Arum italicum Miller tuber extracts: evaluation of synergistic activities with ciprofloxacin against some pathogens

Abstract

Antibiotic misuse or overuse leads antibiotic resistance. Antibiotic resistant bacteria infections cause significant clinical problem. Recently, antibiotic resistant bacteria numbers have increased, this situation has become a global public health treat. To achieve these problems, development of new antibacterial compounds is still popular among researchers. The focus on natural compounds/plant extracts in combination with antibiotics increase their activities and decrease the doses of antibiotics and their side effects. Despite known as poisonous, Arum italicum Miller is used as food and/or is used for the treatment such ailments as furuncle, eczema, peptic ulcer, wounds, etc. This interesting species was found as anticancer, cytotoxic, apoptotic agent against some human cancers. In the present study, the fractions of A. italicum tuber extract against human pathogens (Pseudomonas aeruginosa ATCC 27853, Bacillus cereus NRRL B-3711, Staphylococcus aureus ATCC 6538) were evaluated for their antibacterial activities by microdilution method. Each fraction was combined with ciprofloxacin and their synergistic activities were tested by checkerboard method. The MIC (minimum inhibitory concentrations) and FICI (fractional inhibitory concentration indexes) values were calculated. Totally, seven synergic interactions, ten additive interactions, and four indifferent interactions of tested fractions with ciprofloxacin were found.

Keywords

• Arum italicum Miller
• polar subfractions
• antibacterial activity
• checkerboard method
• synergy.

References

1. World Health Organization. Antibiotic resistance. Available at: https://www.who.int/news-room/fact-sheets/detail/antibiotic-resistance (Accessed on January 19, 2021).
2. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P&T. 2015;40(4):277.
3. Kuok CF, Hoi SO, Hoi CF, Chan CH, Fong IH, Ngok CK, Meng LR, Fong P. Synergistic antibacterial effects of herbal extracts and antibiotics on methicillin-resistant Staphylococcus aureus: A computational and experimental study. Exp Biol Med. 2017;242(7):731-743. https://doi.org/10.1177/1535370216689828
4. Wagner H, Ulrich-Merzenich G. Synergy research: approaching a new generation of phytopharmaceuticals. Phytomed. 2009;16(2-3):97-110. https://doi.org/10.1016/j.phymed.2008.12.018
5. Yam TS, Hamilton-Miller JM, Shah S. The effect of a component of tea (Camellia sinensis) on methicillin resistance, PBP2’ synthesis, and beta-lactamase production in Staphylococcus aureus. J Antimicrob Chemother. 1998;42:211-216. https://doi.org/10.1093/jac/42.2.211
6. Nascimento GGF, Locatelli J, Freitas, FC, Silva GL. Antibacterial activity of plant extracts and phytochemicals on antibiotic resistant bacteria. Braz J Microbiol. 2000;31:247-256. https://doi.org/10.1590/S1517-83822000000400003
7. Rafiq Z, Narasimhan S, Haridoss M, Vennila R, Vaidyanathan R. Punica granatum rind extract: Antibiotic potentiator and efflux pump inhibitor of multidrug resistant Klebsiella pneumoniae clinical isolates. Asian J Pharm Clin Res. 2017;10:1-5. https://doi.org/10.22159/ajpcr.2017.v10i3.16000
8. Bouarab-Chibane L, Forquet V, Lanteri P, et al. Antibacterial Properties of Polyphenols: Characterisation and QSAR (Quantitative Structure- Activity Relationship) Models. Front Microbiol. 2019;10:829. https://doi.org/10.3389/fmicb.2019.00829

9. Othman L, Sleiman A, Abdel-Massih RM. Antimicrobial Activity of Polyphenols and Alkaloids in Middle Eastern Plants. Front Microbiol. 2019;10:911. https://doi.org/10.3389/fmicb.2019.00911
10. Ibitoye OB, Ajiboye TO. Ferulic acid potentiates the antibacterial activity of quinolone-based antibiotics against Acinetobacter baumannii. Mic Path. 2019;126:393-398. https://doi.org/10.1016/j.micpath.2018.11.033
11. De Natale A, Pollio A. Plants species in the folk medicine of Montecorvino Rovella (inland Campania, Italy). J Ethnopharmacol. 2007;109:295-303. https://doi.org/10.1016/j.jep.2006.07.038
12. Cornara L, La Rocca A, Marsili S, Mariotti MG. Traditional uses of plants in the Eastern Riviera (Liguria, Italy). J Ethnopharmacol. 2009;125:16-30. https://doi.org/10.1016/j.jep.2009.06.021
13. Tuzlacı E, Alparslan DF. Turkish folk medicinal plants, Part V: Babaeski (Kırklareli). J Fac Pharm Ist Univ. 2007;39:11-23. Available at: https://dergipark.org.tr/tr/pub/iujfp/issue/577/5694
14. Genç GE, Özhatay N. An ethnobotanical study in Çatalca (European part of İstanbul) II. Turk J Pharm Sci. 2006;3(2):73-89.
15. Wright CA. Mediterranean Vegetables: A Cook’s ABC of Vegetables and Their Preparation in Spain, France, Italy, Greece, Turkey, the Middle East, and North Africa with More Than 200 Authentic Recipes for the Home Cook. Harvard Common Press; 2001.
16. Luczaj L, Dolina K. A hundred years of change in wild vegetable use in Southern Herzegovina. J Ethnopharmacol. 2015;166:297-304. https://doi.org/10.1016/j.jep.2015.02.033
17. Della Greca M, Molinaro A, Monaco P, Previtera L. Two new lignan glucosides from Arum italicum. Heterocycl. 1993;36(9):2081-2086. https://doi.org/10.3987/COM-93-6424
18. Della Greca M, Fiorentino A, Molinaro A, Monaco P, Previtera L. Steroidal 5,6-epoxides from Arum italicum. Nat Prod Lett. 1993;2(1):27-32. https://doi.org/10.1080/10575639308043450
19. Della Greca M, Molinaro A, Monaco P, Previtera L. Dihydrobenzofuran neolignans from Arum italicum. Heterocycl. 1994;38(5):1099-1102. https://doi.org/10.3987/COM-94-6681
20. Della Greca M, Fiorentino A, Molinaro A, Monaco P, Previtera L. Hydroperoxysterols in Arum italicum. Nat Prod Lett. 1994;5(1):7-14. https://doi.org/10.1080/10575639408043928
21. Agalar HG, Akalın Çiftci G, Goger F, Kırımer N. Activity guided fractionation of Arum italicum Miller tubers and the LC/MS-MS profiles. Rec Nat Prod. 2018; 12(1):64-75. https://doi.org/10.25135/rnp.06.17.05.089
22. Quave CL, Plano LRW, Pantuso T, Bennett BC. Effects of extracts from Italian medicinal plants on planktonic growth, biofilm formation and adherence of methicillin-resistant Staphylococcus aureus. J Ethnopharmacol. 2008;118:418-428. https://doi.org/10.1016/j.jep.2008.05.005
23. Yılmaz AD. Karaciğer ve safra rahatsızlıklarında kullanılan tıbbi bitkilerin antioksidan aktiviteleri üzerinde farmakognozik araştırmalar [master’s thesis]. İstanbul: Marmara University; 2008.
24. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Sixteenth Informational Supplement. CLSI document M100-S16. vol. 26–3; M7-A7, vol. 26–2; M2-A9, vol. 26–1. Wayne, PA: USA; 2006.
25. Demirci F, Güven K, Demirci B, Dadandı MY, Baser KHC. Antibacterial activity of two Phlomis essential oils against food pathogens. Food Cont. 2008;19(12):1159-1164. https://doi.org/10.1016/j.foodcont.2008.01.001
26. Van Vuuren SF, Suliman S, Viljoen AM. The antimicrobial activity of four commercial essential oils in combination with conventional antimicrobials. Lett Appl Microbiol. 2009;48(4):440-446. https://doi.org/10.1111/j.1472-765X.2008.02548.x
27. Stanojevic D, Comic L, Stefanovic O, Solujic-Sukdolak S. In vitro synergistic antibacterial activity of Salvia officinalis L. and some preservatives. Arch Biol Sci. 2010;62(1):175-183. https://doi.org/10.2298/ABS1001167S
28. Jain SN, Vishwanatha T, Reena V, et al. Antibiotic synergy test: checkerboard method on multidrug resistant Pseudomonas aeruginosa. Int Res J Pharm. 2011;2(12):196-198.
29. Clinical and Laboratory Standards Institute. Clinical and Laboratory Standards Institute methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approve Standard M7-A7, CLSI, 7th ed, Wayne, PA: USA; 2006.
30. Goldberg JB, Pier GB. The role of the CFTR in susceptibility to Pseudomonas aeruginosa infections in cystic fibrosis. Trend Microbiol. 2000;8(11):514-520. https://doi.org/10.1016/S0966-842X(00)01872-2
31. Wolska K, Szweda P. Genetic Features of Clinical Pseudomonas aeruginosa Strains. Polish J Microbiol. 2009;58(3):255-260.
32. Fields PI, Swanson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci. 1986;83:5189-5193. https://doi.org/10.1073/pnas.83.14.5189
33. Kotiranta A, Lounatmaa K, Haapasalo M. Epidemiology and pathogenesis of Bacillus cereus infections. Microb Infect. 2000;2(2):189-198. https://doi.org/10.1016/S1286-4579(00)00269-0
34. El Demeiry M, Ali A, Abouleila Y, et al. Quantification and targeted detection of ciprofloxacin in dosage form and human urine by direct injection nano-electrospray ionization multi-stage mass spectrometry. Microchem J. 2020;153:104534. https://doi.org/10.1016/j.microc.2019.104534
35. Martin M, Boixeda R, Munoz A, Felip A. Ciprofloxacin as a cause of acute renal failure. Enferm Infect Microbiol Clin. 2020;38(8):402-403. https://doi.org/10.1016/j.eimc.2020.01.010
36. Wang X, Zhao X, Malik M, Drlica K. Contribution of reactive oxygen species to pathways of quinolone-mediated bacterial cell death. J Antimicrob Chemother. 2010;65:520-524. https://doi.org/10.1093/jac/dkp486
37. Borges A, Ferreira C, Saavedra MJ, Simões M. Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb Drug Resist. 2013;19:256-265. https://doi.org/10.1089/mdr.2012.0244
38. Naz S, Ahmad S, Ajaz Rasool S, Asad Sayeed S, Siddiqi R. Antibacterial activity directed isolation of compounds from Onosma hispidum. Microbiol Res. 2006;161:43-48. https://doi.org/10.1016/j.micres.2005.05.001
39. Tsou MF, Hung CF, Lu HF, et al. Effects of caffeic acid, chlorogenic acid and ferulic acid on growth and arylamine N-acetyltransferase activity in Shigella sonnei (group D). Microbios. 2000;101:37-46.
40. Takahashi H, Kashimura M, Koiso H, Kuda T, Kimura B. Use of ferulic acid as a novel candidate of growth inhibiting agent against Listeria monocytogenes in ready-to-eat food. Food Cont. 2013;33(1):244-248. https://doi.org/10.1016/j.foodcont.2013.03.013
41. Ganan M, Martinez-Rodriguez AJ, Carrascosa AV. Antimicrobial activity of phenolic compounds of wine against Campylobacter jejuni. Food Cont. 2009;20:739-742. https://doi.org/10.1016/j.foodcont.2008.09.012
42. Lou Z, Wang H, Rao S, Sun J, Ma C, Li J. p-Coumaric acid kills bacteria through dual damage mechanisms. Food Cont. 2012;25(2):550-554. https://doi.org/10.1016/j.foodcont.2011.11.022
43. Bag A, Chattopadhyay RR. On the basis of fractional inhibitory concentration indices values, nisin/p‐coumaric acid combination exhibited synergistic antibiofilm activity. Lett Appl Microbiol. 2017;65(5):366-372. https://doi.org/10.1111/lam.12793
44. Giacomini D, Musumeci R, Galletti P, et al. 4-alkyliden-azetidinones modified with plant derived polyphenols: antibacterial and antioxidant properties. Eur J Med Chem. 2017;140:604-614. https://doi.org/10.1016/j.ejmech.2017.09.048
45. Edreva AM, Velikova VB, Tsonev TD. Phenylamides in Plants. Russ J Plant Physiol. 2007;54(3):287-301. https://doi.org/10.1134/S1021443707030016
46. Tiburcio AF, Altabella T, Bitrian M, Alcazar R. The roles of polyamines during the lifespan of plants: from development to stress. Planta. 2014;240:1-18. https://doi.org/10.1007/s00425-014-2055-9
47. Walters DR. Polyamines and plant disease. Phytochem. 2003;64(1):97-107. https://doi.org/10.1016/S0031-9422(03)00329-7
48. Kwon DH, Lu CD. Polyamines Increase Antibiotic Susceptibility in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2006;50(5):1623-1627. https://doi.org/10.1128/AAC.50.5.1623-1627.2006
49. Zhang H, Liu R, Lu Q. Separation and Characterization of phenolamines and flavonoids from rape bee pollen, and comparison of their antioxidant activities and protective effects against oxidative stress. Molecules. 2020;25(6):1264. https://doi.org/10.3390/molecules25061264