ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)
Biotechnologia Acta Т. 17, No. 1 , 2024
P. 5-19, Bibliography 50, Engl.
UDC:: 579.663
DOI: https://doi.org/10.15407/biotech17.01.005
Full text: (PDF, in English)
SYNERGISM OF ANTIMICROBIAL ACTIVITY OF ANTIBIOTICS WITH BIOCIDES OF NATURAL ORIGIN
1National University of Food Technologies, Kyiv, Ukraine
2Institute of Microbiology and Virology of NASU, Kyiv, Ukraine
Antibiotic therapy remains the primary method for treating infectious diseases in humans. Nevertheless, its effectiveness is rapidly decreasing due to the widespread emergence of resistant pathogens, necessitating the exploration of new treatment options. One potential approach involves using antibiotics in combination with other natural compounds.
Aim. The review was purposed to summarize the literature data on the synergy of the antimicrobial action of combinations of antibiotics with various biocides against Gram-positive and Gram-negative pathogenic microorganisms.
The analysis of literature data has shown that promising compounds for use in combinations with antibiotics include essential oils, other plant components, antimicrobial peptides (both natural and synthetic), and microbial surfactants. In most studies, the researchers calculated the fractional inhibitory concentration index, confirming the synergistic antimicrobial activity of antibiotics and the mentioned compounds. The use of natural biocides in combination with commercial antibiotics, particularly against Gram-negative (including methicillin-resistant) Staphylococcus species and Gram-positive microorganisms (Escherichia coli, Pseudomonas aureginosa, Klebsiella pneumoniae, Proteus mirabilis, Acinetobacter baumannii), enabled to consider these mixtures not only as effective antimicrobial agents but as one of the ways to reduce the effective concentration of antibiotics as well.
It should be noted that in the presented studies, the researchers only observed the synergy of antimicrobial activity between a combination of antibiotics and other biocides without emphasizing the potential mechanisms of interaction between the components of the complex. This likely depended on various factors, including the qualitative composition of natural compounds. Therefore, it was essential to continue research not only on the synergy of antimicrobial activity in compound mixtures but also on the underlying mechanisms of their interaction. This would provide insights to enhance their effectiveness in combating resistant microorganisms.
Key words: antimicrobial effect, pathogenic microorganisms, fractional inhibitory concentration.
{accordion title="References" open="false"}
1. Zaman S.B., Hussain M.A., Nye R., Mehta V., Mamun K.T., Hossain N.A. Review on antibiotic resistance: alarm bells are ringing. Cureus. 2017, 9(6):e1403. https://doi.org/10.7759/cureus.1403
2. Sommer M. O. A., Munck C., Toft-Kehler R. V., & Andersson D. I. Prediction of antibiotic resistance: time for a new preclinical paradigm? Nature reviews Microbiology. 2017, 15(11):689‒696. https://doi.org/10.1038/nrmicro.2017.75
3. Mlynarczyk-Bonikowska B., Kowalewski C., Krolak-Ulinska A., Marusza W. Molecular mechanisms of drug resistance in Staphylococcus aureus. Int. J. Mol. Sci. 2022, 23(15):8088. https://doi.org/10.3390/ijms23158088
4. Murugaiyan J., Kumar P. A., Rao G. S., Iskandar, K., Hawser S., at al. Progress in alternative strategies to combat antimicrobial resistance: focus on antibiotics. Antibiotics (Basel, Switzerland). 2022, 11(2):200. https://doi.org/10.3390/antibiotics11020200
5. Naylor N.R., Atun R., Zhu N., Kulasabanathan K., Silva S., et al. Estimating the burden of antimicrobial resistance: a systematic literature review. Antimicrob. Resist. Infect. Control. 2018, 7(1):58. https://doi.org/10.1186/s13756-018-0336-y
6. Iguchi S., Mizutani T., Hiramatsu K., Kikuchi K. Rapid acquisition of linezolid resistance in methicillin-resistant Staphylococcus aureus: role of hypermutation and homologous recombination. PLoS One. 2016, 11(5):e0155512. https://doi.org/10.1371/journal.pone.0155512
7. Giddins M.J., Macesic N., Annavajhala M.K., Stump S., Khan S., et al. Successive emergence of ceftazidime-avibactam resistance through distinct genomic adaptations in bla(KPC-2)-harboring Klebsiella pneumoniae sequence type 307 isolates. Antimicrob. Agents Chemother. 2018, 62(3):e02101‒17. https://doi.org/10.1128/AAC.02101-17
8. Singh V., Phukan U.J. Interaction of host and Staphylococcus aureus protease-system regulates virulence and pathogenicity. Med. Microbiol. Immunol. 2018, 208(5):585–607. https://doi.org/10.1007/s00430-018-0573-y
9. Coimbra A., Miguel S., Ribeiro M., et al. Thymus zygis essential oil: phytochemical characterization, bioactivity evaluation and synergistic effect with antibiotics against Staphylococcus aureus. Antibiotics (Basel). 2022, 11(2):146. https://doi.org/10.3390/antibiotics11020146
10. De Oliveira D. M. P., Forde B. M., Kidd T. J., Harris P. N. A., Schembri M. A., Beatson S. A., Paterson D. L., Walker M. J. Antimicrobial Resistance in ESKAPE рathogens. Clinical microbiology reviews. 2020, 33(3): e00181. https://doi.org/10.1128/CMR.00181-19
11. Lahmar A., Bedoui A., Mokdad-Bzeouich I., et al. Reversal of resistance in bacteria underlies synergistic effect of essential oils with conventional antibiotics. Microb. Pathog. 2017, 106:50‒59. https://doi.org/10.1016/j.micpath.2016.10.018
12. Pirog T. P., Kliuchka I. V., Kliuchka L. V. Synergistic action of essential oils with the biocides on microorganisms. Biotechnologia Acta. 2019, 12(4):5‒18. https://doi.org/10.15407/biotech12.04.005
13. Buldain D, Buchamer AV, Marchetti ML, Aliverti F, Bandoni A, Mestorino N. Combination of cloxacillin and essential oil of melaleuca armillaris as an alternative against Staphylococcus aureus. Front. Vet. Sci. 2018, 5(177). https://doi.org/10.3389/fvets.2018.00177
14. Araújo Silva V. Pereira da Sousa J., de Luna Freire Pessôa H., Fernanda Ramos de Freitas A., Douglas Melo Coutinho H., Beuttenmuller Nogueira Alves L., Oliveira Lima E. Ocimum basilicum: antibacterial activity and association study with antibiotics against bacteria of clinical importance. Pharm. Biol. 2016, 54(5):863‒867. https://doi.org/10.3109/13880209.2015.1088551
15. Grădinaru A.C., Trifan A., Şpac A., Brebu M., Miron A., Aprotosoaie A.C. Antibacterial activity of traditional spices against lower respiratory tract pathogens: combinatorial effects of Trachyspermum ammi essential oil with conventional antibiotics. Lett. Appl. Microbiol. 2018, 67(5):449‒457. https://doi.org/10.1111/lam.13069
16. Rosato A., Carocci A., Catalano A., Clodoveo M.L., Franchini C., Corbo F., Carbonara G.G., Carrieri A., Fracchiolla G. Elucidation of the synergistic action of Mentha Piperita essential oil with common antimicrobials. PLoS One. 2018, 13(8):e0200902. https://doi.org/10.1371/journal.pone.0200902
17. El Atki Y., Aouam I., El Kamari F., Taroq A., Nayme K., Timinouni M., Lyoussi B., Abdellaoui A. Antibacterial activity of cinnamon essential oils and their synergistic potential with antibiotics. J. Adv. Pharm. Technol. Res. 2019, 10(2):63‒67. https://doi.org/10.4103/japtr.JAPTR_366_18
18. Malik T., Singh P., Pant S., Chauhan N., Lohani H. Potentiation of antimicrobial activity of ciprofloxacin by Pelargonium graveolens essential oil against selected uropathogens. Phytother Res. 2011, 25(8):1225‒1228. https://doi.org/10.1002/ptr.3479
19. Rosato A., Vitali C., De Laurentis N., Armenise D., Antonietta Milillo M. Antibacterial effect of some essential oils administered alone or in combination with norfloxacin. Phytomedicine. 2007, 14(11):727‒732. https://doi.org/10.1016/j.phymed.2007.01.005
20. Vitanza L., Maccelli A., Marazzato M., et al. Satureja montana L. essential oil and its antimicrobial activity alone or in combination with gentamicin. Microb Pathog. 2019, 126:323‒331. https://doi.org/10.1016/j.micpath.2018.11.025
21. Oliveira G.D,. Rocha W.R.V., Rodrigues J.F.B., Alves H.S. Synergistic and Antibiofilm effects of the essential oil from Сroton Сonduplicatus (euphorbiaceae) against methicillin-resistant Staphylococcus aureus. Pharmaceuticals. 2022, 16(1):55. https://doi.org/10.3390/ph16010055
22. Mun S.H., Joung D.K., Kim Y.S., Kang O.H., Kim S.B., Seo Y.S., Kim Y.C., Lee D.S., Shin D.W., Kweon K.T., Kwon D.Y. Synergistic antibacterial effect of curcumin against methicillin-resistant Staphylococcus aureus. Phytomedicine. 2013, 20(8-9):714‒718. https://doi.org/10.1016/j.phymed.2013.02.006
23. Lee Y.S., Kang O.H., Choi J.G., Oh Y.C., Keum J.H., Kim S.B., Jeong G.S., Kim Y.C., Shin D.W., Kwon D.Y. Synergistic effect of emodin in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. Pharm. Biol. 2010, 48(11):1285‒1290. https://doi.org/10.3109/13880201003770150
24. Joung D.K., Joung H., Yang D.W., Kwon D.Y., Choi J.G., Woo S., Shin D.Y., Kweon O.H., Kweon K.T., Shin D.W. Synergistic effect of rhein in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. Exp. Ther. Med. 2012, 3(4):608‒612. https://doi.org/10.3892/etm.2012.459
25. Kang H.K., Kim H.Y., Cha J.D. Synergistic effects between silibinin and antibiotics on methicillin-resistant Staphylococcus aureus isolated from clinical specimens. Biotechnol. J. 2011, 6(11):1397‒1408. https://doi.org/10.1002/biot.201000422
26. Joung D.K., Choi S.H., Kang O.H., Kim S.B., Mun S.H., Seo Y.S., Kang D.H., Gong R., Shin D.W., Kim Y.C., Kwon D.Y. Synergistic effects of oxyresveratrol in conjunction with antibiotics against methicillin-resistant Staphylococcus aureus. Mol. Med. Rep. 2015, 12(1): 663‒667. https://doi.org/10.3892/mmr.2015.33452
27. Joung D.K., Kang O.H., Seo Y.S., Zhou T., Lee Y.S., Han S.H., Mun S.H., Kong R., Song H.J., Shin D.W., Kwon D.Y. Luteolin potentiates the effects of aminoglycoside and β-lactam antibiotics against methicillin-resistant Staphylococcus aureus in vitro. Exp. Ther. Med. 2016, 11(6):2597‒2601. https://doi.org/10.3892/etm.2016.3212
28. Mun S.H., Lee Y.S., Han S.H., Lee S.W., Cha S.W., Kim S.B., Seo Y.S., Kong R., Kang D.H., Shin D.W., Kang O.H., Kwon D.Y. In vitro Potential effect of morin in the combination with β-lactam antibiotics against methicillin-resistant Staphylococcus aureus. Foodborne Pathog. Dis. 2015, 12(6):545‒550. https://doi.org/10.1089/fpd.2014.1923
29. Pereira F., Madureira A.M., Sancha S., Mulhovo S., Luo X., Duarte A., Ferreira M.J. Cleistochlamys kirkii chemical constituents: Antibacterial activity and synergistic effects against resistant Staphylococcus aureus strains. J. Ethnopharmacol. 2016, 178:180‒187. https://doi.org/10.1016/j.jep.2015.12.009
30. Yu H.H., Kim K.J., Cha J.D., Kim H.K., Lee Y.E., Choi N.Y., You Y.O. Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. J. Med. Food. 2005, 8(4):454‒461. https://doi.org/10.1089/jmf.2005.8.454
31. Yang W., Liu J., Blažeković B. et al. In vitro antibacterial effects of Tanreqing injection combined with vancomycin or linezolid against methicillin-resistant Staphylococcus aureus. BMC Complement. Altern. Med. 2018, 18(1):169. https://doi.org/10.1186/s12906-018-2231-8
32. Breijyeh Z., Jubeh B., Karaman R. Resistance of gram-negative bacteria to current antibacterial agents and approaches to resolve it. Molecules. 2020, 25(6):1340. https://doi.org/10.3390/molecules25061340
33. Jean S.S., Harnod D., Hsueh P.R. Global threat of carbapenem-resistant gram-negative bacteria. Front. Cell. Infect. Microbiol. 2022, V.12:823684. https://doi.org/10.3389/fcimb.2022.823684
34. Duarte A., Ferreira S., Silva F., Domingues F.C. Synergistic activity of coriander oil and conventional antibiotics against Acinetobacter baumannii. Phytomedicine. 2012, 19(3‒4):236‒238. https://doi.org/10.1016/j.phymed.2011.11.010
35. Grădinaru A.C., Trifan A., Şpac A., Brebu M., Miron A., Aprotosoaie A.C. Antibacterial activity of traditional spices against lower respiratory tract pathogens: combinatorial effects of Trachyspermum ammi essential oil with conventional antibiotics. Lett. App.l Microbiol. 2018, 67(5):449‒457. https://doi.org/10.1111/lam.13069
36. Bhattacharya D., Ghosh D., Bhattacharya S., Sarkar S., Karmakar P., Koley H., Gachhui R. Antibacterial activity of polyphenolic fraction of kombucha against Vibrio cholerae: targeting cell membrane. Lett. Appl. Microbiol. 2018, 66(2):145‒152. https://doi.org/10.1111/lam.12829
37. Kakarla P., Floyd J., Mukherjee M., Devireddy A.R., Inupakutika M.A., Ranweera I., Kc R., Shrestha U., Cheeti U.R., Willmon T.M., et al. Inhibition of the multidrug efflux pump lmrs from Staphylococcus aureus by cumin spice Cuminum cyminum. Arch. Microbiol. 2017, 199(3):465–474. https://doi.org/10.1007/s00203-016-1314-5
38. Dwivedi G.R., Tyagi R., Sanchita , Tripathi S., Pati S., Srivastava S.K., Darokar M.P., Sharma A. Antibiotics potentiating potential of catharanthine against superbug Pseudomonas aeruginosa. J. Biomol. Struct. Dyn. 2018, 36(16):4270–4284. https://doi.org/10.1080/07391102.2017.1413424
39. Bag A., Chattopadhyay R.R. Efflux-pump inhibitory activity of a gallotannin from Terminalia chebula fruit against multidrug-resistant uropathogenic Escherichia coli. Nat. Prod. Res. 2014, 28(16):1280‒1283. https://doi.org/10.1080/14786419.2014.895729
40. Aghayan S.S., Mogadam H.K., Fazli M., Darban-Sarokhalil D., Khoramrooz S.S., Jabalameli F., Yaslianifard S., Mirzaii M. The effects of berberine and palmatine on efflux pumps inhibition with different gene patterns in Pseudomonas aeruginosa isolated from burn infections. Avicenna J. Med. Biotechnol. 2017, 9(1):2–7.
41. Lavigne J.P., Ranfaing J., Dunyach-Rémy C., Sotto A. Synergistic Effect of propolis and antibiotics on uropathogenic Escherichia coli. Antibiotics (Basel). 2020, 9(11):739. https://doi.org/10.3390/antibiotics9110739
42. Yasir M., Dutta D., Willcox M.D.P. Enhancement of antibiofilm activity of ciprofloxacin against Staphylococcus aureus by administration of antimicrobial peptides. Antibiotics (Basel). 2021, 10(10):1159. https://doi.org/10.3390/antibiotics10101159
43. Kampshoff F., Willcox M.D.P., Dutta D. A pilot study of the synergy between two antimicrobial peptides and two common antibiotics. Antibiotics (Basel). 2019, 8(2):60. https://doi.org/10.3390/antibiotics8020060
44. Jahangiri A., Neshani A., Mirhosseini S.A., Ghazvini K., Zare H., Sedighian H. Synergistic effect of two antimicrobial peptides, nisin and p10 with conventional antibiotics against extensively drug-resistant Acinetobacter baumannii and colistin-resistant Pseudomonas aeruginosa isolates. Microb. Pathog. 2021, V.150:104700. https://doi.org/10.1016/j.micpath.2020.104700
45. Song M., Liu Y., Huang X., Ding S., Wang Y., HEN J. Zhu K.. A broad-spectrum antibiotic adjuvant reverses multidrug-resistant gram-negative pathogens. Nat. Microbiol. 2020, 5(8):1040-1050. https://doi.org/10.1038/s41564-020-0723-z
46. Liu J., Chen F., Wang X., Peng H., Zhang H., Wang K.J. The synergistic effect of mud crab antimicrobial peptides Sphistin and Sph12-38 with antibiotics azithromycin and rifampicin enhances bactericidal activity against Pseudomonas aeruginosa. Front. Cell. Infect. Microbiol. 2020, V.10:572849. https://doi.org/10.3389/fcimb.2020.572849
47. Rishi P., Vij S., Maurya I.K., Kaur U.J., Bharati S., Tewari R. Peptides as adjuvants for ampicillin and oxacillin against methicillin-resistant Staphylococcus aureus (MRSA). Microb. Pathog. 2018, V.124:11‒20. https://doi.org/10.1016/j.micpath.2018.08.023
48. Rossi C.C., Santos-Gandelman J.F., Barros E.M., Alvarez V.M., Laport M.S., Giambiagi-deMarval M. Staphylococcus haemolyticus as a potential producer of biosurfactants with antimicrobial, anti-adhesive and synergistic properties. Lett. Appl. Microbiol. 2016, 63(3):215‒221. https://doi.org/10.1111/lam.12611
49. Joshi-Navare K., Prabhune A. A biosurfactant-sophorolipid acts in synergy with antibiotics to enhance their efficiency. Biomed. Res. Int. 2013, V.2013:512495. https://doi.org/10.1155/2013/512495
50. Rivardo F., Martinotti M.G., Turner R.J., Ceri H. Synergistic effect of lipopeptide biosurfactant with antibiotics against Escherichia coli CFT073 biofilm. Int. J. Antimicrob. Agents. 2011, 37(4):324‒331. https://doi.org/10.1016/j.ijantimicag.2010.12.011
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