Skip to main content
Erschienen in:

06.01.2022 | Original Article

Comparison of the antibacterial activity of Australian Terminalia spp. extracts against Klebsiella pneumoniae: a potential treatment for ankylosing spondylitis

verfasst von: Reece Courtney, Ian Edwin Cock

Erschienen in: Inflammopharmacology | Ausgabe 1/2022

Einloggen, um Zugang zu erhalten

Abstract

Traditional medicines prepared using Terminalia species have been used globally to treat inflammation and pathogenic infections. Recent studies have demonstrated that multiple Asian and African Terminalia spp. inhibit bacterial triggers of some autoimmune inflammatory diseases, including ankylosing spondylitis. Despite this, the effects of Australian Terminalia spp. on a bacterial trigger of ankylosing spondylitis (K. pneumoniae) remain unexplored. Fifty-five extracts from five Australian Terminalia spp. were investigated for K. pneumoniae growth inhibitory activity. Methanolic, aqueous and ethyl acetate extracts of most species and plant parts inhibited K. pneumoniae growth, with varying potencies. Methanolic leaf extracts were generally the most potent bacterial growth inhibitors, with minimum inhibitory concentration (MIC) values of 66 μg/mL (T. ferdinandiana), 128 μg/mL (T. carpenteriae) and 83 μg/mL (T. petiolares). However, the aqueous leaf extract was the most potent T. grandiflora extract (MIC = 87 μg/mL). All T. catappa extracts displayed low growth inhibitory activity. The Terminalia spp. methanolic leaf extracts were examined by liquid chromatography-mass spectrometry (LC–MS) and gas chromatography-mass spectrometry (GC–MS). All contained a relative abundance of simple gallotannins (particularly gallic and chebulic acids), the flavonoid luteolin, as well as the monoterpenoids cineole and terpineol. Notably, all Terminalia spp. were non-toxic or of low toxicity in ALA and HDF toxicity assays, highlighting their potential for preventing the onset of ankylosing spondylitis and treating its symptoms once the disease is established, although this needs to be verified in in vivo systems.
Literatur
Zurück zum Zitat Ashayeri-Panah M, Feizabadi MM, Eftekhar F (2014) Correlation of multi-drug resistance, integron and blaESBL gene carriage with genetic fingerprints of extended-spectrum β-lactamase producing Klebsiella pneumoniae. Jundishapur J Microbiol 7(2):e8747PubMedPubMedCentralCrossRef Ashayeri-Panah M, Feizabadi MM, Eftekhar F (2014) Correlation of multi-drug resistance, integron and blaESBL gene carriage with genetic fingerprints of extended-spectrum β-lactamase producing Klebsiella pneumoniae. Jundishapur J Microbiol 7(2):e8747PubMedPubMedCentralCrossRef
Zurück zum Zitat Brandt J, Haibel H, Cornely D, Golder W et al (2000) Successful treatment of active ankylosing spondylitis with the anti-tumor necrosis factor α monoclonal antibody infliximab. Arthritis Rheum 43(6):1346–1352CrossRef Brandt J, Haibel H, Cornely D, Golder W et al (2000) Successful treatment of active ankylosing spondylitis with the anti-tumor necrosis factor α monoclonal antibody infliximab. Arthritis Rheum 43(6):1346–1352CrossRef
Zurück zum Zitat Brem-Stecher B, Johnson EA (2003) Sensitisation of Staphylococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids nerolidol, farnesol, bisabolol, and apritone. Antimicrob Agents Chemother 47(10):3357–3360CrossRef Brem-Stecher B, Johnson EA (2003) Sensitisation of Staphylococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids nerolidol, farnesol, bisabolol, and apritone. Antimicrob Agents Chemother 47(10):3357–3360CrossRef
Zurück zum Zitat Buzzini P, Arapitsas P, Goretti M et al (2008) Antimicrobial and antiviral activity of hydrolysable tannins. Mini Rev Med Chem 8:1179–1187PubMedCrossRef Buzzini P, Arapitsas P, Goretti M et al (2008) Antimicrobial and antiviral activity of hydrolysable tannins. Mini Rev Med Chem 8:1179–1187PubMedCrossRef
Zurück zum Zitat Cheesman MJ, Ilanko A, Blonk B et al (2017) Developing new antimicrobial therapies: are synergistic combinations of plant extracts/compounds with conventional antibiotics the solution? Pharmacogn Rev 11:57–72PubMedPubMedCentralCrossRef Cheesman MJ, Ilanko A, Blonk B et al (2017) Developing new antimicrobial therapies: are synergistic combinations of plant extracts/compounds with conventional antibiotics the solution? Pharmacogn Rev 11:57–72PubMedPubMedCentralCrossRef
Zurück zum Zitat Cheesman MJ, White A, Matthews B et al (2019) Terminalia ferdinandiana fruit and leaf extracts inhibit methicillin-resistant Staphylococcus aureus growth. Planta Med 85(16):1253–1262PubMedCrossRef Cheesman MJ, White A, Matthews B et al (2019) Terminalia ferdinandiana fruit and leaf extracts inhibit methicillin-resistant Staphylococcus aureus growth. Planta Med 85(16):1253–1262PubMedCrossRef
Zurück zum Zitat Claussen MC, Korn T (2012) Immune mechanisms of new therapeutic strategies in MS—Teriflunomide. Clin Immunol 142(1):49–56PubMedCrossRef Claussen MC, Korn T (2012) Immune mechanisms of new therapeutic strategies in MS—Teriflunomide. Clin Immunol 142(1):49–56PubMedCrossRef
Zurück zum Zitat Cock IE (2015) The medicinal properties and phytochemistry of plants of the genus Terminalia (Combretaceae). Inflammopharmacology 23(5):203–229PubMedCrossRef Cock IE (2015) The medicinal properties and phytochemistry of plants of the genus Terminalia (Combretaceae). Inflammopharmacology 23(5):203–229PubMedCrossRef
Zurück zum Zitat 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. Inflammopharmacology 21(1):23–36CrossRef 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. Inflammopharmacology 21(1):23–36CrossRef
Zurück zum Zitat Cock IE, van Vuuren SF (2015) The potential of selected some South African plants with anti-Klebsiella activity for the treatment and prevention of ankylosing spondylitis. Inflammopharmacology 23(1):21–35PubMedCrossRef Cock IE, van Vuuren SF (2015) The potential of selected some South African plants with anti-Klebsiella activity for the treatment and prevention of ankylosing spondylitis. Inflammopharmacology 23(1):21–35PubMedCrossRef
Zurück zum Zitat Cock IE, Winnett V, Sirdaarta J et al (2015) The potential of selected Australian medicinal plants with anti-Proteus activity for the treatment and prevention of rheumatoid arthritis. Pharmacogn Mag 11(42):S190–S208PubMedPubMedCentralCrossRef Cock IE, Winnett V, Sirdaarta J et al (2015) The potential of selected Australian medicinal plants with anti-Proteus activity for the treatment and prevention of rheumatoid arthritis. Pharmacogn Mag 11(42):S190–S208PubMedPubMedCentralCrossRef
Zurück zum Zitat Cock IE, Cheesman MJ (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 diseases, 2nd edn. Elsevier Publishing Cock IE, Cheesman MJ (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 diseases, 2nd edn. Elsevier Publishing
Zurück zum Zitat Cock IE, Wright MH, Matthews B et al (2019) Bioactive compounds sourced from Terminalia spp. in bacterial malodour prevention: an effective alternative to chemical additives. Int J Cosmet Sci 41(5):496–508PubMedCrossRef Cock IE, Wright MH, Matthews B et al (2019) Bioactive compounds sourced from Terminalia spp. in bacterial malodour prevention: an effective alternative to chemical additives. Int J Cosmet Sci 41(5):496–508PubMedCrossRef
Zurück zum Zitat Courtney R, Sirdaarta J, Matthews B et al (2015) Tannin components and inhibitory activity of Kakadu plum leaf extracts against microbial triggers of autoimmune inflammatory diseases. Pharmacogn J 7(1):18–31CrossRef Courtney R, Sirdaarta J, Matthews B et al (2015) Tannin components and inhibitory activity of Kakadu plum leaf extracts against microbial triggers of autoimmune inflammatory diseases. Pharmacogn J 7(1):18–31CrossRef
Zurück zum Zitat Cristani M, D’Arrigo M, Mandalari G et al (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 55:6300–6308PubMedCrossRef Cristani M, D’Arrigo M, Mandalari G et al (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 55:6300–6308PubMedCrossRef
Zurück zum Zitat Di Pasqua R, Hoskins N, Betts G et al (2006) Changes in membrane fatty acid composition of microbial cells induced by addition of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J Agric Food Chem 54:2745–2749PubMedCrossRef Di Pasqua R, Hoskins N, Betts G et al (2006) Changes in membrane fatty acid composition of microbial cells induced by addition of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J Agric Food Chem 54:2745–2749PubMedCrossRef
Zurück zum Zitat Hogg S, Embery G (1982) Blood-group-reactive glycoprotein from human saliva interacts with lipoteichoic acid on the surface of Streptococcus sanguis cells. Arch Oral Biol 27:261–268PubMedCrossRef Hogg S, Embery G (1982) Blood-group-reactive glycoprotein from human saliva interacts with lipoteichoic acid on the surface of Streptococcus sanguis cells. Arch Oral Biol 27:261–268PubMedCrossRef
Zurück zum Zitat Hűbsck Z, Van Zyl RL, Cock IE et al (2014) Interactive antimicrobial and toxicity profiles of conventional antimicrobials with Southern African medicinal plants. S Afr J Bot 93:185–197CrossRef Hűbsck Z, Van Zyl RL, Cock IE et al (2014) Interactive antimicrobial and toxicity profiles of conventional antimicrobials with Southern African medicinal plants. S Afr J Bot 93:185–197CrossRef
Zurück zum Zitat Ilanko A, Cock IE (2019) The interactive antimicrobial activity of conventional antibiotics and Petalostigma spp. extracts against bacterial triggers of some autoimmune inflammatory diseases. Pharmacogn J 11(2):292–309CrossRef Ilanko A, Cock IE (2019) The interactive antimicrobial activity of conventional antibiotics and Petalostigma spp. extracts against bacterial triggers of some autoimmune inflammatory diseases. Pharmacogn J 11(2):292–309CrossRef
Zurück zum Zitat La Mantia L, Capsoni F (2010) Psoriasis during interferon beta treatment for multiple sclerosis. Neurol Sci 31(3):337–339PubMedCrossRef La Mantia L, Capsoni F (2010) Psoriasis during interferon beta treatment for multiple sclerosis. Neurol Sci 31(3):337–339PubMedCrossRef
Zurück zum Zitat Lee CJ, Wright MH, Arnold MSJ et al (2016) Inhibition of Streptococcus pyogenes growth by native Australian plants: new approaches towards the management of impetigo, pharyngitis and rheumatic heart disease. Pharmacogn Commun 6(3):164–173CrossRef Lee CJ, Wright MH, Arnold MSJ et al (2016) Inhibition of Streptococcus pyogenes growth by native Australian plants: new approaches towards the management of impetigo, pharyngitis and rheumatic heart disease. Pharmacogn Commun 6(3):164–173CrossRef
Zurück zum Zitat Mandeville A, Cock IE (2018) Terminalia chebula Retz. fruit extracts inhibit bacterial triggers of some autoimmune diseases and potentiate the activity of tetracycline. Indian J Microbiol 58:496–506PubMedPubMedCentralCrossRef Mandeville A, Cock IE (2018) Terminalia chebula Retz. fruit extracts inhibit bacterial triggers of some autoimmune diseases and potentiate the activity of tetracycline. Indian J Microbiol 58:496–506PubMedPubMedCentralCrossRef
Zurück zum Zitat Moreira DD, Teixeira SS, Monteiro MH et al (2014) Traditional use and safety of herbal medicines. Rev Bras Farmacogn 24:248–257CrossRef Moreira DD, Teixeira SS, Monteiro MH et al (2014) Traditional use and safety of herbal medicines. Rev Bras Farmacogn 24:248–257CrossRef
Zurück zum Zitat Nel AL, Murhekar S, Matthews B et al (2020) The interactive antimicrobial activity of Terminalia sericea Burch ex DC. leaf extracts and conventional antibiotics against bacterial triggers of selected autoimmune inflammatory diseases. S Afr J Bot 133:17–29CrossRef Nel AL, Murhekar S, Matthews B et al (2020) The interactive antimicrobial activity of Terminalia sericea Burch ex DC. leaf extracts and conventional antibiotics against bacterial triggers of selected autoimmune inflammatory diseases. S Afr J Bot 133:17–29CrossRef
Zurück zum Zitat Paduch R, Kandefer-Szerszen M, Trytek M et al (2007) Terpenes: substances useful in human healthcare. Arch Immunol Ther Exp 55:315–327CrossRef Paduch R, Kandefer-Szerszen M, Trytek M et al (2007) Terpenes: substances useful in human healthcare. Arch Immunol Ther Exp 55:315–327CrossRef
Zurück zum Zitat Rashid T, Ebringer A (2007) Ankylosing spondylitis is linked to Klebsiella—the evidence. Clin Rheumatol 26:858–864PubMedCrossRef Rashid T, Ebringer A (2007) Ankylosing spondylitis is linked to Klebsiella—the evidence. Clin Rheumatol 26:858–864PubMedCrossRef
Zurück zum Zitat Rayan P, Matthews B, McDonnell A et al (2015) Terminalia ferdinandiana extracts as inhibitors of Giardia duodenalis proliferation: a new treatment for giardiasis. Parasitol Res 114:2611–2620PubMedCrossRef Rayan P, Matthews B, McDonnell A et al (2015) Terminalia ferdinandiana extracts as inhibitors of Giardia duodenalis proliferation: a new treatment for giardiasis. Parasitol Res 114:2611–2620PubMedCrossRef
Zurück zum Zitat Resende FA, Nogueira LG, Bauab TM et al (2018) Antibacterial potential of flavonoids with different hydroxylation patterns. Eclet Quim 40:173–179CrossRef Resende FA, Nogueira LG, Bauab TM et al (2018) Antibacterial potential of flavonoids with different hydroxylation patterns. Eclet Quim 40:173–179CrossRef
Zurück zum Zitat Ruebhart DR, Wickramasinghe W, Cock IE (2009) Protective efficacy of the antioxidants vitamin E and Trolox against Microcystis aeruginosa and microcystin-LR in Artemia franciscana nauplii. J Toxicol Environ Health Part A 72:1567–1575CrossRef Ruebhart DR, Wickramasinghe W, Cock IE (2009) Protective efficacy of the antioxidants vitamin E and Trolox against Microcystis aeruginosa and microcystin-LR in Artemia franciscana nauplii. J Toxicol Environ Health Part A 72:1567–1575CrossRef
Zurück zum Zitat Saag KG, Koehnke R, Caldwell JR et al (1994) Low dose long-term corticosteroid therapy in rheumatoid arthritis: an analysis of serious adverse events. Am J Med 96(2):115–123PubMedCrossRef Saag KG, Koehnke R, Caldwell JR et al (1994) Low dose long-term corticosteroid therapy in rheumatoid arthritis: an analysis of serious adverse events. Am J Med 96(2):115–123PubMedCrossRef
Zurück zum Zitat Salminen A, Lehtonen M, Suuronen T et al (2008) Terpenoids: natural inhibitors of NF-κB signalling with anti-inflammatory and anticancer potential. Cell Mol Life Sci 65(19):2979–2999PubMedCrossRef Salminen A, Lehtonen M, Suuronen T et al (2008) Terpenoids: natural inhibitors of NF-κB signalling with anti-inflammatory and anticancer potential. Cell Mol Life Sci 65(19):2979–2999PubMedCrossRef
Zurück zum Zitat Sanford M (2014) Fingolimod: a review of its use in relapsing-remitting multiple sclerosis. Drugs 74(12):1411–1433PubMedCrossRef Sanford M (2014) Fingolimod: a review of its use in relapsing-remitting multiple sclerosis. Drugs 74(12):1411–1433PubMedCrossRef
Zurück zum Zitat 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 70(4):579–593PubMedCrossRef 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 70(4):579–593PubMedCrossRef
Zurück zum Zitat Sirdaarta J, Matthews B, White A et al (2015a) GC–MS and LC–MS analysis of Kakadu plum fruit extracts displaying inhibitory activity against microbial triggers of multiple sclerosis. Pharmacogn Commun 5(2):100–115CrossRef Sirdaarta J, Matthews B, White A et al (2015a) GC–MS and LC–MS analysis of Kakadu plum fruit extracts displaying inhibitory activity against microbial triggers of multiple sclerosis. Pharmacogn Commun 5(2):100–115CrossRef
Zurück zum Zitat Sirdaarta J, Matthews B, Cock IE (2015b) Inhibitory activity of Kakadu plum fruit extracts against microbial triggers of rheumatoid arthritis: Identification of stilbene and tannin components. J Funct Food 17:610–620CrossRef Sirdaarta J, Matthews B, Cock IE (2015b) Inhibitory activity of Kakadu plum fruit extracts against microbial triggers of rheumatoid arthritis: Identification of stilbene and tannin components. J Funct Food 17:610–620CrossRef
Zurück zum Zitat Wiendl H, Kieseier B (2013) Multiple sclerosis: reprogramming the immune repertoire with alemtuzumab in MS. Nat Rev Neurol 9(3):125PubMedCrossRef Wiendl H, Kieseier B (2013) Multiple sclerosis: reprogramming the immune repertoire with alemtuzumab in MS. Nat Rev Neurol 9(3):125PubMedCrossRef
Zurück zum Zitat Winnett V, Boyer H, Sirdaarta J et al (2014) The potential of Tasmannia lanceolata as a natural preservative and medicinal agent: antimicrobial activity and toxicity. Pharmacogn Commun 4(1):42–52CrossRef Winnett V, Boyer H, Sirdaarta J et al (2014) The potential of Tasmannia lanceolata as a natural preservative and medicinal agent: antimicrobial activity and toxicity. Pharmacogn Commun 4(1):42–52CrossRef
Zurück zum Zitat Wright MH, Sirdaarta J, White A et al (2016b) GC–MS headspace analysis of Terminalia ferdinandiana fruit and leaf extracts which inhibit Bacillus anthracis growth. Pharmacogn J 9:73–82CrossRef Wright MH, Sirdaarta J, White A et al (2016b) GC–MS headspace analysis of Terminalia ferdinandiana fruit and leaf extracts which inhibit Bacillus anthracis growth. Pharmacogn J 9:73–82CrossRef
Zurück zum Zitat Wright MH, Shalom J, Matthews B et al (2019) Terminalia ferdinandiana Exell: extracts inhibit Shewanella spp. growth and prevent fish spoilage. Food Microbiol 78:114–122PubMedCrossRef Wright MH, Shalom J, Matthews B et al (2019) Terminalia ferdinandiana Exell: extracts inhibit Shewanella spp. growth and prevent fish spoilage. Food Microbiol 78:114–122PubMedCrossRef
Zurück zum Zitat Wright MH, Arnold MSJ, Lee CJ et al (2016a) Qualitative phytochemical analysis and antibacterial activity evaluation of Indian Terminalia spp. against the pharyngitis causing pathogen Streptococcus pyogenes. Pharmacogn Commun 6(2):85–92CrossRef Wright MH, Arnold MSJ, Lee CJ et al (2016a) Qualitative phytochemical analysis and antibacterial activity evaluation of Indian Terminalia spp. against the pharyngitis causing pathogen Streptococcus pyogenes. Pharmacogn Commun 6(2):85–92CrossRef
Zurück zum Zitat Wu-Yuan C, Chen C, Wu R (1988) Gallotannins inhibit growth, water-insoluble glucan synthesis, and aggregation of Mutans streptococci. J Dent Res 67:51–55PubMedCrossRef Wu-Yuan C, Chen C, Wu R (1988) Gallotannins inhibit growth, water-insoluble glucan synthesis, and aggregation of Mutans streptococci. J Dent Res 67:51–55PubMedCrossRef
Zurück zum Zitat Yin Y, Wang M, Liu M et al (2020) Efficacy and safety of IL-17 inhibitors for the treatment of ankylosing spondylitis: a systematic review and meta-analysis. Arthritis Res Ther 22:1–11CrossRef Yin Y, Wang M, Liu M et al (2020) Efficacy and safety of IL-17 inhibitors for the treatment of ankylosing spondylitis: a systematic review and meta-analysis. Arthritis Res Ther 22:1–11CrossRef
Zurück zum Zitat Zenegin H, Baysal AH (2014) Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 19:17773–17798CrossRef Zenegin H, Baysal AH (2014) Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 19:17773–17798CrossRef
Metadaten
Titel
Comparison of the antibacterial activity of Australian Terminalia spp. extracts against Klebsiella pneumoniae: a potential treatment for ankylosing spondylitis
verfasst von
Reece Courtney
Ian Edwin Cock
Publikationsdatum
06.01.2022
Verlag
Springer International Publishing
Erschienen in
Inflammopharmacology / Ausgabe 1/2022
Print ISSN: 0925-4692
Elektronische ISSN: 1568-5608
DOI
https://doi.org/10.1007/s10787-021-00914-8