Plant phenolics and terpenoids as adjuvants of antibacterial and antifungal drugs

Phytomedicine

Volumn 37, Issue , 2017, Pages 27-48

  Zacchino, Susana A ^a   Butassi, Estefania ^a   Liberto, Melina Di ^a   Raimondi, Marcela ^a   Postigo, Agustina ^a   Sortino, Maximiliano ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

Antifungal drugs; Combination, Antibacterial drugs; Low molecular weight natural products; Potentiation

Indexed keywords

ANTIBIOTIC AGENT; ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT; CURCUMIN; GALLIC ACID; PHENOL DERIVATIVE; POLYPHENOL; TERPENE; TERPENOID; TRITERPENE; BIOLOGICAL PRODUCT; PHARMACEUTICAL VEHICLES AND ADDITIVES;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL THERAPY; ARTICLE; DRUG MECHANISM; FRACTIONAL INHIBITORY CONCENTRATION INDEX; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; CHEMISTRY; COMBINATION DRUG THERAPY; DRUG EFFECTS; FUNGUS; HUMAN; PLANT;

ADJUVANTS, PHARMACEUTIC; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; ANTIFUNGAL AGENTS; BIOLOGICAL PRODUCTS; DRUG RESISTANCE, BACTERIAL; DRUG THERAPY, COMBINATION; FUNGI; HUMANS; PLANTS; POLYPHENOLS; TERPENES;

EID: 85034660873     PISSN: 09447113     EISSN: 1618095X     Source Type: Journal    
DOI: 10.1016/j.phymed.2017.10.018     Document Type: Article

References (156)

1. Afeltra, J., Vitale, R., Mouton, J., Verweij, P., Potent synergistic in vitro interaction between nonantimicrobial membrane-active compounds and itraconazole against clinical isolates of Aspergillus fumigatus resistant to itraconazole. Antimicrob. Agents Chemother. 48 (2004), 1335–1343.
2. Ahmad, A., Khan, A., Ahmad Khan, L., Manzoor, N., In vitro synergy of eugenol and methyleugenol with fluconazole against Candida isolates. J. Med. Microbiol. 59 (2010), 1178–1184.
3. Ahmad, A., Khan, A., Manzoor, N., Reversal of efflux mediated antifungal resistance underlies synergistic activity of two monoterpenes with fluconazole. Eur. J. Pharm. Sci. 48 (2013), 80–86.
4. Ali, I., Sharma, P., Suri, K.A., Satti, N.K., Dutt, P., Afrin, F., Khan, I.A., In vitro antifungal activities of amphotericin B in combination with acteoside, a phenylethanoid glycoside from Colebrookea oppositifolia. J. Med. Microbiol. 60 (2011), 1326–1336.
5. An, J., Zuo, G., Hao, X., Wang, G., Li, Z., Antibacterial and synergy of a flavanolol rhamnoside with antibiotic against clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA). Phytomedicine 18 (2011), 990–993.
6. Andersson, D.I., Diarmaid, H., Antibiotic resistance and its cost: is it possible to reverse resistance?. Nat. Microbiol. Rev. 8 (2010), 260–269.
7. Andersson, D.I., Hughes, D., Gene amplification and adaptive evolution in bacteria. Annu. Rev. Genet. 43 (2009), 167–195.
8. Arendrup, M., Perlin, D., Echinocandin resistance: an emerging clinical problem. Inf. Dis. 27 (2014), 484–492.
9. Arias, C.A., Murray, B.E., A new antibiotic and the evolution of resistance. N. Engl. J. Med. 372 (2015), 1168–1170.
10. Ballard, E., Coote, P.J., Enhancement of antibiotic efficacy against multi-drug resistant Pseudomonas aeruginosa infections via combination with curcumin and 1-(1-naphthylmethyl)-piperazine. J. Antimicrob. Agents, 2, 2016, 1000116.
11. Baroud, M., Dandache, I., Araj., G.F., Wakim, R., Kanj, S., Kanafani, Z., Khairallah, M., Sabra, A., Shehab, M., Dbaibo, G., Matar, G.M., Underlying mechanisms of carbapenem resistance in extended-spectrum β-lactamase-producing Klebsiella pneumoniae and Escherichia coli isolates at a tertiary care centre in Lebanon: role of OXA-48 and NDM-1 carbapenemases. Int. J. Antimicrob. Agents 41 (2013), 75–79.
12. Basri, D.F., Zin, N.M., Bakar, N.S., Rahmat, F., Mohtar, M., Synergistic effects of phytochemicals and oxacillin on laboratory passage-derived vancomycin-intermediate Staphylococcus aureus strain. J. Med. Sci. 8 (2008), 131–136.
13. Berembaum, M.C., Criteria for analyzing interactions between biologically active agents. Adv. Cancer Res. 35 (1981), 269–332.
14. Berembaum, M.C., What is synergy?. Pharmacol. Rev. 41 (1989), 93–139.
15. Blair, J.M.A., Webber, M.A., Baylay, A.J., Ogbolu, D.O., Piddock, LJ., Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol. 13 (2015), 42–51.
16. Braga, P.C., Sasso, M.D., Culici, M., Alfieri, M., Eugenol and thymol, alone or in combination, induce morphological alterations in the envelope of Candida albicans. Fitoterapia 78 (2007), 396–400.
17. Brown, D., Cantón, R., Dubreuil, L., Gatermann, S., Giske, C., MacGowan, A., Martínez-Martínez, L., Mouton, J., Skov, R., Steinbakk, M., Walton, C., Heuer, O., Struelens, M.J., Diaz Högberg, L., Kahlmeter, G., Widespread implementation of EUCAST breakpoints for antibacterial susceptibility testing in Europe. Eur. Surveill., 20, 2015 pii=21008.
18. Bush, K., Courvalin, P., Dantas, G., Davies, J., Eisenstein, B., Huovinen, P., Jacoby, G., Kishony, R., Kreiswirth, B., Kutter, E., Lerner, S., Levy, S., Lewis, K., Lomovskaya, O., Miller, J., Mobashery, S., Piddock, L., Projan, S., Thomas, C., Tomasz, A., Tulkens, P., Walsh, T., Watson, J., Witkowski, J., Witte, W., Wright, G., Yeh, P., Zgurskaya, H., Tackling antibiotic resistance. Nat. Rev. Microbiol. 9 (2011), 894–896.
19. Campbell, B., Chan, K., Kim, J., Chemosensitization as a means to augment commercial antifungal agents. Front. Microbiol., 3, 2012, 79.
20. Campoy, S., Adrio, J., Antifungals. Biochem. Pharmacol. 133 (2017), 86–96.
21. Cannon, R.D., Lamping, E., Holmesetal, A.R., Efflux-mediated antifungal drug resistance. Clin. Microbiol. Rev. 22 (2009), 291–321.
22. Choi, J., Kang, O., Lee, Y., Oh, Y., Chae, H., Jan, H., Shin, D., Kwon, D., Antibacterial activity of methyl gallate isolated from Galla rhois or carvacrol combined with nalidixic acid against nalidixic acid resistant bacteria. Molecules 14 (2009), 1773–1780.
23. Chou, T.C., Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 58 (2006), 621–681.
24. Chou, T.C., Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 70 (2010), 440–446.
25. Cuenca-Estrella, M., Combinations of antifungal agents in therapy-what value are they?. J. Antimicrob. Chemother. 54 (2004), 854–869.
26. da Silva, D.L., Magalhães, T.F.F., dos Santos, J.R.A., de Paula, T.P., Modolo, L.V., de Fatima, A., Buzanello Martins, C.V., Santos, D.A., de Resende-Stoianoff, M.A., Curcumin enhances the activity of fluconazole against Cryptococcus gattii-induced cryptococcosis infection in mice. J. Appl. Microbiol. 120 (2015), 41–48.
27. Darius, A.J., Meintjes, G, Brown, G.D., A neglected epidemic: fungal infections in HIV/AIDS. Trends Microbiol. 22 (2014), 120–127.
28. D'Auria, F.D., Tecca, M., Strippoli, R., Simonetti, N., In vitro activity of propyl gallate-azole drug combination against fluconazole‐and itraconazole‐resistant Candida albicans strains. Lett. Appl. Microbiol. 32 (2001), 220–223.
29. Denning, D., Perlin, D., Azole resistance in Aspergillus: a growing public health menace. Future Microbiol. 6 (2011), 1229–1232.
30. ECDC/EMEA. Technical Report: the Bacterial Challenge: Time to React., 2009, European Centre for Disease Prevention and Control/European Medicines Agency Joint Working Group, Stockholm.
31. Ejim, L., Farha, M.A., Falconer, S.B., Combinations of antibiotics and nonantibiotic drugs enhance antimicrobial efficacy. Nat. Chem. Biol. 7 (2011), 348–350.
32. Endo, E.H., Cortez, D.A., Ueda-Nakamura, T., Nakamura, C.V., Dias Filho, B.P., Potent antifungal activity of extracts and pure compound isolated from pomegranate peels and synergism with fluconazole against Candida albicans. Res. Microbiol. 161 (2010), 534–540.
33. Esimone, C., Okoye, F., Nworu, C., Agubata, C., In vitro interaction between caffeine and some penicillin antibiotics against Staphylococcus aureus. Trop. J. Pharm. Res. 7 (2008), 969–974.
34. Eumkeb, G., Sakdarat, S., Siriwong, S., Reversing β-lactam antibiotic resistance of Staphylococcus aureus with galangin from Alpinia officinarum Hance and synergism with ceftazidime. Phytomedicine 18 (2010), 40–45.
35. Falcão-Silva, V., Silva, D., Souza, M.F., Siqueira-Junior, J., Modulation of drug resistance in Staphylococcus aureus by a kaempferol glycoside from Herissantia tiubae (Malvaceae). Phytother. Res. 23 (2009), 1367–1370.
36. Faria, N.C., Kim, J.H., Goncalves, L.A., Martins Mde, L., Chan, K.L., Campbell, B.C., Enhanced activity of antifungal drugs using natural phenolics against yeast strains of Candida and Cryptococcus. Lett. Appl. Microbiol. 52 (2011), 506–513.
37. Frost, K., An overview of antibiotic therapy. Nurs. Stand. 22 (2007), 51–57.
38. Furuya, Y.E., Lowy, F.D., Antimicrobial resistant bacteria in the community setting. Nat. Rev. Microbiol. 4 (2006), 36–45.
39. Gallucci, N., Casero, C., Oliva, M., Zygadlo, J., Demo, M., Interaction between terpenes and penicillin on bacterial strains resistant to beta-lactam antibiotics. Mol. Med. Chem. 10 (2006), 30–32.
40. García Gomes, A.S., Curvelo, J.A., Soares, R.M., Ferrerira-Pereira, A., Curcumin acts synergistically with fluconazole to sensitize a clinical isolate of Candida albicans showing a MDR phenotype. Med. Mycol. 50 (2012), 26–32.
41. Gonçalves, O., Pereira, R., Gonçalves, F., Mendo, S., Coimbra, M.A., Rocha, S.M., Evaluation of the mutagenicity of sesquiterpenic compounds and their influence on the susceptibility towards antibiotics of two clinically relevant bacterial strains. Mutat. Res. 723 (2011), 18–25.
42. Gunes, H., Dogan, M., Gumus, A., Mutlu, R., Topkaya, A., Investigation of synergistic effects of curcumin with some antibiotics in extended spectrum beta lactamase positive or negative Escherichia coli and Klebsiella pneumoniae isolates. Acta Med. Medit 29 (2013), 761–765.
43. Guo, N., Ling, G., Liang, X., Jin, J., Fan, J., Qiu, J., Deng, X., In vitro synergy of pseudolaric acid B and fluconazole against clinical isolates of Candida albicans. Mycoses 54 (2010), e400–e406.
44. Guo, N., Liu, J., Wu, X., Bi, X., Meng, R., Wang, X., Xiang, H., Deng, X., Yu, L., Antifungal activity of thymol against clinical isolates of fluconazole-sensitive and –resistant Candida albicans. J. Med. Microbiol. 58 (2009), 1074–1079.
45. Guo, N., Wu, X., Jingbo, L.Y., Meng, L.R., Huijun, J.J., Wang, L., Yan, S., Deng, X., In vitro and in vivo interactions between fluconazole and allicin against clinical isolates of fluconazole-resistant Candida albicans determined by alternative methods. FEMS Immunol. Med. Microbiol. 58 (2010), 193–201.
46. Gupta, V.K., Tiwari, N., Gupta, P., Verma, S., Pal, A., Srivastava, S.K., Darokar, M.P., A clerodane diterpene from Polyalthia longifolia as a modifying agent of the resistance of methicillin-resistant Staphylococcus aureus. Phytomedicine 23 (2016), 654–661.
47. Gupta, V.K., Verma, S., Pal, A., Srivastava, S.K., Srivastava, P.K., Darokar, M.P., In vivo efficacy and synergistic interaction of 16α-hydroxycleroda-3, 13 (14) Z-dien-15, 16-olide, a clerodane diterpene from Polyalthia longifolia against methicillin-resistant Staphylococcus aureus. Appl. Microbiol. Biotechnol. 97 (2013), 9121–9131.
48. Han, Y., Synergic anticandidal effect of epigallocatechin-O-gallate combined with amphotericin B in a murine model of disseminated candidiasis and its anticandidal mechanism. Biol. Pharm. Bull. 30 (2007), 1693–1696.
49. Han, Y., Lee, J.-H., Berberine synergy with amphotericin B against disseminated candidiasis in mice. Biol. Pharm. Bull. 28 (2005), 541–544.
50. Hemaiswarya, S., Doble, M., Synergistic interaction of eugenol with antibiotics against gram negative bacteria. Phytomedicine 16 (2009), 997–1005.
51. Hemaiswarya, S., Doble, M., Synergistic interaction of phenylpropanoids with antibiotics against bacteria. J. Med. Microbiol. 59 (2010), 1469–1476.
52. Hemaiswarya, S., Kumar, A., Doble, M., Synergism between natural products and antibiotics against infectious diseases. Phytomedicine 15 (2008), 639–652.
53. Hirasawa, M., Takada, K, Multiple effects of green tea catechin on the antifungal activity of antimycotics against Candida albicans. J. Antimicrob. Chemother. 53 (2004), 225–229.
54. Hornby, J.M., Jensen, E.C., Lisec, A.D., Tasto, J.J., Jahnke, B., Shoemaker, R., Dussault, P., Nickerson, K.W., Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67 (2001), 2982–2992.
55. Hornby, J.M., Nickerson, K.W., Enhanced production of farnesol by Candida albicans treated with four azoles. Antimicrob. Agents Chemother. 48 (2004), 2305–2307.
56. Hosseinzadeh, H., Sedigheh, B., Bazzaz, F., Sadati, M., In vitro evaluation of methylxanthines and some antibiotics: interaction against Staphylococcus aureus and Pseudomonas aeruginosa. Iran. Biomed. J. 10 (2006), 163–167.
57. Hu, Z.-Q., Zhao, W.-H., Yoda, Y., Asano, N., Hara, Y., Shimamura, T., Additive, indifferent and antagonistic effects in combinations of epigallocatechin gallate with 12 non β-lactam antibiotics against methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 50 (2002), 1051–1054.
58. Hu, Z-Q, Zhao, W-H, Asano, N., Yoda, Y., Hara, Y., Shimamura, T., Epigallocatechin gallate synergistically enhances the activity of carbapenems against methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 46 (2002), 558–560.
59. Hu, Z-Q, Zhao, W-H, Hara, Y., Shimamura, T., Epigallocatechin gallate synergism with ampicillin/sulbactame against 28 clinical isolates of methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 48 (2001), 361–364.
60. Huang, S., Cao, Y.Y., Dai, B.D., Sun, X.R., Zhu, Z.Y., Cao, Y.B., Wang, Y., Gao, P., Jiang, Y.Y., In vitro synergism of fluconazole and baicalein against clinical isolates of Candida albicans resistant to fluconazole. Biol. Pharm. Bull. 31 (2008), 2234–2236.
61. Iwazaki, R.S., Endo, E.H., Ueda-Nakamura, T., Vataru Nakamura, C., Botelho Garcia, L., Prado Dias Filho, B., In vitro antifungal activity of the berberine and its synergism with fluconazole. Antonie van Leeuwenhoek 97 (2010), 201–205.
62. Jabra-Rizk, M.A., Shirtliff, M., James, C., Meiller, T., Effect of farnesol on Candida dubliniensis biofilm formation and fluconazole resistance. FEMS Yeast Res. 6 (2006), 1063–1073.
63. Jevons, M.P., Coe, A.W., Parker, M.T., Methicillin resistance in staphylococci. Lancet 1 (1963), 904–907.
64. Jin, J., Guo, N., Zhang, J., Ding, Y., Tang, X., Liang, J., Li, L., Deng, X., Yu, L., The synergy of honokiol and fluconazole against clinical isolates of azole-resistant Candida albicans. Lett Appl. Microbiol. 51 (2010), 351–357.
65. Joshi, P., Singh, S., Wani, A., Sharma, S., Jain, S.K., Singh, B., Gupta, B.D., Satti, N.K., Koul, S., Khan, I., Kumar, A., Bharate, S., Vishwakarma, R.A., Osthol and curcumin as inhibitors of human Pgp and multidrug efflux pumps of Staphylococcus aureus: reversing the resistance against frontline antibacterial drugs. Med. Chem. Commun. 5 (2014), 1540–1547.
66. Kanafani, Z., Perfect, J.R., Resistance to antifungal agents: mechanisms and clinical impact. Antimicrob. Resist. 46 (2008), 120–128.
67. Khan, A.M., Ahmad, I., Antifungal activity of essential oils and their synergy with fluconazole against drug-resistant strains of Aspergillus fumigatus and Trichophyton rubrum. Appl. Microbiol. Biotechnol. 99 (2011), 1083–1094.
68. Khodavandi, A., Alizadeh, F., Aala, F., Sewaki, Z., Chong, P, In vitro investigation of antifungal activity of allicin alone and in combination with azoles against Candida species. Mycopathologia 169 (2010), 287–295.
69. Kim, J., Campbell, B., Mahoney, N., Chan, K., Molyneux, R., May, G., Chemosensitization prevents tolerance of Aspergillus fumigatus to antimycotic drugs. Biochem. Biophys. Res. Commun. 372 (2008), 266–271.
70. Kim, J.H., Mahoney, N., Chan, K.L., Molyneux, R.J., May, G.S., Campbell, B.C., Chemosensitization of fungal pathogens to antimicrobial agents using benzo analogs. FEMS Microbiol. Lett. 281 (2008), 64–72.
71. Kohanski, M.A., Dwyer, D., Collins, J., How antibiotics kill bacteria: from targets to networks. Nat. Rev. Microbiol. 8 (2010), 423–435.
72. Kollanoor Johny, A.K., Hoagland, T., Venkitanarayanan, K., Effect of sub-inhibitory concentrations of plant-derived molecules in increasing the sensitivity of multidrug-resistant Salmonella enterica serovar Typhimurium DT104 to antibiotics. Foodborne Pathogens Dis. 7 (2010), 1165–1170.
73. Kontoyiannis, D., Marr, K., Park, B., Alexander, B., Anaissie, E., Walsh, T., Ito, J., Andes, D., Baddley, J., Brown, J., Brumble, L., Freifeld, A., Hadley, S., Herwaldt, L., Kauffman, C., Knapp, K., Marshall Lyon, G., Morrison, V., Papanicolaou, G., Patterson, T., Perl, T., Schuster, M., Walker, R., Wannemuehler, K., Wingard, J., Chiller, T., Pappas, P., Prospective surveillance for invasive fungal infections in hematopoietic stem cell transplant recipients, 2001-2006: overview of the Transplant-Associated Infection Surveillance Network (TRANSNET) database. Clin. Inf. Dis. 50 (2010), 1091–1100.
74. Kristiansen, J.E., Hendricks, O., Delvin, T., Butterworth, T.S., Aagaard, L., Christensen, J.B., Flores, V., Keyzer, H., Reversal of resistance in microorganisms by help of non-antibiotics. J. Antimicrob. Chemother. 59 (2007), 1271–1279.
75. Langeveld, W., Veldhuizen, E., Burt, S., Synergy between oil components and antibiotics: a review. Crit. Rev. Microbiol. 40 (2014), 76–94.
76. Ledezma, E., Maniscalchi, M.T., Espinoza, D.L., Sinergismo entre ajoeno y ketoconazol en aislamientos de Microsporum canis. Un estudio preliminar mediante la determinación de la concentración inhibitoria fraccional (CIF). Rev. Iberoam. Micol. 25 (2008), 157–162.
77. Lee, J., Choi, Y., Woo, E., Lee, D., Antibacterial and synergistic activity of isocryptomerin isolated from Selaginella tamariscina. J. Microbiol. Biotechnol. 19 (2009), 204–207.
78. Lehtinen, J., Lilius, E-M., Promethazine renders Escherichia coli susceptible to penicillin G: real-time measurement of bacterial susceptibility by fluoro-luminometry. Int. J. Antimicrob. Agents 30 (2007), 44–51.
79. Lewis, R., Kontoyiannis, D., Rationale for combination antifungal therapy. Suppl. Pharmacother. 21 (2001), 149S–164S.
80. Lewis, R.E, Current concepts in antifungal pharmacology. Mayo Clin. Proc. 86 (2011), 805–817.
81. Li, Y., Chang, W., Zhang, M., Li, X., Jiao, Y., Lou, H., Synergistic and drug-resistant reversing effects of diorcinol D combined with fluconazole agaist Candida albicans. FEMS Yeast Res., 15, 2015, fov001.
82. Liu, Q., Niu, H., Zhang, W., Mu, H., Sun, C., Duan, J., Synergy among thymol, eugenol, berberine, cinnamaldehyde and streptomycin against planktonic and biofilm-associated foodborne pathogens. Lett. Appl. Microbiol. 60 (2015), 421–430.
83. Lorenzi, V., Muselli, A., Bernardini, A., Berti, L., Pagés, J-M., Amaral, L., Bolla, J-M., Geraniol restores antibiotic activities against multidrug-resistant isolates from gram negative species. Antimicrob. Agents Chemother. 53 (2009), 2209–2211.
84. Ma, D., Alberti, M., Lynch, C., Nikaido, H., Hearst, J.E., The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 19 (1996), 101–112.
85. Macedo, L., Fernandes, T., Silveira, L., Mesquita, A., Franchitti, A., Ximenes, E., β-Lapachone activity in synergy with conventional antimicrobials against Methicillin Resistant-Staphylococcus aureus strains. Phytomedicine 21 (2013), 25–29.
86. Magiorakos, A., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., Harbarth, J.F., Kahlmeter, B., Olsson-Liljequist, B., Paterson, D.L., Rice, L.B., Stelling, J., Struelens, M.J., Vatopoulos, A., Weber, J., Monnet, J.T., Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18 (2012), 268–281.
87. Martínez Irujo, J.J., Villahnosu, M.L., Alberdi, E., Santiago, E., A checkerboard method to evaluate interactions between drugs. Biochem. Pharmacol. 51 (1996), 635–644.
88. Moon, S.E., Kim, H.Y., Cha, J.D., Synergistic effect between clove oil and its major compounds and antibiotics against oral bacteria. Arch. Oral Biol. 56 (2011), 907–916.
89. Moore, D., 2013. Antibiotic classification and mechanism. Orthobullets.com. accessed April, 7th, 2017.
90. Mun, S-H., Joung, D-K., Kim, Y.S., Kang, O-H., Kim, B., Seo, Y., 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 20 (2013), 714–718.
91. Mun, S-H., Kim, S-B, Kong, R., Choi, J-G., Kim, Y-C., Shin, D-W., Kang, O-H., Kwon, D-Y., Curcumin reverses methicillin resistance in Staphylococcus aureus. Molecules 19 (2014), 19283–19295.
92. Muroi, H., Nihei, K-I., Tsujimoto, K., Kubo, I., Synergistic effects of anacardic acids and methicillin against methicillin resistant Staphylococcus aureus. Bioorg. Med. Chem. 12 (2004), 583–587.
93. Musiol, R., Mrozek-Wilczkiewicz, A., Polanski, J., Synergy against fungal pathogens: working together is better than working alone. Curr. Med. Chem. 21 (2014), 870–893.
94. Nagoshi, C., Shiota, S., Kuroda, T., Hatano, T., Yoshida, T., Kariyama, R., Tsuchiya, T., Synergistic effect of [10]-gingerol and aminoglycosides against vancomycin-resistant enterococci (VRE). Biol. Pharm. Bull. 29 (2006), 443–447.
95. Natarajan, P., Katta, S., Andrei, I., Babu, V., Ambati, R., Leonida, M., Haas, G.J., Positive antibacterial co-action between hop (Humulus lupulus) constituents and selected antibiotics. Phytomedicine 15 (2008), 194–201.
96. Nikaido, H., Multidrug efflux pumps of Gram-negative bacteria. J. Bacteriol. 178 (1996), 5853–5859.
97. Ning, Y., Ling, J., Wu, C., Synergistic effects of tea catechin epigallocatechin gallate and antimycotics against oral Candida species. Arch. Oral Biol. 60 (2015), 1565–1570.
98. Novy, P., Rondevaldova, J., Kourimska, L., Kokoska, L., Synergistic interactions of epigallocatechingallate and oxytetracycline against various drug resistant Staphylococcus aureus strains in vitro. Phytomedicine 20 (2013), 432–435.
99. Paiva, J.A., Pereira, J.M., New antifungal antibiotics. Curr. Opin. Inf. Dis. 26 (2013), 168–174.
100. Palaniappan, K., Holley, R., Unse of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. Int. J. Food Microbiol. 140 (2010), 164–168.
101. Pemán, J., Cantón, E., Espinel-Ingroff, A., Antifungal drug resistance mechanisms. Expert Rev. Anti-Infect. Ther. 74 (2009), 453–460.
102. Pfaller, M., Antifungal drug resistance: mechanisms, epidemiology and consequences for treatment. Am. J. Med. 125:1A (2012), S3–S11.
103. Pfaller, M., Castanheira, M., Messer, S., Moet, G., Jones, R., Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY antimicrobial surveillance program (2008-2009). Diagn. Microbiol Infect. Dis. 68 (2010), 278–283.
104. Qian, M., Tang, S., Wu, C., Wang, Y., He, T., Chen, T., Xiao, X., Synergy between baicalein and penicillins against penicillinase-producing Staphylococcus aureus. Int. J. Med. Microbiol. 305 (2015), 501–504.
105. Quan, H., Cao, Y-Y., Xu, Z., Zhao, J-X., Gao, P-H., Qin, X-F., Jiang, Y-Y., Potent in vitro synergism of fluconazole and berberine chloride against clinical isolates of Candida albicans resistant to fluconazole. Antimicrob. Agents Chemother. 50 (2006), 1096–1099.
106. Rodloff, A., Bauer, T., Ewig, S., Kujath, P., Müller, E., Susceptible, intermediate, and resistant-the intensity of antibiotic action. Dtsch. Arztebl. Int. 105 (2008), 657–662.
107. Rodríguez, M.V., Sortino, M.A., Ivancovich, J.J., Pellegrino, J.M., Favier, L.S., Raimondi, M.P., Gattuso, M., Zacchino, S.A., Detection of synergistic combinations of Baccharis extracts with terbinafine against Trichophyton rubrum with high throughput screening synergy assay (HTSS) followed by 3D graphs. Behavior of some of their components. Phytomedicine 20 (2013), 1230–1239.
108. Saavedra, M.J., Borges, A., Dias, C., Aires, A., Bennett, R.N., Rosa, E.S., Simões, M., Antimicrobial activity of phenolics and glucosinolate hydrolysis products and their synergy with streptomycin against pathogenic bacteria. Med. Chem. 6 (2010), 174–183.
109. Sakagami, Y., Iinuma, M., Piyasena, K.G., Dharmaratne, H.R., Antibacterial activity of α-mangostin against vancomycin resistant enterococci (VRE) and synergism with antibiotics. Phytomedicine 12 (2005), 203–208.
110. Sandegren, L., Andersson, D.I., Bacterial gene amplification: implications for the evolution of antibiotic resistance. Nat. Rev. Microbiol. 7 (2009), 578–588.
111. Schelz, Z., Molnar, J., Hohmann, J., Antimicrobial and antiplasmid activities of essential oils. Fitoterapia 77 (2006), 279–285.
112. Seesom, W., Jaratrungtawee, A., Suksamrarn, S., Mekseepralard, C., Ratananukul, P., Sukhumsirichart, W., Antileptospiral activity of xanthones from Garcinia mangostana and synergy of gamma-mangostin with penicillin G. BMC Complem. Altern. Med., 13, 2013, 182.
113. Segatore, B., Bellio, P., Setacci, D., Brisdelli, F., Piovano, M., Garbarino, J.A., Nicoletti, M., Amicosante, G., Perilli, M., Celenza, G., In vitro interaction of usnic acid in combination with antimicrobial agents against methicillin-resistant Staphylococcus aureus clinical isolates determined by FICI and delta-E model methods. Phytomedicine 19 (2012), 341–347.
114. Shahverdi, A.R., Monsef-Esfahani, H.R., Tavasoli, F., Zaheri, A., Mirjani, R., Trans-cinnamaldehyde from Cinnamomum zeylanicum bark essential oil reduces the clindamycin resistance of Clostridium difficile in vitro. J. Food Sci., 72, 2007 S55–S58.
115. Sharma, M., Manoharlal, R, Puri, N., Prasad, R., Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressor TUP1 in Candida albicans. Biosci. Rep. 30 (2010), 391–404.
116. Sharma, M., Manoharlal, R., Negi, A.S., Prasad, R., Synergistic anticandidal activity of pure polyphenol curcumin in combination with azoles and polyenes generates reactive oxygen species leading to apoptosis. FEMS Yeast Res. 10 (2010), 570–578.
117. Sharma, M., Manoharlal, R., Shukla, S., Puri, N., Prasad, T., Ambudkar, S.V., Prasad, R., Curcumin modulates efflux mediated by yeast ABC multidrug transporters and is synergistic with antifungals. Antimicrob. Agents Chemother. 53 (2009), 3256–3265.
118. Shen, J., Davis, L., Wallace, J., Cai, Y., Lawson, L., Enhanced diallyltrisulfide has in vitro synergy with amphotericin B against Cryptococcus neoformans. Planta Med. 62 (1996), 415–418.
119. Shibata, H., Kondo, K., Katsuyama, R., Kawazoe, K., Sato, Y., Murakami, K., Takaishi, Y., Arakaki, N., Higuti, T., Alkyl gallates intensifiers of β-lactam susceptibilities to methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 49 (2005), 549–555.
120. Shibata, H., Nakano, T., Parvez, M.A., Furukawa, Y., Tomoishi, A., Niimi, S., Arakaki, N., Higuti, T., Triple combinations of lower and lower alkyl gallates and oxacillin improve antibiotic synergy against methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 53 (2009), 2218–2220.
121. Shimizu, M., Shiota, S., Mizushima, T., Ito, H., Hatano, T., Yoshida, T., Tsuchiya, T., Marked potentiation of activity of β-lactams against methicillin-resistant Staphylococcus aureus by corilagin. Antimicrob. Agents Chemother. 45 (2001), 3198–3201.
122. Shin, B., Park, W., Synergistic effect of oleanolic acid on aminoglycoside antibiotics against Acinetobacter baumanii. PLOS One, 10, 2015, e0137751.
123. Shin, S., Essential oil compounds from Agastache rugosa as antifungal agents against Trichophyton species. Arch. Pharm. Res. 27 (2004), 295–299.
124. Shin, S., Kim, J., In vitro inhibitory activities of essential oils from two Korean Thymus species against antibiotic-resistant pathogens. Arch. Pharmacal. Res. 28 (2005), 897–901.
125. Shin, S., Lim, S., Antifungal effects of herbal essential oils alone and in combination with ketoconazole against Trichophyton spp. J. Appl. Microbiol. 97 (2004), 1289–1296.
126. Shin, S., Pyun, M.S., Anti-Candida effects of estragole in combination with ketoconazole or amphotericin B. Phytother. Res. 18 (2004), 827–830.
127. Shukla, S., Zaher, H., Hartz, A., Bauer, B., Ware, J.A., Ambudkar, S.V., Curcumin inhibits the activity of ABCG2/BCRP1, a multidrug resistance-linked ABC drug transporter in mice. Pharm. Res. 26 (2009), 480–487.
128. Simões, M., Rocha, S., Coimbra, M.A., Vieira, M.J., Enhancement of Escherichia coli and Staphylococcus aureus antibiotic susceptibility using sesquiterpenoids. Med. Chem. 4 (2008), 616–623.
129. Singh, S., Young, K., Silver, L.L., What is an ‘‘ideal” antibiotic? Discovery challenges and path forward. Biochem. Pharmacol. 133 (2017), 63–73.
130. Soriano, F., Nuevos antibióticos frente a gram-positivos: linezolid, tigeciclina, daptomicina, dalbavancina, telavancina, ceftobiprole. Enferm. Infecc. Microbiol. Clin. 26:Suppl 2 (2008), 13–26.
131. Spampinato, C., Leonardi, D., Candida infections, causes, targets, and resistance mechanisms: traditional and alternative antifungal agents. Biomed. Res. Int., 2013 Article Id. 204237.
132. Stapleton, P., Shah, S., Anderson, J., Hara, Y., Hamilston-Miller, J., Taylor, P., Modulation of β-lactam resistance in Staphylococcus aureus by catechin and gallates. Int. J. Antimicrob. Agents 23 (2004), 462–467.
133. Strippoli, V., D'Auria, F.D., Tecca, M., Callari, A., Simonetti, G., Propyl gallate increases in vitro antifungal imidazole activity against Candida albicans. Int. J. Antimicrob. Agents 16 (2000), 73–76.
134. Sudano Roccaro, A., Blanco, A.R., Giuliano, F., Rusciano, D., Enea, V., Epigallocatechin-gallate enhances the activity of tetracycline in staphylococci by inhibiting its efflux from bacterial cells. Antimicrob. Agents Chemother. 48 (2004), 1968–1973.
135. Sun, L., Sun, S., Cheng, A., Wu, X., Zhang, Y., Lou, H., In vitro activities of retigeric acid B alone and in combination with azole antifungal agents against Candida albicans. Antimicrob. Agents Chemother. 53 (2009), 1586–1591.
136. Sun, S., Li, Y., Guo, Q., Shi, C., Yuy, J., Ma, L., In vitro interactions between tacrolimus and azoles against Candida albicans determined by different methods. Antimicrob. Agents Chemother. 52 (2008), 409–417.
137. Tran, T-D., Do, T-H., Tran, N-C., Ngo, T.-D., Huynh, T-N-P., Tran, C-D., Thai, K-M., Synthesis and anti methicillin resistant Staphylococcus aureus activity of substituted chalcones alone and in combination with non-beta-lactam antibiotics. Bioorg. Med. Chem. Lett. 22 (2012), 4555–4560.
138. Tsao, S-M., Yin, M-C., Enhanced inhibitory effect from interaction of curcumin with amphotericin B or fluconazole against Candida species. J. Food Drug Anal. 8 (2000), 208–212.
139. Veras, H., Rodrigues, F., Colares, A., Menezes, I., Coutinho, H., Botelho, M., Costa, J., Synergistic antibiotic activity of volatile compounds from the essential oil of Lippia sidoides and thymol. Fitoterapia 83 (2012), 508–512.
140. Wagner, H., Ulrich Merzenich, G., Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine 16 (2009), 97–110.
141. Walsh, C., Molecular mechanisms that confer antibacterial drug resistance. Nature, 406, 2000 775–761.
142. Wei, G-X., Xu, X., Wu, C.D., In vitro synergism between berberine and miconazole against planktonic and biofilm Candida cultures. Arch. Oral Biol. 56 (2011), 565–572.
143. Weinke, T., Schiller, R., Fehrenbach, F.J., Pohle, H.D., Association between Staphylococcus aureus nasopharyngeal colonization and septicemia in patients infected with the human immunodeficiency virus. Eur. J. Clin. Microbiol. Infect. Dis. 11 (1992), 985–989.
144. Weitzman, I., Summerbell, R.C., The dermatophytes. Clin. Microbiol. Rev. 8 (1995), 240–259.
145. Wenzel, R.P., Perl, T.M., The significance of nasal carriage of Staphylococcus aureus and the incidence of postoperative wound infection. J. Hosp. Infect. 31 (1995), 13–24.
146. White, R., Burgess, D., Manduru, M., Bosso, J., Comparison of three different in vitro methods of detecting synergy: time-kill, checkerboard, and E-test. Antimicrob. Agents Chemother. 40 (1996), 1914–1918.
147. Wozniak, A., Villagra, N.A., Undabarrena, A., Gallardo, N., Keller, N., Moraga, M., Román, J.C., Mora, G.C., García, P., Porin alterations present in non carbapenemase-producing Enterobacteriaceae with high and intermediate levels of carbapenem resistance in Chile. J. Med. Microbiol. 61 (2012), 1270–1279.
148. Yu, L.H., Wei, X., Ma, M., Chen, X.J., Xu, S.B., Possible inhibitory molecular mechanism of farnesol on the developmentof fluconazole resistance in Candida albicans biofilm. Antimicrob. Agents Chemother. 56 (2012), 770–775.
149. Zhang, D., Hu, H., Rao, Q., Zhao, Z., Synergistic effects and physiological responses of selected bacterial isolates from animal feed to four natural antibacterials and two antibiotics. Foodborne Pathogens Dis. 8 (2011), 1055–1062.
150. Zhang, H., Wang, K., Zhang, G., Ho, H.I., Gao, A., Synergistic anti-candidal activity of tetrandrine on ketoconazole: an experimental study. Planta Med. 76 (2010), 53–61.
151. Zhang, X-J., Zuo, G.-Y., Wang, T., Zhang, Y-L., Wang, G-C., Xiu-shuang, L., In vitro study on synergetic anti-MRSA effects of luteolin combined with antibacterial drugs. Progress Pharm. Sci., 4, 2012, 008.
152. Zhao, W-H., Hu, Z-Q., Okubo, S., Hara, Y., Shimamura, T., Mechanism of synergy between epigallocatechin gallate and β-lactams against methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 45 (2001), 1737–1742.
153. Zhao, W-H., Hu, Z-Q., Okubo, S., Hara, Y., Shimamura, T., Inhibition of penicillinase by epigallocatechin gallate resulting in restoration of antibacterial activity of penicillin against penicillinase-producing Staphylococcus aureus. Antimicrob. Agents Chemother. 46 (2002), 2266–2268.
154. Zuo, G., Li, Y., Wang, T., Han, J., Wang, G-C., Zhang, Y-L., Synergistic antibacterial and antibiotic effects of bisbenzylisoquinoline alkaloids on clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA). Molecules 16 (2011), 9819–9826.
155. Zuo, G.Y., Han, Z.Q., Hao, X.Y., Han, J., Li, Z.S., Wang, G.C., Synergy of aminoglycoside antibiotics by benzylchromane derivatives from the Chinese drug Caesalpinia sappan against clinical methicillin-resistant Staphylococcus aureus (MRSA). Phytomedicine 21 (2014), 936–941.
156. Zuo, G-Y., An, J., Han, J., Zhang, Y-L., Wang, G-C., Hao, X-Y., Bian, Z-Q., Isojacareubin from the Chinese herb Hypericum japonicum: potent antibacterial and synergistic effects on clinical methicillin-resistant Staphylococcus aureus (MRSA). Int. J. Mol. Sci. 13 (2012), 8210–8218.