Cycling Empirical Antibiotic Therapy in Hospitals: Meta-Analysis and Models

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Abel zur Wiesch, Pia ^a,b   Kouyos, Roger ^a,c   Abel, Sören ^b   Viechtbauer, Wolfgang ^d   Bonhoeffer, Sebastian ^a  

^a ETH ZURICH   (Switzerland)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT;

ALGORITHM; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; HOSPITAL INFECTION; HUMAN; META ANALYSIS; MORBIDITY; THEORETICAL MODEL; BACTERIAL INFECTIONS; BIOLOGICAL MODEL; DRUG EFFECTS; DRUG MONITORING; EMPIRICAL RESEARCH; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GROWTH, DEVELOPMENT AND AGING; HOSPITAL SUBDIVISIONS AND COMPONENTS; INCIDENCE; MICROBIOLOGY; MULTIDRUG RESISTANCE; TIME;

ANTI-BACTERIAL AGENTS; BACTERIAL INFECTIONS; DRUG MONITORING; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; EMPIRICAL RESEARCH; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HOSPITAL UNITS; HUMANS; INCIDENCE; MODELS, BIOLOGICAL; TIME FACTORS;

EID: 84903453394     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004225     Document Type: Article

References (83)

1. World Health Organisation (2005) Global patient safety challenge: clean care is safer care. In: World Alliance for Patient Safety, editor. Geneva.
2. Livermore DM, (2003) Bacterial resistance: origins, epidemiology, and impact. Clin Infect Dis 36: S11-23.
3. Lambert ML, Suetens C, Savey A, Palomar M, Hiesmayr M, et al. (2011) Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis 11: 30-38.
4. Levin BR, Bonten MJ, (2004) Cycling antibiotics may not be good for your health. Proc Natl Acad Sci U S A 101: 13101-13102.
5. Bergstrom CT, Lo M, Lipsitch M, (2004) Ecological theory suggests that antimicrobial cycling will not reduce antimicrobial resistance in hospitals. Proc Natl Acad Sci U S A 101: 13285-13290.
6. Bonhoeffer S, Lipsitch M, Levin BR, (1997) Evaluating treatment protocols to prevent antibiotic resistance. Proc Natl Acad Sci U S A 94: 12106-12111.
7. Masterton RG, (2005) Antibiotic cycling: more than it might seem? J Antimicrob Chemother 55: 1-5.
8. Masterton RG, (2010) Antibiotic heterogeneity. Int J Antimicrob Agents 36 (Suppl 3):: S15-18.
9. Brown EM, Nathwani D, (2005) Antibiotic cycling or rotation: a systematic review of the evidence of efficacy. J Antimicrob Chemother 55: 6-9.
10. Bal AM, Kumar A, Gould IM, (2010) Antibiotic heterogeneity: from concept to practice. Ann N Y Acad Sci 1213: 81-91.
11. Nijssen S, Bootsma M, Bonten M, (2006) Potential confounding in evaluating infection-control interventions in hospital settings: changing antibiotic prescription. Clin Infect Dis 43: 616-623.
12. de Kraker ME, Davey PG, Grundmann H, (2011) Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med 8: e1001104.
13. Paul M, Kariv G, Goldberg E, Raskin M, Shaked H, et al. (2010) Importance of appropriate empirical antibiotic therapy for methicillin-resistant Staphylococcus aureus bacteraemia. J Antimicrob Chemother 65: 2658-2665.
14. Vincent JL, (2003) Nosocomial infections in adult intensive-care units. Lancet 361: 2068-2077.
15. Damas P, Canivet JL, Ledoux D, Monchi M, Melin P, et al. (2006) Selection of resistance during sequential use of preferential antibiotic classes. Intensive Care Med 32: 67-74.
16. Dominguez EA, Smith TL, Reed E, et al. (2000) A pilot study of antibiotic cycling in a haematology-oncology unit. Control and Hospital Epidemiology 21: S4-S8.
17. Evans HL, Milburn ML, Hughes MG, Smith RL, Chong TW, et al. (2005) Nature of gram-negative rod antibiotic resistance during antibiotic rotation. Surg Infect (Larchmt) 6: 223-231.
18. Francetic I, Kalenic S, Huic M, Mercep I, Makar-Ausperger K, et al. (2008) Impact of aminoglycoside cycling in six tertiary intensive care units: prospective longitudinal interventional study. Croat Med J 49: 207-214.
19. Gerding DNL, T A, (1985) Aminoglycoside resistance in gram-negative bacilli during increased amikacin use: comparison of experience in fourteen United States hospitals with experience in the Minneapolis Veterans Administration Medical Center. American Journal of Medicine 79 (Suppl. 1A),:: 1-7.
20. Hughes MG, Evans HL, Chong TW, et al. (2004) Effect of an intensive care unit rotating empiric antibiotic schedule on the development of hospital-acquired infections on the non-intensive care unit ward. Critical Care Medicine 32: 53-60.
21. Kollef MH, Vlasnik J, Sharpless L, et al. (1997) Scheduled rotation of antibiotic classes. A strategy to decrease the incidence of ventilator-associated pneumonia due to antibiotic-resistant gramnegative bacteria. American Journal of Respiratory Critical Care Medicine 156: 1040-1048.
22. Kollef MH, Ward S, Sherman G, et al. (2000) Inadequate treatment of nosocomial infections is associated with certain empiric antibiotic choices. Critical Care Medicine 28: 3456-3464.
23. Martinez JA, Nicolás JM, Marco F, et al. (2005) Comparison of antimicrobial cycling and mixing in two medical intensive care units. Critical Care Medicine 34: 329-336.
24. Martinez JA, Delgado E, Marti S, Marco F, Vila J, et al. (2009) Influence of antipseudomonal agents on Pseudomonas aeruginosa colonization and acquisition of resistance in critically ill medical patients. Intensive Care Med 35: 439-447.
25. Puzniak LA, Mayfield J, Leet T, et al. (2001) Acquisition of vancomycin-resistant enterococci during scheduled antimicrobial rotation in an intensive care unit. Clinical Infectious Diseases 33: 151-157.
26. Raineri E, Crema L, Dal Zoppo S, et al. (2010) Rotation of antimicrobial therapy in the intensive care unit: impact on incidence of ventilator-associated pneumonia caused by antibiotic-resistant Gram-negative bacteria. European Journal of Clinical Microbiology and Infectious Diseases 29: 1015-1024.
27. Raymond DP, Pelletier SJ, Crabtree TD, et al. (2001) Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Critical Care Medicine 29: 1101-1108.
28. Sandiumenge A, Diaz E, Rodriguez A, et al. (2006) Impact of diversity of antibiotic use on development of antimicrobial resistance. Journal of Antimicrobial Chemotherapy 57: 1197-1204.
29. Sandiumenge A, Lisboa T, Gomez F, Hernandez P, Canadell L, et al. (2011) Effect of antibiotic diversity on ventilator-associated pneumonia caused by ESKAPE Organisms. Chest 140: 643-651.
30. Takesue Y, Nakajima K, Ichiki K, et al. (2010) Impact of a hospital-wide programme of heterogeneous antibiotic use on the development of antibiotic-resistant Gram-negative bacteria. Journal of Hospital Infection 75: 28-32.
31. Takesue Y, Ohge H, Sakashita M, et al. (2006) Effect of antibiotic heterogeneity on the development of infections with antibiotic-resistant gram-negative organisms in a nonintensive care unit surgical ward. World Journal of Surgery 30: 1269-1276.
32. Young EJ, Sewell CM, Koza MA, et al. (1985) Antibiotic resistance patterns during aminoglycoside restriction. American Journal of Medical Sciences 290: 223-227.
33. Barie PS, Hydo LJ, Shou J, Larone DH, Eachempati SR, (2005) Influence of antibiotic therapy on mortality of critical surgical illness caused or complicated by infection. Surg Infect (Larchmt) 6: 41-54.
34. Bradley SJ, Wilson AL, Allen MC, et al. (1999) The control of hyperendemic glycopeptide-resistant Enterococcus spp. on a haematology unit by changing antibiotic usage. Journal of Antimicrobial Chemotherapy 43: 261-266.
35. Craig M, Cumpston AD, Hobbs GR, et al. (2007) The clinical impact of antibacterial prophylaxis and cycling antibiotics for febrile neutropenia in a hematological malignancy and transplantation unit. Bone Marrow Transplant 39: 477-482.
36. Dortch MJ, Fleming SB, Kauffmann RM, Dossett LA, Talbot TR, et al. (2011) Infection reduction strategies including antibiotic stewardship protocols in surgical and trauma intensive care units are associated with reduced resistant gram-negative healthcare-associated infections. Surg Infect (Larchmt) 12: 15-25.
37. Slain D, Sarwari AR, Petros KO, McKnight RL, Sager RB, et al. (2011) Impact of a Multimodal Antimicrobial Stewardship Program on Pseudomonas aeruginosa Susceptibility and Antimicrobial Use in the Intensive Care Unit Setting. Crit Care Res Pract 2011: 416426.
38. Warren DK, Hill HA, Merz LR, et al. (2004) Cycling empirical antimicrobial agents to prevent emergence of antimicrobial-resistant Gram-negative bacteria among intensive care unit patients. Critical Care Medicine 32: 2450-2456.
39. Merz LR, Warren DK, Kollef MH, et al. (2006) The impact of an antibiotic cycling program on empirical therapy for gram-negative infections. Chest 130: 1672-1678.
40. Van Loon H, Vriens M, Fluit A, et al. (2005) Antibiotic rotation and development of Gram-negative antibiotic resistance. American Journal of Respiratory Critical Care Medicine 171: 480-487.
41. Moss WJ, Beers MC, Johnson E, et al. (2002) Pilot study of antibiotic cycling in a pediatric intensive care unit. Critical Care Medicine 30: 1877-1882.
42. Pakyz ALBMF, (2009) Rates of Stenotrophomonas maltophilia colonization and infection in relation to antibiotic cycling protocols. Epidemiology and Infection 137: 1679.
43. Hashino S, Morita L, Kanamori H, Takahata M, Onozawa M, et al. (2012) Clinical impact of cycling the administration of antibiotics for febrile neutropenia in Japanese patients with hematological malignancy. Eur J Clin Microbiol Infect Dis 31: 173-178.
44. Bruno-Murtha LA, Brusch J, Bor D, et al. (2005) A pilot study of antibiotic cycling in the community hospital setting. Infection Control Hospital Epidemiology 26: 81-87.
45. Bennett KM, Scarborough JE, Sharpe M, et al. (2007) Implementation of antibiotic rotation protocol improves antibiotic susceptibility profile in a surgical intensive care unit. Journal of Trauma 63: 307-311.
46. Gerding DN, Larson TA, Hughes RA, et al. (1991) Aminoglycoside resistance and aminoglycoside usage: ten years of experience in one hospital. Antimicrobial Agents and Chemotherapy 35.
47. Gruson D, Hilbert G, Vargas F, et al. (2000) Rotation and restricted use of antibiotics in a medical intensive care unit: impact on the incidence of ventilator-associated pneumonia caused by antibioticresistant Gram-negative bacteria. American Journal of Respiratory Critical Care Medicine 162: 837-843.
48. Gruson D, Hilbert G, Vargas F, et al. (2003) Strategy of antibiotic rotation: long term effect on incidence and susceptibilities of Gram-negative bacilli responsible for ventilator-associated pneumonia.∧. Critical Care Medicine 31: 1908-1914.
49. Cadena J, Taboada CA, Burgess DS, Ma JZ, Lewis JS 2nd, et al. (2007) Antibiotic cycling to decrease bacterial antibiotic resistance: a 5-year experience on a bone marrow transplant unit. Bone Marrow Transplant 40: 151-155.
50. Hedrick TL, Schulman AS, McElearney ST, et al. (2008) Outbreak of resistant Pseudomonas aeruginosa infections during a quarterly cycling antibiotic regimen. Surgical Infections 9: 139-152.
51. Kheder SI, Eltayeb I, Shaddad SA, AlKhedir I, (2012) Optimizing Antimicrobial Drug Use in Surgery: An Intervention Strategy in A Sudanese Hospital to Combat The Emergence of Bacterial Resistant. Sudan Journal of Medical Sciences 6.
52. Nijssen S, Fluit A, van de Vijver D, et al. (2010) Effects of reducing beta-lactam antibiotic pressure on intestinal colonization of antibiotic-resistant gram-negative bacteria. Intensive Care Medicine 36: 512-519.
53. Toltzis P, Dul M, Hoyen C, et al. (2002) The effect of antibiotic rotation on colonization with antibiotic-resistant bacilli in a neonatal intensive care unit. Peaditrics 110: 707-711.
54. Smith RL, Evans HL, Chong TW, et al. (2008) Reduction in rates of methicillin-resistant Staphylococcus aureus infection after introduction of quarterly linezolidvancomycin cycling in a surgical intensive care unit. Surgical Infections 9: 423-431.
55. Ginn AN, Wiklendt AM, Gidding HF, George N, O'Driscoll JS, et al. (2012) The ecology of antibiotic use in the ICU: homogeneous prescribing of cefepime but not tazocin selects for antibiotic resistant infection. PLoS One 7: e38719.
56. Cumpston A, Craig M, Hamadani M, Abraham J, Hobbs GR, et al. (2013) Extended follow-up of an antibiotic cycling program for the management of febrile neutropenia in a hematologic malignancy and hematopoietic cell transplantation unit. Transpl Infect Dis 15: 142-149.
57. Kontopidou FV, Antoniadou A, Tsirigotis P, Venetis E, Polemis M, et al. (2013) The impact of an antimicrobial cycling strategy for febrile neutropenia in a haematology unit. J Chemother 25: 279-285.
58. Sarraf-Yazdi S, Sharpe M, Bennett KM, Dotson TL, Anderson DJ, et al. (2012) A 9-Year retrospective review of antibiotic cycling in a surgical intensive care unit. J Surg Res 176: e73-78.
59. Chong Y, Shimoda S, Yakushiji H, Ito Y, Miyamoto T, et al. (2013) Antibiotic rotation for febrile neutropenic patients with hematological malignancies: clinical significance of antibiotic heterogeneity. PLoS One 8: e54190.
60. Merz LR, Warren DK, Kollef MH, Fraser VJ, (2004) Effects on antibiotic cycling programon antibiotic prescribing practices in an intensive care unit. Antimicrobial Agents and Chemotherapy 48: 2861-2865.
61. Beardmore RE, Pena-Miller R, (2010) Antibiotic cycling versus mixing: the difficulty of using mathematical models to definitively quantify their relative merits. Math Biosci Eng 7: 923-933.
62. Chow K, Wang X, Curtiss R 3rd, Castillo-Chavez C, (2011) Evaluating the efficacy of antimicrobial cycling programmes and patient isolation on dual resistance in hospitals. J Biol Dyn 5: 27-43.
63. Martínez JA, Nicolás JM, Marco F, et al. (2005) Comparison of antimicrobial cycling and mixing in two medical intensive care units. Critical Care Medicine 34: 329-336.
64. Kouyos RD, Abel Zur Wiesch P, Bonhoeffer S, (2011) Informed switching strongly decreases the prevalence of antibiotic resistance in hospital wards. PLoS Comput Biol 7: e1001094.
65. Viechtbauer W, (2010) Conducting meta-analyses in R with the metafor package. Journal of.
66. Berkey CS, Hoaglin DC, Antczak-Bouckoms A, Mosteller F, Colditz GA, (1998) Meta-analysis of multiple outcomes by regression with random effects. Stat Med 17: 2537-2550.
67. Riley RD, Thompson JR, (2008) An alternative model for bivariate random-effects meta-analysis when the within-study correlations are unknown. Biostatistics 9: 172-186.
68. Riley RD, (2009) Multivariate meta-analysis: The effect of ignoring within-study correlation. Journal of the Royal Statistical Society, Series A 178: 789-811.
69. Higgins JP, Thompson SG, Deeks JJ, Altman DG, (2003) Measuring inconsistency in meta-analyses. BMJ 327: 557-560.
70. Egger M, Davey Smith G, Schneider M, Minder C, (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629-634.
71. Begg CB, Mazumdar M, (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50: 1088-1101.
72. Kouyos RD, Abel Zur Wiesch P, Bonhoeffer S, (2011) On being the right size: the impact of population size and stochastic effects on the evolution of drug resistance in hospitals and the community. PLoS Pathog 7: e1001334.
73. Neely AN, Maley MP, (2000) Survival of enterococci and staphylococci on hospital fabrics and plastic. J Clin Microbiol 38: 724-726.
74. European Center for Disease Prevention and Control (2008) Annual Epidemiological Report on Communicable Diseases in Europe 2008. In: Control ECfDPa, editor. Stockholm.
75. Luciani F, Sisson SA, Jiang H, Francis AR, Tanaka MM, (2009) The epidemiological fitness cost of drug resistance in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 106: 14711-14715.
76. Trindade S, Sousa A, Xavier KB, Dionisio F, Ferreira MG, et al. (2009) Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet 5: e1000578.
77. Johnsen PJ, Townsend JP, Bohn T, Simonsen GS, Sundsfjord A, et al. (2011) Retrospective evidence for a biological cost of vancomycin resistance determinants in the absence of glycopeptide selective pressures. J Antimicrob Chemother 66: 608-610.
78. Dennesen PJ, van der Ven AJ, Kessels AG, Ramsay G, Bonten MJ, (2001) Resolution of infectious parameters after antimicrobial therapy in patients with ventilator-associated pneumonia. Am J Respir Crit Care Med 163: 1371-1375.
79. Ottiger C, Schaer G, Huber AR, (2007) Time-course of quantitative urinary leukocytes and bacteria counts during antibiotic therapy in women with symptoms of urinary tract infection. Clin Chim Acta 379: 36-41.
80. Grundmann H, Hellriegel B, (2006) Mathematical modelling: a tool for hospital infection control. Lancet Infect Dis 6: 39-45.
81. Bootsma MC, Wassenberg MW, Trapman P, Bonten MJ, (2011) The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus. J R Soc Interface 8: 578-584.
82. Bonten MJ, Hayden MK, Nathan C, Rice TW, Weinstein RA, (1998) Stability of vancomycin-resistant enterococcal genotypes isolated from long-term-colonized patients. J Infect Dis 177: 378-382.
83. McFarland LV, Mulligan ME, Kwok RY, Stamm WE, (1989) Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320: 204-210.