practices in an intensive care unit. Antimicrob Agents Chemother 48: 2861–2865.
- Milatovic D & Braveny I (1987) Development of resistance during antibiotic therapy. Eur J Clin Microbiol 6: 234–244.
- Monnet DL, Lopez-Lozano JM, Campillos P, Burgos A, Yague A & Gonzalo N (2001) Making sense of antimicrobial use and resistance surveillance data: application of ARIMA and transfer function models. Clin Microbiol Infect 7 (Suppl. 5), 29–36.
- Moss WJ, Beers MC, Johnson E, Nichols DG, Perl TM, Dick JD, Veltri MA & Willoughby RE Jr (2002) Pilot study of antibiotic cycling in a pediatric intensive care unit. Crit Care Med 30: 1877–1882.
- Mouton JW (1999) Combination therapy as a tool to prevent emergence of bacterial resistance. Infection 27 (Suppl. 2), S24–S28.
- Nathwani D, Rubinstein E, Barlow G & Davey P (2001) Do guidelines for community-acquired pneumonia improve the cost-effectiveness of hospital care? Clin Infect Dis 32: 728–741.
- Paterson DL (2006) The epidemiological profile of infections with multidrug-resistant Pseudomonas aeruginosa and Acinetobacter species. Clin Infect Dis 43 (Suppl. 2), S43–S48.
- Paul M & Leibovici L (2005) Combination antibiotic therapy for Pseudomonas aeruginosa bacteraemia. Lancet Infect Dis 5: 192–193.
- Paul M, Soares-Weiser K & Leibovici L (2003) Beta lactam monotherapy versus beta lactam – aminoglycoside combination therapy for fever with neutropenia: systematic review and meta-analysis. Br Med J 326: 1111–1119.
- Paul M, Benuri-Silbiger I, Soares-Weiser K & Leibovici L (2004) Beta lactam monotherapy versus beta lactam – aminoglycoside combination therapy for sepsis in immunocompetent patients: systematic review and meta-analysis of randomised trials. Br Med J 328: 668–682.
- Pedersen G, Schonheyder HC, Steffensen FH & Sorensen HT (1999) Risk of resistance related to antibiotic use before admission in patients with community-acquired bacteraemia. J Antimicrob Chemother 43: 119–126.
- Perz JF, Craig AS, Coffey CS, Jorgensen DM, Mitchel E, Hall S, Schaffner W & Griffin MR (2002) Changes in antibiotic prescribing for children after a community-wide campaign. J Am Med Assoc 287: 3103–3109.
- Phelps CE (1989) Bug/drug resistance. Sometimes less is more. Med Care 27: 194–203.
- Quale J, Landman D, Saurina G, Atwood E, DiTore V & Patel K (1996) Manipulation of a hospital antimicrobial formulary to control an outbreak of vancomycin-resistant enterococci. Clin Infect Dis 23: 1020–1025.
- Rahal JJ, Urban C, Horn D et al. (1998) Class restriction of cephalosporin use to control total cephalosporin resistance in nosocomial Klebsiella. J Am Med Assoc 280: 1233–1237.
- Raymond DP, Pelletier SJ, Crabtree TD, Gleason TG, Hamm LL, Pruett TL & Sawyer RG (2001) Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Crit Care Med 29: 1101–1108.
- Raz R, Hefter H, Oren B, Kennes Y & Potasman I (1993) Antimicrobial resistance of urinary isolates in the community and its relation to antibiotic use. Isr J Med Sci 29: 207–210.
- Reichler MR, Rakovsky J, Sobotova A, Slacikova M, Hlavacova B, Hill B, Krajcikova L, Tarina P, Facklam RR & Breiman RF (1995) Multiple antimicrobial resistance of pneumococci in children with otitis media, bacteremia, and meningitis in Slovakia. J Infect Dis 171: 1491–1496.
- Ringertz S & Kronvall G (1987) Increased use of erythromycin causes resistance in Haemophilus influenzae. Scand J Infect Dis 19: 247–256.
- Safdar N, Handelsman J & Maki DG (2004) Does combination antimicrobial therapy reduce mortality in Gram-negative bacteraemia? A meta-analysis. Lancet Infect Dis 4: 519–527.
- Sanders CC & Sanders WE Jr. (1987) Clinical importance of inducible beta-lactamases in gram-negative bacteria. Eur J Clin Microbiol 6: 435–438.
- Sanders WE Jr. & Sanders CC (1997) Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin Microbiol Rev 10: 220–241.
- Schaffner W, Ray WA, Federspiel CF & Miller WO (1983) Improving antibiotic prescribing in office practice. A controlled trial of three educational methods. J Am Med Assoc 250: 1728–1732.
- Seppala H, Klaukka T, Lehtonen R, Nenonen E & Huovinen P (1995) Outpatient use of erythromycin: link to increased erythromycin resistance in group A streptococci. Clin Infect Dis 21: 1378–1385.
- Seppala H, Klaukka T, Vuopio-Varkila J, Muotiala A, Helenius H, Lager K & Huovinen P (1997) The effect of changes in the consumption of macrolide antibiotics on erythromycin resistance in group A streptococci in Finland. Finnish Study Group for Antimicrobial Resistance. N Engl J Med 337: 441–446.
- Shaikh ZH, Osting CA, Hanna HA, Arbuckle RB, Tarr JJ & Raad II (2002) Effectiveness of a multifaceted infection control policy in reducing vancomycin usage and vancomycin-resistant enterococci at a tertiary care cancer centre. J Hosp Infect 51: 52–58.
- Shlaes DM, Gerding DN, John JF Jr. et al. (1997) 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. Clin Infect Dis 25: 584–599.
- Soe JA, Hall JM, Collyns TA, Witherden IR, Parnell P, Woodrow G & Kerr KG (2002) An outbreak of vancomycin-resistant enterococci associated with major ward refurbishment. J Hosp Infect 50: 79–80.
- Steinke D & Davey P (2001) Association between antibiotic resistance and community prescribing: a critical review of bias and confounding in published studies. Clin Infect Dis 33 (Suppl. 3), S193–S205.
- Steinke DT, Seaton RA, Phillips G, MacDonald TM & Davey PG (1999) Factors associated with trimethoprim-resistant bacteria isolated from urine samples. J Antimicrob Chemother 43: 841–843.
- Steinke DT, Seaton RA, Phillips G, MacDonald TM & Davey PG (2001) Prior trimethoprim use and trimethoprim-resistant urinary tract infection: a nested case–control study with multivariate analysis for other risk factors. J Antimicrob Chemother 47: 781–787.
- Struelens MJ & Denis O (2006) Can we control the spread of antibiotic-resistant nosocomial pathogens? The methicillin-resistant Staphylococcus aureus paradigm. Curr Opin Infect Dis 19: 321–322.
- Suchyta MR, Dean NC, Narus S & Hadlock CJ (2001) Effects of a practice guideline for community-acquired pneumonia in an outpatient setting. Am J Med 110: 306–309.
- Tenover FC & Hughes JM (1996) The challenges of emerging infectious diseases. Development and spread of multiply-resistant bacterial pathogens. J Am Med Assoc 275: 300–304.
- Thiolas A, Bollet C, La Scola B, Raoult D & Pages JM (2005) Successive emergence of Enterobacter aerogenes strains resistant to imipenem and colistin in a patient. Antimicrob Agents Chemother 49: 1354–1358.
- Toltzis P, Yamashita T, Vilt L, Green M, Morrissey A, Spinner-Block S & Blumer J (1998) Antibiotic restriction does not alter endemic colonization with resistant gram-negative rods in a pediatric intensive care unit. Crit Care Med 26: 1893–1899.
- Troillet N, Samore MH & Carmeli Y (1997) Imipenem-resistant Pseudomonas aeruginosa: risk factors and antibiotic susceptibility patterns. Clin Infect Dis 25: 1094–1098.
- Vriens M, Blok H, Fluit A, Troelstra A, Van Der Werken C & Verhoef J (2002) Costs associated with a strict policy to eradicate methicillin-resistant Staphylococcus aureus in a Dutch University Medical Center: a 10-year survey. Eur J Clin Microbiol Infect Dis 21: 782–786.
- Weinstein RA (2001) Controlling antimicrobial resistance in hospitals: infection control and use of antibiotics. Emerg Infect Dis 7: 188–192.
- Weinstein RA & Kabins SA (1981) Strategies for prevention and control of multiple drug-resistant nosocomial infection. Am J Med 70: 449–454.
- Weinstein RA, Nathan C, Gruensfelder R & Kabins SA (1980) Endemic aminoglycoside resistance in gram-negative bacilli: epidemiology and mechanisms. J Infect Dis 141: 338–345.
- White AC Jr., Atmar RL, Wilson J, Cate TR, Stager CE & Greenberg SB (1997) Effects of requiring prior authorization for selected antimicrobials: expenditures, susceptibilities, and clinical outcomes. Clin Infect Dis 25: 230–239.
- Wiener J, Quinn JP, Bradford PA, Goering RV, Nathan C, Bush K & Weinstein RA (1999) Multiple antibiotic-resistant Klebsiella and Escherichia coli in nursing homes. J Am Med Assoc 281: 517–523.
- Young EJ, Sewell CM, Koza MA & Clarridge JE (1985) Antibiotic resistance patterns during aminoglycoside restriction. Am J Med Sci 290: 223–227.
