- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Study design.
- Patients.
- Data collection.
- Sample collection and processing.
- Antimicrobial susceptibility testing (AST).
- Storage of quinolone-resistant isolates.
- Biofilm production by the microtiter plate method.
- Minimum inhibitory concentration determination.
- Minimum biofilm inhibitory concentration determination.
- Molecular analysis.
- STATISTICAL ANALYSES
- RESULTS
- Age and sex distributions of COVID-19 patients.
- Incidence(s) of bacterial infection in COVID-19 patients.
- Bacterial species isolated from COVID-19 patients.
- Antimicrobial susceptibility profile of the isolates.
- Biofilm formation among multidrug-resistant (MDR) and non-MDR isolates.
- Minimal inhibitory concentration and MBIC trends for quinolones.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in E. coli.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in C. freundii.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in K. pneumoniae.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in ACB complex.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in S. aureus.
- In vitro quinolone susceptibilities and PMQR genes in other infrequent isolates.
- Fold changes from MIC-to-MBIC values among F-GNB.
- Fold changes from MIC-to-MBIC values among NF-GNB.
- Fold changes from MIC-to-MBIC values among GPC.
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Macia MD, Rojo-Molinero E, Oliver A, 2014. Antimicrobial susceptibility testing in biofilm-growing bacteria. Clin Microbiol Infect 20: 981–990.
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Thieme L, Hartung A, Tramm K, Klinger-Strobel M, Jandt KD, Makarewicz O, Pletz MW, 2019. MBEC versus MBIC: The lack of differentiation between biofilm reducing and inhibitory effects as a current problem in biofilm methodology. Biol Proced Online 21: 18.
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Stefanini I, De Renzi G, Foddai E, Cordani E, Mognetti B, 2021. Profile of bacterial infections in COVID-19 patients: Antimicrobial resistance in the time of SARS-CoV-2. Biology (Basel) 10: 822.
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Hedberg P, Johansson N, Ternhag A, Abdel-Halim L, Hedlund J, Nauclér P, 2022. Bacterial co-infections in community-acquired pneumonia caused by SARS-CoV-2, influenza virus and respiratory syncytial virus. BMC Infect Dis 22: 108–111.
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Biofilm Formation and Plasmid-Mediated Quinolone Resistance Genes at Varying Quinolone Inhibitory Concentrations in Quinolone-Resistant Bacteria Superinfecting COVID-19 Inpatients
Ajaya Basnet
Ajaya Basnet
Department of Medical Microbiology, Shi-Gan International College of Science and Technology, Tribhuvan University, Kathmandu, Nepal;
Department of Microbiology, Nepal Armed Police Force Hospital, Kathmandu, Nepal;
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Department of Microbiology, Nepal Armed Police Force Hospital, Kathmandu, Nepal;
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Arun Bahadur Chand
Arun Bahadur Chand
Department of Microbiology, KIST Medical College and Teaching Hospital, Lalitpur, Nepal;
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Sohani Bajracharya
Sohani Bajracharya
Department of Microbiology, Kanti Children’s Hospital, Kathmandu, Nepal;
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Mahendra Raj Shrestha
Mahendra Raj Shrestha
Department of Clinical Laboratory, Nepal Armed Police Force Hospital, Kathmandu, Nepal;
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Shila Shrestha
Shila Shrestha
Department of Medical Microbiology, Shi-Gan International College of Science and Technology, Tribhuvan University, Kathmandu, Nepal;
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Basanta Tamang
Basanta Tamang
Department of Microbiology, Nepal Armed Police Force Hospital, Kathmandu, Nepal;
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Maina Dulal
Maina Dulal
Department of Medical Microbiology, Shi-Gan International College of Science and Technology, Tribhuvan University, Kathmandu, Nepal;
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Nayanum Pokhrel
drmahendrapath@gmail.com
Nayanum Pokhrel
Research Section, Nepal Health Research Council, Kathmandu, Nepal;
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Lok Bahadur Shrestha
Lok Bahadur Shrestha
School of Medical Sciences and The Kirby Institute, University of New South Wales, Sydney, Australia
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ABSTRACT.
The likelihood of antimicrobial failure in COVID-19 patients with bacterial superinfection arises from both phenotypic (biofilms) and genotypic mechanisms. This cross-sectional study aimed to determine the inhibitory concentrations of quinolones—nalidixic acid, norfloxacin, ciprofloxacin, ofloxacin, and levofloxacin—in biofilm formers (minimum biofilm inhibitory concentration [MBIC]) and nonformers (minimum inhibitory concentration [MIC]) and correlate inhibitory concentrations with plasmid-mediated quinolone resistance (PMQR) genes in quinolone-resistant bacteria isolated from COVID-19 inpatients. Quinolone-resistant bacteria (n = 193), verified through disc diffusion, were tested for quinolone inhibitory concentrations using broth microdilution and biofilm formation using microtiter plate methods. The polymerase chain reaction was used to detect PMQR genes. Study variables were analyzed using SPSS v.17.0, with a significance level set at P <0.05. MIC-to-MBIC median fold increases for ciprofloxacin, ofloxacin, and levofloxacin were 128 (2–8,192), 64 (4–1,024), and 32 (4–512) in gram-positive cocci (GPC, n = 43), respectively, whereas they were 32 (4–8,192), 32 (4–2,048), and 16 (2–1,024) in fermentative gram-negative bacilli (F-GNB, n = 126) and 16 (4–4,096), 64 (2–64), and 16 (8–512) in nonfermentative gram-negative bacilli (NF-GNB, n = 24). In biofilm-forming F-GNB and NF-GNB, qnrB (10/32 versus 3/10), aac(6′)-Ib-cr (10/32 versus 4/10), and qnrS (9/32 versus 0/10) genes were detected. A 32-fold median increase in the MIC-to-MBIC of ciprofloxacin was significantly (P <0.05) associated with qnrA in F-GNB and qnrS in NF-GNB. Biofilms formed by F-GNB and NF-GNB were significantly associated with the aac(6′)-Ib-cr and qnrS genes, respectively. Nearly one-third of the superinfecting bacteria in COVID-19 patients formed biofilms and had at least one PMQR gene, thus increasing the need for quinolones at higher inhibitory concentrations.
- Supplemental Materials (PDF 2610.0 KB)
Author Notes
Financial support: This study was funded by the
Disclosures: Ethical approval (2078.03.03) was obtained from the Institutional Review Committee of the Shi-Gan Health Foundation in Kathmandu, Nepal. Written informed consent was obtained from patients or their relatives (if the patient was incapable) before sample collection.
Current contact information: Ajaya Basnet, Department of Medical Microbiology, Shi-Gan International College of Science and Technology, Tribhuvan University, Kathmandu, Nepal, and Department of Microbiology, Nepal Armed Police Force Hospital, Kathmandu, Nepal, E-mail: abasnet.microbereserach@gmail.com. Arun Bahadur Chand, Department of Microbiology, KIST Medical College and Teaching Hospital, Lalitpur, Nepal, E-mail: arunbchand@gmail.com. Sohani Bajracharya, Department of Microbiology, Kanti Children’s Hospital, Kathmandu, Nepal, E-mail: bjr.sohani@gmail.com. Mahendra Raj Shrestha, Department of Clinical Laboratory, Nepal Armed Police Force Hospital, Kathmandu, Nepal, E-mail: xlcprk@gmail.com. Shila Shrestha and Maina Dulal, Department of Medical Microbiology, Shi-Gan International College of Science and Technology, Tribhuvan University, Kathmandu, Nepal, E-mails: microbiologistshila@gmail.com and timalsinamaina@gmail.com. Basanta Tamang, Department of Microbiology, Nepal Armed Police Force Hospital, Kathmandu, Nepal, E-mail: tamangbasanta222@yahoo.com. Nayanum Pokhrel, Research Section, Nepal Health Research Council, Kathmandu, Nepal, E-mail: drmahendrapath@gmail.com. Lok Bahadur Shrestha, School of Medical Sciences and The Kirby Institute, University of New South Wales, Sydney, Australia, E-mail: lok.shrestha@bpkihs.edu.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Study design.
- Patients.
- Data collection.
- Sample collection and processing.
- Antimicrobial susceptibility testing (AST).
- Storage of quinolone-resistant isolates.
- Biofilm production by the microtiter plate method.
- Minimum inhibitory concentration determination.
- Minimum biofilm inhibitory concentration determination.
- Molecular analysis.
- STATISTICAL ANALYSES
- RESULTS
- Age and sex distributions of COVID-19 patients.
- Incidence(s) of bacterial infection in COVID-19 patients.
- Bacterial species isolated from COVID-19 patients.
- Antimicrobial susceptibility profile of the isolates.
- Biofilm formation among multidrug-resistant (MDR) and non-MDR isolates.
- Minimal inhibitory concentration and MBIC trends for quinolones.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in E. coli.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in C. freundii.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in K. pneumoniae.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in ACB complex.
- Plasmid-mediated quinolone resistance genes and MIC and MBIC values in S. aureus.
- In vitro quinolone susceptibilities and PMQR genes in other infrequent isolates.
- Fold changes from MIC-to-MBIC values among F-GNB.
- Fold changes from MIC-to-MBIC values among NF-GNB.
- Fold changes from MIC-to-MBIC values among GPC.
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Zhu Z, Lian X, Su X, Wu W, Marraro GA, Zeng Y, 2020. From SARS and MERS to COVID-19: A brief summary and comparison of severe acute respiratory infections caused by three highly pathogenic human coronaviruses. Respir Res 21: 224–214.
-
2.
Huang J, Teoh JYC, Wong SH, Wong MC, 2020. The potential impact of previous exposure to SARS or MERS on control of the COVID-19 pandemic. Eur J Epidemiol 35: 1099–1103.
-
3.
Feldman C, Anderson R, 2021. The role of co-infections and secondary infections in patients with COVID-19. Pneumonia (Nathan) 13: 5.
-
4.
Soltani S, Faramarzi S, Zandi M, Shahbahrami R, Jafarpour A, Akhavan Rezayat S, Pakzad I, Abdi F, Malekifar P, Pakzad R, 2021. Bacterial coinfection among coronavirus disease 2019 patient groups: An updated systematic review and meta-analysis. New Microbes New Infect 43: 100910.
-
5.
Westblade LF, Simon MS, Satlin MJ, 2021. Bacterial coinfections in coronavirus disease 2019. Trends Microbiol 29: 930–941.
-
6.
Langford BJ, So M, Raybardhan S, Leung V, Westwood D, MacFadden DR, Soucy JR, Daneman N, 2020. Bacterial co-infection and secondary infection in patients with COVID-19: A living rapid review and meta-analysis. Clin Microbiol Infect 26: 1622–1629.
-
7.
Reygaert WC, 2018. An overview of the antimicrobial resistance mechanisms of bacteria. AIMS Microbiol 4: 482–501.
-
8.
Redgrave LS, Sutton SB, Webber MA, Piddock LJ, 2014. Fluoroquinolone resistance: Mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22: 438–445.
-
9.
Yang P, Chen Y, Jiang S, Shen P, Lu X, Xiao Y, 2020. Association between the rate of fluoroquinolones-resistant gram-negative bacteria and antibiotic consumption from China based on 145 tertiary hospitals data in 2014. BMC Infect Dis 20: 269–210.
-
10.
Sharma D, Misba L, Khan AU, 2019. Antibiotics versus biofilm: An emerging battleground in microbial communities. Antimicrob Resist Infect Control 8: 76.
-
11.
Ramadan R, Omar N, Dawaba M, Moemen D, 2021. Bacterial biofilm dependent catheter associated urinary tract infections: Characterization, antibiotic resistance pattern and risk factors. Egypt J Basic Appl Sci 8: 64–74.
-
12.
Subramanian P, Shanmugam N, Sivaraman U, Kumar S, Selvaraj S, 2012. Antiobiotic resistance pattern of biofilm-forming uropathogens isolated from catheterised patients in Pondicherry.Australas Med J 5: 344–348.
-
13.
Macia MD, Rojo-Molinero E, Oliver A, 2014. Antimicrobial susceptibility testing in biofilm-growing bacteria. Clin Microbiol Infect 20: 981–990.
-
14.
Thieme L, Hartung A, Tramm K, Klinger-Strobel M, Jandt KD, Makarewicz O, Pletz MW, 2019. MBEC versus MBIC: The lack of differentiation between biofilm reducing and inhibitory effects as a current problem in biofilm methodology. Biol Proced Online 21: 18.
-
15.
Procop GW, Church DL, Hall GS, Janda WM, 2020. Koneman’s Color Atlas and Textbook of Diagnostic Microbiology. Burlington, MA: Jones & Bartlett Learning.
-
16.
Russell CD et al., 2021. Co-infections, secondary infections, and antimicrobial use in patients hospitalised with COVID-19 during the first pandemic wave from the ISARIC WHO CCP-UK study: A multicentre, prospective cohort study. Lancet Microbe 2: e354–e365.
-
17.
Humphries R, Bobenchik AM, Hindler JA, Schuetz AN, 2021. Overview of changes to the Clinical and Laboratory Standards Institute performance standards for antimicrobial susceptibility testing, M100. J Clin Microbiol 59: e0021321.
-
18.
Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, Beachey EH, 1985. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: A quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22: 996–1006.
-
19.
Waitz JA, 1990. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. Villanova, PA: National Committee for Clinical Laboratory Standards.
-
20.
Ankit G, 2015. Biofilm quantification and comparative analysis of MIC (minimum inhibitory concentration) & MBIC (minimum biofilm inhibitory concentration) value for different antibiotics against E. coli. Int J Curr Microbiol Appl Sci 4: 198–224.
-
21.
Green MR, Sambrook J, 2016. Preparation of plasmid DNA by alkaline lysis with sodium dodecyl sulfate: Minipreps. Cold Spring Harb Protoc 2016: pdb-prot093344.
-
22.
Xing QS et al., 2020. Precautions are needed for COVID-19 patients with coinfection of common respiratory pathogens. medRxiv doi: 10.1101/2020.02.29.20027698.
-
23.
Stefanini I, De Renzi G, Foddai E, Cordani E, Mognetti B, 2021. Profile of bacterial infections in COVID-19 patients: Antimicrobial resistance in the time of SARS-CoV-2. Biology (Basel) 10: 822.
-
24.
Hedberg P, Johansson N, Ternhag A, Abdel-Halim L, Hedlund J, Nauclér P, 2022. Bacterial co-infections in community-acquired pneumonia caused by SARS-CoV-2, influenza virus and respiratory syncytial virus. BMC Infect Dis 22: 108–111.
-
25.
Kaplan E, Marano RB, Jurkevitch E, Cytryn E, 2018. Enhanced bacterial fitness under residual fluoroquinolone concentrations is associated with increased gene expression in wastewater-derived qnr plasmid-harboring strains. Front Microbiol 9: 1176.
-
26.
Zhou F et al., 2020. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 395: 1054–1062.
-
27.
Huang C et al., 2020. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395: 497–506.
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