Authors:
, , , , , , , , , , , , , , , , , and
- ABSTRACT.
- INTRODUCTION
- METHODS
- RESULTS
- Trends in antimicrobial consumption.
- Trends in the numbers of isolates and proportion of carbapenem-resistant Gram-negative bacteria.
- Trend in the antimicrobial resistance of carbapenem-resistant Gram-negative bacteria.
- Association between antibiotic consumption and the prevalence of carbapenem-resistant Gram-negative bacteria.
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Friedman ND , Temkin E , Carmeli Y , 2016. The negative impact of antibiotic resistance. Clin Microbiol Infect 22: 416–422.
-
2.
Mendelson M , Matsoso MP , 2015. The World Health Organization Global Action Plan for antimicrobial resistance. S Afr Med J 105: 325.
-
3.
Thakur S , Gray GC , 2019. The mandate for a global “One Health” approach to antimicrobial resistance surveillance. Am J Trop Med Hyg 100: 227–228.
-
4.
Bell BG , Schellevis F , Stobberingh E , Goossens H , Pringle M , 2014. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis 14: 13.
-
5.
Klein EY , Van Boeckel TP , Martinez EM , Pant S , Gandra S , Levin SA , Goossens H , Laxminarayan R , 2018. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA 115: E3463–E3470.
-
6.
Van Boeckel TP , Gandra S , Ashok A , Caudron Q , Grenfell BT , Levin SA , Laxminarayan R , 2014. Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14: 742–750.
-
7.
Davey P , Marwick CA , Scott CL , Charani E , McNeil K , Brown E , Gould IM , Ramsay CR , Michie S , 2017. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2: CD003543.
-
8.
Friedman ND , Carmeli Y , Walton AL , Schwaber MJ , 2017. Carbapenem-resistant Enterobacteriaceae: a strategic roadmap for infection control. Infect Control Hosp Epidemiol 38: 580–594.
-
9.
Martin A , Fahrbach K , Zhao Q , Lodise T , 2018. Association between carbapenem resistance and mortality among adult, hospitalized patients with serious infections due to Enterobacteriaceae: results of a systematic literature review and meta-analysis. Open Forum Infect Dis 5: ofy150.
-
10.
Marchaim D et al., 2012. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship. Infect Control Hosp Epidemiol 33: 817–830.
-
11.
Hsueh PR , Chen WH , Luh KT , 2005. Relationships between antimicrobial use and antimicrobial resistance in Gram-negative bacteria causing nosocomial infections from 1991–2003 at a university hospital in Taiwan. Int J Antimicrob Agents 26: 463–472.
-
12.
Lee CM , Lai CC , Wang YY , Lee MC , Hsueh PR , 2013. Impact of susceptibility profiles of Gram-negative bacteria before and after the introduction of ertapenem at a medical center in northern Taiwan from 2004 to 2010. Diagn Microbiol Infect Dis 75: 94–100.
-
13.
Borg MA , Zarb P , Scicluna EA , Rasslan O , Gür D , Ben Redjeb S , Elnasser Z , Daoud Z , 2010. Antibiotic consumption as a driver for resistance in Staphylococcus aureus and Escherichia coli within a developing region. Am J Infect Control 38: 212–216.
-
14.
Lee MC , Lu CH , Lee WY , Lee CM , 2020. Correlation between nosocomial carriage of vancomycin-resistant enterococci and antimicrobial use in Taiwan. Am J Trop Med Hyg 104: 1131–1136.
-
15.
Zhu WM , Yuan Z , Zhou HY , 2020. Risk factors for carbapenem-resistant Klebsiella pneumoniae infection relative to two types of control patients: a systematic review and meta-analysis. Antimicrob Resist Infect Control 9: 23.
-
16.
Federico MP , Furtado GH , 2018. Immediate and later impacts of antimicrobial consumption on carbapenem-resistant Acinetobacter spp., Pseudomonas aeruginosa, and Klebsiella spp. in a teaching hospital in Brazil: a 10-year trend study. Eur J Clin Microbiol Infect Dis 37: 2153–2158.
-
17.
Taiwan Centers for Disease Control , n.d. Statistical Analysis of Nosocomial Infection Surveillance and Notification System. Available at: https://www.cdc.gov.tw/Category/MPage/4G8HuDdUN1k4xaBJhbPzKQ. Accessed April 4, 2022.
-
18.
Prakobsrikul N , Malathum K , Santanirand P , Chumnumwat S , Piebpien P , Montakantikul P , 2019. Correlation between antimicrobial consumption and the prevalence of carbapenem-resistant Escherichia coli and carbapenem-resistant Klebsiella pneumoniae at a university hospital in Thailand. J Clin Pharm Ther 44: 292–299.
-
19.
Yang P , Chen Y , Jiang S , Shen P , Lu X , Xiao Y , 2018. Association between antibiotic consumption and the rate of carbapenem-resistant Gram-negative bacteria from China based on 153 tertiary hospitals data in 2014. Antimicrob Resist Infect Control 7: 137.
-
20.
Lesho EP et al., 2015. Carbapenem-resistant Enterobacteriaceae and the correlation between carbapenem and fluoroquinolone usage and resistance in the US military health system. Diagn Microbiol Infect Dis 81: 119–125.
-
21.
Cannon JP , Lee TA , Clark NM , Setlak P , Grim SA , 2014. The risk of seizures among the carbapenems: a meta-analysis. J Antimicrob Chemother 69: 2043–2055.
-
22.
Zeng L , Zhang J , Li C , Fu Y , Zhao Y , Wang Y , Zhao J , Guo Y , Zhang X , 2020. The determination of gyrA and parC mutations and the prevalence of plasmid-mediated quinolone resistance genes in carbapenem resistant Klebsiella pneumonia ST11 and ST76 strains isolated from patients in Heilongjiang Province, China. Infect Genet Evol 82: 104319.
-
23.
Zhan Q , Xu Y , Wang B , Yu J , Shen X , Liu L , Cao X , Guo Y , Yu F , 2021. Distribution of fluoroquinolone resistance determinants in carbapenem-resistant Klebsiella pneumoniae clinical isolates associated with bloodstream infections in China. BMC Microbiol 21: 164.
-
24.
Liu P , Li X , Luo M , Xu X , Su K , Chen S , Qing Y , Li Y , Qiu J , 2018. Risk factors for carbapenem-resistant Klebsiella pneumoniae infection: a meta-analysis. Microb Drug Resist 24: 190–198.
-
25.
Akgul F , Bozkurt I , Sunbul M , Esen S , Leblebicioglu H , 2016. Risk factors and mortality in the carbapenem-resistant Klebsiella pneumoniae infection: case control study. Pathog Glob Health 110: 321–325.
-
26.
Wong A , 2017. Epistasis and the evolution of antimicrobial resistance. Front Microbiol 8: 246.
-
27.
Guo W , Sun F , Liu F , Cao L , Yang J , Chen Y , 2019. Antimicrobial resistance surveillance and prediction of Gram-negative bacteria based on antimicrobial consumption in a hospital setting: a 15-year retrospective study. Medicine (Baltimore) 98: e17157.
-
28.
López-Lozano JM et al., 2019. A nonlinear time-series analysis approach to identify thresholds in associations between population antibiotic use and rates of resistance. Nat Microbiol 4: 1160–1172.
-
29.
Huang F , Armando M , Dufau S , Florea O , Brouqui P , Boudjema S , 2021. COVID-19 outbreak and healthcare worker behavioural change toward hand hygiene practices. J Hosp Infect 111: 27–34.
-
30.
Grabowski ME , Kang H , Wells KM , Sifri CD , Mathers AJ , Lobo JM , 2017. Provider role in transmission of carbapenem-resistant Enterobacteriaceae. Infect Control Hosp Epidemiol 38: 1329–1334.
-
31.
Nicolas-Chanoine MH , Vigan M , Laouénan C , Robert J , 2019. Risk factors for carbapenem-resistant Enterobacteriaceae infections: a French case-control-control study. Eur J Clin Microbiol Infect Dis 38: 383–393.
-
32.
Predic M , Delano JP , Tremblay E , Iovine N , Brown S , Prins C , 2020. Evaluation of patient risk factors for infection with carbapenem-resistant Enterobacteriaceae. Am J Infect Control 48: 1028–1031.
-
33.
Hu L et al., 2014. The prevalence of carbapenemase genes and plasmid-mediated quinolone resistance determinants in carbapenem-resistant Enterobacteriaceae from five teaching hospitals in central China. Epidemiol Infect 142: 1972–1977.
-
34.
Peterson LR , 2005. Squeezing the antibiotic balloon: the impact of antimicrobial classes on emerging resistance. Clin Microbiol Infect 11 (Suppl 5):4–16.
-
35.
Bartley PS et al., 2019. Antibiotic resistance in Enterobacteriaceae from surface waters in urban Brazil highlights the risks of poor sanitation. Am J Trop Med Hyg 100: 1369–1377.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 4019 | 2104 | 398 |
| Full Text Views | 174 | 15 | 0 |
| PDF Downloads | 135 | 11 | 0 |
Association between Antimicrobial Consumption and the Prevalence of Nosocomial Carbapenem-Resistant Escherichia coli and Klebsiella pneumoniae in a Tertiary Hospital in Northern Taiwan
Mei-Chun Lee
Mei-Chun Lee
Department of Pharmacy, MacKay Memorial Hospital, Taipei, Taiwan;
Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan;
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Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan;
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Hsun Chang
Hsun Chang
Division of Infectious Diseases, Department of Internal Medicine, MacKay Memorial Hospital, Taipei, Taiwan;
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Fang-Ju Sun
Fang-Ju Sun
Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan;
Department of Medical Research, MacKay Memorial Hospital, Taipei, Taiwan;
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Department of Medical Research, MacKay Memorial Hospital, Taipei, Taiwan;
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Alice Ying-Jung Wu
Alice Ying-Jung Wu
Division of Infectious Diseases, Department of Internal Medicine, MacKay Memorial Hospital, Taipei, Taiwan;
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Chien-Hung Lu
Chien-Hung Lu
Department of Pharmacy, MacKay Memorial Hospital, Taipei, Taiwan;
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Chun-Ming Lee
Chun-Ming Lee
Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan;
Division of Infectious Diseases, Department of Internal Medicine, MacKay Memorial Hospital, Taipei, Taiwan;
MacKay Medical College, New Taipei City, Taiwan;
Department of Internal Medicine, St. Joseph’s Hospital, Yunlin County, Taiwan
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Division of Infectious Diseases, Department of Internal Medicine, MacKay Memorial Hospital, Taipei, Taiwan;
MacKay Medical College, New Taipei City, Taiwan;
Department of Internal Medicine, St. Joseph’s Hospital, Yunlin County, Taiwan
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ABSTRACT.
Carbapenem-resistant Enterobacteriales has become a threat in Taiwan. This is the first local study focusing on the association between carbapenem-resistant Enterobacteriales and antimicrobial consumption. From January 2012 to December 2020, data were collected in a tertiary care hospital in Taipei, Taiwan. Antimicrobial consumption was estimated by the defined daily dose/1,000 patient-days. During the same period, the prevalence of carbapenem-resistant Escherichia coli (CREC) and carbapenem-resistant Klebsiella pneumoniae (CRKP) were collected through routine surveillance data. The following retrospective analyses were conducted: 1) analysis of antimicrobial consumption over time, (2) analysis and forecast of CREC and CRKP prevalence over time, and 3) analysis of correlation between antimicrobial consumption and the prevalence of CREC and CRKP. The consumption of piperacillin/tazobactam (β = 0.615), fluoroquinolones (β = 0.856), meropenem (β = 0.819), and doripenem (β = 0.891) increased during the observation period (P < 0.001), and the consumption of aminoglycosides (β = −0.852) and imipenem/cilastatin (β = −0.851) decreased (P < 0.001). The prevalence of CRKP rose over time (β = 0.522, P = 0.001) and correlated positively with the consumption of fluoroquinolones, levofloxacin, penicillin/β-lactamase inhibitor, piperacillin/tazobactam, meropenem, and doripenem (P < 0.05). The prevalence of CRKP and CREC both correlated negatively with consumption of aminoglycosides (P < 0.01). The prevalence of CRKP in our hospital increased as the forecast predicted based on an autoregressive integrated moving average model. This study provides alarming messages for members participating in antimicrobial stewardship programs, including the increasing prevalence of CRKP, the increasing consumption of broad-spectrum antibiotics, and the positive correlation between them.
- Supplemental Materials (PDF 95 KB)
Author Notes
These authors contributed equally to this work.
Authors’ addresses: Mei-Chun Lee, Department of Pharmacy, MacKay Memorial Hospital, Taipei, Taiwan, and Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan, E-mail: a5787@mmh.org.tw. Hsun Chang and Alice Ying-Jung Wu, Division of Infectious Diseases, Department of Internal Medicine, MacKay Memorial Hospital, Taipei, Taiwan, E-mails: rrscbta24@gmail.com and watrlilies@gmail.com. Fang-Ju Sun, Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan, and Department of Medical Research, MacKay Memorial Hospital, Taipei, Taiwan, E-mail: fjsun.b612@mmh.org.tw. Chien-Hung Lu, Department of Pharmacy, MacKay Memorial Hospital, Taipei, Taiwan, E-mail: horng22@mmh.org.tw. Chun-Ming Lee, Nursing and Management, Mackay Junior College of Medicine, Taipei, Taiwan, Division of Infectious Diseases, Department of Internal Medicine, MacKay Memorial Hospital, Taipei, Taiwan, MacKay Medical College, New Taipei City, Taiwan, and Department of Internal Medicine, St. Joseph’s Hospital, Yunlin County, Taiwan, E-mail: leecm4014@yahoo.com.tw.
- ABSTRACT.
- INTRODUCTION
- METHODS
- RESULTS
- Trends in antimicrobial consumption.
- Trends in the numbers of isolates and proportion of carbapenem-resistant Gram-negative bacteria.
- Trend in the antimicrobial resistance of carbapenem-resistant Gram-negative bacteria.
- Association between antibiotic consumption and the prevalence of carbapenem-resistant Gram-negative bacteria.
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Friedman ND , Temkin E , Carmeli Y , 2016. The negative impact of antibiotic resistance. Clin Microbiol Infect 22: 416–422.
-
2.
Mendelson M , Matsoso MP , 2015. The World Health Organization Global Action Plan for antimicrobial resistance. S Afr Med J 105: 325.
-
3.
Thakur S , Gray GC , 2019. The mandate for a global “One Health” approach to antimicrobial resistance surveillance. Am J Trop Med Hyg 100: 227–228.
-
4.
Bell BG , Schellevis F , Stobberingh E , Goossens H , Pringle M , 2014. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis 14: 13.
-
5.
Klein EY , Van Boeckel TP , Martinez EM , Pant S , Gandra S , Levin SA , Goossens H , Laxminarayan R , 2018. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA 115: E3463–E3470.
-
6.
Van Boeckel TP , Gandra S , Ashok A , Caudron Q , Grenfell BT , Levin SA , Laxminarayan R , 2014. Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14: 742–750.
-
7.
Davey P , Marwick CA , Scott CL , Charani E , McNeil K , Brown E , Gould IM , Ramsay CR , Michie S , 2017. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2: CD003543.
-
8.
Friedman ND , Carmeli Y , Walton AL , Schwaber MJ , 2017. Carbapenem-resistant Enterobacteriaceae: a strategic roadmap for infection control. Infect Control Hosp Epidemiol 38: 580–594.
-
9.
Martin A , Fahrbach K , Zhao Q , Lodise T , 2018. Association between carbapenem resistance and mortality among adult, hospitalized patients with serious infections due to Enterobacteriaceae: results of a systematic literature review and meta-analysis. Open Forum Infect Dis 5: ofy150.
-
10.
Marchaim D et al., 2012. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship. Infect Control Hosp Epidemiol 33: 817–830.
-
11.
Hsueh PR , Chen WH , Luh KT , 2005. Relationships between antimicrobial use and antimicrobial resistance in Gram-negative bacteria causing nosocomial infections from 1991–2003 at a university hospital in Taiwan. Int J Antimicrob Agents 26: 463–472.
-
12.
Lee CM , Lai CC , Wang YY , Lee MC , Hsueh PR , 2013. Impact of susceptibility profiles of Gram-negative bacteria before and after the introduction of ertapenem at a medical center in northern Taiwan from 2004 to 2010. Diagn Microbiol Infect Dis 75: 94–100.
-
13.
Borg MA , Zarb P , Scicluna EA , Rasslan O , Gür D , Ben Redjeb S , Elnasser Z , Daoud Z , 2010. Antibiotic consumption as a driver for resistance in Staphylococcus aureus and Escherichia coli within a developing region. Am J Infect Control 38: 212–216.
-
14.
Lee MC , Lu CH , Lee WY , Lee CM , 2020. Correlation between nosocomial carriage of vancomycin-resistant enterococci and antimicrobial use in Taiwan. Am J Trop Med Hyg 104: 1131–1136.
-
15.
Zhu WM , Yuan Z , Zhou HY , 2020. Risk factors for carbapenem-resistant Klebsiella pneumoniae infection relative to two types of control patients: a systematic review and meta-analysis. Antimicrob Resist Infect Control 9: 23.
-
16.
Federico MP , Furtado GH , 2018. Immediate and later impacts of antimicrobial consumption on carbapenem-resistant Acinetobacter spp., Pseudomonas aeruginosa, and Klebsiella spp. in a teaching hospital in Brazil: a 10-year trend study. Eur J Clin Microbiol Infect Dis 37: 2153–2158.
-
17.
Taiwan Centers for Disease Control , n.d. Statistical Analysis of Nosocomial Infection Surveillance and Notification System. Available at: https://www.cdc.gov.tw/Category/MPage/4G8HuDdUN1k4xaBJhbPzKQ. Accessed April 4, 2022.
-
18.
Prakobsrikul N , Malathum K , Santanirand P , Chumnumwat S , Piebpien P , Montakantikul P , 2019. Correlation between antimicrobial consumption and the prevalence of carbapenem-resistant Escherichia coli and carbapenem-resistant Klebsiella pneumoniae at a university hospital in Thailand. J Clin Pharm Ther 44: 292–299.
-
19.
Yang P , Chen Y , Jiang S , Shen P , Lu X , Xiao Y , 2018. Association between antibiotic consumption and the rate of carbapenem-resistant Gram-negative bacteria from China based on 153 tertiary hospitals data in 2014. Antimicrob Resist Infect Control 7: 137.
-
20.
Lesho EP et al., 2015. Carbapenem-resistant Enterobacteriaceae and the correlation between carbapenem and fluoroquinolone usage and resistance in the US military health system. Diagn Microbiol Infect Dis 81: 119–125.
-
21.
Cannon JP , Lee TA , Clark NM , Setlak P , Grim SA , 2014. The risk of seizures among the carbapenems: a meta-analysis. J Antimicrob Chemother 69: 2043–2055.
-
22.
Zeng L , Zhang J , Li C , Fu Y , Zhao Y , Wang Y , Zhao J , Guo Y , Zhang X , 2020. The determination of gyrA and parC mutations and the prevalence of plasmid-mediated quinolone resistance genes in carbapenem resistant Klebsiella pneumonia ST11 and ST76 strains isolated from patients in Heilongjiang Province, China. Infect Genet Evol 82: 104319.
-
23.
Zhan Q , Xu Y , Wang B , Yu J , Shen X , Liu L , Cao X , Guo Y , Yu F , 2021. Distribution of fluoroquinolone resistance determinants in carbapenem-resistant Klebsiella pneumoniae clinical isolates associated with bloodstream infections in China. BMC Microbiol 21: 164.
-
24.
Liu P , Li X , Luo M , Xu X , Su K , Chen S , Qing Y , Li Y , Qiu J , 2018. Risk factors for carbapenem-resistant Klebsiella pneumoniae infection: a meta-analysis. Microb Drug Resist 24: 190–198.
-
25.
Akgul F , Bozkurt I , Sunbul M , Esen S , Leblebicioglu H , 2016. Risk factors and mortality in the carbapenem-resistant Klebsiella pneumoniae infection: case control study. Pathog Glob Health 110: 321–325.
-
26.
Wong A , 2017. Epistasis and the evolution of antimicrobial resistance. Front Microbiol 8: 246.
-
27.
Guo W , Sun F , Liu F , Cao L , Yang J , Chen Y , 2019. Antimicrobial resistance surveillance and prediction of Gram-negative bacteria based on antimicrobial consumption in a hospital setting: a 15-year retrospective study. Medicine (Baltimore) 98: e17157.
-
28.
López-Lozano JM et al., 2019. A nonlinear time-series analysis approach to identify thresholds in associations between population antibiotic use and rates of resistance. Nat Microbiol 4: 1160–1172.
-
29.
Huang F , Armando M , Dufau S , Florea O , Brouqui P , Boudjema S , 2021. COVID-19 outbreak and healthcare worker behavioural change toward hand hygiene practices. J Hosp Infect 111: 27–34.
-
30.
Grabowski ME , Kang H , Wells KM , Sifri CD , Mathers AJ , Lobo JM , 2017. Provider role in transmission of carbapenem-resistant Enterobacteriaceae. Infect Control Hosp Epidemiol 38: 1329–1334.
-
31.
Nicolas-Chanoine MH , Vigan M , Laouénan C , Robert J , 2019. Risk factors for carbapenem-resistant Enterobacteriaceae infections: a French case-control-control study. Eur J Clin Microbiol Infect Dis 38: 383–393.
-
32.
Predic M , Delano JP , Tremblay E , Iovine N , Brown S , Prins C , 2020. Evaluation of patient risk factors for infection with carbapenem-resistant Enterobacteriaceae. Am J Infect Control 48: 1028–1031.
-
33.
Hu L et al., 2014. The prevalence of carbapenemase genes and plasmid-mediated quinolone resistance determinants in carbapenem-resistant Enterobacteriaceae from five teaching hospitals in central China. Epidemiol Infect 142: 1972–1977.
-
34.
Peterson LR , 2005. Squeezing the antibiotic balloon: the impact of antimicrobial classes on emerging resistance. Clin Microbiol Infect 11 (Suppl 5):4–16.
-
35.
Bartley PS et al., 2019. Antibiotic resistance in Enterobacteriaceae from surface waters in urban Brazil highlights the risks of poor sanitation. Am J Trop Med Hyg 100: 1369–1377.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 4019 | 2104 | 398 |
| Full Text Views | 174 | 15 | 0 |
| PDF Downloads | 135 | 11 | 0 |