The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings

M.A. Aldeyab; S. Harbarth; N. Vernaz; M.P. Kearney; M.G. Scott; F.W. Darwish Elhajji; M.A. Aldiab; J.C. Mcelnay

doi:10.1111/j.1365-2125.2011.04161.x

The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings

M.A. Aldeyab, S. Harbarth, N. Vernaz, M.P. Kearney, M.G. Scott, F.W. Darwish Elhajji, M.A. Aldiab, J.C. Mcelnay

Dept of Mgmt, Leadership & Marketing

Research output: Contribution to journal › Article › peer-review

85 Citations (Scopus)

Abstract

Aims: The objective of the present study was to study the relationship between hospital antibiotic use, community antibiotic use and the incidence of extended-spectrum beta-lactamase (ESBL)-producing bacteria in hospitals, while assessing the impact of a fluoroquinolone restriction policy on ESBL-producing bacteria incidence rates. METHODS: The study was retrospective and ecological in design. A multivariate autoregressive integrated moving average (ARIMA) model was built to relate antibiotic use to ESB-producing bacteria incidence rates and resistance patterns over a 5 year period (January 2005-December 2009). Results: Analysis showed that the hospital incidence of ESBLs had a positive relationship with the use of fluoroquinolones in the hospital (coefficient = 0.174, P= 0.02), amoxicillin-clavulanic acid in the community (coefficient = 1.03, P= 0.03) and mean co-morbidity scores for hospitalized patients (coefficient = 2.15, P= 0.03) with various time lags. The fluoroquinolone restriction policy was implemented successfully with the mean use of fluoroquinolones (mainly ciprofloxacin) being reduced from 133 to 17 defined daily doses (DDDs)/1000 bed days (P <0.001) and from 0.65 to 0.54 DDDs/1000 inhabitants/day (P= 0.0007), in both the hospital and its surrounding community, respectively. This was associated with an improved ciprofloxacin susceptibility in both settings [ciprofloxacin susceptibility being improved from 16% to 28% in the community (P <0.001)] and with a statistically significant reduction in ESBL-producing bacteria incidence rates. Discussion: This study supports the value of restricting the use of certain antimicrobial classes to control ESBL, and demonstrates the feasibility of reversing resistance patterns post successful antibiotic restriction. The study also highlights the potential value of the time-series analysis in designing efficient antibiotic stewardship. © 2011 The Authors. British Journal of Clinical Pharmacology © 2011 The British Pharmacological Society.

Original language	English
Pages (from-to)	171-179
Number of pages	9
Journal	British Journal of Clinical Pharmacology
Volume	74
Issue number	1
Early online date	9 Dec 2011
DOIs	https://doi.org/10.1111/j.1365-2125.2011.04161.x
Publication status	Published online - 9 Dec 2011

Bibliographical note

Cited By :38

Export Date: 15 September 2018

CODEN: BCPHB

Correspondence Address: Aldeyab, M.A.; Clinical and Practice Research Group, School of Pharmacy, Queen's University, Belfast BT97BL, United Kingdom; email: [email protected]

Chemicals/CAS: amoxicillin plus clavulanic acid, 74469-00-4, 79198-29-1; carbapenem, 83200-96-8; cephalosporin, 11111-12-9; ciprofloxacin, 85721-33-1; lincosamide, 80738-43-8; nitrofuran, 27194-24-7; penicillin G, 1406-05-9, 61-33-6; tetracycline, 23843-90-5, 60-54-8, 64-75-5, 8021-86-1; trimethoprim, 738-70-5; Amoxicillin-Potassium Clavulanate Combination, 74469-00-4; Anti-Bacterial Agents; Disinfectants; Fluoroquinolones; beta-Lactamases, 3.5.2.6

References: Pitout, J.D., Laupland, K.B., Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern (2008) Lancet Infect Dis, 8, pp. 159-166; Falagas, M.E., Karageorgopoulos, D.E., Extended-spectrum beta-lactamase-producing organisms (2009) J Hosp Infect, 73, pp. 345-354; Ramphal, R., Ambrose, P.G., Extended-spectrum beta-lactamases and clinical outcomes: current data (2006) Clin Infect Dis, 42 (4), pp. S164-S172. , SUPPL; Paterson, D.L., Bonomo, R.A., Extended-spectrum beta-lactamases: a clinical update (2005) Clin Microbiol Rev, 18, pp. 657-686; Pfaller, M.A., Segreti, J., Overview of the epidemiological profile and laboratory detection of extended-spectrum beta-lactamases (2006) Clin Infect Dis, 42 (4), pp. S153-S163. , SUPPL; Rodríguez-Baño, J., Navarro, M.D., Romero, L., Muniain, M.A., Cueto, M., Gálvez, J., Perea, E.J., Pascual, A., Risk-factors for emerging bloodstream infections caused by extended-spectrum beta-lactamase-producing Escherichia coli (2008) Clin Microbiol Infect, 14, pp. 180-183; Kaier, K., Frank, U., Hagist, C., Conrad, A., Meyer, E., The impact of antimicrobial drug consumption and alcohol-based hand rub use on the emergence and spread of extended-spectrum beta-lactamase-producing strains: a time-series analysis (2009) J Antimicrob Chemother, 63, pp. 609-614; MacDougall, C., Powell, J.P., Johnson, C.K., Edmond, M.B., Polk, R.E., Hospital and community fluoroquinolone use and resistance in Staphylococcus aureus and Escherichia coli in 17 US hospitals (2005) Clin Infect Dis, 41, pp. 435-440; Gallini, A., Degris, E., Desplas, M., Bourrel, R., Archambaud, M., Montastruc, J.L., Lapeyre-Mestre, M., Sommet, A., Influence of fluoroquinolone consumption in inpatients and outpatients on ciprofloxacin-resistant Escherichia coli in a university hospital (2010) J Antimicrob Chemother, 65, pp. 2650-2657; Vernaz, N., Huttner, B., Muscionico, D., Salomon, J.L., Bonnabry, P., López-Lozano, J.M., Beyaert, A., Harbarth, S., Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-based data from a large hospital and its surrounding community (2011) J Antimicrob Chemother, 66, pp. 928-935; Dellit, T.H., Owens, R.C., McGowan Jr., J.E., Gerding, D.N., Weinstein, R.A., Burke, J.P., Huskins, W.C., Hooton, T.M., Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship (2007) Clin Infect Dis, 44, pp. 159-177. , Infectious Diseases Society of America, Society for Healthcare Epidemiology of America; MacDougall, C., Polk, R.E., Antimicrobial stewardship programs in health care systems (2005) Clin Microbiol Rev, 18, pp. 638-656; Gottesman, B.S., Carmeli, Y., Shitrit, P., Chowers, M., Impact of quinolone restriction on resistance patterns of Escherichia coli isolated from urine by culture in a community setting (2009) Clin Infect Dis, 49, pp. 869-875; Aldeyab, M.A., Devine, M.J., Flanagan, P., Mannion, M., Craig, A., Scott, M.G., Harbarth, S., Kearney, M.P., Multi-hospital outbreak of Clostridium difficile ribotype 027 infection: epidemiology and analysis of control measures (2011) Infect Control Hosp Epidemiol, 32, pp. 210-219; Shardell, M., Harris, A.D., El-Kamary, S.S., Furuno, J.P., Miller, R.R., Perencevich, E.N., Statistical analysis and application of quasi experiments to antimicrobial resistance intervention studies (2007) Clin Infect Dis, 45, pp. 901-907; Aldeyab, M.A., Monnet, D.L., López-Lozano, J.M., Hughes, C.M., Scott, M.G., Kearney, M.P., Magee, F.A., McElnay, J.C., Modelling the impact of antibiotic use and infection control practices on the incidence of hospital-acquired methicillin-resistant Staphylococcus aureus: a time-series analysis (2008) J Antimicrob Chemother, 62, pp. 593-600; Aldeyab, M.A., Harbarth, S., Vernaz, N., Kearney, M.P., Scott, M.G., Funston, C., Savage, K., McElnay, J.C., Quasiexperimental study of the effects of antibiotic use, gastric acid-suppressive agents, and infection control practices on the incidence of Clostridium difficile-associated diarrhea in hospitalized patients (2009) Antimicrob Agents Chemother, 53, pp. 2082-2088; Leigh, D.A., Williams, J.D., Method for the detection of significant bacteriuria in large groups of patients (1964) J Clin Pathol, 17, pp. 498-503; Tobacman, J.K., Assessment of comorbidity: a review (1994) Clin Perform Qual Health Care, 2, pp. 23-32; (2002) Guidelines for ATC Classifications and Ddds Assignment, , WHO Collaborating Center for Drug Statistics Methodology. Oslo: WHO Collaborating Center; Helfenstein, U., Box-Jenkins modelling in medical research (1996) Stat Methods Med Res, 5, pp. 3-22; McGowan Jr., J.E., Antimicrobial resistance in hospital organisms and its relation to antibiotic use (1983) Rev Infect Dis, 5, pp. 1033-1048; McCorry, A., Damani, N., Rajendran, R., McCaffrey, P., Muckian, D., Loughran, P., Reducing the use of 'high-risk' antibiotics through implementation of an antibiotic stewardship programme (2010) BJ Clin Pharm, 2, pp. 341-344; Vernaz, N., Sax, H., Pittet, D., Bonnabry, P., Schrenzel, J., Harbarth, S., Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile (2008) J Antimicrob Chemother, 62, pp. 601-607; Quan, H., Sundararajan, V., Halfon, P., Fong, A., Burnand, B., Luthi, J.C., Saunders, L.D., Ghali, W.A., Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data (2005) Med Care, 43, pp. 1130-1139; Davey, P., Brown, E., Fenelon, L., Finch, R., Gould, I., Hartman, G., Holmes, A., Wiffen, P., Interventions to improve antibiotic prescribing practices for hospital inpatients (2005) Cochrane Database Syst Rev, (4), pp. CD003543; Lipsitch, M., The rise and fall of antimicrobial resistance (2001) Trends Microbiol, 9, pp. 438-444; Harris, A.D., Lautenbach, E., Perencevich, E., A systematic review of quasi-experimental study designs in the fields of infection control and antibiotic resistance (2005) Clin Infect Dis, 41, pp. 77-82; Rawat, D., Nair, D., Extended-spectrum β-lactamases in gram negative bacteria (2010) J Glob Infect Dis, 2, pp. 263-274; Aldeyab, M.A., Kearney, M.P., McElnay, J.C., Magee, F.A., Conlon, G., Gill, D., Davey, P., Scott, M.G., A point prevalence survey of antibiotic prescriptions: benchmarking and patterns of use (2011) Br J Clin Pharmacol, 71, pp. 293-296. , ESAC Hospital Care Subproject Group

Keywords

Antibiotic stewardship
ESBL
Fluoroquinolones restriction policy
Time series analysis
aminoglycoside
amoxicillin plus clavulanic acid
carbapenem
cephalosporin
ciprofloxacin
glycopeptide
imidazole derivative
lincosamide
macrolide
nitrofuran
penicillin G
quinoline derived antiinfective agent
sulfonamide
tetracycline
trimethoprim
antibiotic resistance
antibiotic sensitivity
antibiotic therapy
article
comorbidity
drug use
extended spectrum beta lactamase producing Enterobacteriaceae
health care policy
hospital patient
human
incidence
primary health care
priority journal
retrospective study
Amoxicillin-Potassium Clavulanate Combination
Anti-Bacterial Agents
Bacteria
beta-Lactam Resistance
beta-Lactamases
Cross Infection
Disinfectants
Fluoroquinolones
Hospitals
Humans
Incidence
Multivariate Analysis
Primary Health Care
Regression Analysis
Retrospective Studies
Risk Factors

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1111/j.1365-2125.2011.04161.x

https://www.scopus.com/inward/record.uri?eid=2-s2.0-84862128157&doi=10.1111%2fj.1365-2125.2011.04161.x&partnerID=40&md5=bf209da891b5075633e91216ce0fb09b

Cite this

Aldeyab, M. A., Harbarth, S., Vernaz, N., Kearney, M. P., Scott, M. G., Darwish Elhajji, F. W., Aldiab, M. A., & Mcelnay, J. C. (2011). The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings. British Journal of Clinical Pharmacology, 74(1), 171-179. Advance online publication. https://doi.org/10.1111/j.1365-2125.2011.04161.x

@article{f2f439add77d4988825f05f2062254b0,

title = "The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings",

abstract = "Aims: The objective of the present study was to study the relationship between hospital antibiotic use, community antibiotic use and the incidence of extended-spectrum beta-lactamase (ESBL)-producing bacteria in hospitals, while assessing the impact of a fluoroquinolone restriction policy on ESBL-producing bacteria incidence rates. METHODS: The study was retrospective and ecological in design. A multivariate autoregressive integrated moving average (ARIMA) model was built to relate antibiotic use to ESB-producing bacteria incidence rates and resistance patterns over a 5 year period (January 2005-December 2009). Results: Analysis showed that the hospital incidence of ESBLs had a positive relationship with the use of fluoroquinolones in the hospital (coefficient = 0.174, P= 0.02), amoxicillin-clavulanic acid in the community (coefficient = 1.03, P= 0.03) and mean co-morbidity scores for hospitalized patients (coefficient = 2.15, P= 0.03) with various time lags. The fluoroquinolone restriction policy was implemented successfully with the mean use of fluoroquinolones (mainly ciprofloxacin) being reduced from 133 to 17 defined daily doses (DDDs)/1000 bed days (P <0.001) and from 0.65 to 0.54 DDDs/1000 inhabitants/day (P= 0.0007), in both the hospital and its surrounding community, respectively. This was associated with an improved ciprofloxacin susceptibility in both settings [ciprofloxacin susceptibility being improved from 16% to 28% in the community (P <0.001)] and with a statistically significant reduction in ESBL-producing bacteria incidence rates. Discussion: This study supports the value of restricting the use of certain antimicrobial classes to control ESBL, and demonstrates the feasibility of reversing resistance patterns post successful antibiotic restriction. The study also highlights the potential value of the time-series analysis in designing efficient antibiotic stewardship. {\textcopyright} 2011 The Authors. British Journal of Clinical Pharmacology {\textcopyright} 2011 The British Pharmacological Society.",

keywords = "Antibiotic stewardship, ESBL, Fluoroquinolones restriction policy, Time series analysis, aminoglycoside, amoxicillin plus clavulanic acid, carbapenem, cephalosporin, ciprofloxacin, glycopeptide, imidazole derivative, lincosamide, macrolide, nitrofuran, penicillin G, quinoline derived antiinfective agent, sulfonamide, tetracycline, trimethoprim, antibiotic resistance, antibiotic sensitivity, antibiotic therapy, article, comorbidity, drug use, extended spectrum beta lactamase producing Enterobacteriaceae, health care policy, hospital patient, human, incidence, primary health care, priority journal, retrospective study, Amoxicillin-Potassium Clavulanate Combination, Anti-Bacterial Agents, Bacteria, beta-Lactam Resistance, beta-Lactamases, Cross Infection, Disinfectants, Fluoroquinolones, Hospitals, Humans, Incidence, Multivariate Analysis, Primary Health Care, Regression Analysis, Retrospective Studies, Risk Factors",

author = "M.A. Aldeyab and S. Harbarth and N. Vernaz and M.P. Kearney and M.G. Scott and {Darwish Elhajji}, F.W. and M.A. Aldiab and J.C. Mcelnay",

note = "Cited By :38 Export Date: 15 September 2018 CODEN: BCPHB Correspondence Address: Aldeyab, M.A.; Clinical and Practice Research Group, School of Pharmacy, Queen's University, Belfast BT97BL, United Kingdom; email: [email protected] Chemicals/CAS: amoxicillin plus clavulanic acid, 74469-00-4, 79198-29-1; carbapenem, 83200-96-8; cephalosporin, 11111-12-9; ciprofloxacin, 85721-33-1; lincosamide, 80738-43-8; nitrofuran, 27194-24-7; penicillin G, 1406-05-9, 61-33-6; tetracycline, 23843-90-5, 60-54-8, 64-75-5, 8021-86-1; trimethoprim, 738-70-5; Amoxicillin-Potassium Clavulanate Combination, 74469-00-4; Anti-Bacterial Agents; Disinfectants; Fluoroquinolones; beta-Lactamases, 3.5.2.6 References: Pitout, J.D., Laupland, K.B., Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern (2008) Lancet Infect Dis, 8, pp. 159-166; Falagas, M.E., Karageorgopoulos, D.E., Extended-spectrum beta-lactamase-producing organisms (2009) J Hosp Infect, 73, pp. 345-354; Ramphal, R., Ambrose, P.G., Extended-spectrum beta-lactamases and clinical outcomes: current data (2006) Clin Infect Dis, 42 (4), pp. S164-S172. , SUPPL; Paterson, D.L., Bonomo, R.A., Extended-spectrum beta-lactamases: a clinical update (2005) Clin Microbiol Rev, 18, pp. 657-686; Pfaller, M.A., Segreti, J., Overview of the epidemiological profile and laboratory detection of extended-spectrum beta-lactamases (2006) Clin Infect Dis, 42 (4), pp. S153-S163. , SUPPL; Rodr{\'i}guez-Ba{\~n}o, J., Navarro, M.D., Romero, L., Muniain, M.A., Cueto, M., G{\'a}lvez, J., Perea, E.J., Pascual, A., Risk-factors for emerging bloodstream infections caused by extended-spectrum beta-lactamase-producing Escherichia coli (2008) Clin Microbiol Infect, 14, pp. 180-183; Kaier, K., Frank, U., Hagist, C., Conrad, A., Meyer, E., The impact of antimicrobial drug consumption and alcohol-based hand rub use on the emergence and spread of extended-spectrum beta-lactamase-producing strains: a time-series analysis (2009) J Antimicrob Chemother, 63, pp. 609-614; MacDougall, C., Powell, J.P., Johnson, C.K., Edmond, M.B., Polk, R.E., Hospital and community fluoroquinolone use and resistance in Staphylococcus aureus and Escherichia coli in 17 US hospitals (2005) Clin Infect Dis, 41, pp. 435-440; Gallini, A., Degris, E., Desplas, M., Bourrel, R., Archambaud, M., Montastruc, J.L., Lapeyre-Mestre, M., Sommet, A., Influence of fluoroquinolone consumption in inpatients and outpatients on ciprofloxacin-resistant Escherichia coli in a university hospital (2010) J Antimicrob Chemother, 65, pp. 2650-2657; Vernaz, N., Huttner, B., Muscionico, D., Salomon, J.L., Bonnabry, P., L{\'o}pez-Lozano, J.M., Beyaert, A., Harbarth, S., Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-based data from a large hospital and its surrounding community (2011) J Antimicrob Chemother, 66, pp. 928-935; Dellit, T.H., Owens, R.C., McGowan Jr., J.E., Gerding, D.N., Weinstein, R.A., Burke, J.P., Huskins, W.C., Hooton, T.M., Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship (2007) Clin Infect Dis, 44, pp. 159-177. , Infectious Diseases Society of America, Society for Healthcare Epidemiology of America; MacDougall, C., Polk, R.E., Antimicrobial stewardship programs in health care systems (2005) Clin Microbiol Rev, 18, pp. 638-656; Gottesman, B.S., Carmeli, Y., Shitrit, P., Chowers, M., Impact of quinolone restriction on resistance patterns of Escherichia coli isolated from urine by culture in a community setting (2009) Clin Infect Dis, 49, pp. 869-875; Aldeyab, M.A., Devine, M.J., Flanagan, P., Mannion, M., Craig, A., Scott, M.G., Harbarth, S., Kearney, M.P., Multi-hospital outbreak of Clostridium difficile ribotype 027 infection: epidemiology and analysis of control measures (2011) Infect Control Hosp Epidemiol, 32, pp. 210-219; Shardell, M., Harris, A.D., El-Kamary, S.S., Furuno, J.P., Miller, R.R., Perencevich, E.N., Statistical analysis and application of quasi experiments to antimicrobial resistance intervention studies (2007) Clin Infect Dis, 45, pp. 901-907; Aldeyab, M.A., Monnet, D.L., L{\'o}pez-Lozano, J.M., Hughes, C.M., Scott, M.G., Kearney, M.P., Magee, F.A., McElnay, J.C., Modelling the impact of antibiotic use and infection control practices on the incidence of hospital-acquired methicillin-resistant Staphylococcus aureus: a time-series analysis (2008) J Antimicrob Chemother, 62, pp. 593-600; Aldeyab, M.A., Harbarth, S., Vernaz, N., Kearney, M.P., Scott, M.G., Funston, C., Savage, K., McElnay, J.C., Quasiexperimental study of the effects of antibiotic use, gastric acid-suppressive agents, and infection control practices on the incidence of Clostridium difficile-associated diarrhea in hospitalized patients (2009) Antimicrob Agents Chemother, 53, pp. 2082-2088; Leigh, D.A., Williams, J.D., Method for the detection of significant bacteriuria in large groups of patients (1964) J Clin Pathol, 17, pp. 498-503; Tobacman, J.K., Assessment of comorbidity: a review (1994) Clin Perform Qual Health Care, 2, pp. 23-32; (2002) Guidelines for ATC Classifications and Ddds Assignment, , WHO Collaborating Center for Drug Statistics Methodology. Oslo: WHO Collaborating Center; Helfenstein, U., Box-Jenkins modelling in medical research (1996) Stat Methods Med Res, 5, pp. 3-22; McGowan Jr., J.E., Antimicrobial resistance in hospital organisms and its relation to antibiotic use (1983) Rev Infect Dis, 5, pp. 1033-1048; McCorry, A., Damani, N., Rajendran, R., McCaffrey, P., Muckian, D., Loughran, P., Reducing the use of 'high-risk' antibiotics through implementation of an antibiotic stewardship programme (2010) BJ Clin Pharm, 2, pp. 341-344; Vernaz, N., Sax, H., Pittet, D., Bonnabry, P., Schrenzel, J., Harbarth, S., Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile (2008) J Antimicrob Chemother, 62, pp. 601-607; Quan, H., Sundararajan, V., Halfon, P., Fong, A., Burnand, B., Luthi, J.C., Saunders, L.D., Ghali, W.A., Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data (2005) Med Care, 43, pp. 1130-1139; Davey, P., Brown, E., Fenelon, L., Finch, R., Gould, I., Hartman, G., Holmes, A., Wiffen, P., Interventions to improve antibiotic prescribing practices for hospital inpatients (2005) Cochrane Database Syst Rev, (4), pp. CD003543; Lipsitch, M., The rise and fall of antimicrobial resistance (2001) Trends Microbiol, 9, pp. 438-444; Harris, A.D., Lautenbach, E., Perencevich, E., A systematic review of quasi-experimental study designs in the fields of infection control and antibiotic resistance (2005) Clin Infect Dis, 41, pp. 77-82; Rawat, D., Nair, D., Extended-spectrum β-lactamases in gram negative bacteria (2010) J Glob Infect Dis, 2, pp. 263-274; Aldeyab, M.A., Kearney, M.P., McElnay, J.C., Magee, F.A., Conlon, G., Gill, D., Davey, P., Scott, M.G., A point prevalence survey of antibiotic prescriptions: benchmarking and patterns of use (2011) Br J Clin Pharmacol, 71, pp. 293-296. , ESAC Hospital Care Subproject Group",

year = "2011",

month = dec,

day = "9",

doi = "10.1111/j.1365-2125.2011.04161.x",

language = "English",

volume = "74",

pages = "171--179",

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publisher = "John Wiley & Sons, Inc.",

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}

Aldeyab, MA, Harbarth, S, Vernaz, N, Kearney, MP, Scott, MG, Darwish Elhajji, FW, Aldiab, MA & Mcelnay, JC 2011, 'The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings', British Journal of Clinical Pharmacology, vol. 74, no. 1, pp. 171-179. https://doi.org/10.1111/j.1365-2125.2011.04161.x

The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings. / Aldeyab, M.A.; Harbarth, S.; Vernaz, N. et al.
In: British Journal of Clinical Pharmacology, Vol. 74, No. 1, 09.12.2011, p. 171-179.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings

AU - Aldeyab, M.A.

AU - Harbarth, S.

AU - Vernaz, N.

AU - Kearney, M.P.

AU - Scott, M.G.

AU - Darwish Elhajji, F.W.

AU - Aldiab, M.A.

AU - Mcelnay, J.C.

N1 - Cited By :38 Export Date: 15 September 2018 CODEN: BCPHB Correspondence Address: Aldeyab, M.A.; Clinical and Practice Research Group, School of Pharmacy, Queen's University, Belfast BT97BL, United Kingdom; email: [email protected] Chemicals/CAS: amoxicillin plus clavulanic acid, 74469-00-4, 79198-29-1; carbapenem, 83200-96-8; cephalosporin, 11111-12-9; ciprofloxacin, 85721-33-1; lincosamide, 80738-43-8; nitrofuran, 27194-24-7; penicillin G, 1406-05-9, 61-33-6; tetracycline, 23843-90-5, 60-54-8, 64-75-5, 8021-86-1; trimethoprim, 738-70-5; Amoxicillin-Potassium Clavulanate Combination, 74469-00-4; Anti-Bacterial Agents; Disinfectants; Fluoroquinolones; beta-Lactamases, 3.5.2.6 References: Pitout, J.D., Laupland, K.B., Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern (2008) Lancet Infect Dis, 8, pp. 159-166; Falagas, M.E., Karageorgopoulos, D.E., Extended-spectrum beta-lactamase-producing organisms (2009) J Hosp Infect, 73, pp. 345-354; Ramphal, R., Ambrose, P.G., Extended-spectrum beta-lactamases and clinical outcomes: current data (2006) Clin Infect Dis, 42 (4), pp. S164-S172. , SUPPL; Paterson, D.L., Bonomo, R.A., Extended-spectrum beta-lactamases: a clinical update (2005) Clin Microbiol Rev, 18, pp. 657-686; Pfaller, M.A., Segreti, J., Overview of the epidemiological profile and laboratory detection of extended-spectrum beta-lactamases (2006) Clin Infect Dis, 42 (4), pp. S153-S163. , SUPPL; Rodríguez-Baño, J., Navarro, M.D., Romero, L., Muniain, M.A., Cueto, M., Gálvez, J., Perea, E.J., Pascual, A., Risk-factors for emerging bloodstream infections caused by extended-spectrum beta-lactamase-producing Escherichia coli (2008) Clin Microbiol Infect, 14, pp. 180-183; Kaier, K., Frank, U., Hagist, C., Conrad, A., Meyer, E., The impact of antimicrobial drug consumption and alcohol-based hand rub use on the emergence and spread of extended-spectrum beta-lactamase-producing strains: a time-series analysis (2009) J Antimicrob Chemother, 63, pp. 609-614; MacDougall, C., Powell, J.P., Johnson, C.K., Edmond, M.B., Polk, R.E., Hospital and community fluoroquinolone use and resistance in Staphylococcus aureus and Escherichia coli in 17 US hospitals (2005) Clin Infect Dis, 41, pp. 435-440; Gallini, A., Degris, E., Desplas, M., Bourrel, R., Archambaud, M., Montastruc, J.L., Lapeyre-Mestre, M., Sommet, A., Influence of fluoroquinolone consumption in inpatients and outpatients on ciprofloxacin-resistant Escherichia coli in a university hospital (2010) J Antimicrob Chemother, 65, pp. 2650-2657; Vernaz, N., Huttner, B., Muscionico, D., Salomon, J.L., Bonnabry, P., López-Lozano, J.M., Beyaert, A., Harbarth, S., Modelling the impact of antibiotic use on antibiotic-resistant Escherichia coli using population-based data from a large hospital and its surrounding community (2011) J Antimicrob Chemother, 66, pp. 928-935; Dellit, T.H., Owens, R.C., McGowan Jr., J.E., Gerding, D.N., Weinstein, R.A., Burke, J.P., Huskins, W.C., Hooton, T.M., Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship (2007) Clin Infect Dis, 44, pp. 159-177. , Infectious Diseases Society of America, Society for Healthcare Epidemiology of America; MacDougall, C., Polk, R.E., Antimicrobial stewardship programs in health care systems (2005) Clin Microbiol Rev, 18, pp. 638-656; Gottesman, B.S., Carmeli, Y., Shitrit, P., Chowers, M., Impact of quinolone restriction on resistance patterns of Escherichia coli isolated from urine by culture in a community setting (2009) Clin Infect Dis, 49, pp. 869-875; Aldeyab, M.A., Devine, M.J., Flanagan, P., Mannion, M., Craig, A., Scott, M.G., Harbarth, S., Kearney, M.P., Multi-hospital outbreak of Clostridium difficile ribotype 027 infection: epidemiology and analysis of control measures (2011) Infect Control Hosp Epidemiol, 32, pp. 210-219; Shardell, M., Harris, A.D., El-Kamary, S.S., Furuno, J.P., Miller, R.R., Perencevich, E.N., Statistical analysis and application of quasi experiments to antimicrobial resistance intervention studies (2007) Clin Infect Dis, 45, pp. 901-907; Aldeyab, M.A., Monnet, D.L., López-Lozano, J.M., Hughes, C.M., Scott, M.G., Kearney, M.P., Magee, F.A., McElnay, J.C., Modelling the impact of antibiotic use and infection control practices on the incidence of hospital-acquired methicillin-resistant Staphylococcus aureus: a time-series analysis (2008) J Antimicrob Chemother, 62, pp. 593-600; Aldeyab, M.A., Harbarth, S., Vernaz, N., Kearney, M.P., Scott, M.G., Funston, C., Savage, K., McElnay, J.C., Quasiexperimental study of the effects of antibiotic use, gastric acid-suppressive agents, and infection control practices on the incidence of Clostridium difficile-associated diarrhea in hospitalized patients (2009) Antimicrob Agents Chemother, 53, pp. 2082-2088; Leigh, D.A., Williams, J.D., Method for the detection of significant bacteriuria in large groups of patients (1964) J Clin Pathol, 17, pp. 498-503; Tobacman, J.K., Assessment of comorbidity: a review (1994) Clin Perform Qual Health Care, 2, pp. 23-32; (2002) Guidelines for ATC Classifications and Ddds Assignment, , WHO Collaborating Center for Drug Statistics Methodology. Oslo: WHO Collaborating Center; Helfenstein, U., Box-Jenkins modelling in medical research (1996) Stat Methods Med Res, 5, pp. 3-22; McGowan Jr., J.E., Antimicrobial resistance in hospital organisms and its relation to antibiotic use (1983) Rev Infect Dis, 5, pp. 1033-1048; McCorry, A., Damani, N., Rajendran, R., McCaffrey, P., Muckian, D., Loughran, P., Reducing the use of 'high-risk' antibiotics through implementation of an antibiotic stewardship programme (2010) BJ Clin Pharm, 2, pp. 341-344; Vernaz, N., Sax, H., Pittet, D., Bonnabry, P., Schrenzel, J., Harbarth, S., Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile (2008) J Antimicrob Chemother, 62, pp. 601-607; Quan, H., Sundararajan, V., Halfon, P., Fong, A., Burnand, B., Luthi, J.C., Saunders, L.D., Ghali, W.A., Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data (2005) Med Care, 43, pp. 1130-1139; Davey, P., Brown, E., Fenelon, L., Finch, R., Gould, I., Hartman, G., Holmes, A., Wiffen, P., Interventions to improve antibiotic prescribing practices for hospital inpatients (2005) Cochrane Database Syst Rev, (4), pp. CD003543; Lipsitch, M., The rise and fall of antimicrobial resistance (2001) Trends Microbiol, 9, pp. 438-444; Harris, A.D., Lautenbach, E., Perencevich, E., A systematic review of quasi-experimental study designs in the fields of infection control and antibiotic resistance (2005) Clin Infect Dis, 41, pp. 77-82; Rawat, D., Nair, D., Extended-spectrum β-lactamases in gram negative bacteria (2010) J Glob Infect Dis, 2, pp. 263-274; Aldeyab, M.A., Kearney, M.P., McElnay, J.C., Magee, F.A., Conlon, G., Gill, D., Davey, P., Scott, M.G., A point prevalence survey of antibiotic prescriptions: benchmarking and patterns of use (2011) Br J Clin Pharmacol, 71, pp. 293-296. , ESAC Hospital Care Subproject Group

PY - 2011/12/9

Y1 - 2011/12/9

N2 - Aims: The objective of the present study was to study the relationship between hospital antibiotic use, community antibiotic use and the incidence of extended-spectrum beta-lactamase (ESBL)-producing bacteria in hospitals, while assessing the impact of a fluoroquinolone restriction policy on ESBL-producing bacteria incidence rates. METHODS: The study was retrospective and ecological in design. A multivariate autoregressive integrated moving average (ARIMA) model was built to relate antibiotic use to ESB-producing bacteria incidence rates and resistance patterns over a 5 year period (January 2005-December 2009). Results: Analysis showed that the hospital incidence of ESBLs had a positive relationship with the use of fluoroquinolones in the hospital (coefficient = 0.174, P= 0.02), amoxicillin-clavulanic acid in the community (coefficient = 1.03, P= 0.03) and mean co-morbidity scores for hospitalized patients (coefficient = 2.15, P= 0.03) with various time lags. The fluoroquinolone restriction policy was implemented successfully with the mean use of fluoroquinolones (mainly ciprofloxacin) being reduced from 133 to 17 defined daily doses (DDDs)/1000 bed days (P <0.001) and from 0.65 to 0.54 DDDs/1000 inhabitants/day (P= 0.0007), in both the hospital and its surrounding community, respectively. This was associated with an improved ciprofloxacin susceptibility in both settings [ciprofloxacin susceptibility being improved from 16% to 28% in the community (P <0.001)] and with a statistically significant reduction in ESBL-producing bacteria incidence rates. Discussion: This study supports the value of restricting the use of certain antimicrobial classes to control ESBL, and demonstrates the feasibility of reversing resistance patterns post successful antibiotic restriction. The study also highlights the potential value of the time-series analysis in designing efficient antibiotic stewardship. © 2011 The Authors. British Journal of Clinical Pharmacology © 2011 The British Pharmacological Society.

AB - Aims: The objective of the present study was to study the relationship between hospital antibiotic use, community antibiotic use and the incidence of extended-spectrum beta-lactamase (ESBL)-producing bacteria in hospitals, while assessing the impact of a fluoroquinolone restriction policy on ESBL-producing bacteria incidence rates. METHODS: The study was retrospective and ecological in design. A multivariate autoregressive integrated moving average (ARIMA) model was built to relate antibiotic use to ESB-producing bacteria incidence rates and resistance patterns over a 5 year period (January 2005-December 2009). Results: Analysis showed that the hospital incidence of ESBLs had a positive relationship with the use of fluoroquinolones in the hospital (coefficient = 0.174, P= 0.02), amoxicillin-clavulanic acid in the community (coefficient = 1.03, P= 0.03) and mean co-morbidity scores for hospitalized patients (coefficient = 2.15, P= 0.03) with various time lags. The fluoroquinolone restriction policy was implemented successfully with the mean use of fluoroquinolones (mainly ciprofloxacin) being reduced from 133 to 17 defined daily doses (DDDs)/1000 bed days (P <0.001) and from 0.65 to 0.54 DDDs/1000 inhabitants/day (P= 0.0007), in both the hospital and its surrounding community, respectively. This was associated with an improved ciprofloxacin susceptibility in both settings [ciprofloxacin susceptibility being improved from 16% to 28% in the community (P <0.001)] and with a statistically significant reduction in ESBL-producing bacteria incidence rates. Discussion: This study supports the value of restricting the use of certain antimicrobial classes to control ESBL, and demonstrates the feasibility of reversing resistance patterns post successful antibiotic restriction. The study also highlights the potential value of the time-series analysis in designing efficient antibiotic stewardship. © 2011 The Authors. British Journal of Clinical Pharmacology © 2011 The British Pharmacological Society.

KW - Antibiotic stewardship

KW - ESBL

KW - Fluoroquinolones restriction policy

KW - Time series analysis

KW - aminoglycoside

KW - amoxicillin plus clavulanic acid

KW - carbapenem

KW - cephalosporin

KW - ciprofloxacin

KW - glycopeptide

KW - imidazole derivative

KW - lincosamide

KW - macrolide

KW - nitrofuran

KW - penicillin G

KW - quinoline derived antiinfective agent

KW - sulfonamide

KW - tetracycline

KW - trimethoprim

KW - antibiotic resistance

KW - antibiotic sensitivity

KW - antibiotic therapy

KW - article

KW - comorbidity

KW - drug use

KW - extended spectrum beta lactamase producing Enterobacteriaceae

KW - health care policy

KW - hospital patient

KW - human

KW - incidence

KW - primary health care

KW - priority journal

KW - retrospective study

KW - Amoxicillin-Potassium Clavulanate Combination

KW - Anti-Bacterial Agents

KW - Bacteria

KW - beta-Lactam Resistance

KW - beta-Lactamases

KW - Cross Infection

KW - Disinfectants

KW - Fluoroquinolones

KW - Hospitals

KW - Humans

KW - Incidence

KW - Multivariate Analysis

KW - Primary Health Care

KW - Regression Analysis

KW - Retrospective Studies

KW - Risk Factors

U2 - 10.1111/j.1365-2125.2011.04161.x

DO - 10.1111/j.1365-2125.2011.04161.x

M3 - Article

SN - 0306-5251

VL - 74

SP - 171

EP - 179

JO - British Journal of Clinical Pharmacology

JF - British Journal of Clinical Pharmacology

IS - 1

ER -

Aldeyab MA, Harbarth S, Vernaz N, Kearney MP, Scott MG, Darwish Elhajji FW et al. The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings. British Journal of Clinical Pharmacology. 2011 Dec 9;74(1):171-179. Epub 2011 Dec 9. doi: 10.1111/j.1365-2125.2011.04161.x

The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings

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