Interactions of naturally occurring compounds with antimicrobials

Izabela Malczak; Anna Gajda

doi:10.1016/j.jpha.2023.09.014

Volume 13 Issue 12

Dec. 2023

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Izabela Malczak, Anna Gajda. Interactions of naturally occurring compounds with antimicrobials[J]. Journal of Pharmaceutical Analysis, 2023, 13(12): 1452-1470. doi: 10.1016/j.jpha.2023.09.014

Citation:

Izabela Malczak, Anna Gajda. Interactions of naturally occurring compounds with antimicrobials[J]. Journal of Pharmaceutical Analysis, 2023, 13(12): 1452-1470. doi: 10.1016/j.jpha.2023.09.014

Izabela Malczak, Anna Gajda. Interactions of naturally occurring compounds with antimicrobials[J]. Journal of Pharmaceutical Analysis, 2023, 13(12): 1452-1470. doi: 10.1016/j.jpha.2023.09.014

Citation:

Izabela Malczak, Anna Gajda. Interactions of naturally occurring compounds with antimicrobials[J]. Journal of Pharmaceutical Analysis, 2023, 13(12): 1452-1470. doi: 10.1016/j.jpha.2023.09.014

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Interactions of naturally occurring compounds with antimicrobials

doi: 10.1016/j.jpha.2023.09.014

Izabela Malczak,
Anna Gajda^,

Department of Pharmacology and Toxicology, National Veterinary Research Institute, Partyzantów 57, 24-100, Poland

Received Date: Jun. 23, 2023
Accepted Date: Sep. 19, 2023
Rev Recd Date: Sep. 12, 2023
Publish Date: Sep. 23, 2023

Abstract

Abstract

Antibiotics are among the most often used medications in human healthcare and agriculture. Overusing these substances can lead to complications such as increasing antibiotic resistance in bacteria or a toxic effect when administering large amounts. To solve these problems, new solutions in antibacterial therapy are needed. The use of natural products in medicine has been known for centuries. Some of them have antibacterial activity, hence the idea to combine their activity with commercial antibiotics to reduce the latter's use. This review presents collected information on natural compounds (terpenes, alkaloids, flavonoids, tannins, sulfoxides, and mycotoxins), of which various drug interactions have been observed. Many of the indicated compounds show synergistic or additive interactions with antibiotics, which suggests their potential for use in antibacterial therapy, reducing the toxicity of the antibiotics used and the risk of further development of bacterial resistance. Unfortunately, there are also compounds which interact antagonistically, potentially hindering the therapy of bacterial infection. Depending on its mechanism of action, each compound can behave differently in combination with different antibiotics and when acting against various bacterial strains.
- Interactions,
- Antimicrobials,
- Natural compounds,
- Antibiotics

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References(155)

References

[1]	M. Pecanac, Z. Janjic, A. Komarcevic, et al., Burns treatment in ancient times, Med. Pregl. 66 (2013) 263-267.
[2]	A.J. Browne, M.G. Chipeta, G. Haines-Woodhouse, et al., Global antibiotic consumption and usage in humans, 2000-18: A spatial modelling study, Lancet Planet. Health 5 (2021) e893-e904.
[3]	D.K. Yimenu, A. Emam, E. Elemineh, et al., Assessment of antibiotic prescribing patterns at outpatient pharmacy using World Health Organization prescribing indicators, J. Prim. Care Community Heath. 10 (2019), 215013271988694.
[4]	T.P. Van Boeckel, C. Brower, M. Gilbert, et al., Global trends in antimicrobial use in food animals, Proc. Natl. Acad. Sci. U S A 112 (2015) 5649-5654.
[5]	B. Walker, S. Barrett, S. Polasky, et al., Looming global-scale failures and missing institutions, Science 325 (2009) 1345-1346.
[6]	Penicillin’s finder assays its future; Sir Alexander Fleming says improved dosage method is needed to extend use other scientists praised self-medication decried, The New York Times. https://www.nytimes.com/1945/06/26/archives/penicillins-finder-assays-its-future-sir-alexander-fleming-says.html. (Accessed 9 June 2023).
[7]	Neil Fishman, Society for Healthcare Epidemiology of America, Infectious Diseases Society of America, et al., Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS), Infect. Control Hosp. Epidemiol. 33 (2012) 322-327.
[8]	Infectious Diseases Society of America (IDSA), Combating antimicrobial resistance: Policy recommendations to save lives, Clin. Infect. Dis. 52 (2011) S397-S428.
[9]	Antimicrobial Resistance Collaborators, Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis, Lancet 399 (2022) 629-655.
[10]	P. Dadgostar, Antimicrobial resistance: Implications and costs, Infect. Drug Resist. 12 (2019) 3903-3910.
[11]	C.D. Iwu, L. Korsten, A.I. Okoh, The incidence of antibiotic resistance within and beyond the agricultural ecosystem: A concern for public health, Microbiologyopen 9 (2020), e1035.
[12]	P.M. Mertes, G.W. Volcheck, L.H. Garvey, et al., Epidemiology of perioperative anaphylaxis, Presse Med. 45 (2016) 758-767.
[13]	J.F. Westphal, D. Vetter, J.M. Brogard, Hepatic side-effects of antibiotics, J. Antimicrob. Chemother. 33 (1994) 387-401.
[14]	A. Manten, Side effects of antibiotics, Vet. Q. 3 (1981) 179-182.
[15]	A. Redwan Haque, M. Sarker, R. Das, et al., A review on antibiotic residue in foodstuffs from animal source: Global health risk and alternatives, Int. J. Environ. Anal. Chem. 103 (2023) 3704-3721.
[16]	M. Bacanli, N. Basaran, Importance of antibiotic residues in animal food, Food Chem. Toxicol. 125 (2019) 462-466.
[17]	H.W. Boucher, G.H. Talbot, J.S. Bradley, et al., Bad bugs, no drugs: No ESKAPE! an update from the infectious diseases society of America, Clin. Infect. Dis. 48 (2009) 1-12.
[18]	A. Scalbert, Antimicrobial properties of tannins, Phytochemistry 30 (1991) 3875-3883.
[19]	U. Abbasoglu, B. Sener, Y. Gunay, et al., Antimicrobial activity of some isoquinoline alkaloids, Arch. Pharm. (Weinheim) 324 (1991) 379-380.
[20]	A.C. Guimaraes, L.M. Meireles, M.F. Lemos, et al., Antibacterial activity of terpenes and terpenoids present in essential oils, Molecules 24 (2019), 2471.
[21]	T.P. Cushnie, A.J. Lamb, Antimicrobial activity of flavonoids, Int. J. Antimicrob. Agents 26 (2005) 343-356.
[22]	M.P. Pai, K.M. Momary, K.A. Rodvold, Antibiotic drug interactions, Med. Clin. North Am. 90 (2006) 1223-1255.
[23]	P.D. Cardona, Drug-food interactions, Nutr. Hosp. 14 (1999) 129S-140S.
[24]	M.M. Cowan, Plant products as antimicrobial agents, Clin. Microbiol. Rev. 12 (1999) 564-582.
[25]	M. Stavri, L.J.V. Piddock, S. Gibbons, Bacterial efflux pump inhibitors from natural sources, J. Antimicrob. Chemother. 59 (2007) 1247-1260.
[26]	N.S. Radulovic, P.D. Blagojevic, Z.Z. Stojanovic-Radic, et al., Antimicrobial plant metabolites: Structural diversity and mechanism of action, Curr. Med. Chem. 20 (2013) 932-952.
[27]	A. Smith-Palmer, J. Stewart, L. Fyfe, Inhibition of listeriolysin O and phosphatidylcholine-specific production in Listeria monocytogenes by subinhibitory concentrations of plant essential oils, J. Med. Microbiol. 51 (2002) 567-608.
[28]	A. Ultee, E.J. Smid, Influence of carvacrol on growth and toxin production by Bacillus cereus, Int. J. Food Microbiol. 64 (2001) 373-378.
[29]	S. Mooyottu, A. Kollanoor-Johny, G. Flock, et al., Carvacrol and trans-Cinnamaldehyde Reduce Clostridium difficile Toxin Production and Cytotoxicity in Vitro, Int. J. Mol. Sci. 15 (2014) 4415-4430.
[30]	A.J. Seukep, V. Kuete, L. Nahar, et al., Plant-derived secondary metabolites as the main source of efflux pump inhibitors and methods for identification, J. Pharm. Anal. 10 (2020) 277-290.
[31]	T. Chou, Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies, Pharmacol. Rev. 58 (2006) 621-681.
[32]	W.R. Greco, G. Bravo, J.C. Parsons, The search for synergy: A critical review from a response surface perspective, Pharmacol. Rev. 47 (1995) 331-385.
[33]	K.D. Rakholiya, M.J. Kaneria, S.V. Chanda, Medicinal plants as alternative sources of therapeutics against multidrug-resistant pathogenic microorganisms based on their antimicrobial potential and synergistic properties. Fighting Multidrug Resistance with Herbal Extracts, Essential Oils and Their Components. Amsterdam: Elsevier, 2013, pp. 165-179.
[34]	I. Nikolic, D. Vukovic, D. Gavric, et al., An optimized checkerboard method for phage-antibiotic synergy detection, Viruses 14 (2022), 1542.
[35]	E. Breitmaier, Terpenes: Flavors, Fragrances, Pharmaca, Pheromones by eberhard, Wiley-VCH Verlag GmbH & Co., KGaA, 2006.
[36]	J. Rico, K. Duquesne, J.L. Petit, et al., Exploring natural biodiversity to expand access to microbial terpene synthesis, Microb. Cell Fact. 18 (2019), 23.
[37]	K.R. Riella, R.R. Marinho, J.S. Santos, et al., Anti-inflammatory and cicatrizing activities of thymol, a monoterpene of the essential oil from Lippia gracilis, in rodents, J. Ethnopharmacol. 143 (2012) 656-663.
[38]	P.C. Braga, M. Dal Sasso, M. Culici, et al., Anti-inflammatory activity of thymol: Inhibitory effect on the release of human neutrophil elastase, Pharmacology 77 (2006) 130-136.
[39]	N.V. Yanishlieva, E.M. Marinova, M.H. Gordon, et al., Antioxidant activity and mechanism of action of thymol and carvacrol in two lipid systems, Food Chem. 64 (1999) 59-66.
[40]	M. Nikolic, J. Glamoclija, I.C.F.R. Ferreira, et al., Chemical composition, antimicrobial, antioxidant and antitumor activity of Thymus serpyllum L., Thymus algeriensis Boiss. and Reut and Thymus vulgaris L. essential oils, Ind. Crops Prod. 52 (2014) 183-190.
[41]	N. Guo, J. Liu, X. Wu, et al., Antifungal activity of thymol against clinical isolates of fluconazole-sensitive and-resistant Candida albicans, J. Med. Microbiol. 58 (2009) 1074-1079.
[42]	R. Paduch, M. Kandefer-Szerszen, M. Trytek, et al., Terpenes: Substances useful in human healthcare, Arch. Immunol. Ther. Exp. 55 (2007) 315-327.
[43]	F. Reyes-Jurado, T. Cervantes-Rincon, H. Bach, et al., Antimicrobial activity of Mexican oregano (Lippia berlandieri), thyme (Thymus vulgaris), and mustard (Brassica nigra) essential oils in gaseous phase, Ind. Crops Prod. 131 (2019) 90-95.
[44]	J. Rua, P. Del Valle, D. de Arriaga, et al., Combination of carvacrol and thymol: Antimicrobial activity against Staphylococcus aureus and antioxidant activity, Foodborne Pathog. Dis. 16 (2019) 622-629.
[45]	H.N.H. Veras, F.F.G. Rodrigues, M.A. Botelho, et al., Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the Thymol, Arab. J. Chem. 10 (2017) S2790-S2795.
[46]	R. Hamoud, S. Zimmermann, J. Reichling, et al., Synergistic interactions in two-drug and three-drug combinations (thymol, EDTA and vancomycin) against multi drug resistant bacteria including E. coli, Phytomedicine 21 (2014) 443-447.
[47]	F.P.K. Jesus, L. Ferreiro, K.S. Bizzi, et al., In vitro activity of carvacrol and thymol combined with antifungals or antibacterials against Pythium insidiosum, J. De Mycol. Medicale 25 (2015) e89-e93.
[48]	I.C.D.S. Cirino, S.M.P. Menezes-Silva, H.T. Silva, et al., The essential oil from Origanum vulgare L. and its individual constituents carvacrol and thymol enhance the effect of tetracycline against Staphylococcus aureus, Chemotherapy 60 (2014) 290-293.
[49]	W. Kissels, X. Wu, R.R. Santos, Short communication: Interaction of the isomers carvacrol and thymol with the antibiotics doxycycline and tilmicosin: in vitro effects against pathogenic bacteria commonly found in the respiratory tract of calves, J. Dairy Sci. 100 (2017) 970-974.
[50]	S.F. Zanini, A.B. Silva-Angulo, A. Rosenthal, et al., Effect of citral and carvacrol on the susceptibility of Listeria monocytogenes and Listeria innocua to antibiotics, Lett. Appl. Microbiol. 58 (2014) 486-492.
[51]	G. Magi, E. Marini, B. Facinelli, Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin, against clinical, erythromycin-resistant Group A Streptococci, Front. Microbiol. 6 (2015), 165.
[52]	P.Y. Chung, P. Navaratnam, L.Y. Chung, Synergistic antimicrobial activity between pentacyclic triterpenoids and antibiotics against Staphylococcus aureus strains, Ann. Clin. Microbiol. Antimicrob. 10 (2011), 25.
[53]	M. Dettweiler, R.J. Melander, G. Porras, et al., A clerodane diterpene from Callicarpa americana resensitizes methicillin-resistant Staphylococcus aureus to β-lactam antibiotics, ACS Infect. Dis. 6 (2020) 1667-1673.
[54]	V.K. Gupta, N. Tiwari, P. Gupta, et al., A clerodane diterpene from Polyalthia longifolia as a modifying agent of the resistance of methicillin resistant Staphylococcus aureus, Phytomedicine 23 (2016) 654-661.
[55]	A. Tetard, S. Foley, G.L.A. Mislin, et al., Negative impact of citral on susceptibility of Pseudomonas aeruginosa to antibiotics, Front. Microbiol. 12 (2021), 709838.
[56]	A. Escobar, M. Perez, G. Romanelli, et al., Thymol bioactivity: A review focusing on practical applications, Arab. J. Chem. 13 (2020) 9243-9269.
[57]	H. Nikaido, Outer membrane barrier as a mechanism of antimicrobial resistance, Antimicrob. Agents Chemother. 33 (1989) 1831-1836.
[58]	Z.E. Suntres, J. Coccimiglio, M. Alipour, The bioactivity and toxicological actions of carvacrol, Crit. Rev. Food Sci. Nutr. 55 (2015) 304-318.
[59]	A. Nostro, A.R. Blanco, M.A. Cannatelli, et al., Susceptibility of methicillin-resistant staphylococci to oregano essential oil, carvacrol and thymol, FEMS Microbiol. Lett. 230 (2004) 191-195.
[60]	R.J. Lambert, P.N. Skandamis, P.J. Coote, et al., A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol, J. Appl. Microbiol. 91 (2001) 453-462.
[61]	A.S. Olsen, R. Warrass, S. Douthwaite, Macrolide resistance conferred by rRNA mutations in field isolates of Mannheimia haemolytica and Pasteurella multocida, J. Antimicrob. Chemother. 70 (2015) 420-423.
[62]	N.J. Sadgrove, G.F. Padilla-Gonzalez, M. Phumthum, Fundamental chemistry of essential oils and volatile organic compounds, methods of analysis and authentication, Plants 11 (2022), 789.
[63]	S. Jager, H. Trojan, T. Kopp, et al., Pentacyclic triterpene distribution in various plants - rich sources for a new group of multi-potent plant extracts, Molecules 14 (2009) 2016-2031.
[64]	M.H. Ghante, P.G. Jamkhande, Role of pentacyclic triterpenoids in chemoprevention and anticancer treatment: An overview on targets and underling mechanisms, J. Pharmacopuncture 22 (2019) 55-67.
[65]	R. Li, S.L. Morris-Natschke, K.H. Lee, Clerodane diterpenes: Sources, structures, and biological activities, Nat. Prod. Rep. 33 (2016) 1166-1226.
[66]	W.C. Evans, D. Evans, Chapter 26 - Alkaloids, W.C. Evans, D. Evans, Trease and Evans’ Pharmacognosy, sixteenth ed., 2009, pp. 353-415.
[67]	D. Mabhiza, T. Chitemerere, S. Mukanganyama, Antibacterial properties of alkaloid extracts from Callistemon citrinus and Vernonia adoensis against Staphylococcus aureus and Pseudomonas aeruginosa, Int. J. Med. Chem. 2016 (2016), 6304163.
[68]	S. Parthasarathy, J. Bin Azizi, S. Ramanathan, et al., Evaluation of antioxidant and antibacterial activities of aqueous, methanolic and alkaloid extracts from Mitragyna speciosa (rubiaceae family) leaves, Molecules 14 (2009) 3964-3974.
[69]	S. Singh, S.K. Verma, Antibacterial properties of Alkaloid rich fractions obtained from various parts of Prosopis juliflora, Int. J. Pharma. Sci. Res. 2 (2011) 114-120.
[70]	D.E. Okwu, E.C. Igara, Isolation, characterization and antibacterial activity of alkaloid from Datura metel Linn leaves, Afr. J. Pharm. Pharmacol. 3 (2009) 277-281.
[71]	N.P. Kalia, P. Mahajan, R. Mehra, et al., Capsaicin, a novel inhibitor of the NorA efflux pump, reduces the intracellular invasion of Staphylococcus aureus, J. Antimicrob. Chemother. 67 (2012) 2401-2408.
[72]	E.E. Mgbeahuruike, M. Stalnacke, H. Vuorela, et al., Antimicrobial and synergistic effects of commercial piperine and piperlongumine in combination with conventional antimicrobials, Antibiotics 8 (2019), 55.
[73]	B. Bisso Ndezo, C.R. Tokam Kuate, J.P. Dzoyem, Synergistic antibiofilm efficacy of thymol and piperine in combination with three aminoglycoside antibiotics against Klebsiella pneumoniae biofilms, Can. J. Infect. Dis. Med. Microbiol. 2021 (2021), 7029944.
[74]	C.R. Tokam Kuate, B. Bisso Ndezo, J.P. Dzoyem, Synergistic antibiofilm effect of thymol and piperine in combination with aminoglycosides antibiotics against four Salmonella enterica serovars, Evid. Based Complement. Alternat. Med. 2021 (2021), 1567017.
[75]	X. Li, Y. Song, L. Wang, et al., A potential combination therapy of berberine hydrochloride with antibiotics against multidrug-resistant Acinetobacter baumannii, Front. Cell. Infect. Microbiol. 11 (2021), 660431.
[76]	X. Zhou, X. Ye, L. He, et al., In vitro characterization and inhibition of the interaction between ciprofloxacin and berberine against multidrug-resistant Klebsiella pneumoniae, J. Antibiot. 69 (2016) 741-746.
[77]	R. Wojtyczka, A. Dziedzic, M. Kepa, et al., Berberine enhances the antibacterial activity of selected antibiotics against coagulase-negative Staphylococcus strains in vitro, Molecules 19 (2014) 6583-6596.
[78]	A. Dziedzic, R.D. Wojtyczka, R. Kubina, Inhibition of oral streptococci growth induced by the complementary action of berberine chloride and antibacterial compounds, Molecules 20 (2015) 13705-13724.
[79]	G. Zuo, Y. Li, T. Wang, et al., Synergistic antibacterial and antibiotic effects of bisbenzylisoquinoline alkaloids on clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA), Molecules 16 (2011) 9819-9826.
[80]	B.W. Obiang-Obounou, O.H. Kang, J.G. Choi, et al., In vitro potentiation of ampicillin, oxacillin, norfloxacin, ciprofloxacin, and vancomycin by sanguinarine against methicillin-resistant Staphylococcus aureus, Foodborne Pathog. Dis. 8 (2011) 869-874.
[81]	R. Hamoud, J. Reichling, M. Wink, Synergistic antibacterial activity of the combination of the alkaloid sanguinarine with EDTA and the antibiotic streptomycin against multidrug resistant bacteria, J. Pharm. Pharmacol. 67 (2015) 264-273.
[82]	A. Maurya, G.R. Dwivedi, M.P. Darokar, et al., Antibacterial and synergy of clavine alkaloid lysergol and its derivatives against nalidixic acid-resistant Escherichia coli, Chem. Biol. Drug Des. 81 (2013) 484-490.
[83]	J.P. Lavigne, J.M. Brunel, J. Chevalier, et al., Squalamine, an original chemosensitizer to combat antibiotic-resistant Gram-negative bacteria, J. Antimicrob. Chemother. 65 (2010) 799-801.
[84]	G. Mitchell, M. Lafrance, S. Boulanger, et al., Tomatidine acts in synergy with aminoglycoside antibiotics against multiresistant Staphylococcus aureus and prevents virulence gene expression, J. Antimicrob. Chemother. 67 (2012) 559-568.
[85]	A. Woziwodzka, M. Krychowiak-Masnicka, G. Golunski, et al., New life of an old drug: Caffeine as a modulator of antibacterial activity of commonly used antibiotics, Pharmaceuticals 15 (2022), 872.
[86]	C. Esimone, F. Okoye, C. Nworu, et al., In vitro interaction between caffeine and some penicillin antibiotics against Staphylococcus aureus, Trop. J. Pharm. Res. 7 (2008) 969-974.
[87]	O.O. Olajuyigbe, M.O. Adeoye-Isijola, V. Okon, et al., In vitro pharmacological interaction of caffeine and first-line antibiotics is antagonistic against clinically important bacterial pathogens, Acta Biochim. Pol. 64 (2017) 255-263.
[88]	S. Fuchtbauer, S. Mousavi, S. Bereswill, et al., Antibacterial properties of capsaicin and its derivatives and their potential to fight antibiotic resistance - A literature survey, Eur. J. Microbiol. Immunol. 11 (2021) 10-17.
[89]	E. Marini, G. Magi, M. Mingoia, et al., Antimicrobial and anti-virulence activity of capsaicin against erythromycin-resistant, cell-invasive group A streptococci, Front. Microbiol. 6 (2015), 1281.
[90]	P. Agarwal, C. Das, O. Dias, et al., Antimicrobial property of Capsaicin, Int. J. Biol. Sci. 6 (2017) 7-11.
[91]	A. Bouraoui, A. Toumi, H. Ben Mustapha, et al., Effects of capsicum fruit on theophylline absorption and bioavailability in rabbits, Drug Nutr. Interact. 5 (1988) 345-350.
[92]	S.K. Bedada, R. Appani, P.K. Boga, Capsaicin pretreatment enhanced the bioavailability of fexofenadine in rats by P-glycoprotein modulation: In vitro, in situ and in vivo evaluation, Drug Dev. Ind. Pharm. 43 (2017) 932-938.
[93]	H. Sumano-Lopez, L. Gutierrez-Olvera, R. Aguilera-Jimenez, et al., Administration of ciprofloxacin and capsaicin in rats to achieve higher maximal serum concentrations, Arzneimittelforschung 57 (2007) 286-290.
[94]	C.A. Reilly, J.L. Taylor, D.L. Lanza, et al., Capsaicinoids cause inflammation and epithelial cell death through activation of vanilloid receptors, Toxicol. Sci. 73 (2003) 170-181.
[95]	O.L. Gutierrez, L.H. Sumano, Q.M. Zamora, Administration of enrofloxacin and capsaicin to chickens to achieve higher maximal serum concentrations, Vet. Rec. 150 (2002) 350-353.
[96]	Y. Komori, T. Aiba, C. Nakai, et al., Capsaicin-induced increase of intestinal cefazolin absorption in rats, Drug Metab. Pharmacokinet. 22 (2007) 445-449.
[97]	Y. Komori, T. Aiba, R. Sugiyama, et al., Effects of capsaicin on intestinal cephalexin absorption in rats, Biol. Pharm. Bull. 30 (2007) 547-551.
[98]	G. Derosa, P. Maffioli, A. Sahebkar, Piperine and its role in chronic diseases. Anti-inflammatory Nutraceuticals and Chronic Diseases, Springer Cham, 2016, pp. 173-184.
[99]	K. Janakiraman, R. Manavalan, Studies on effect of piperine on oral bioavailability of ampicillin and norfloxacin, Afr. J. Tradit. Complement. Altern. Med. 5 (2008) 257-262.
[100]	A.R. Hiwale, J.N. Dhuley, S.R. Naik, Effect of co-administration of piperine on pharmacokinetics of beta-lactam antibiotics in rats, Indian J. Exp. Biol. 40 (2002) 277-281.
[101]	L. Manosalva, A. Mutis, A. Urzua, et al., Antibacterial activity of alkaloid fractions from Berberis microphylla G. forst and study of synergism with ampicillin and cephalothin, Molecules 21 (2016), 76.
[102]	F. Burdan, Pharmacology of caffeine. Coffee in Health and Disease Prevention. Amsterdam: Elsevier, (2015) 823-829.
[103]	R. Hamoud, J. Reichling, M. Wink, Synergistic antimicrobial activity of combinations of sanguinarine and EDTA with vancomycin against multidrug resistant bacteria, Drug Metab. Lett. 8 (2014) 119-128.
[104]	A.N. Panche, A.D. Diwan, S.R. Chandra, Flavonoids: An overview, J. Nutr. Sci. 5 (2016), e47.
[105]	G. Donadio, F. Mensitieri, V. Santoro, et al., Interactions with microbial proteins driving the antibacterial activity of flavonoids, Pharmaceutics 13 (2021), 660.
[106]	B.C.L. Chan, M. Ip, H. Gong, et al., Synergistic effects of diosmetin with erythromycin against ABC transporter over-expressed methicillin-resistant Staphylococcus aureus (MRSA) RN4220/pUL5054 and inhibition of MRSA pyruvate kinase, Phytomedicine 20 (2013) 611-614.
[107]	A.C. Pushkaran, V. Vinod, M. Vanuopadath, et al., Combination of repurposed drug diosmin with amoxicillin-clavulanic acid causes synergistic inhibition of mycobacterial growth, Sci. Rep. 9 (2019), 6800.
[108]	H.K. Kang, H.Y. Kim, J.D. Cha, Synergistic effects between silibinin and antibiotics on methicillin-resistant Staphylococcus aureus isolated from clinical specimens, Biotechnol. J. 6 (2011) 1397-1408.
[109]	Y.S. Lee, K.A. Jang, J.D. Cha, Synergistic antibacterial effect between silibinin and antibiotics in oral bacteria, J. Biomed. Biotechnol. 2012 (2012), 618081.
[110]	B.C.L. Chan, M. Ip, C.B.S. Lau, et al., Synergistic effects of baicalein with ciprofloxacin against NorA over-expressed methicillin-resistant Staphylococcus aureus (MRSA) and inhibition of MRSA pyruvate kinase, J. Ethnopharmacol. 137 (2011) 767-773.
[111]	M. Fujita, S. Shiota, T. Kuroda, et al., Remarkable synergies between baicalein and tetracycline, and baicalein and beta-lactams against methicillin-resistant Staphylococcus aureus, Microbiol. Immunol. 49 (2005) 391-396.
[112]	T. Liu, J. Luo, G. Bi, et al., Antibacterial synergy between linezolid and baicalein against methicillin-resistant Staphylococcus aureus biofilm in vivo, Microb. Pathog. 147 (2020), 104411.
[113]	W. Cai, Y. Fu, W. Zhang, et al., Synergistic effects of baicalein with cefotaxime against Klebsiella pneumoniae through inhibiting CTX-M-1 gene expression, BMC Microbiol. 16 (2016), 181.
[114]	J. Wang, M. Qiao, Y. Zhou, et al., In vitro synergistic effect of baicalin with azithromycin against Staphylococcus saprophyticus isolated from francolins with ophthalmia, Poult. Sci. 98 (2019) 373-380.
[115]	T. Hatano, Y. Shintani, Y. Aga, et al., Phenolic constituents of licorice. VIII. Structures of glicophenone and glicoisoflavanone, and effects of licorice phenolics on methicillin-resistant Staphylococcus aureus, Chem. Pharm. Bull. 48 (2000) 1286-1292.
[116]	M.U. Amin, M. Khurram, B. Khattak, et al., Antibiotic additive and synergistic action of rutin, morin and quercetin against methicillin resistant Staphylococcus aureus, BMC Complement. Altern. Med. 15 (2015), 59.
[117]	M. Usman Amin, M. Khurram, T.A. Khan, et al., Effects of luteolin and quercetin in combination with some conventional antibiotics against methicillin-resistant Staphylococcus aureus, Int. J. Mol. Sci. 17 (2016), 1947.
[118]	X. Zhang, L. Wang, H. Mu, et al., Synergistic antibacterial effects of Buddleja albiflora metabolites with antibiotics against Listeria monocytogenes, Lett. Appl. Microbiol. 68 (2019) 38-47.
[119]	C.A. Torres, M.B. Nunez, M.I. Isla, et al., Antibacterial synergism of extracts from climbers belonging to Bignoniaceae family and commercial antibiotics against multi-resistant bacteria, J. Herb. Med. 8 (2017) 24-30.
[120]	W.M. Al-Jewari, Z.O. Ibraheem, S.Shukur Mohammed, et al., Effect of silibinin on the sensitivity of Enterobacter cloacae resistant isolate to gentamicin: In vitro study, Asian J. Microbiol. Biotechnol. Environ. Sci. 22 (2020) 248-253.
[121]	B.J. Denny, P.W.J. West, T.C. Mathew, Antagonistic interactions between the flavonoids hesperetin and naringenin and beta-lactam antibiotics against Staphylococcus aureus, Br. J. Biomed. Sci. 65 (2008) 145-147.
[122]	H. Veras, I.J.M. Santos, A.C.B. dos Santos, et al., Comparative evaluation of antibiotic and antibiotic modifying activity of quercetin and isoquercetin in vitro, Curr. Top. Nutraceutical Res. 9 (2011) 25-30.
[123]	PubChem, Silibinin, https://pubchem.ncbi.nlm.nih.gov/compound/31553. (Accessed 30 August 2023).
[124]	J. Fiett, A. Palucha, B. Miaczynska, et al., A novel complex mutant β-lactamase, TEM-68, identified in a Klebsiella pneumoniae isolate from an outbreak of extended-spectrum β-lactamase-producing Klebsiellae, Antimicrob. Agents Chemother. 44 (2000) 1499-1505.
[125]	D. Yang, T. Wang, M. Long, et al., Quercetin: Its main pharmacological activity and potential application in clinical medicine, Oxid. Med. Cell. Longev. 2020 (2020), 8825387.
[126]	F.M. Campos, J.A. Couto, A.R. Figueiredo, et al., Cell membrane damage induced by phenolic acids on wine lactic acid bacteria, Int. J. Food Microbiol. 135 (2009) 144-151.
[127]	Tannins: An antinutrient with positive effect to manage diabetes, Res. J. Recent Sci. 1 (2012) 70-73.
[128]	E. Sieniawska, T. Baj, Tannins. Pharmacognosy, Elsevier, 2017, pp. 199-232.
[129]	M. Shimizu, S. Shiota, T. Mizushima, et al., Marked potentiation of activity of β-lactams against methicillin-resistant Staphylococcus aureus by corilagin, Antimicrob. Agents Chemother. 45 (2001) 3198-3201.
[130]	S. Shiota, M. Shimizu, J. Sugiyama, et al., Mechanisms of action of corilagin and tellimagrandin I that remarkably potentiate the activity of beta-lactams against methicillin-resistant Staphylococcus aureus, Microbiol. Immunol. 48 (2004) 67-73.
[131]	Y. Chang, W. Huang, C. Lin, et al., Tellimagrandin II, A type of plant polyphenol extracted from Trapa bispinosa inhibits antibiotic resistance of drug-resistant Staphylococcus aureus, Int. J. Mol. Sci. 20 (2019), 5790.
[132]	S.H. Mun, O.H. Kang, R. Kong, et al., Punicalagin suppresses methicillin resistance of Staphylococcus aureus to oxacillin, J. Pharmacol. Sci. 137 (2018) 317-323.
[133]	H. Akiyama, K. Fujii, O. Yamasaki, et al., Antibacterial action of several tannins against Staphylococcus aureus, J. Antimicrob. Chemother. 48 (2001) 487-491.
[134]	B.M. Kyaw, S. Arora, C.S. Lim, Bactericidal antibiotic-phytochemical combinations against methicillin resistant Staphylococcus aureus, Braz. J. Microbiol. 43 (2012) 938-945.
[135]	T.R. Neyestani, N. Khalaji, A. Gharavi, Selective microbiologic effects of tea extract on certain antibiotics against Escherichia coli in vitro, J. Altern. Complement. Med. 13 (2007) 1119-1124.
[136]	D.H. Dusane, C. O'May, N. Tufenkji, Effect of tannic and Gallic acids alone or in combination with carbenicillin or tetracycline on Chromobacterium violaceum CV026 growth, motility, and biofilm formation, Can. J. Microbiol. 61 (2015) 487-494.
[137]	X. Li, Y. Deng, Z. Zheng, et al., Corilagin, a promising medicinal herbal agent, Biomed. Pharmacother. 99 (2018) 43-50.
[138]	H. Robles, Tannic Acid. Encyclopedia of Toxicology (Third Edition), Academic Press, Oxford, 2014, pp. 474-475.
[139]	K.S. Currie, L. Patel, K.F. Sedillo, Small-molecule agents for the treatment of inflammatory bowel disease, Bioorg. Med. Chem. Lett. 29 (2019) 2034-2041.
[140]	S.M. Pal, G. Avneet, S.S. Siddhraj, Gallic acid: Pharmacological promising lead molecule: A review, Int. J. Pharmacogn. Phytochem. 10 (2018) 132-138.
[141]	R. Gutierrez-Escobar, M.J. Aliano-Gonzalez, E. Cantos-Villar, Wine polyphenol content and its influence on wine quality and properties: A review, Molecules 26 (2021), 718.
[142]	S. Patai, Z. Rappoport, Syntheses of Sulphones, Sulphoxides and Cyclic Sulphides (1995), John Wiley & Sons, Ltd., Chichester, 1995.
[143]	J. Borlinghaus, F. Albrecht, M.C. Gruhlke, et al., Allicin: Chemistry and biological properties, Molecules 19 (2014) 12591-12618.
[144]	Y. Cai, R. Wang, F. Pei, et al., Antibacterial activity of allicin alone and in combination with β-lactams against Staphylococcus spp. and Pseudomonas aeruginosa, J. Antibiot. 60 (2007) 335-338.
[145]	S. Bhattacharya, P. Chakraborty, D. Sen, et al., Kinetics of bactericidal potency with synergistic combination of allicin and selected antibiotics, J. Biosci. Bioeng. 133 (2022) 567-578.
[146]	I. Cirkovic, M. Jovalekic, B. Jegorovic, In vitro antibacterial activity of garlic and synergism between garlic and antibacterial drugs, Arch. Biol. Sci. 64 (2012) 1369-1375.
[147]	D. Jonkers, J. Sluimer, E. Stobberingh, Effect of garlic on vancomycin-resistant enterococci, Antimicrob. Agents Chemother. 43 (1999), 3045.
[148]	P.S. Chakarborty, H. Sapkota, P.K. Prabhakar, Synergistic interaction of cannabis and garlic with commercial antibiotics, Int. J. Pharmacogn. Phytochem. 7 (2015) 193-196.
[149]	R. Leontiev, N. Hohaus, C. Jacob, et al., A comparison of the antibacterial and antifungal activities of thiosulfinate analogues of allicin, Sci. Rep. 8 (2018), 6763.
[150]	C. Gruber-Dorninger, T. Jenkins, G. Schatzmayr, Global mycotoxin occurrence in feed: A ten-year survey, Toxins 11 (2019), 375.
[151]	L. Broom, Mycotoxins and the intestine, Anim. Nutr. 1 (2015) 262-265.
[152]	J. Goossens, M. Devreese, F. Pasmans, et al., Chronic exposure to the mycotoxin T-2 promotes oral absorption of chlortetracycline in pigs, J. Vet. Pharmacol. Ther. 36 (2013) 621-624.
[153]	J. Goossens, F. Pasmans, E. Verbrugghe, et al., Porcine intestinal epithelial barrier disruption by the Fusarium mycotoxins deoxynivalenol and T-2 toxin promotes transepithelial passage of doxycycline and paromomycin, BMC Vet. Res. 8 (2012), 245.
[154]	G. Martinez, D.S. Perez, A.L. Soraci, et al., Penetration of fosfomycin into IPEC-J2 cells in the presence or absence of deoxynivalenol, PLoS One 8 (2013), e75068.
[155]	M. Mendel, W. Karlik, U. Latek, et al., Does deoxynivalenol affect amoxicillin and doxycycline absorption in the gastrointestinal tract? Ex vivo study on swine jejunum mucosa explants, Toxins 14 (2022), 743.