Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Restoring Ampicillin Sensitivity in Multidrug-Resistant Escherichia coli Following Treatment in Combination with Coffee Pulp Extracts

  • Anchalee Rawangkan (Division of Microbiology and Parasitology, School of Medical Sciences, University of Phayao) ;
  • Atchariya Yosboonruang (Division of Microbiology and Parasitology, School of Medical Sciences, University of Phayao) ;
  • Anong Kiddee (Division of Microbiology and Parasitology, School of Medical Sciences, University of Phayao) ;
  • Achiraya Siriphap (Division of Microbiology and Parasitology, School of Medical Sciences, University of Phayao) ;
  • Grissana Pook-In (Division of Microbiology and Parasitology, School of Medical Sciences, University of Phayao) ;
  • Ratsada Praphasawat (Department of Pathology, School of Medicine, University of Phayao) ;
  • Surasak Saokaew (Division of Social and Administrative Pharmacy, Department of Pharmaceutical Care, School of Pharmaceutical Sciences, University of Phayao) ;
  • Acharaporn Duangjai (Unit of Excellence in Research and Product Development of Coffee, Division of Physiology, School of Medical Sciences, University of Phayao)
  • Received : 2023.05.03
  • Accepted : 2023.05.15
  • Published : 2023.09.28
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Abstract

Escherichia coli, particularly multidrug-resistant (MDR) strains, is a serious cause of healthcare-associated infections. Development of novel antimicrobial agents or restoration of drug efficiency is required to treat MDR bacteria, and the use of natural products to solve this problem is promising. We investigated the antimicrobial activity of dried green coffee (DGC) beans, coffee pulp (CP), and arabica leaf (AL) crude extracts against 28 isolated MDR E. coli strains and restoration of ampicillin (AMP) efficiency with a combination test. DGC, CP, and AL extracts were effective against all 28 strains, with a minimum inhibitory concentration (MIC) of 12.5-50 mg/ml and minimum bactericidal concentration of 25-100 mg/ml. The CP-AMP combination was more effective than CP or AMP alone, with a fractional inhibitory concentration index value of 0.01. In the combination, the MIC of CP was 0.2 mg/ml (compared to 25 mg/ml of CP alone) and that of AMP was 0.1 mg/ml (compared to 50 mg/ml of AMP alone), or a 125-fold and 500-fold reduction, respectively, against 13-drug resistant MDR E. coli strains. Time-kill kinetics showed that the bactericidal effect of the CP-AMP combination occurred within 3 h through disruption of membrane permeability and biofilm eradication, as verified by scanning electron microscopy. This is the first report indicating that CP-AMP combination therapy could be employed to treat MDR E. coli by repurposing AMP.

Keywords

Acknowledgement

We gratefully acknowledge Miss Chatchaya Sumana of the University of Phayao and Dr. Surasak Kulmalee from the Science and Technology Service Center, Faculty of Science, Maejo University for their technical assistance. This research was funded by the Unit of Excellence in Research and Product Development of Coffee (grant no. UoE65001), University of Phayao, Thailand.

References

  1. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. 2022. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399: 629-655. https://doi.org/10.1016/S0140-6736(21)02724-0
  2. Haque M, Sartelli M, McKimm J, Abu Bakar M. 2018. Health care-associated infections - an overview. Infect. Drug Resist. 11: 2321-2333. https://doi.org/10.2147/IDR.S177247
  3. Bassetti M, Peghin M, Vena A, Giacobbe DR. 2019. Treatment of infections due to MDR Gram-negative bacteria. Front. Med. 6: 74.
  4. Matlock A, Garcia JA, Moussavi K, Long B, Liang SY. 2021. Advances in novel antibiotics to treat multidrug-resistant gram-negative bacterial infections. Intern. Emerg. Med. 16: 2231-2241. https://doi.org/10.1007/s11739-021-02749-1
  5. Li M, Liu Q, Teng Y, Ou L, Xi Y, Chen S, et al. 2019. The resistance mechanism of Escherichia coli induced by ampicillin in laboratory. Infect. Drug Resist. 12: 2853-2863. https://doi.org/10.2147/IDR.S221212
  6. Herrera-Hidalgo L, Lomas-Cabezas JM, Lopez-Cortes LE, Luque-Marquez R, Lopez-Cortes LF, Martinez-Marcos FJ, et al. 2021. Ampicillin plus ceftriaxone combined therapy for Enterococcus faecalis infective endocarditis in OPAT. J. Clin. Med. 11: 7.
  7. Jimenez-Toro I, Rodriguez CA, Zuluaga AF, Otalvaro JD, Vesga O. 2020. A new pharmacodynamic approach to study antibiotic combinations against enterococci in vivo: Application to ampicillin plus ceftriaxone. PLoS One 15: e0243365.
  8. Marino A, Munafo A, Zagami A, Ceccarelli M, Campanella E, Cosentino F, et al. 2022. Ampicillin plus ceftriaxone therapy against Enterococcus faecalis endocarditis: A case report, guidelines considerations, and literature review. IDCases 28: e01462.
  9. Ghaffar F, Muniz LS, Katz K, Reynolds J, Smith JL, Davis P, et al. 2000. Effects of amoxicillin/clavulanate or azithromycin on nasopharyngeal carriage of Streptococcus pneumoniae and haemophilus influenzae in children with acute otitis media. Clin. Infect. Dis. 31: 875-880. https://doi.org/10.1086/318160
  10. Majhi A, Kundu K, Adhikary R, Banerjee M, Mahanti S, Basu A, et al. 2014. Combination therapy with ampicillin and azithromycin in an experimental pneumococcal pneumonia is bactericidal and effective in down regulating inflammation in mice. J. Inflamm. (Lond) 11: 5.
  11. Chemura A, Mudereri BT, Yalew AW, Gornott C. 2021. Climate change and specialty coffee potential in Ethiopia. Sci. Rep. 11: 8097.
  12. Oliveira G, Passos CP, Ferreira P, Coimbra MA, Goncalves I. 2021. Coffee by-products and their suitability for developing active food packaging materials. Foods 10: 683.
  13. Duangjai A, Suphrom N, Wungrath J, Ontawong A, Nuengchamnong N, Yosboonruang A. 2016. Comparison of antioxidant, antimicrobial activities and chemical profiles of three coffee (Coffea arabica L.) pulp aqueous extracts. Integr. Med. Res. 5: 324-331. https://doi.org/10.1016/j.imr.2016.09.001
  14. Rawangkan A, Siriphap A, Yosboonruang A, Kiddee A, Pook-In G, Saokaew S, et al. 2022. Potential antimicrobial properties of coffee beans and coffee by-products against drug-resistant Vibrio cholerae. Front. Nutr. 9: 865684.
  15. Yosboonruang A, Ontawong A, Thapmamang J, Duangjai A. 2022. Antibacterial activity of coffea robusta leaf extract against foodborne pathogens. J. Microbiol. Biotechnol. 32: 1003-1010. https://doi.org/10.4014/jmb.2204.04003
  16. Siriphap A, Kiddee A, Duangjai A, Yosboonruang A, Pook-In G, Saokaew S, et al. 2022. Antimicrobial activity of the green tea polyphenol (-)-epigallocatechin-3-gallate (EGCG) against clinical isolates of multidrug-resistant Vibrio cholerae. Antibiotics 11: 518.
  17. Yosboonruang A, Kiddee A, Boonduang C, Pibalpakdee P. 2018. Integron expression in multidrug-resistant Escherichia coli isolated from house Flies within the Hospital. Walailak J. Sci. Technol. (WJST) 16: 319-327. https://doi.org/10.48048/wjst.2019.6286
  18. CLSI. 2015. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-fifth Informational Supplement M100-S25., Ed. Wayne, PA, Clinical and Laboratory Standards Institute.
  19. Magi G, Marini E, Facinelli B. 2015. Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin, against clinical, erythromycin-resistant group A streptococci. Front. Microbiol. 6: 165.
  20. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52: 1.
  21. Zimmermann S, Klinger-Strobel M, Bohnert JA, Wendler S, Rodel J, Pletz MW, et al. 2019. Clinically approved drugs inhibit the Staphylococcus aureus multidrug NorA efflux pump and reduce biofilm formation. Front. Microbiol. 10: 2762.
  22. Sateriale D, Facchiano S, Colicchio R, Pagliuca C, Varricchio E, Paolucci M, et al. 2020. In vitro synergy of polyphenolic extracts from honey, myrtle and pomegranate against oral pathogens, S. mutans and R. dentocariosa. Front. Microbiol. 11: 1465.
  23. Lou Z, Wang H, Zhu S, Ma C, Wang Z. 2011. Antibacterial activity and mechanism of action of chlorogenic acid. J. Food Sci. 76: M398-403. https://doi.org/10.1111/j.1750-3841.2011.02213.x
  24. Buommino E, Vollaro A, Nocera FP, Lembo F, DellaGreca M, De Martino L, et al. 2021. Synergistic effect of abietic acid with oxacillin against methicillin-resistant Staphylococcus pseudintermedius. Antibiotics (Basel) 10: 80.
  25. Vollaro A, Catania MR, Iesce MR, Sferruzza R, D'Abrosca B, Donnarumma G, et al. 2019. Antimicrobial and anti-biofilm properties of novel synthetic lignan-like compounds. New Microbiol. 42: 21-28.
  26. Vollaro A, Esposito A, Esposito EP, Zarrilli R, Guaragna A, De Gregorio E. 2020. PYED-1 inhibits biofilm formation and disrupts the preformed biofilm of Staphylococcus aureus. Antibiotics (Basel) 9: 240.
  27. Rawangkan A, Wongsirisin P, Pook-In G, Siriphap A, Yosboonruang A, Kiddee A, et al. 2022. Dinactin: A new antitumor antibiotic with cell cycle progression and cancer stemness inhibiting activities in lung cancer. Antibiotics 11: 1845.
  28. Koley D, Bard AJ. 2010. Triton X-100 concentration effects on membrane permeability of a single HeLa cell by scanning electrochemical microscopy (SECM). Proc. Natl. Acad. Sci. USA 107: 16783-16787. https://doi.org/10.1073/pnas.1011614107
  29. Huang L, Ahmed S, Gu Y, Huang J, An B, Wu C, et al. 2021. The effects of natural products and environmental conditions on antimicrobial resistance. Molecules 26: 4277.
  30. Guran M. 2021. Natural products in the fight against multi-drug-resistant bacteria: natural antibiotics and resistance, pp. 130-159. Ed.
  31. Giri K, Shrestha BK, Shakya J, Sah SN, Khanal H. 2020. Antibacterial effect of green tea extract against multi drug resistant Escherichia coli isolated from urine sample of patients visiting tertiary care hospital of Eastern Nepal. Int. J. Appl. Sci. Biotechnol. 8: 45-51. https://doi.org/10.3126/ijasbt.v8i1.27313
  32. Reygaert W, Jusufi I. 2013. Green tea as an effective antimicrobial for urinary tract infections caused by Escherichia coli. Front. Microbiol. 4: 162.
  33. Haghjoo B, Lee L, Habiba U, Tahir H, Olabi M, Chu T. 2013. The synergistic effects of green tea polyphenols and antibiotics against potential pathogens. Adv. Biosci. Biotechnol. 4: 959-967. https://doi.org/10.4236/abb.2013.411127
  34. Nuhu AA. 2014. Bioactive micronutrients in coffee: Recent analytical approaches for characterization and quantification. ISRN Nutr. 2014: 384230.
  35. Esquivel P, Vinas M, Steingass CB, Gruschwitz M, Guevara E, Carle R, et al. 2020. Coffee (Coffea arabica L.) by-products as a source of carotenoids and phenolic compounds-Evaluation of varieties with different peel color. Front. Sustain. Food Syst. 4. doi.org/10.3389/fsufs.2020.590597.
  36. Cangeloni L, Bonechi C, Leone G, Consumi M, Andreassi M, Magnani A, et al. 2022. Characterization of extracts of coffee leaves (Coffea arabica L.) by spectroscopic and chromatographic/spectrometric techniques. Foods 11: 2495.
  37. Almeida AA, Farah A, Silva D, Nunan E, Gloria MBA. 2006. Antibacterial activity of coffee extracts and selected coffee chemical compounds against enterobacteria. J. Agric. Food Chem. 54: 8738-8743. https://doi.org/10.1021/jf0617317
  38. Naveed M, Hejazi V, Abbas M, Kamboh AA, Khan GJ, Shumzaid M, et al. 2018. Chlorogenic acid (CGA): a pharmacological review and call for further research. Biomed. Pharmacother. 97: 67-74. https://doi.org/10.1016/j.biopha.2017.10.064
  39. Khan F, Bamunuarachchi NI, Tabassum N, Kim Y-M. 2021. Caffeic acid and its derivatives: antimicrobial drugs toward microbial pathogens. J. Agric. Food Chem. 69: 2979-3004. https://doi.org/10.1021/acs.jafc.0c07579
  40. Tasew T, Mekonnen Y, Gelana T, Redi-Abshiro M, Chandravanshi BS, Ele E, et al. 2020. In vitro antibacterial and antioxidant activities of roasted and green coffee beans originating from different regions of Ethiopia. Int. J. Food Sci. 2020: 8490492.
  41. Gonzalez-Gonzalez GM, Palomo-Ligas L, Nery-Flores SD, Ascacio-Valdes JA, Saenz-Galindo A, Flores-Gallegos AC, et al. 2022. Coffee pulp as a source for polyphenols extraction using ultrasound, microwave, and green solvents. Environ. Qual. Manag.32: 451-461. https://doi.org/10.1002/tqem.21903
  42. Tian L, Wu M, Guo W, Li H, Gai Z, Gong G. 2021. Evaluation of the membrane damage mechanism of chlorogenic acid against Yersinia enterocolitica and Enterobacter sakazakii and its application in the preservation of raw pork and skim milk. Molecules 26: 6748.
  43. Rathi B, Gupta S, Kumar P, Kesarwani V, Dhanda RS, Kushwaha SK, et al. 2022. Anti-biofilm activity of caffeine against uropathogenic E. coli is mediated by curli biogenesis. Sci. Rep. 12: 18903.
  44. Chakraborty P, Dastidar DG, Paul P, Dutta S, Basu D, Sharma SR, et al. 2020. Inhibition of biofilm formation of Pseudomonas aeruginosa by caffeine: a potential approach for sustainable management of biofilm. Arch. Microbiol. 202: 623-635. https://doi.org/10.1007/s00203-019-01775-0
  45. Rathi B, Gupta S, Kumar P, Kesarwani V, Dhanda RS, Kushwaha SK, et al. 2022. Anti-biofilm activity of caffeine against uropathogenic E. coli is mediated by curli biogenesis. Sci. Rep. 12: 18903.
  46. Chen K, Peng C, Chi F, Yu C, Yang Q, Li Z. 2022. Antibacterial and antibiofilm activities of chlorogenic acid against Yersinia enterocolitica. Front. Microbiol. 13: 885092.
  47. Diamond E, Hewlett K, Penumutchu S, Belenky A, Belenky P. 2021. Coffee consumption modulates amoxicillin-induced dysbiosis in the murine gut microbiome. Front. Microbiol. 12: 6372822.
  48. Wang L, Pan X, Jiang L, Chu Y, Gao S, Jiang X, et al. 2022. The biological activity mechanism of chlorogenic acid and its applications in food industry: A review. Front. Nutr. 9: 943911.
  49. Zhang K, Li X, Yu C, Wang Y. 2020. Promising therapeutic strategies against microbial biofilm challenges. Front. Cell. Infect. Microbiol. 10: 359.
  50. Srinivasan R, Santhakumari S, Poonguzhali P, Geetha M, Dyavaiah M, Xiangmin L. 2021. Bacterial biofilm inhibition: A focused review on recent therapeutic strategies for combating the biofilm mediated infections. Front. Microbiol. 12: 676458.