ANTIBIOTIC SUSCEPTIBILITY PATTERN AND BIOFILM-FORMING POTENTIAL OF GRAM-NEGATIVE CLINICAL BACTERIAL ISOLATES
Main Article Content
Keywords
Gram-negative, Biofilm, Virulence, Antimicrobial resistance, MDR
Abstract
Bacteria can shift between planktonic forms (living as single cells) or establishing communities in the form of biofilms, rising on hard surfaces or rooted in a layer of exopolysaccharides (EPS). Biofilm formation by pathogens reduces vulnerability to antimicrobial treatments by making them more virulent and it may result in the development of persistent infections; hence, microbial biofilm can add to its pathogenesis. This study was designed to determine the biofilm forming potential of clinically isolated Gram-negative bacteria, and its relationship with antibiotic resistance. A total of 150 Gram-negative clinical samples were collected from Memon Medical Institute (MMI) Hospital in Karachi, Pakistan. To screen bacteria for the production of biofilm, Congo Red Agar (CRA) method was used. Quantitative analysis for No/Weak/Moderate and Strong biofilm producers was done with microtiter plate method.Furthermore, the crystal violet staining was also used by taking optical density (OD) at 595nm. Antibiogram pattern of strong biofilm forming isolates was done using clinical laboratory standards institute (CLSI) guidelines and the bacteria was classified as resistant to one, two and multi drug resistant (MDR). Most of the strong biofilm forming bacteria were observed as MDR (84.61%) which clearly reveals the involvement of biofilm in increased antimicrobial drug resistance. Monoplex PCR (polymerase chain reaction) expressed the presences of papC biofilm associated gene in five strong biofilm forming isolates.
References
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29. Habib, A.; Lo, S.; Villageois-Tran, K.; Petitjean, M.; Malik, S.A.; Armand-Lefevre, L.; Ruppe, E.; Zahra, R. Dissemination of carbapenemase-producing Enterobacterales in the community of Rawalpindi, Pakistan. Plos one 2022, 17, e0270707.
30. Ahmed, N.; Tahir, K.; Aslam, S.; Cheema, S.M.; Rabaan, A.A.; Turkistani, S.A.; Garout, M.; Halwani, M.A.; Aljeldah, M.; Al Shammari, B.R. Heavy Metal (Arsenic) Induced Antibiotic Resistance among Extended-Spectrum β-Lactamase (ESBL) Producing Bacteria of Nosocomial Origin. Pharmaceuticals 2022, 15, 1426.
31. Ahmed, N.; Zeshan, B.; Naveed, M.; Afzal, M.; Mohamed, M. Antibiotic resistance profile in relation to virulence genes fimH, hlyA and usp of uropathogenic E. coli isolates in Lahore, Pakistan. Trop. Biomed 2019, 36, 559-568.
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33. Ahmed, N.; Khalid, H.; Mushtaq, M.; Basha, S.; Rabaan, A.A.; Garout, M.; Halwani, M.A.; Al Mutair, A.; Alhumaid, S.; Al Alawi, Z. The Molecular Characterization of Virulence Determinants and Antibiotic Resistance Patterns in Human Bacterial Uropathogens. Antibiotics 2022, 11, 516.
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35. Zahra, N.; Zeshan, B.; Qadri, M.M.A.; Ishaq, M.; Afzal, M.; Ahmed, N. Phenotypic and genotypic evaluation of antibiotic resistance of Acinetobacter baumannii bacteria isolated from surgical intensive care unit patients in Pakistan. Jundishapur Journal of Microbiology 2021, 14.
36. Zeshan, B.; Karobari, M.I.; Afzal, N.; Siddiq, A.; Basha, S.; Basheer, S.N.; Peeran, S.W.; Mustafa, M.; Daud, N.H.A.; Ahmed, N. The usage of antibiotics by COVID-19 patients with comorbidities: the risk of increased antimicrobial resistance. Antibiotics 2021, 11, 35.
37. Hasan, D.L.; Khalid, H.M.; Mero, W.M. Phenotypic and Molecular Study of Extended-Spectrum β-lactamases Producing Enterobacteriaceae from Urinary Tract Infection in Zakho city, Kurdistan Region/Iraq. Academic Journal of Nawroz University 2022, 11, 305-313.
38. Rizvi, A.; Saeed, M.U.; Nadeem, A.; Yaqoob, A.; Rabaan, A.A.; Bakhrebah, M.A.; Al Mutair, A.; Alhumaid, S.; Aljeldah, M.; Al Shammari, B.R. Evaluation of Bi-Lateral Co-Infections and Antibiotic Resistance Rates among COVID-19 Patients in Lahore, Pakistan. Medicina 2022, 58, 904.
39. Wayne, P. Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing. 2011.
40. Mustafai, M.M.; Hafeez, M.; Munawar, S.; Basha, S.; Rabaan, A.A.; Halwani, M.A.; Alawfi, A.; Alshengeti, A.; Najim, M.A.; Alwarthan, S. Prevalence of Carbapenemase and Extended-Spectrum β-Lactamase Producing Enterobacteriaceae: A Cross-Sectional Study. Antibiotics 2023, 12, 148.
41. Abe, R.; Akeda, Y.; Iida, T.; Hamada, S. Population Analysis Profiling: Is It Still the Gold Standard for the Determination of Heteroresistance in Carbapenemase-Producing Enterobacteriaceae? 2022, 106644.
42. Dhital, R.; Shen, Z.; Zhang, S.; Mustapha, A. Detection of virulence and extended spectrum β‐lactamase genes in Salmonella by multiplex high‐resolution melt curve real‐time PCR assay. Journal of Applied Microbiology 2022, 132, 2355-2367.
43. Naderi Mezajin, M.; Fatemizadeh, M.; Rostami, Z.; Khaki, P.; Shirzad, M.; Noorbakhsh, F. Antibiotic resistance pattern and frequency of SHV, CTX, TEM, and OXA resistance gene among salmonella serotypes. Health Biotechnology and Biopharma (HBB) 2022, 6, 64-77.
44. Suranadee, Y.; Jyalathacrachchi, H.; Gamage, S.; Gunasekara, S. P32 Occurrence of bla KPC, bla NDM and bla OXA-48 genes among carbapenemase-producing Enterobacteriaceae (CRE) in National Cancer Institute, Sri Lanka. JAC-Antimicrobial Resistance 2022, 4, dlac004. 031.
45. Mohammed, A.B.; Anwar, K.A. Phenotypic and genotypic detection of extended spectrum beta lactamase enzyme in Klebsiella pneumoniae. PloS one 2022, 17, e0267221.
46 Fattahi, S., Kafil, H. S., Nahai, M. R., Asgharzadeh, M., Nori, R., & Aghazadeh, M. (2015). Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS hygiene and infection control, 10, Doc11. https://doi.org/10.3205/dgkh000254
2. Cantón, R.; Morosini, M.-I. Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS microbiology reviews 2011, 35, 977-991.
3. Rabaan, A.A.; Eljaaly, K.; Alhumaid, S.; Albayat, H.; Al-Adsani, W.; Sabour, A.A.; Alshiekheid, M.A.; Al-Jishi, J.M.; Khamis, F.; Alwarthan, S. An Overview on Phenotypic and Genotypic Characterisation of Carbapenem-Resistant Enterobacterales. Medicina 2022, 58, 1675.
4. Shukla, S.K.; Rao, T.S. An improved crystal violet assay for biofilm quantification in 96-well microtitre plate. Biorxiv 2017, 100214.
5. Wu, D.; Ding, Y.; Yao, K.; Gao, W.; Wang, Y. Antimicrobial resistance analysis of clinical Escherichia coli isolates in neonatal ward. Frontiers in Pediatrics 2021, 9, 670470.
6. Flemming, H.-C.; Wingender, J.; Szewzyk, U.; Steinberg, P.; Rice, S.A.; Kjelleberg, S. Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology 2016, 14, 563-575.
7. Vestby, L.K.; Grønseth, T.; Simm, R.; Nesse, L.L. Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics 2020, 9, 59.
8. Sohail, M.; Muzzammil, M.; Ahmad, M.; Rehman, S.; Garout, M.; Khojah, T.M.; Al-Eisa, K.M.; Breagesh, S.A.; Hamdan, R.M.A.; Alibrahim, H.I. Molecular Characterization of Community-and Hospital-Acquired Methicillin-Resistant Staphylococcus aureus Isolates during COVID-19 Pandemic. Antibiotics 2023, 12, 157.
9. Harding, M.W.; Marques, L.L.; Howard, R.J.; Olson, M.E. Can filamentous fungi form biofilms? Trends in microbiology 2009, 17, 475-480.
10. Fujii, K.; Matsumoto, H.N.; Koyama, Y.; Iwasaki, Y.; Ishihara, K.; Takakuda, K. Prevention of biofilm formation with a coating of 2-methacryloyloxyethyl phosphorylcholine polymer. Journal of Veterinary Medical Science 2008, 70, 167-173.
11. Lajhar, S.A.; Brownlie, J.; Barlow, R. Characterization of biofilm-forming capacity and resistance to sanitizers of a range of E. coli O26 pathotypes from clinical cases and cattle in Australia. BMC microbiology 2018, 18, 1-15.
12. Gebreyohannes, G.; Nyerere, A.; Bii, C.; Sbhatu, D.B. Challenges of intervention, treatment, and antibiotic resistance of biofilm-forming microorganisms. Heliyon 2019, 5, e02192.
13. Rabaan, A.A.; Alhumaid, S.; Mutair, A.A.; Garout, M.; Abulhamayel, Y.; Halwani, M.A.; Alestad, J.H.; Bshabshe, A.A.; Sulaiman, T.; AlFonaisan, M.K. Application of Artificial Intelligence in Combating High Antimicrobial Resistance Rates. Antibiotics 2022, 11, 784.
14. Mirani, Z.A.; Aziz, M.; Khan, M.N.; Lal, I.; ul Hassan, N.; Khan, S.I. Biofilm formation and dispersal of Staphylococcus aureus under the influence of oxacillin. Microbial Pathogenesis 2013, 61, 66-72.
15. Qian, W.; Li, X.; Yang, M.; Liu, C.; Kong, Y.; Li, Y.; Wang, T.; Zhang, Q. Relationship Between Antibiotic Resistance, Biofilm Formation, and Biofilm-Specific Resistance in Escherichia coli Isolates from Ningbo, China. Infection and Drug Resistance 2022, 15, 2865.
16. Merritt, J.H.; Kadouri, D.E.; O'Toole, G.A. Growing and analyzing static biofilms. Current protocols in microbiology 2011, 22, 1B. 1.1-1B. 1.18.
17. Pena, R.T.; Blasco, L.; Ambroa, A.; González-Pedrajo, B.; Fernández-García, L.; López, M.; Bleriot, I.; Bou, G.; García-Contreras, R.; Wood, T.K. Relationship between quorum sensing and secretion systems. Frontiers in microbiology 2019, 10, 1100.
18. Singh, A.K.; Prakash, P.; Achra, A.; Singh, G.P.; Das, A.; Singh, R.K. Standardization and classification of in vitro biofilm formation by clinical isolates of Staphylococcus aureus. Journal of global infectious diseases 2017, 9, 93.
19. Qi, L.; Li, H.; Zhang, C.; Liang, B.; Li, J.; Wang, L.; Du, X.; Liu, X.; Qiu, S.; Song, H. Relationship between antibiotic resistance, biofilm formation, and biofilm-specific resistance in Acinetobacter baumannii. Frontiers in microbiology 2016, 7, 483.
20. Folliero, V.; Franci, G.; Dell’Annunziata, F.; Giugliano, R.; Foglia, F.; Sperlongano, R.; De Filippis, A.; Finamore, E.; Galdiero, M. Evaluation of antibiotic resistance and biofilm production among clinical strain isolated from medical devices. International Journal of Microbiology 2021, 2021.
21. Rutherford, S.T.; Bassler, B.L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor perspectives in medicine 2012, 2, a012427.
22. Bhandari, S.; Adhikari, S.; Karki, D.; Chand, A.B.; Sapkota, S.; Dhungel, B.; Banjara, M.R.; Joshi, P.; Lekhak, B.; Rijal, K.R. Antibiotic Resistance, Biofilm Formation and Detection of mexA/mexB Efflux-Pump Genes Among Clinical Isolates of Pseudomonas aeruginosa in a Tertiary Care Hospital, Nepal. Frontiers in Tropical Diseases 2022, 2, 75.
23. Cepas, V.; López, Y.; Muñoz, E.; Rolo, D.; Ardanuy, C.; Martí, S.; Xercavins, M.; Horcajada, J.P.; Bosch, J.; Soto, S.M. Relationship between biofilm formation and antimicrobial resistance in gram-negative bacteria. Microbial Drug Resistance 2019, 25, 72-79.
24. Kamali, E.; Jamali, A.; Ardebili, A.; Ezadi, F.; Mohebbi, A. Evaluation of antimicrobial resistance, biofilm forming potential, and the presence of biofilm-related genes among clinical isolates of Pseudomonas aeruginosa. BMC research notes 2020, 13, 1-6.
25. Sahm, D.F.; Critchley, I.A.; Kelly, L.J.; Karlowsky, J.A.; Mayfield, D.C.; Thornsberry, C.; Mauriz, Y.R.; Kahn, J. Evaluation of current activities of fluoroquinolones against gram-negative bacilli using centralized in vitro testing and electronic surveillance. Antimicrobial agents and chemotherapy 2001, 45, 267-274.
26. Braun, S.D.; Jamil, B.; Syed, M.A.; Abbasi, S.A.; Weiß, D.; Slickers, P.; Monecke, S.; Engelmann, I.; Ehricht, R. Prevalence of carbapenemase-producing organisms at the Kidney Center of Rawalpindi (Pakistan) and evaluation of an advanced molecular microarray-based carbapenemase assay. Future microbiology 2018, 13, 1225-1246.
27. Choi, Y.s.; Kim, J.H.; Kim, Y.; Cho, H.J.; Sung, J.H.; Choi, S.J.; Oh, S.y.; Kim, Y.J.; Roh, C.R. Growing threat of extended‐spectrum β‐lactamase‐producing Enterobacteriaceae colonisation in high‐risk pregnancies: A cross‐sectional study. BJOG: An International Journal of Obstetrics & Gynaecology 2022.
28. Coque, T.M.; Baquero, F.; Canton, R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Eurosurveillance 2008, 13, 19044.
29. Habib, A.; Lo, S.; Villageois-Tran, K.; Petitjean, M.; Malik, S.A.; Armand-Lefevre, L.; Ruppe, E.; Zahra, R. Dissemination of carbapenemase-producing Enterobacterales in the community of Rawalpindi, Pakistan. Plos one 2022, 17, e0270707.
30. Ahmed, N.; Tahir, K.; Aslam, S.; Cheema, S.M.; Rabaan, A.A.; Turkistani, S.A.; Garout, M.; Halwani, M.A.; Aljeldah, M.; Al Shammari, B.R. Heavy Metal (Arsenic) Induced Antibiotic Resistance among Extended-Spectrum β-Lactamase (ESBL) Producing Bacteria of Nosocomial Origin. Pharmaceuticals 2022, 15, 1426.
31. Ahmed, N.; Zeshan, B.; Naveed, M.; Afzal, M.; Mohamed, M. Antibiotic resistance profile in relation to virulence genes fimH, hlyA and usp of uropathogenic E. coli isolates in Lahore, Pakistan. Trop. Biomed 2019, 36, 559-568.
32. Ahmed, N.; Khan, M.; Saleem, W.; Karobari, M.; Mohamed, R.; Heboyan, A.; Rabaan, A.; Mutair, A.; Alhumaid, S.; Alsadiq, S. Evaluation of Bi-Lateral Co-Infections and Antibiotic Resistance Rates among COVID-19 Patients. Antibiotics 2022, 276.
33. Ahmed, N.; Khalid, H.; Mushtaq, M.; Basha, S.; Rabaan, A.A.; Garout, M.; Halwani, M.A.; Al Mutair, A.; Alhumaid, S.; Al Alawi, Z. The Molecular Characterization of Virulence Determinants and Antibiotic Resistance Patterns in Human Bacterial Uropathogens. Antibiotics 2022, 11, 516.
34. Hussain, S.; Zeshan, B.; Arshad, R.; Kabir, S.; Ahmed, N. MRSA Clinical Isolates Harboring mecC Gene Imply Zoonotic Transmission to Humans and Colonization by Biofilm Formation. Pakistan J. Zool 2022.
35. Zahra, N.; Zeshan, B.; Qadri, M.M.A.; Ishaq, M.; Afzal, M.; Ahmed, N. Phenotypic and genotypic evaluation of antibiotic resistance of Acinetobacter baumannii bacteria isolated from surgical intensive care unit patients in Pakistan. Jundishapur Journal of Microbiology 2021, 14.
36. Zeshan, B.; Karobari, M.I.; Afzal, N.; Siddiq, A.; Basha, S.; Basheer, S.N.; Peeran, S.W.; Mustafa, M.; Daud, N.H.A.; Ahmed, N. The usage of antibiotics by COVID-19 patients with comorbidities: the risk of increased antimicrobial resistance. Antibiotics 2021, 11, 35.
37. Hasan, D.L.; Khalid, H.M.; Mero, W.M. Phenotypic and Molecular Study of Extended-Spectrum β-lactamases Producing Enterobacteriaceae from Urinary Tract Infection in Zakho city, Kurdistan Region/Iraq. Academic Journal of Nawroz University 2022, 11, 305-313.
38. Rizvi, A.; Saeed, M.U.; Nadeem, A.; Yaqoob, A.; Rabaan, A.A.; Bakhrebah, M.A.; Al Mutair, A.; Alhumaid, S.; Aljeldah, M.; Al Shammari, B.R. Evaluation of Bi-Lateral Co-Infections and Antibiotic Resistance Rates among COVID-19 Patients in Lahore, Pakistan. Medicina 2022, 58, 904.
39. Wayne, P. Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing. 2011.
40. Mustafai, M.M.; Hafeez, M.; Munawar, S.; Basha, S.; Rabaan, A.A.; Halwani, M.A.; Alawfi, A.; Alshengeti, A.; Najim, M.A.; Alwarthan, S. Prevalence of Carbapenemase and Extended-Spectrum β-Lactamase Producing Enterobacteriaceae: A Cross-Sectional Study. Antibiotics 2023, 12, 148.
41. Abe, R.; Akeda, Y.; Iida, T.; Hamada, S. Population Analysis Profiling: Is It Still the Gold Standard for the Determination of Heteroresistance in Carbapenemase-Producing Enterobacteriaceae? 2022, 106644.
42. Dhital, R.; Shen, Z.; Zhang, S.; Mustapha, A. Detection of virulence and extended spectrum β‐lactamase genes in Salmonella by multiplex high‐resolution melt curve real‐time PCR assay. Journal of Applied Microbiology 2022, 132, 2355-2367.
43. Naderi Mezajin, M.; Fatemizadeh, M.; Rostami, Z.; Khaki, P.; Shirzad, M.; Noorbakhsh, F. Antibiotic resistance pattern and frequency of SHV, CTX, TEM, and OXA resistance gene among salmonella serotypes. Health Biotechnology and Biopharma (HBB) 2022, 6, 64-77.
44. Suranadee, Y.; Jyalathacrachchi, H.; Gamage, S.; Gunasekara, S. P32 Occurrence of bla KPC, bla NDM and bla OXA-48 genes among carbapenemase-producing Enterobacteriaceae (CRE) in National Cancer Institute, Sri Lanka. JAC-Antimicrobial Resistance 2022, 4, dlac004. 031.
45. Mohammed, A.B.; Anwar, K.A. Phenotypic and genotypic detection of extended spectrum beta lactamase enzyme in Klebsiella pneumoniae. PloS one 2022, 17, e0267221.
46 Fattahi, S., Kafil, H. S., Nahai, M. R., Asgharzadeh, M., Nori, R., & Aghazadeh, M. (2015). Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS hygiene and infection control, 10, Doc11. https://doi.org/10.3205/dgkh000254
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Dec 23, 2023
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Faryal Anjum, Saima Saleem, Muhammad Hashim Zubairi, Rabia Noor, Urooj Haroon, Maryam Fatima, Zeba Parveen Imran, Sadaf Naeem, & Asma Naim. (2023). ANTIBIOTIC SUSCEPTIBILITY PATTERN AND BIOFILM-FORMING POTENTIAL OF GRAM-NEGATIVE CLINICAL BACTERIAL ISOLATES. Journal of Population Therapeutics and Clinical Pharmacology, 30(19), 1106–1115. https://doi.org/10.53555/jptcp.v30i19.3805
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Author Biographies
Faryal Anjum
Department of Microbiology, University of Karachi
Saima Saleem
Department of Pharmacy Practice, Faculty of Pharmavy , Jinnah University for Women
Muhammad Hashim Zubairi
Department of environmental sciences, Sindh Madressatul Islam University
Rabia Noor
Department of pharmacy practice, Faculty of Pharmacy, Salim Habib University
Urooj Haroon
Department of Chemistry, Federal Urdu Univesity of Arts, Science and Technology
Maryam Fatima
Registered Pharmasist, Liaquat National Hospital Karachi
Zeba Parveen Imran
Department of Microbilogy, Federal Urdu Univesity of Arts, Science and Technology
Sadaf Naeem
Department of Biochemistry, Univesity of Karachi
Asma Naim
Department of Microbiology, University of Karachi