Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2017

Open Access 01-12-2017 | Research article

Inhibitory activities of selected Sudanese medicinal plants on Porphyromonas gingivalis and matrix metalloproteinase-9 and isolation of bioactive compounds from Combretum hartmannianum (Schweinf) bark

Authors: Ebtihal Abdalla M. Mohieldin, Ali Mahmoud Muddathir, Tohru Mitsunaga

Published in: BMC Complementary Medicine and Therapies | Issue 1/2017

Login to get access

Abstract

Background

Periodontal diseases are one of the major health problems and among the most important preventable global infectious diseases. Porphyromonas gingivalis is an anaerobic Gram-negative bacterium which has been strongly implicated in the etiology of periodontitis. Additionally, matrix metalloproteinases-9 (MMP-9) is an important factor contributing to periodontal tissue destruction by a variety of mechanisms. The purpose of this study was to evaluate the selected Sudanese medicinal plants against P. gingivalis bacteria and their inhibitory activities on MMP-9.

Methods

Sixty two methanolic and 50% ethanolic extracts from 24 plants species were tested for antibacterial activity against P. gingivalis using microplate dilution assay method to determine the minimum inhibitory concentration (MIC). The inhibitory activity of seven methanol extracts selected from the 62 extracts against MMP-9 was determined by Colorimetric Drug Discovery Kit. In search of bioactive lead compounds, Combretum hartmannianum bark which was found to be within the most active plant extracts was subjected to various chromatographic (medium pressure liquid chromatography, column chromatography on a Sephadex LH-20, preparative high performance liquid chromatography) and spectroscopic methods (liquid chromatography-mass spectrometry, Nuclear Magnetic Resonance (NMR)) to isolate and characterize flavogalonic acid dilactone and terchebulin as bioactive compounds.

Results

About 80% of the crude extracts provided a MIC value ≤4 mg/ml against bacteria. The extracts which revealed the highest potency were: methanolic extracts of Terminalia laxiflora (wood; MIC = 0.25 mg/ml) followed by Acacia totrtilis (bark), Ambrosia maritima (aerial part), Argemone mexicana (seed), C. hartmannianum (bark), Terminalia brownii (wood) and 50% ethanolic extract of T. brownii (bark) with MIC values of 0.5 mg/ml. T. laxiflora (wood) and C. hartmannianum (bark) which belong to combretaceae family showed an inhibitory activity over 50% at the concentration of 10 μg/ml against MMP-9. Additionally, MMP-9 was significantly inhibited by terchebulin with IC50 value of 6.7 μM.

Conclusions

To the best of our knowledge, flavogalonic acid dilactone and terchebulin were isolated from C. hartmannianium bark for the first time in this study. Because of terchebulin and some crude extracts acting on P. gingivalis bacteria and MMP-9 enzyme that would make them promising natural preference for preventing and treating periodontal diseases.
Appendix
Available only for authorised users
Literature
1.
go back to reference Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent Jr RL. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134–44.CrossRefPubMed Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent Jr RL. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134–44.CrossRefPubMed
2.
go back to reference Slots J, Bragd L, Wikstro MM, Dahlen G. The occurrence of actinobacillus actinomycetemcomitans, bacteroides gingivalis bacteroides intermedius in destructive periodontal disease in adults. J Clin periodontal. 1986;13:570–7.CrossRef Slots J, Bragd L, Wikstro MM, Dahlen G. The occurrence of actinobacillus actinomycetemcomitans, bacteroides gingivalis bacteroides intermedius in destructive periodontal disease in adults. J Clin periodontal. 1986;13:570–7.CrossRef
3.
go back to reference Holt SC, Felton J, Brunsvold M, Kornman KS. Implantation of bacteroide gingivalis in non-human primate initiates progression of periodontitis. Science (WashDC). 1988;1239:55–7.CrossRef Holt SC, Felton J, Brunsvold M, Kornman KS. Implantation of bacteroide gingivalis in non-human primate initiates progression of periodontitis. Science (WashDC). 1988;1239:55–7.CrossRef
4.
go back to reference Schwartz Z, Goultschin J, Dean DD, Boyan BD. Mechanisms of alveolar bone destruction in periodontitis. Periodontol. 1997;14:158–72.CrossRef Schwartz Z, Goultschin J, Dean DD, Boyan BD. Mechanisms of alveolar bone destruction in periodontitis. Periodontol. 1997;14:158–72.CrossRef
5.
go back to reference Chang YC, Lai CC, Yang SF, Chan Y, Hsieh YS. Stimulation of matrix metalloproteinases by black-pigmented bacteroides in human pulp and periodontal ligament cell cultures. J Endodon. 2002;28:90–3.CrossRef Chang YC, Lai CC, Yang SF, Chan Y, Hsieh YS. Stimulation of matrix metalloproteinases by black-pigmented bacteroides in human pulp and periodontal ligament cell cultures. J Endodon. 2002;28:90–3.CrossRef
6.
go back to reference Chang YC, Chu SC, Yang SF, Hsieh YS, Yang LC, Huang FM. Examination of the signal transduction pathways leading to activation of gelatinolytic activity by interleukin-1 and Porphyromonas gingivalis in human osteosarcoma cells. J Periodontal Res. 2004;39:168–74.CrossRefPubMed Chang YC, Chu SC, Yang SF, Hsieh YS, Yang LC, Huang FM. Examination of the signal transduction pathways leading to activation of gelatinolytic activity by interleukin-1 and Porphyromonas gingivalis in human osteosarcoma cells. J Periodontal Res. 2004;39:168–74.CrossRefPubMed
7.
go back to reference Chang YC, Yang SF, Lai CC, Liu JY, Hsieh YS. Regulation of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal pathogens in human periodontal ligament fibroblast cultures. J Periodontal Res. 2002;37:196–203.CrossRefPubMed Chang YC, Yang SF, Lai CC, Liu JY, Hsieh YS. Regulation of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal pathogens in human periodontal ligament fibroblast cultures. J Periodontal Res. 2002;37:196–203.CrossRefPubMed
8.
go back to reference Varghese J, Tumkur VK, Ballal V, Bhat GS. Antimicrobial effect of Anacardium occidentale leaf extract against pathogens causing periodontal disease. Adv Biosci Biotechnol. 2013;4:15–8.CrossRef Varghese J, Tumkur VK, Ballal V, Bhat GS. Antimicrobial effect of Anacardium occidentale leaf extract against pathogens causing periodontal disease. Adv Biosci Biotechnol. 2013;4:15–8.CrossRef
9.
go back to reference Ohara A, Saito F, Matsuhisa T. Screening of antibacterial activities of edible plants against Streptococcus mutans. Food Sci Technol Res. 2008;14:190–3.CrossRef Ohara A, Saito F, Matsuhisa T. Screening of antibacterial activities of edible plants against Streptococcus mutans. Food Sci Technol Res. 2008;14:190–3.CrossRef
10.
go back to reference Palombo EA. Traditional plant extracts and natural products with activity against oral bacteria: potential application in the prevention and treatment of oral diseases. Evid Based Complement Alternat Med. 2011;201:1–15.CrossRef Palombo EA. Traditional plant extracts and natural products with activity against oral bacteria: potential application in the prevention and treatment of oral diseases. Evid Based Complement Alternat Med. 2011;201:1–15.CrossRef
11.
go back to reference Patra JK, Kim ES, Oh K, Kim HJ, Kim Y, Baek KH. Antibacterial effect of crude extract and metabolites of Phytolacca americana on pathogens responsible for periodontal inflammatory diseases and dental caries. BMC Complement Altern Med. 2014;14:343.CrossRefPubMedPubMedCentral Patra JK, Kim ES, Oh K, Kim HJ, Kim Y, Baek KH. Antibacterial effect of crude extract and metabolites of Phytolacca americana on pathogens responsible for periodontal inflammatory diseases and dental caries. BMC Complement Altern Med. 2014;14:343.CrossRefPubMedPubMedCentral
12.
go back to reference Maydell HJV. Trees and Shrubs of the Sahel. Their Characteristics and Uses, (GTZ) GmbH, Germany, 1990. Maydell HJV. Trees and Shrubs of the Sahel. Their Characteristics and Uses, (GTZ) GmbH, Germany, 1990.
13.
go back to reference Elegami AA, El-Nima EI, El Tohami MS, Muddathir AK. Antimicrobial activity of some species of the family Combretaceae. Phytother Res. 2002;16:555–61.CrossRefPubMed Elegami AA, El-Nima EI, El Tohami MS, Muddathir AK. Antimicrobial activity of some species of the family Combretaceae. Phytother Res. 2002;16:555–61.CrossRefPubMed
14.
go back to reference Eldeen MS, Van Staden J. Anti-inflammatory and mycobacterial activity of leaf extracts of Coleonema album. South Afr J Bot. 2008;74:345–7.CrossRef Eldeen MS, Van Staden J. Anti-inflammatory and mycobacterial activity of leaf extracts of Coleonema album. South Afr J Bot. 2008;74:345–7.CrossRef
15.
go back to reference Muddathir AM, Mitsunaga T, Kosei Y. Anti-acne activity of tannin-related compounds isolated from Terminalia laxiflora. J Wood Sci. 2013;5:426–31.CrossRef Muddathir AM, Mitsunaga T, Kosei Y. Anti-acne activity of tannin-related compounds isolated from Terminalia laxiflora. J Wood Sci. 2013;5:426–31.CrossRef
16.
go back to reference Hirano Y, Kondo R, Sakai K. 5α-Reductase inhibitory tannin-related compound isolated from Shorea laevifolia. J Wood Sci. 2003;49:339–42.CrossRef Hirano Y, Kondo R, Sakai K. 5α-Reductase inhibitory tannin-related compound isolated from Shorea laevifolia. J Wood Sci. 2003;49:339–42.CrossRef
17.
go back to reference Lin TC, Nonaka GI, Nishioka I, Ho FC. Tannins and related compounds, CII. Structures of terchebulin, an ellagitannin having a novel tetraphenyl carboxylic acid (terchebulic acid) moiety, and biogenetically related tannins from Terminalia chebula Retz. L. Chem Pharm Bull. 1990;38:3004–8.CrossRef Lin TC, Nonaka GI, Nishioka I, Ho FC. Tannins and related compounds, CII. Structures of terchebulin, an ellagitannin having a novel tetraphenyl carboxylic acid (terchebulic acid) moiety, and biogenetically related tannins from Terminalia chebula Retz. L. Chem Pharm Bull. 1990;38:3004–8.CrossRef
18.
go back to reference Iwaki K, Koya-Miyata S, Kohno K, Ushio S, Fukuda S. Antimicrobial activity of Polygonum tinctorium lour: extract against oral pathogenic bacteria. J Nat Med. 2006;60:121–5.CrossRef Iwaki K, Koya-Miyata S, Kohno K, Ushio S, Fukuda S. Antimicrobial activity of Polygonum tinctorium lour: extract against oral pathogenic bacteria. J Nat Med. 2006;60:121–5.CrossRef
19.
go back to reference Eloff JN. Antibacterial activity of Marula (Sclerocarya birrea (a. Rich) Hochst. Subsp. Caffra (Sond) Kokwaro) (Anacardiaceae) bark and leaves. J Ethnopharmacol. 2001;76:305–8.CrossRefPubMed Eloff JN. Antibacterial activity of Marula (Sclerocarya birrea (a. Rich) Hochst. Subsp. Caffra (Sond) Kokwaro) (Anacardiaceae) bark and leaves. J Ethnopharmacol. 2001;76:305–8.CrossRefPubMed
20.
go back to reference Choi JS1, Ha YM, Joo CU, Cho KK, Kim SJ, Choi IS. Inhibition of oral pathogens and collagenase activity by seaweed extracts. J Environ Biol. 2012;33:115–21.PubMed Choi JS1, Ha YM, Joo CU, Cho KK, Kim SJ, Choi IS. Inhibition of oral pathogens and collagenase activity by seaweed extracts. J Environ Biol. 2012;33:115–21.PubMed
22.
go back to reference Gulati V, Harding IH, Palombo EA. Enzyme inhibitory and antioxidant activities of traditional medicinal plants: potential application in the management of hyperglycemia. BMC Complement Altern Med. 2012;12:77.CrossRefPubMedPubMedCentral Gulati V, Harding IH, Palombo EA. Enzyme inhibitory and antioxidant activities of traditional medicinal plants: potential application in the management of hyperglycemia. BMC Complement Altern Med. 2012;12:77.CrossRefPubMedPubMedCentral
23.
go back to reference Muddathir AM, Mitsunaga T. Evaluation of anti-acne activity of selected Sudanese medicinal plants. J Wood Sci. 2013;59:73–9.CrossRef Muddathir AM, Mitsunaga T. Evaluation of anti-acne activity of selected Sudanese medicinal plants. J Wood Sci. 2013;59:73–9.CrossRef
24.
go back to reference Eloff JN, Katerel DR, McGaw LJ. The biological activity and chemistry of the southern African Combretaceae. J Ethnopharmacol. 2008;119:686–99.CrossRefPubMed Eloff JN, Katerel DR, McGaw LJ. The biological activity and chemistry of the southern African Combretaceae. J Ethnopharmacol. 2008;119:686–99.CrossRefPubMed
25.
go back to reference Martini ND, Katerere DRP, Eloff JN. Biological activity of seven antibacterial flavonoids isolated from Combretum erythrophyllum (Combretaceae). J Ethnopharmacol. 2004;93:207–12.CrossRefPubMed Martini ND, Katerere DRP, Eloff JN. Biological activity of seven antibacterial flavonoids isolated from Combretum erythrophyllum (Combretaceae). J Ethnopharmacol. 2004;93:207–12.CrossRefPubMed
26.
go back to reference Basile A, Giordano S, Lopez-Saez JA, Cobianchi RC. Antibacterial activity of pure flavonoids isolated from mosses. Phytochemistry. 1999;52:1479–82.CrossRefPubMed Basile A, Giordano S, Lopez-Saez JA, Cobianchi RC. Antibacterial activity of pure flavonoids isolated from mosses. Phytochemistry. 1999;52:1479–82.CrossRefPubMed
27.
go back to reference Eldeen IMS, Van SJ. In vitro pharmacological investigation of extracts from some trees used in Sudanese traditional medicine. South Afr J Bot. 2007;73:435–40.CrossRef Eldeen IMS, Van SJ. In vitro pharmacological investigation of extracts from some trees used in Sudanese traditional medicine. South Afr J Bot. 2007;73:435–40.CrossRef
28.
go back to reference Zanatta FB, Antoniazzi RP, Rösing CK. Staining and calculus formation after 0.12% chlorhexidine rinses in plaque-free and plaque covered surfaces: a randomized trial. J Appl Oral Sci. 2010;18:515–21.CrossRefPubMedPubMedCentral Zanatta FB, Antoniazzi RP, Rösing CK. Staining and calculus formation after 0.12% chlorhexidine rinses in plaque-free and plaque covered surfaces: a randomized trial. J Appl Oral Sci. 2010;18:515–21.CrossRefPubMedPubMedCentral
29.
go back to reference Amanlou M, Beitollahi JM, Abdollahzadeh S, Tohidast-Ekrad Z. Miconazole gel compared with Zataria multiflora Boiss. Gel in the treatment of denture stomatitis. Phytother Res. 2006;20:966–9.CrossRefPubMed Amanlou M, Beitollahi JM, Abdollahzadeh S, Tohidast-Ekrad Z. Miconazole gel compared with Zataria multiflora Boiss. Gel in the treatment of denture stomatitis. Phytother Res. 2006;20:966–9.CrossRefPubMed
30.
go back to reference Kitano S, Irimura K, Sasaki T, Abe N, Baba A, Miyake Y, Katunuma N, Yamamoto K. Suppression of gingival inflammation induced by Porphyromonas gingivalis in rats by leupeptin. Jpn J Pharmacol. 2001;85:84–91.CrossRefPubMed Kitano S, Irimura K, Sasaki T, Abe N, Baba A, Miyake Y, Katunuma N, Yamamoto K. Suppression of gingival inflammation induced by Porphyromonas gingivalis in rats by leupeptin. Jpn J Pharmacol. 2001;85:84–91.CrossRefPubMed
31.
go back to reference Preshaw PM, Hefti AF, Jepsen S, Etienne D, Walker C, Bradshaw MH. Subantimicrobial dose doxycycline as adjunctive treatment for periodontitis. A review. J Clin Periodontol. 2004;31:697–707.CrossRefPubMed Preshaw PM, Hefti AF, Jepsen S, Etienne D, Walker C, Bradshaw MH. Subantimicrobial dose doxycycline as adjunctive treatment for periodontitis. A review. J Clin Periodontol. 2004;31:697–707.CrossRefPubMed
32.
go back to reference Kusumoto T, Nakabayashi T, Kida H, Miyashiro H, Hattori M, Namba T. Screening of various plant extracts used in Ayurvedic medicine for inhibitory effects on human immunodeficiency virus type 1 (HIV-1) protease. Phytother Res. 1995;9:180–4.CrossRef Kusumoto T, Nakabayashi T, Kida H, Miyashiro H, Hattori M, Namba T. Screening of various plant extracts used in Ayurvedic medicine for inhibitory effects on human immunodeficiency virus type 1 (HIV-1) protease. Phytother Res. 1995;9:180–4.CrossRef
33.
go back to reference Dell'Agli M, Galli GV, Bulgari M, Basilico N, Romeo S, Bhattacharya D, Taramelli D, Bosisio E. Ellagitannins of the fruit rind of pomegranate (Punica granatum) antagonize in vitro the host inflammatory response mechanisms involved in the onset of malaria. Malar J. 2010;9:208.CrossRefPubMedPubMedCentral Dell'Agli M, Galli GV, Bulgari M, Basilico N, Romeo S, Bhattacharya D, Taramelli D, Bosisio E. Ellagitannins of the fruit rind of pomegranate (Punica granatum) antagonize in vitro the host inflammatory response mechanisms involved in the onset of malaria. Malar J. 2010;9:208.CrossRefPubMedPubMedCentral
34.
go back to reference Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol. 2004;48:411–24.CrossRefPubMed Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol. 2004;48:411–24.CrossRefPubMed
35.
go back to reference Seigler DS. Phytochemistry of Acacia-sensu lato. Biochem Syst Ecology. 2003;31:845–73.CrossRef Seigler DS. Phytochemistry of Acacia-sensu lato. Biochem Syst Ecology. 2003;31:845–73.CrossRef
36.
go back to reference Kosei Y, Mitsunaga T, Ali MM. Screening for melanogenesis-controlled agents using Sudanese medicinal plants and identification of active compounds in the methanol extract of Terminalia brownii bark. J Wood Sci. 2016;62:285–93.CrossRef Kosei Y, Mitsunaga T, Ali MM. Screening for melanogenesis-controlled agents using Sudanese medicinal plants and identification of active compounds in the methanol extract of Terminalia brownii bark. J Wood Sci. 2016;62:285–93.CrossRef
37.
go back to reference El Ghazali GEB, El Tohamy MS, El Egami AB. Medicinal plants of the Sudan. Part III. Sudan: Medicinal Plants of the White Nile Province Khartoum University Press; 1994. El Ghazali GEB, El Tohamy MS, El Egami AB. Medicinal plants of the Sudan. Part III. Sudan: Medicinal Plants of the White Nile Province Khartoum University Press; 1994.
38.
go back to reference Al Magboul AZ, Bashir AK, Salih AM, Farouk A, Khalid SA. Antimicrobial activity of certain Sudanese plants used in folkloric medicine: screening for antibacterial activity (V). Fitoterapia. 1988;59:57–62. Al Magboul AZ, Bashir AK, Salih AM, Farouk A, Khalid SA. Antimicrobial activity of certain Sudanese plants used in folkloric medicine: screening for antibacterial activity (V). Fitoterapia. 1988;59:57–62.
39.
go back to reference Ali H, König GM, Khalid SA, Wright AD, Kaminsky R. Evaluation of selected Sudanese medicinal plants for their in vitro activity against hemoflagellates, selected bacteria, HIV-1-RT and tyrosine kinase inhibitory, and for cytotoxicity. J Ethnopharmacol. 2002;83:219–28.CrossRefPubMed Ali H, König GM, Khalid SA, Wright AD, Kaminsky R. Evaluation of selected Sudanese medicinal plants for their in vitro activity against hemoflagellates, selected bacteria, HIV-1-RT and tyrosine kinase inhibitory, and for cytotoxicity. J Ethnopharmacol. 2002;83:219–28.CrossRefPubMed
40.
go back to reference Marquis A, Genovese S, Epifano F, Grenier D. The plant coumarins auraptene and lacinartin as potential multifunctional therapeutic agents for treating periodontal disease. BMC Complement Altern Med. 2012;2:80. Marquis A, Genovese S, Epifano F, Grenier D. The plant coumarins auraptene and lacinartin as potential multifunctional therapeutic agents for treating periodontal disease. BMC Complement Altern Med. 2012;2:80.
41.
go back to reference Silva O, Viegas S, de Mello-Sampayo C, Costa MJ, Serrano R, Cabrita J, Gomes ET. Anti-Helicobacter pylori activity of Terminalia macroptera root. Fitoterapia. 2012;83:872–6.CrossRefPubMed Silva O, Viegas S, de Mello-Sampayo C, Costa MJ, Serrano R, Cabrita J, Gomes ET. Anti-Helicobacter pylori activity of Terminalia macroptera root. Fitoterapia. 2012;83:872–6.CrossRefPubMed
42.
go back to reference Ohtsuki T, Yokosawa E, Koyano T, Preeprame S, Kowithayakorn T, Sakai S, Toida T, Ishibashi M. Quinic acid esters from Pluchea indica with collagenase, MMP-2 and MMP-9 inhibitory activities. Phytother Res. 2008;22:264–6.CrossRefPubMed Ohtsuki T, Yokosawa E, Koyano T, Preeprame S, Kowithayakorn T, Sakai S, Toida T, Ishibashi M. Quinic acid esters from Pluchea indica with collagenase, MMP-2 and MMP-9 inhibitory activities. Phytother Res. 2008;22:264–6.CrossRefPubMed
43.
go back to reference Arabaci T, Türkez H, Çanakçi CF, Özgöz M. Assessment of cytogenetic and cytotoxic effects of chlorhexidine digluconate on cultured human lymphocytes. Acta Odontol Scand. 2013;71:1255–60.CrossRefPubMed Arabaci T, Türkez H, Çanakçi CF, Özgöz M. Assessment of cytogenetic and cytotoxic effects of chlorhexidine digluconate on cultured human lymphocytes. Acta Odontol Scand. 2013;71:1255–60.CrossRefPubMed
44.
go back to reference Shuaibu MN, Wuyep PA, Yanagi T, Hirayama K, Tanaka T, Kouno I. The use of microfluorometric method for activity-guided isolation of antiplasmodial compound from plant extracts. Parasitol Res. 2008;102:1119–27.CrossRefPubMed Shuaibu MN, Wuyep PA, Yanagi T, Hirayama K, Tanaka T, Kouno I. The use of microfluorometric method for activity-guided isolation of antiplasmodial compound from plant extracts. Parasitol Res. 2008;102:1119–27.CrossRefPubMed
45.
go back to reference Mossa JS, Tarig M, Mohsin A, Rafatulla S. Pharmacological studies on aerial parts of Calotropis procera. Am J Chin Med. 1991;19:223–31.CrossRefPubMed Mossa JS, Tarig M, Mohsin A, Rafatulla S. Pharmacological studies on aerial parts of Calotropis procera. Am J Chin Med. 1991;19:223–31.CrossRefPubMed
46.
go back to reference El Ghazali GEB, Bari EA, Bashir AK, Salih AM. Medicinal plants of Sudan part II. Medicinal plants of eastern Nuba Mountains. Khartoum: National Council for Research; 1987. El Ghazali GEB, Bari EA, Bashir AK, Salih AM. Medicinal plants of Sudan part II. Medicinal plants of eastern Nuba Mountains. Khartoum: National Council for Research; 1987.
47.
go back to reference El Ghazali GEB, El Tohami MS, El Egami AA, Abdalla WE, Galal M. Medicinal plants of the Sudan part IV. Medicinal plants of north Kordofan. Khartoum: National Council for Research; 1997. El Ghazali GEB, El Tohami MS, El Egami AA, Abdalla WE, Galal M. Medicinal plants of the Sudan part IV. Medicinal plants of north Kordofan. Khartoum: National Council for Research; 1997.
48.
go back to reference El Ghazali GEB, Abdalla WE, Khalid HE, Khalafalla MM, Hamad AA. Medicinal plants of the Sudan part V. Medicinal plants of Ingassana area. Khartoum: National Council for Research; 2003. El Ghazali GEB, Abdalla WE, Khalid HE, Khalafalla MM, Hamad AA. Medicinal plants of the Sudan part V. Medicinal plants of Ingassana area. Khartoum: National Council for Research; 2003.
49.
go back to reference El Kamali HM, El Khalifa KF. Folk medicinal plants of riverside forests of the southern Blue Nile district. Sudan Fitoterapia. 1999;70:493–7.CrossRef El Kamali HM, El Khalifa KF. Folk medicinal plants of riverside forests of the southern Blue Nile district. Sudan Fitoterapia. 1999;70:493–7.CrossRef
50.
go back to reference Hussein G, Miyashiro H, Nakamura N, Hattori M, Kawahata T, Otake T. Inhibitory effects of Sudanese plant extracts on HIV-1 replication and HIV-1 protease. Phytother Res. 1999;13:31–6.CrossRefPubMed Hussein G, Miyashiro H, Nakamura N, Hattori M, Kawahata T, Otake T. Inhibitory effects of Sudanese plant extracts on HIV-1 replication and HIV-1 protease. Phytother Res. 1999;13:31–6.CrossRefPubMed
51.
go back to reference Nour AM, Khalid SA, Kaiser M, Brun R, Abdallah WE, Schmidt TJ. The antiprotozoal activity of sixteen asteraceae species native to Sudan and bioactivity-guided isolation of xanthanolides from Xanthium brasilicum. Planta Med. 2009;75:1363–8.CrossRefPubMed Nour AM, Khalid SA, Kaiser M, Brun R, Abdallah WE, Schmidt TJ. The antiprotozoal activity of sixteen asteraceae species native to Sudan and bioactivity-guided isolation of xanthanolides from Xanthium brasilicum. Planta Med. 2009;75:1363–8.CrossRefPubMed
52.
go back to reference Dahab MM, Koko WS, Osman EE. In vitro antitrichomonal activity of Xanthium brasilicum vell and Argemone mexicana L different extracts. J Med Plant Res. 2011;5:151–5. Dahab MM, Koko WS, Osman EE. In vitro antitrichomonal activity of Xanthium brasilicum vell and Argemone mexicana L different extracts. J Med Plant Res. 2011;5:151–5.
53.
go back to reference Rahman MA, Mossa JS, AL-Said MS, AL-Yahya MA. Medicinal plant diversity in the flora of Saudi Arabia 1: a report on seven plant families. Fitoterapia. 2004;75:149–61.CrossRefPubMed Rahman MA, Mossa JS, AL-Said MS, AL-Yahya MA. Medicinal plant diversity in the flora of Saudi Arabia 1: a report on seven plant families. Fitoterapia. 2004;75:149–61.CrossRefPubMed
54.
go back to reference Kinghorn AD, Chai HB, Sung CK, Keller WJ. The classical discovery approach to defining bioactive constituent of botanicals. Fitoterapia. 2011;82:71–9.CrossRefPubMed Kinghorn AD, Chai HB, Sung CK, Keller WJ. The classical discovery approach to defining bioactive constituent of botanicals. Fitoterapia. 2011;82:71–9.CrossRefPubMed
55.
go back to reference Musa S, Abdelrasool F, El E, Ahmed L, Mahmoud A, Yagi S. Ethnobotanical study of medicinal plants in the Blue Nile state, South-eastern Sudan. J Med Plants Res. 2011;5:4287–97. Musa S, Abdelrasool F, El E, Ahmed L, Mahmoud A, Yagi S. Ethnobotanical study of medicinal plants in the Blue Nile state, South-eastern Sudan. J Med Plants Res. 2011;5:4287–97.
56.
go back to reference Ogbazghi W, Bein E. Assessment of non-wood forest products and their role in the livelihoods of rural communities in the gash-Barka region, Eritrea. Drylands Coordination Group Report. 2006;40:26–7. Ogbazghi W, Bein E. Assessment of non-wood forest products and their role in the livelihoods of rural communities in the gash-Barka region, Eritrea. Drylands Coordination Group Report. 2006;40:26–7.
57.
go back to reference Mahmoud AA, Ahmed AA, El Bassuony AA. A new chlorosesquiterpene lactone from Ambrosia maritima. Fitoterapia. 1999;70:575–8.CrossRef Mahmoud AA, Ahmed AA, El Bassuony AA. A new chlorosesquiterpene lactone from Ambrosia maritima. Fitoterapia. 1999;70:575–8.CrossRef
58.
go back to reference Hatil HE. Medicinal plants in east and central Africa: challenges and constraints. Ethnobot leaflet. 2009;13:364–9. Hatil HE. Medicinal plants in east and central Africa: challenges and constraints. Ethnobot leaflet. 2009;13:364–9.
59.
go back to reference Ferraz AC, Angelucci ME, Da Costa ML, Batista IR, De Oliveira BH, Da Cunha C. Pharmacological evaluation of ricinine, a central nervous system stimulant isolated from Ricinus communis. Pharmacol Biochem Behav. 1999;63:367–75.CrossRefPubMed Ferraz AC, Angelucci ME, Da Costa ML, Batista IR, De Oliveira BH, Da Cunha C. Pharmacological evaluation of ricinine, a central nervous system stimulant isolated from Ricinus communis. Pharmacol Biochem Behav. 1999;63:367–75.CrossRefPubMed
60.
go back to reference Holfelder MG, Steck M, Komor E, Seifert K. Ricinine in phloem sap of Ricinus communis. Phytochemistry. 1998;47:1461–3.CrossRef Holfelder MG, Steck M, Komor E, Seifert K. Ricinine in phloem sap of Ricinus communis. Phytochemistry. 1998;47:1461–3.CrossRef
61.
go back to reference Duke JA. Medicinal plants of the bible. Owerri, NY: Trado-Medic Books; 1983. Duke JA. Medicinal plants of the bible. Owerri, NY: Trado-Medic Books; 1983.
62.
63.
go back to reference Louhaichi M, Salkini AK, Estita HE, Belkhir S. Initial assessment of medicinal plants across the Libyan Mediterranean coast. Adv Environ Biol. 2011;5:359–70. Louhaichi M, Salkini AK, Estita HE, Belkhir S. Initial assessment of medicinal plants across the Libyan Mediterranean coast. Adv Environ Biol. 2011;5:359–70.
64.
go back to reference El Ghazali GEB. Medicinal plants of Sudan part I. Khartoum: Medicinal Plants of Erkawit, National Council for Research; 1986. El Ghazali GEB. Medicinal plants of Sudan part I. Khartoum: Medicinal Plants of Erkawit, National Council for Research; 1986.
65.
go back to reference Masoko P, Gololo SS, Mokgotho MP, Eloff JN, Howard RL, Mampuru LJ. Evaluation of the antioxidant, antibacterial, and antiproliferative activities of the acetone extract of the roots of Senna italica (Fabaceae). Afr J Tradit Complement Altern Med. 2010;7:138–48. Masoko P, Gololo SS, Mokgotho MP, Eloff JN, Howard RL, Mampuru LJ. Evaluation of the antioxidant, antibacterial, and antiproliferative activities of the acetone extract of the roots of Senna italica (Fabaceae). Afr J Tradit Complement Altern Med. 2010;7:138–48.
66.
go back to reference Hatil HE. Effect of certain medicinal plants extracts against storage pest, Tribolium castaneum Herbst. Am Eurasian J Sustain Agric. 2009;3:139–42. Hatil HE. Effect of certain medicinal plants extracts against storage pest, Tribolium castaneum Herbst. Am Eurasian J Sustain Agric. 2009;3:139–42.
67.
go back to reference El Kheir YM, Salih MH. Investigation of certain plants used in Sudanese folk medicine. Fitoterapia. 1980;51:143–7. El Kheir YM, Salih MH. Investigation of certain plants used in Sudanese folk medicine. Fitoterapia. 1980;51:143–7.
68.
go back to reference El Kamali HM, Khalid SA. The most common herbal remedies in Central Sudan. Fitoterapia. 1996;57:301–6. El Kamali HM, Khalid SA. The most common herbal remedies in Central Sudan. Fitoterapia. 1996;57:301–6.
69.
go back to reference Neuwinger DH. African traditional medicine. A dictionary of plant use and application. Stuttgart, Germany: Med. Pharm. Pub; 2000. Neuwinger DH. African traditional medicine. A dictionary of plant use and application. Stuttgart, Germany: Med. Pharm. Pub; 2000.
Metadata
Title
Inhibitory activities of selected Sudanese medicinal plants on Porphyromonas gingivalis and matrix metalloproteinase-9 and isolation of bioactive compounds from Combretum hartmannianum (Schweinf) bark
Authors
Ebtihal Abdalla M. Mohieldin
Ali Mahmoud Muddathir
Tohru Mitsunaga
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2017
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-017-1735-y

Other articles of this Issue 1/2017

BMC Complementary Medicine and Therapies 1/2017 Go to the issue