Abstract
Terminalia chebula Retz. is a northern Indian plant species known for its anti-inflammatory and antimicrobial properties. T. chebula fruit powder was extracted with solvents of varying polarity and screened for bacterial growth inhibition by disc diffusion assay. The minimum inhibitory concentration (MIC) was quantified by both liquid dilution and disc diffusion techniques. To screen for combinatorial effects, the T. chebula fruit extracts were combined with a range of conventional antibiotics and tested against each bacteria using a liquid dilution assay. Where synergy was detected, the optimal ratios were determined using isobologram analysis. Toxicity was examined using Artemia nauplii and HDF bioassays. T. chebula fruit methanolic, aqueous and ethyl acetate extracts displayed strong antimicrobial activity against the bacterial triggers of all autoimmune inflammatory diseases except K. pneumoniae, for which only moderate inhibition was observed. Indeed, MIC values as low as 195 μg/mL were measured for the aqueous extract against a resistant strain of P. aeruginosa. Of further note, both the aqueous and ethyl acetate extracts interacted synergistically in combination with tetracycline against K. pneumoniae (Σ FIC 0.38 and 0.25 respectively). All extracts were nontoxic in the Artemia and HDF toxicity assays, further indicating their potential for medicinal use.
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Abbreviations
- ALA:
-
Brine-shrimp lethality assay
- DMSO:
-
Dimethyl sulfoxide
- HDF:
-
Human dermal fibroblasts
- INT:
-
ρ-iodonitrotetrazolium chloride
- LD50 :
-
Dose of sample necessary to have a lethal effect on 50% of test organisms or cells
- MIC:
-
Minimum inhibitory concentration
- ΣFIC:
-
The sum of the fractional inhibitory concentration
References
Cheesman MJ, Ilanko A, Blonk B, Cock IE (2017) Developing new antimicrobial therapies: are synergistic combinations of plant extracts/compounds with conventional antibiotics the solution? Pharmacog Rev 11:57–72. https://doi.org/10.4103/phrev.phrev_21_17
WHO (2016) Antimicrobial resistance. World Health Organization. http://www.who.int/mediacentre/factsheets/fs194/en/. Last cited on 2017 May 10
Sirdaarta J, Matthews B, Cock IE (2015) Kakadu plum fruit extracts inhibit the growth of the bacterial triggers of rheumatoid arthritis: identification of stilbene and tannin components. J Funct Food 17:610–620. https://doi.org/10.1016/j.jff.2015.06.019
Ilanko A, Cock IE (2018) The interactive antimicrobial activity of contentional antibiotics and Petalostigma spp. extracts against bacterial triggers of some autoimmune inflammatory diseases. BMC Complement Alt Med (in press)
Chowdhury AN, Ashrafuzzaman M, Ali H, Liza LN, Zinnah KMA (2013) Antimicrobial activity of some medicinal plants against multi drug resistant human pathogens. Adv Biosci Bioeng 1:1–24
Cock IE (2015) The medicinal properties and phytochemistry of plants of the genus Terminalia (Combretaceae). Inflammopharmacol 23:203–229. https://doi.org/10.1007/s10787-015-0246-z
Belapurkar P, Goyal P, Tiwari-Barua P (2014) Immunomodulatory effects of Triphala and its individual constituents: a review. Indian J Pharm Sci 76:467–475
Dhiman R, Aggarwal N, Aneja KR, Kaur M (2016) In vitro antimicrobial activity of spices and medicinal herbs against selected microbes associated with juices. Int J Microbiol 2016:9. https://doi.org/10.1155/2016/9015802
Chainani S, Siddana S, Reddy C, Thippeswamy M, Maurya M, Rudraswamy S (2015) Antimicrobial activity of Triphala on Lactobacilli and Candida albicans: an in vitro study. J Orofac Sci 7:104–107. https://doi.org/10.4103/0975-8844.169757
Bag A, Bhattacharyya SK, Chattopadhyay RR (2013) The development of Terminalia chebula Retz. (Combretaceae) in clinical research. Asian Pac J Trop Med 3:244–252. https://doi.org/10.1016/S2221-1691(13)60059-3
Juang LJ, Sheu SJ, Lin TC (2004) Determination of hydrolyzable tannins in the fruit of Terminalia chebula Retz. by high-performance liquid chromatography and capillary electrophoresis. J Sep Sci 27:718–724. https://doi.org/10.1002/jssc.200401741
Courtney R, Sirdaarta J, Matthews B, Cock IE (2015) Tannin components and inhibitory activity of Kakadu plum leaf extracts against microbial triggers of autoimmune inflammatory diseases. Pharmacog J 7:18–31. https://doi.org/10.5530/pj.2015.7.2
Cock IE, Cheesman M (2018) The potential of plants of the genus Syzygium (Myrtaceae) for the prevention and treatment of arthritic and autoimmune diseases. In: Preedy VR, Watson RR (eds) Bioactive foods as dietary interventions for arthritis, osteoarthritis, and related autoimmune siseases, 2nd edn. Elsevier, Netherlands
Boyer H, Cock IE (2013) Evaluation of the potential of Macademia integriflora extracts as antibacterial food agents. Pharmacog Commun 3:53–62. https://doi.org/10.5530/pc.2013.3.10
Vesoul J, Cock IE (2012) The potential of Bunya nut as an antibacterial food agent. Pharmacog Commun 2:72–79. https://doi.org/10.5530/pc.2012.1.13
Winnett V, Boyer H, Sirdaarta J, Cock IE (2014) The potential of Tasmannia lanceolata as a natural preservative and medicinal agent: antimicrobial activity and toxicity. Pharmacog Commun 4:42–52. https://doi.org/10.5530/pc.2014.1.7
Cock IE, van Vuuren SF (2014) Anti-Proteus activity of some South African medicinal plants: their potential for the treatment and prevention of rheumatoid arthritis. Inflammopharmacol 22:23–36. https://doi.org/10.1007/s10787-013-0179-3
Eloff JN (1998) A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 64:711–713. https://doi.org/10.1055/s-2006-957563
Hubsch Z, Van Zyl RL, Cock IE, Van Vuuren SF (2014) Interactive antimicrobial and toxicity profiles of conventional antimicrobials with Southern African medicinal plants. S Afr J Bot 93:185–197. https://doi.org/10.1016/j.sajb.2014.04.005
Arkhipov A, Sirdaarta J, Rayan P, McDonnell PA, Cock IE (2014) An examination of the antibacterial, antifungal, anti-Giardial and anticancer properties of Kigelia africana fruit extracts. Pharmacog Commun 4:62–76. https://doi.org/10.5530/pc.2014.3.7
Ruebhart DR, Wickramasinghe W, Cock IE (2009) Protective efficacy of the antioxidants vitamin E and Trolox™ against Microcystis aeruginosa, microcystin-LR and menadione toxicity in Artemia franciscana nauplii. J Toxicol Environ Health A 72:1567–1575
Vesoul J, Cock IE (2011) An examination of the medicinal potential of Pittosporum phylloraeoides: toxicity, antibacterial and antifungal activities. Pharmacog Commun 1:8–17. https://doi.org/10.5530/pc.2011.2.3
Shalom J, Cock IE (2018) Terminalia ferdinandiana Exell. fruit and leaf extracts inhibit proliferation and induce apoptosis in selected human cancer cell lines. Nutr Cancer. https://doi.org/10.1080/01635581.2018.1460680
Ekambaram SP, Perumal SS, Balakrishnan A (2016) Scope of hydrolysable tannins as possible antimicrobial agents. Phytother Res 30:1035–1045. https://doi.org/10.1002/ptr.5616
Shin WS (2016) Combination antibacterial therapy against β-lactam drug resistance. ProQuest Dissertations Publishing. https://conservancy.umn.edu/handle/11299/182200. Last cited on 2018 April 24
Ba XL, Harrison EM, Lovering AL, Gleadall N, Zadoks R, Parkhill J, Peacock SJ, Holden MT, Paterson GK, Holmes MA (2015) Old drugs to treat resistant bugs: methicillin-resistant Staphylococcus aureus isolates with mecC are susceptible to a combination of penicillin and clavulanic acid. Antimicrob Agents Chemother 59:7396–7404. https://doi.org/10.1128/AAC.01469-15
Parveen RM, Khan MA, Menezes GA, Harish BN, Parija SC, Hays JP (2011) Extended-spectrum β-lactamase producing Klebsiella pneumoniae from blood cultures in Puducherry, India. Indian J Med Res 134:392–395
Sun JJ, Deng ZQ, Yan AX (2014) Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations. Biochem Biophys Res Commun 453:254–267. https://doi.org/10.1016/j.bbrc.2014.05.090
Wang W, Guo Q, Xu X, Z-k Sheng, Ye X, Wang M (2014) High-level tetracycline resistance mediated by efflux pumps Tet(A) and Tet(A)-1 with two start codons. J Med Microbiol 63:1454–1459. https://doi.org/10.1099/jmm.0.078063-0
Weinstein RA, Hooper DC (2005) Efflux pumps and nosocomial antibiotic resistance: a primer for hospital epidemiologists. Clin Infect Dis 40:1811–1817. https://doi.org/10.1086/430381
Bag A, Chattopadhyay RR (2014) Efflux-pump inhibitory activity of a gallotannin from Terminalia chebula fruit against multidrug-resistant uropathogenic Escherichia coli. Nat Prod Res 28:1280–1283. https://doi.org/10.1080/14786419.2014.895729
Chusri S, Villanueva I, Voravuthikunchai SP, Davies J (2009) Enhancing antibiotic activity: a strategy to control Acinetobacter infections. J Antimicrob Chemother 64:1203–1211. https://doi.org/10.1093/jac/dkp381
Oteo J, Campos J, Lázaro E, Cuevas O, Garcia-Cobos S, Pérez-Vázquez M, de Abajo FJ, Spanish Members of EARSS (2008) Increased amoxicillin-clavulanic acid resistance in Escherichia coli blood isolates, Spain. Emerg Infect Dis 14:1259–1262
Acknowledgements
We are most grateful to Dr Paran Rayan for supplying the plant materials used in this study. Financial support for this work was provided by the Environmental Futures Research Institute and the School of Natural Sciences, Griffith University, Australia.
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Mandeville, A., Cock, I.E. Terminalia chebula Retz. Fruit Extracts Inhibit Bacterial Triggers of Some Autoimmune Diseases and Potentiate the Activity of Tetracycline. Indian J Microbiol 58, 496–506 (2018). https://doi.org/10.1007/s12088-018-0754-9
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DOI: https://doi.org/10.1007/s12088-018-0754-9