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Table 1 Characteristics of the studies assessing the correlation between the antimicrobial consumption and bacterial antimicrobial resistance using dynamic regression models

From: Usefulness of dynamic regression time series models for studying the relationship between antimicrobial consumption and bacterial antimicrobial resistance in hospitals: a systematic review

Reference

Country

Duration

Bacteria species studied

Antimicrobial studied

Sample type

AMR / AMC correlated (lag)

R² of the model

Aldeyab 2008

UK

60 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples from patients in the unit for > 48 hours, with deduplication + nasopharyngeal screening samples

MRSA / Macrolides (4 months), Fluoroquinolones (1 month)1, 3rd generation cephalosporins (2 months) and Amoxicillin – Clavulanic Acid (1 month)

78% 2

Bertrand 2012

France

108 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples from patients in the unit for > 48h or positive in the previous 12 months with deduplication

MRSA / Macrolides (2 months), Fluoroquinolones (2 months), Aminoglycoside (1 month)

41%2

Conlon-birgham 2019

UK

72

months

Staphylococcus aureus

All classes of antimicrobials

All types of samples from patients in the unit for > 48 hours, with deduplication of following 7 days samples + nasopharyngeal screening samples

MRSA / Macrolides (1 month), Fluoroquinolones (3 months) and Piperacillin-Tazobactam (1 month)

UC

Erdeljić 2011

Croatia

15 months

Pseudomonas aeruginosa

Piperacillin-Tazobactam, Ciprofloxacin and Carbapenems

All types of samples

Resistance to Ciprofloxacin / Ciprofloxacin (1month)

Resistance to Meropenem / Meropenem (0 months)

Resistance to Cefepime / Cefepime (2 months)

P.aeruginosa MDR / Meropenem (0 months)

UC

Gharbi 2015

UK

72 months

Klebsiella pneumoniae

Meropenem

All types of samples + rectal screening sample

K. pneumoniae OXA-48 / Meropenem (1 year)

79%

Hocquet 2008

France

84 months

Pseudomonas aeruginosa

Aminoglycosides, Fluoroquinolones, Cephalosporins,

Penicillins,

Carbapenems

All types of samples with deduplication

P. aeruginosa displaying MexXY-OprM overproduction / aminoglycoside (0,3,4,6 months) fluoroquinolone (0,5 and 6 months) and antipseudomonal cephalosporin (2 months)

P. aeruginosa displaying MexXY-OprM overproduction (negative correlation) / non-antipseudomonal cephalosporin (0,2 and months), penicillin (0,1,3 and 5 months) and carbapenem (0,2,5 and 6 months)

81%

Hsueh 2005

Taiwan

13 years

Escherichia coli

Pseudomonas aeruginosa

Cefotaxime, ceftazidime

All types of samples with deduplication in the following 7 days

Cefotaxime resistant E.coli / cefotaxime (NS)

Ceftazidime resistant P.aeruginosa / Ceftazidime (NS)

UC

Kaier 2009

Germany

34 months

Escherichia coli,

Enterobacter Cloacae, Klebsiella sp. Acinetobacter sp., Citrobacter sp.

All classes of antimicrobials

All types of samples from patients in the unit for > 48 hours, with deduplication + rectal screening sample

ESBL / 3rd generation Cephalosporins (3 months), Fluoroquinolones (1 month)

75%2

Kaier 2009

Germany

58 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples from patients in the unit for > 48 hours, with deduplication

MRSA /2nd generation Cephalosporins (1 month), 3rd generation Cephalosporins (3–4 months), Fluoroquinolones (4 month), Lincosamides (2 months)

66%2

Kousovista 2021

Greece

48 months

Acinetobacter baumannii

Cephalosporins, Fluoroquinolones,

Meropenem, Colistin

and Piperacillin-Tazobactam

All types of samples with deduplication

Resistance to Meropenem / Meropenem (2 month),

Resistance to Ciprofloxacin / Ciprofloxacin (1 month),

Resistance to Cefepime / Cefepime (2 months)

63%

66%

62%

Kritsotakis 2008

Greece

84 months

Enterococcus sp.

Amoxicillin-Clavulanic acid,

Piperacillin-Tazobactam, Cephalosporins, Fluoroquinolones, Carbapenems, Glycopeptides, Metronidazole, Clindamycin

All types of samples with deduplication + rectal screening sample

ERV / glycopeptides (1 month), 3rd generation Cephalosporins (1 month), Fluoroquinolones (2 months)

ERV (negative correlation) / Amoxicillin- Clavulanic Acid (6 months)

56%

Laffont-Lozes 2023

France

72 months

Escherichia coli

Penicillins, Amoxicillin-Clavulanic Acid, Piperacillin-Tazobactam, Cephalosporins, Fluoroquinolones, Carbapenems, Aminoglycosides, Sulfonamides

All types of samples from patients in the unit for > 48h or positive in the previous 1 months with deduplication

Resistance to Fluoroquinolones / Fluoroquinolones (0 to 5 months), Piperacillin-Tazobactam (0 to 3 months)

Amoxicillin-Clavulanic Acid resistance / Amoxicillin-Clavulanic Acid (0 to 1 months)

Penicillins resistance / 3rd generation Cephalosporins (5 and 8 months), Amoxicillin-Clavulanic Acid (0 and 5 months), Carbapenem (0 month)

Cephalosporins resistance / 4rd generation Cephalosporins (0 month), Piperacillin-Tazobactam (0 to 2 months), Fluoroquinolones (0 to 4 months)

54%

53%

36%

15%

Lee 2012

Taiwan

84 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples with deduplication

MRSA / penicillins, including b-lactamase inhibitors (1 month)

26%2

Lepper 2002

Germany

48 months

Pseudomonas aeruginosa

Imipenem, Cephalosporins, Aminoglycosides, Ciprofloxacin, Piperacillin-Tazobactam

All types of samples

Resistance to Ceftazidime / Imipenem (0 and 1 month)

Resistance to Piperacillin-tazobactam / Imipenem (0 and 1 month),

Resistance to imipenem / Imipenem (0 and 1 month)

UC

López-Lozano 2000

Spain

90 months

Pseudomonas aeruginosa, Escherichia coli, Proteus sp., Klebsiella sp., Enterobacter sp.

Ceftazidime and Imipenem

All types of samples with deduplication

Gram-negative bacilli Resistant to 3rd generation Cephalosporins / Ceftazidime

(1 month)

Pseudomonas aeruginosa resistant to Imipenem / Imipenem (1 month)

44%

63%

Mahamat 2005

France

84 months

Escherichia coli

Fluoroquinolones

Cytobacteriological urine examination with deduplication

Resistance to Ofloxacin / Ofloxacin (4 months), Ciprofloxacin (4 months)

Resistance to Ciprofloxacin / Ciprofloxacin (4 months), Ofloxacin (4 months)

64%

40%

Mahamat 2007

UK

96 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples with deduplication

MRSA / Macrolides (5 months), Fluoroquinolones (2 months)

UC

Monnet 2004

UK

55 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples except for nasopharyngeal screening samples

MRSA / 3rd generation Cephalosporins (4–7 months), Macrolides (1–3 months), Fluoroquinolones (4–5 months)

90%

O’Riordan 2022

Ireland

16 quarters

Enterobacterales and Enterococcus faecium

ceftriaxone, ciprofloxacin, levofloxacin, ertapenem, meropenem, piperacillin-tazobactam, gentamicin, co-trimoxazole and aztreonam; vancomycin

All types of samples with deduplication

E.coli 3rd generation Cephalosporins resistant (negative correlation) / Piperacillin-tazobactam (0 and 1 quarter)

86%

Ortiz-Brizuela 2020

Mexico

66 months

Enterobacterales

All classes of antimicrobials

All types of samples with deduplication

Resistance to Carbapenem non-susceptible Enterobacterales / Piperacillin- Tazobactam (6 months)

Resistance to carbapenemase-producing Enterobacteriaceae/ Piperacillin- Tazobactam (6 months)

Resistance to OXA-232 carbapenemase-producing Enterobacteriaceae / Piperacillin- Tazobactam (6 months)

21%

19%

24%

Qu 2019

China

60 months

Klebsiella pneumoniae

Doxycycline, Cephalosporins, Carbapenems

All types of samples with deduplication

Resistance to Carbapenems / Cephalosporins (0 and 1 quarter), Meropenem (0 and 1 quarter), Doxycyclin (2 quarters)

46–94% (according to antibiotic studied)

Tansarli 2018

Greece

174 months

Klebsiella pneumoniae

Colistin

Blood culture

Resistance to Colistin / Colistin (1 quarter)

69%

Tóth 2019

Hungary

142 months

Escherichia coli, Klebsiella pneumoniae, Klebsiella oxytoca, Pseudomonas aeruginosa, Acinetobacter baumannii

Cephalosporins, Carbapenems, Colistin

All types of samples, with deduplication during the following month

E.coli:

Resistance to Cephalosporins / Cephalosporins (1 month and 4 months)

Klebsiella pneumoniae:

Resistance to Cephalosporins/Cephalosporins (4 months and 5 months)

Resistance to Carbapenems/Carbapenems (6 months)

Pseudomonas aeruginosa:

Resistance to Cephalosporins/Cephalosporins (0 months)

Resistance to Carbapenems/Carbapenems (0 months and 1 month)

Acinetobacter baumannii:

Resistance to Carbapenems/Carbapenems (4 months)

UC

Vernaz 2008

Switzerland

80 months

Staphylococcus aureus

All classes of antimicrobials

All types of samples with deduplication

MRSA / Fluoroquinolones (1 month), Macrolides (1 and 4 month), Cephalosporins (3 to 5 month), Piperacillin-Tazobactam (3 month)

57%2

Vibet 2015

France

84 months

Enterobacterales

All classes of antimicrobials

All types of samples from patients in the unit for > 48 hours, with deduplication

ESBL / 3rd and 4th-generation cephalosporins (5 months), Fluoroquinolones

(3 months), Lincosamides (1 months), other antibacterial agents (4 months), Tetracyclines (3 months)

ESBL (negative correlation) / Nitrofurantoin (1month), Ticarcillin and piperacillin with or without enzyme inhibitor (4 month)

UC

Wang 2021

China

90 months

Klebsiella pneumoniae

Penicillins, Penicillins +

β-lactamases inhibitor, Cephalosporins, Carbapenems,

Aminoglycosides, Fluoroquinolones, Sulfonamides

All types of samples with deduplication

Resistance to Amikacin / Amikacin (0 months)

Resistance to Ciprofloxacin / Ciprofloxacin (0 months)

45%

62%

Willmann 2013

Germany

120 months

Pseudomonas aeruginosa

Carbapenems, Cephalosporins, Aminoglycosides, Fluoroquinolones and Piperacillin-Tazobactam

All types of samples with deduplication

Pseudomonas aeruginosa resistant to one or two antimicrobials classes / Cephalosporins (0 months)

Pseudomonas aeruginosa resistant to 3 or 4 antimicrobials classes / Meropenem (1 month)

UC

Zhang 2018

China

28 quarters

Staphylococcus aureus

All classes of antimicrobials

All types of samples with deduplication

MRSA / Monobactam (2 quarters), Imidazole (1 quarter), sulfonamides (1 quarter)

MRSA (negative correlation) / Glycopeptides (0 quarter), Oxazolidinone (2 quarters) aminoglycosides (2 quarters)

UC

  1. Correlation between MRSA emergence and macrolide use 4 months previously, correlation between MRSA emergence and fluoroquinolone use 1 month previously
  2. 2 Multivariate model also including infection control practices such as consumption of hydroalcoholic solution and/or promotion of hand hygiene and/or screening for the carriage of multi-resistant bacteria
  3. UK: United kingdom, MRSA: Methicillin-resistant Staphylococcus aureus, UC: Uncalculated, MDR: Multidrug resistant, NS: not studied, ESBL: Extended spectrum beta-lactamase, ERV: vancomycin-resistant Enterococcus