Abstract
A wide variety of herbal remedies are used in traditional African medicine to treat rheumatoid arthritis (RA) and inflammation. Thirty-four extracts from 13 South African plant species with a history of ethnobotanical usage in the treatment of inflammation were investigated for their ability to control two microbial triggers for RA (Proteus mirabilis and Proteus vulgaris). Twenty-nine of the extracts (85.3 %) inhibited the growth of P. mirabilis and 23 of them tested (67.7 %) inhibited the growth of P. vulgaris. Methanol and water extracts of Carpobrotus edulis, Lippia javanica, Pelargonium viridflorum, Ptaeroxylon obliquum, Syzygium cordatum leaf and bark, Terminalia pruinoides, Terminalia sericea, Warburgia salutaris bark and an aqueous extract of W. salutaris leaf were effective Proteus inhibitors, with MIC values <2,000 μg/ml. The most potent extracts were examined by Reverse phase high performance liquid chromatography and UV–Vis spectroscopy for the presence of resveratrol. Only extracts from T. pruinoides and T. sericea contained resveratrol, indicating that it was not responsible for the anti-Proteus properties reported here. All extracts with Proteus inhibitory activity were also either non-toxic, or of low toxicity in the Artemia nauplii bioassay. The low toxicity of these extracts and their inhibitory bioactivity against Proteus spp. indicate their potential for blocking the onset of rheumatoid arthritis.
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Alataha D, Kapral T, Smolen JS (2003) Toxicity profiles of traditional disease modifying antirheumatic drugs for rheumatoid arthritis. ARD 62:482–486
Alvarez-Lafuente R, Fernández-Gutierrez B, de Miguel S et al (2005) Potential relationship between herpes viruses and rheumatoid arthritis: analysis and quantitative real time polymerase chain reaction. ARD 64:1357–1359
Auger I, Escola JM, Gorvel JP, Roudier J (1996) HLA-DR4 and HLA-DR10 motifs that carry susceptibility to rheumatoid arthritis bind 70-kD heat shock proteins. Nat Med 2:306–310
Blankenberg-Sprenkels SD, Fielder M, Feltkamp TW et al (1998) Antibodies to Klebsiella pneumoniae in Dutch patients with ankylosing spondylitis and acute anterior uveitis and to Proteus mirabilis in rheumatoid arthritis. J Rheumatol 25:743–747
Chou CT, Uksila J, Toivanen P (1998) Enterobacterial antibodies in Chinese patients with rheumatoid arthritis and ankylosing spondylitis. Clin Exp Rheumatol 16:161–164
Choy EHS, Panayi GS (2001) Cytokine pathways and joint inflammation in rheumatoid arthritis. New Engl J Med 344(12):907–916
Cock IE (2008) Assessment of the toxicity of selected Australian native plant extracts using the Artemia franciscana nauplii bioassay. Internet J Toxicol 5(2)
Cock IE (2009) Antibacterial activity of Eucalyptus major and Eucalyptus baileyana methanolic extracts Internet J Microbiol 6(1)
Cock IE, Kukkonen L (2011) An examination of the medicinal potential of Scaevola spinescens: toxicity, antibacterial and antiviral activities. Pharmacog Res 3(2):85–94
Cock IE, Mohanty S (2011) Evaluation of the antibacterial activity and toxicity of Terminalia ferdinandiana fruit extracts. Pharmacog J 3(20):72–79
Coker C, Poore CA, Li X, Mobley HLT (2000) Pathogenesis of Proteus mirabilis urinary tract infection. Microbes Infect 2:1497–1505
Didry N, Seidel V, Dubreuil L et al (1999) Isolation and antibacterial activity of polypropanoid derivatives from Ballota nigra. J Ethnopharmacol 67:197–202
Ebringer A, Rashid T (2006) Rheumatoid arthritis is an autoimmune disease triggered by Proteus urinary tract infection. Clin Develop Immunol 13(1):41–48
Ebringer A, Ptaszynska T, Corbett M et al (1985) Antibodies to Proteus in rheumatoid arthritis. Lancet ii:305–307
Ebringer A, Cunningham P, Ahmadi K et al (1992) Sequence similarity between HLA-DR1 and DR4 subtypes associated with rheumatoid arthritis and Proteus/Serratia membrane haemolysins. Ann Rheum Dis 51:1245–1246
Elmali N, Baysal O, Harma A et al (2007) Effects of resveratrol in inflammatory arthritis. Inflammation 30:1–6
Firestein GS (2003) Evolving concepts of rheumatoid arthritis. Nature 423:356–361
Holoshitz J, Klajman A, Drucker I et al (1986) T lymphocytes of rheumatoid arthritis patients show augmented reactivity to a fraction of Mycobacteria cross-reactive with cartilage. Lancet 2:305–309
Hutchings A, Scott AH, Lewis G, Cunningham A (1996) Zulu medicinal plants: an inventory. University of Natal Press, Pietermaritzburg
Jeyachandran R, Mahesh A (2007) Antimicrobial evaluation of Kigelia africana (Lam). Res J Microbiol 2(8):645–649
Joseph CC, Moshi MJ, Innocent E, Nkunya MHH (2007) Isolation of a stilbene glycoside and other constituents of Terminalia sericea. Afr J Tradit Complement Altern Med 4(4):383–386
Kopp P (1998) Resveratrol, a phytoestrogen found in red wine. A possible explanation for the conundrum of ‘French paradox’? Eur J Endocrinol 138:619–620
Lawrence RC, Helmick CH, Arnett FC et al (1998) Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States. Arthr Rheum 41:778–799
Liaw SJ, Lai HC, Ho SW et al (2001) Characterisation of p-nitrophenylglycerol-resistant Proteus mirabilis super-swarming mutants. J Med Microbiol 50(12):1039–1048
Masoko P, Eloff JN (2005) The diversity of antifungal compounds of six South African Terminalia species (Combretaceae) determnined by bioautography. African J Biotechnol 4:1425–1431
Meyer BN, Ferrigni NR, Putnam JE et al (1982) Brine shrimp: a convenient general bioassay for active plant constituents. Plant Med 45:31–34
Moshi MJ, Mbwambo ZH (2005) Some pharmacological properties of extracts of Terminalia sericea roots. J Ethnopharmacol 97(1):43–47
Nepom GT, Byers P, Seyfried C et al (1989) HLA genes associated with rheumatoid arthritis. Arthr Rheum 32(1):15–21
Orwa C, Mutua A, Kindt R, Jamnadass R, Simons A (2009) Agroforestree Database: a tree reference and selection guide version 4.0. http://www.worldagroforestry.org/af/treedb/
Paulo L, Ferreira S, Gallardo E et al (2010) Antimicrobial activity and effects of resveratrol on human pathogenic bacteria. World J Microbiol Biotechnol 26:1533–1538
Polunin KE, Schmalz HG, Polunina IA (2002) Organometallic chemistry. Chromium arene complexes in synthesis of trans-resveratrol. Russ Chem B+ (International Edition) 51(7):1319–1324
Pujol J (1990) Naturafrica—the herbalists handbook. Jean Pujol Natural healers foundation, Durban
Rashid T, Darlington G, Kjeldsen-Kragh J et al (1999) Proteus IgG antibodies and C-reactive protein in English, Norwegian and Spanish patients with rheumatoid arthritis. Clin Rheumatol 18:190–195
Sandasi M (2008) The effect of plant extracts on biofilm formation and development. M Tech Dissertation; Tshwane University of Technology, Tshwane
Senior BW, McBride PD, Morley KD, Kerr MA (1995) The detection of raised levels of IgM to Proteus mirabilis in sera from patients with rheumatoid arthritis. J Med Microbiol 43:176–184
Senior BW, Anderson GA, Morley KD, Kerr MA (1999) Evidence that patients with rheumatoid arthritis have asymptomatic ‘non-significant’ Proteus mirabilis bacteriuria more frequently than healthy controls. J Infect 38:99–106
Sibandze GF, van Zyl RL, van Vuuren SF (2010) The anti-diarrhoeal properties of Breonadia salicina, Syzygium cordatum and Ozoroa sphaerocarpa when used in combination in Swazi traditional medicine. J Ethnopharmacol 132(2):506–511
Sirdaarta J, Cock IE (2008) Vitamin E and Trolox™ reduce toxicity of Aloe barbadensis Miller juice in Artemia franciscana nauplii but individually are toxic at high concentrations. Internet J Toxicol 5(1)
Sirdaarta J, Cock IE (2010) Effect of Aloe barbadensis Miller juice on oxidative stress biomarkers in aerobic cells using Artemia franciscana as a model. Phytother Res 24:360–364
Steenkamp V, Fernandes AC, van Rensburg CEJ (2007) Antibacterial activity of Venda medicinal plants. Fitoterapia 78:561–564
Subair H, Tiwana H, Fielder M et al (1995) Elevation in anti-Proteus antibodies in patients with rheumatoid arthritis from Bermuda and England. J Rheumatol 22:1825–1828
Van Wyk BE, van Oudtshoorn B, Gericke N (2009) Medicinal plants of South Africa, 2nd edn. Briza Publications, Pretoria
Vermaak I, Viljoen AM, Hamman JH, van Vuuren SF (2009) The effect of simulated gastrointestinal conditions on the microbial activity and chemical composition of indigenous South African plant extracts. S Afr J Bot 75:594–599
Vesoul J, Cock IE (2011) An examination of the medicinal potential of Pittosporum phylliraeoides: toxicity, antibacterial and antifungal activities. Pharmacogn Commun 1(2):8–17
Wanchu A, Deodhar SD, Sharma M et al (1997) Elevated levels of anti-Proteus antibodies in patients with active rheumatoid arthritis. Indian J Med Res 105:39–42
Wang WB, Lai HC, Hsueh PR et al (2006) Inhibition of swarming and virulence factor expression in Proteus mirabilis by resveratrol. J Med Microbiol 55:1313–1321
Wang M, Guo Q, Xu X et al (2009) New plasmid-mediated quinolone resistance gene qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Ch 53(5):1892–1897
Watt JM, Breyer-Brandwijk MG (1962) The medicinal and poisonous plants of southern and eastern Africa, 2nd edn. Livingstone Publishers, London, UK
Whitehouse M, Butters D, Vernon Roberts D (2013) Conditional pharmacology/toxicology V. Inflammopharmacology 21. doi:10.1007/s10787-013-0173-9
Wilson C, Ebringer A, Ahmadi K et al (1995) Shared amino acid sequences between major histocompatibility complex class II glycoproteins, type XI collagen and Proteus mirabilis in rheumatoid arthritis. Ann Rheum Dis 54:216–220
Acknowledgments
The authors are most grateful to Andrew Hankey, chief botanist at the Walter Sisulu Botanical Gardens in Johannesburg, South Africa for providing and identifying the plant materials used in these studies. We also thank Professor Charles de Koning and Myron Johnson of the Dept Chemistry, Witwatersrand University for access to their HPLC and for assistance with its operation. Financial support was provided by the Department of Pharmacy and Pharmacology, University of the Witwatersrand, South Africa.
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Cock, I.E., van Vuuren, S.F. Anti-Proteus activity of some South African medicinal plants: their potential for the prevention of rheumatoid arthritis. Inflammopharmacol 22, 23–36 (2014). https://doi.org/10.1007/s10787-013-0179-3
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DOI: https://doi.org/10.1007/s10787-013-0179-3