[en] Propolis is a resinous material collected by different bee species from various plant exudates and used to seal holes in honeycombs, smoothen the internal walls, embalm intruders, improve health and prevent diseases. From its n-hexane extract, eight compounds were isolated and characterised as: mangiferonic acid (1); 1-hydroxymangiferonic acid (2), new natural product; mangiferolic acid(3); 27-hydroxymangiferolic acid (4), reported here for the first time as propolis constituent; 27-hydroxymangiferonic acid (5); α-amyrin (6); β-amyrin (7) and lupeol (8). The chemical structures of the isolated compounds were elucidated using spectroscopic methods, such as 1D and 2D-NMR, mass spectrometry and comparison with previous published reports. Compounds 6-8 and n-hexane extract were tested against Gram-negative and Gram-positive bacteria strains using agar disc diffusion and macrodilution techniques. Interestingly, n-hexane extract and compounds 6-8 had good inhibitory activities against Methicillin Resistant Staphylococcus aureus (MRSA) and the clinical Klebsiella pneumoniae isolates. The biological effects of n-hexane extract and its fraction against K. pneumoniae 12 CM and MRSA revealed in the present study suggest that the Cameroonian dark brown propolis could be a potential alternative management of biofilms on medical devices and respiratory skin or infections.
Disciplines :
Chemistry
Author, co-author :
Sakava, Paul ; Department of Chemistry, Higher Teacher Training College, The University of Bamenda, Bambili, Cameroon ; Natural Substances and Valorization Laboratory, Department of Organic Chemistry, Faculty of Science, University of Yaoundé I, Yaoundé, Cameroon
Nyemb, Jean Noël ; Department of Refining and Petrochemistry, National Advanced School of Mines and Petroleum Industries, University of Maroua, Kaélé, Cameroon
Matchawe, Chelea; Institute of Medical Research and Medicinal Plants Studies (IMPM), Ministry of the Scientific Research and innovation, Yaounde, Cameroon ; The University Institute of International Development, Mokolo, Far North, Cameroon
Kumcho, Mangum Patience; School of Health Sciences, Catholic University of Central Africa, Yaounde, Cameroon
Tagatsing, Maurice Fotsing; Natural Substances and Valorization Laboratory, Department of Organic Chemistry, Faculty of Science, University of Yaoundé I, Yaoundé, Cameroon
Nsawir, Bonglaisin J; Institute of Medical Research and Medicinal Plants Studies (IMPM), Ministry of the Scientific Research and innovation, Yaounde, Cameroon
Talla, Emmanuel; School of Chemical Engineering and Mineral Industries, University of Ngaoundere, Ngaoundere, Cameroon ; Department of chemistry, Faculty of Science, University of Ngaoundere, Ngaoundere, Cameroon
Atchadé, Alex De Théodore; Natural Substances and Valorization Laboratory, Department of Organic Chemistry, Faculty of Science, University of Yaoundé I, Yaoundé, Cameroon
Laurent, Sophie ; Université de Mons - UMONS > Faculté de Médecine et de Pharmacie > Service de Chimie générale, organique et biomédicale
Henoumont, Céline ; Université de Mons - UMONS > Faculté de Médecine et de Pharmacie > Service de Chimie générale, organique et biomédicale
Language :
English
Title :
Chemical constituents and antibacterial activities of Cameroonian dark brown propolis against potential biofilm-forming bacteria.
R550 - Institut des Sciences et Technologies de la Santé R100 - Institut des Biosciences
Funding text :
The authors are grateful for the ARC (AUWB-2010\u201410/15UMONS-5), FNRS, ENCITE program, COST TD1004 (Theranostics imaging and therapy: an action to develop novel nanosized systems for imaging-guided drug delivery), UIAP VII program, European Network of Excellence EMIL (European Molecular Imaging Laboratories) program LSCH-2004503569 and the Center for Microscopy and Molecular Imaging (CMMI, supported by the European Regional Development Fund and the Walloon Region).
Abd Jalil MA, Kasmuri AR, Hadi H., 2017. Stingless bee honey, the natural wound healer: a review. Skin Pharmacol Physiol. 30(2):66–75. doi:10.1159/000458416.
Alanazi S., 2022. Antineoplastic and antitrypanosomal properties of propolis from Tetragonula biroi Friese. Molecules. 27(21):7463. doi:10.3390/molecules27217463.
Alenezi SS, Alenezi ND, Ebiloma GU, Natto M, Ungogo MA, Igoli JO, Ferro VA, Gray AI, Fearnley J, de Koning HP, et al.2022. The antiprotozoal activity of papua new guinea propolis and its triterpenes. Molecules. 27(5):1622.
Almuhayawi MS., 2020. Propolis as a novel antibacterial agent. Saudi J Biol Sci. 27(11):3079–3086. doi:10.1016/j.sjbs.2020.09.016.
Alorfi HS., 2022. Antifungal–antiproliferative norcycloartane-type triterpenes from the Red Sea green alga Tydemania expeditionis. Open Chem. 20(1):912–919. doi:10.1515/chem-2022-0179.
Anjaneyulu V, Satyanarayana P, Viswanadham KN, Jyothi VG, Rao KN, Radhika P., 1999. Triterpenoids from mangifera indica part iii in the series triterpenoids from mangifera indica. Phytochemistry. 50(7):1229–1236.
Balderas-Cordero D, Canales-Alvarez O, Sánchez-Sánchez R, Cabrera-Wrooman A, Canales-Martinez MM, Rodriguez-Monroy MA., 2023. Anti-inflammatory and histological analysis of skin wound healing through topical application of mexican propolis. Int J Mol Sci. 24(14):11831. doi:10.3390/ijms241411831.
Bankova V, Popova M, Trusheva B., 2018. The phytochemistry of the honeybee. Phytochem. 155:1–11. doi:10.1016/j.phytochem.2018.07.007.
Béji-Srairi R, Younes I, Snoussi M, Yahyaoui K, Borchard G, Ksouri R, Frachet V, Wided MK., 2020. Ethanolic extract of Tunisian propolis: chemical composition, antioxidant, antimicrobial and antiproliferative properties. J Apic Res. 59(5):917–927. doi:10.1080/.00218839.2020.1732572.
Centers for Disease Control and Prevention. 2013. Antibiotic resistance threats in the United States. https://www.cdc.gov/ drugresistance/pdf/ar-threats-2013-508.
Choi H, Park J-S, Kim K-M, Kim M, Ko K-W, Hyun C-G, Ahn JW, Seo J-H, Kim S-Y., 2018. Enhancing the antimicrobial effect of genistein by biotransformation in microbial system. J Ind Eng Chem. 63:255–261. doi:10.1016/j.jiec.2018.02.023.
Choudhari MK, Punekar SA, Ranade RV, Paknikar KM., 2012. Antimicrobial activity of stingless bee (Trigona sp.) propolis used in the folk medicine of Western Maharashtra, India. J Ethnopharmacol. 141(1):363–367. doi:10.1016/j.jep.2012.02.047.
Chuttong B, Lim K, Praphawilai P, Danmek K, Maitip J, Vit P, Wu M-C, Ghosh S, Jung C, Burgett M, et al.2023. Exploring the functional properties of propolis, geopropolis, and cerumen, with a special emphasis on their antimicrobial effects. Foods. 12(21):3909. doi:10.3390/foods12213909.
Devequi-Nunes D, MaCHado BAS, Barreto G, Rebouças Silva J, da Silva DF, da Rocha JLC, Brandão HN, Borges VM, Umsza-Guez MA, Lightfoot DA., 2018. Chemical characterization and biological activity of six different extracts of propolis through conventional methods and supercritical extraction. PLoS One. 13(12):e0207676. doi:10.1371/journal.pone.0207676.
El-Guendouz S, Aazza S, Lyoussi B, Bankova V, Popova M, Neto L, Faleiro ML, Miguel MdG, 2018. Moroccan Propolis: a natural antioxidant, antibacterial, and antibiofilm against Staphylococcus aureus with no induction of resistance after continuous exposure. Evid Based Complement Alternat Med. 2018(1):9759240. doi:10.1155/2018/9759240.
Escobedo‐Martínez C, Concepción Lozada M, Hernández‐Ortega S, Villarreal ML, Gnecco D, Enríquez RG, Reynolds W., 2012. 1H and 13C NMR characterization of new cycloartane triterpenes from Mangifera indica. Magnetic Reson in Chemistry. 50(1):52–57.
Fitzpatrick MC, Bauch CT, Townsend JP, Galvani AP., 2019. Modelling microbial infection to address global health challenges. Nat Microbiol. 4(10):1612–1619. doi:10.1038/s41564-019-0565-8.
Freitas MO, Ponte FAF, Lima MAS, Silveira ER., 2008. Flavonoids and triterpenes from the nest of the stingless bee trigona spinipes. J Braz Chem Soc. 19(3):532–535.
Gajdács M., 2019. The Continuing Threat of Methicillin-Resistant Staphylococcus aureus. Antibiotics (Basel, Switzerland) 8(2):52. doi:10.3390/antibiotics8020052
Hernández-Vázquez L, Palazon J, Navarro-Ocaña A., 2012. The Pentacyclic Triterpenes, α,β‑amyrins: A Review of Sources and Biological Activities, Phytochemicals ‑ A Global Perspective of Their Role in Nutrition and Health, Dr Venketeshwer Rao (Ed.), ISBN: 978‑953‑51‑0296‑0, InTech, Available from: http://www.intechopen.com/books/phytochemicals‑a‑global‑perspective‑of‑their‑role‑innutrition‑andhealth/the‑pentacyclic‑triterpenes‑amyrins‑a‑review‑of‑sources‑and‑biological‑activities
Jabir SM, Sulaiman MG, Taqi JZ, Li D., 2018. Chemical characterization of Iraqi propolis samples and assessing their antioxidant potentials. Microbes Infect. 20(2):89–100. doi:10.1016/j.micinf.2017.10.007.
Jaqueline C, Uilson S, Paola R, Marcio D, Jose B, Claudia C., 2015. Antimicrobial, antioxidant, anti-inflammatory, and cytotoxic activities of propolis from the stingless Bee Tetragonis cafiebrigi (Jataí). Evid Based Complement Altern Med. 2015:1–11.
Kharsany K, Viljoen A, Leonard C, van Vuuren S., 2019. The new buzz: investigating the antimicrobial interactions between bioactive compounds found in South African propolis. J Ethnopharmacol. 238:111867. doi:10.1016/j.jep.2019.111867.
Kubat M, Karabulut Z, Şengül S., 2021. Effect of propolis on wound healing in sacrococcygeal pilonidal disease: a randomized controlled clinical trial. Pak J Pharm Sci. 34(3(Supplementary):1063–1067.
Kumar N, Mueen Ahmed KK, Dang R, Shivananda TN, Das K., 2009. GC-MS analysis of propolis of Indian origin. J Young Pharmacists. 1(1):46. doi:10.4103/0975-1483.51876.
Kuropatnicki AK, Szliszka E, Krol W., 2013. Historical aspects of propolis research in modern times. Evid Based Complement Alternat Med. 2013:964149. doi:10.1155/2013/964149.
Li F, Awale S, Zhang H, Tezuka Y, Esumi H, Kadota S., 2009. Chemical constituents of propolis from myanmar and their preferential cytotoxicity against a human pancreatic cancer cell line. J Nat Prod. 72(7):1283–1287.
Lotfy M, Badra G, Burham W, Alenzi F., 2006. Combined use of honey, bee propolis and myrrh in healing a deep, infected wound in a patient with diabetes mellitus. Br J Biomed Sci. 63(4):171–173. doi:10.1080/09674845.2006.11732742.
Mahamat AA, Nyemb JN, Gade IS, Ngenge AT, Talla E, Céline H, Sophie L, Mbafor JT., 2020. A New fatty acid and some triterpenoids from propolis of Nkambe (North-West Region, Cameroon) and evaluation of the antiradical scavenging activity of their extracts. Open Chemistry. 18(1):239–243. doi:10.1515/chem-2020-0016.
Marcucci MC., 1995. Propolis: chemical composition, biological properties and therapeutic activity. Apidologie. 26(2):83–99. doi:10.1051/apido:19950202.
Mello CBSB, Petrus CCJ, Hubinger DM., 2010. Concentration of flavonoids and phenolic compounds in aqueous and ethanolic propolis extracts through nanofiltration. J Food Eng. 96(4):533–539. doi:10.1016/j.jfoodeng.2009.08.040.
Miguel MG, Nunes S, Dandlen SA, Cavaco AM, Antunes MD., 2010. Phenols and antioxidant activity of hydro-alcoholic extracts of propolis from Algarve, South of Portugal. Food Chem Toxicol. 48(12):3418–3423.
Nguyen HX, Nguyen MTT, Nguyen NT, Awale S., 2017. Chemical constituents of propolis from vietnamese trigona minor and their antiausterity activity against the panc-1 human pancreatic cancer cell line. J Nat Prod. 80(8):2345–2352.
Peycheva S, Apostolova E, Gardjeva P, Peychev Z, Kokova V, Angelov A, Slavov A, Murdjeva M., 2019. Effect of Bulgarian propolis on the oral microflora in adolescents with plaque-induced gingivitis. Revista Brasileira De Farmacognosia. 29(3):271–277. doi:10.1016/j.bjp.2018.11.001.
Popova M, Silici S, Kaftanoglu O, Bankova V., 2005. Antibacterial activity of Turkish propolis and its qualitative and quantitative chemical composition. Phytomedicine. 12(3):221–228. doi:10.1016/j.phymed.2003.09.007.
Popova M, Trusheva B, Antonova D, Cutajar S, Mifsud D, Farrugia C, Tsvetkova I, Najdenski H, Bankova V., 2011. The specific chemical profile of Mediterranean propolis from Malta. Food Chem. 126(3):1431–1435. doi:10.1016/j.foodchem.2010.11.130.
Przybyłek I, Karpiński TM., 2019. Antibacterial properties of propolis. Molecules. 24(11):2047. doi:10.3390/molecules24112047.
Pujirahayu N, Suzuki T, Katayama T., 2019. Cycloartane-type triterpenes and botanical origin of propolis of stingless indonesian bee Tetragonula sapiens. Plants. 8(3):57. doi:10.3390/plants8030057.
Ristivojević P, Dimkić I, Trifković J, Berić T, Vovk I, Milojković-Opsenica D, Stanković S., 2016. Antimicrobial activity of serbian propolis evaluated by means of MIC, HPTLC, bioautography and chemometrics. PLoS One. 11(6):e0157097. doi:10.1371/journal.pone.0157097.
Rosandy AR, Ishak SSO, Sabri NA, Ahmad WYW, Al Muqarrabun LMR., 2021. Antibacterial activity of lupeol from the bark of Dehaasia cuneate (Lauraceae). Crbb. 2(2):145–148. doi:10.5614/crbb.2021.2.2/BOFY6724.
Sakava P, Tagatsing FM, Zeuko’o ME, Talla E, Laurent S, Hénoumont C, Van Der E, Awantu FA, Atchadé ADT, Mbafor TJ., 2021. Two new cycloartenol and some pentacyclic triterpenoids from cameroonian propolis (Ngaoundal, AD Region) and evaluation of their antimicrobial activity. Nat Prod Chem and Res. 9(8):1–11.
Sakava P, Talla E, Chelea M, Tchinda TA, Zeuko’o ME, Laurent S, Vander EL, Tagatsing FM, Yaya AJ, Atchade DTA, et al.2014. Pentacyclic triterpenes and crude extracts with antimicrobial activity from Cameroonian brown propolis samples. J App Pharm Sci. 4(07):001–009.
Salatino A., 2022. Perspectives for uses of propolis in therapy against infectious diseases. Molecules. 27(14):4594. doi:10.3390/.molecules27144594.
Shabani M, Mokhtarian M, Kalbasi-Ashtari A, Kazempoor R., 2021. Effects of extracted propolis (Apis mellifera) on physicochemical and microbial properties of rainbow-trout fish burger patties. J Food Process Preserv. 45(12):e16027. doi:10.1111/jfpp.16027.
Silva BB, Rosalen LP, Cury AJ, Ikegaki M, Souza CV, Esteves A, Alencar MS., 2008. Chemical composition and botanical origin of red propolis, a new type of brazilian propolis. Evid Based Complement Alternat Med. 5(3):313–316. doi:10.1093/ecam/nem059.
Silva-Carvalho R, Baltazar F, Almeida-Aguiar C., 2015. Propolis: a complex natural product with a plethora of biological activities that can beexplored for drug development. Evid Based Complement Altern Med. 2015:1–29. doi:10.1155/2015/206439.
Sulaiman GM, Ad’hiah AH, Al-Sammarrae KW, Bagnati R, Frapolli R, Bello E, Uboldi S, Romano M, Panini N, Scanziani E, et al.2012. Assessing the anti-tumour properties of Iraqi propolis in vitro and in vivo. Food Chem Toxicol. 50(5):1632–1641. doi:10.1016/j.fct.2012.01.022.
Sulaiman GM, Al Sammarrae KW, Ad’hiah AH, Zucchetti M, Frapolli R, Bello E, Erba E, D’Incalci M, Bagnati R., 2011. Chemical characterization of Iraqi propolis samples and assessing their antioxidant potentials. Food Chem Toxicol. 49(9):2415–2421. doi:10.1016/j.fct.2011.06.060.
Sun C, Wu Z, Wang Z, Zhang H., 2015. Effect of ethanol/water solvents on phenolic profiles and antioxidant properties of Beijing propolis extracts. Evi Based Comp Altern Med. 8:1–9.
Talla E, Tamfu AN, Gade IS, Yanda L, Mbafor JT, Laurent S, Elst LV, Popova M, Bankova V., 2017. New mono-ether of glycerol and triterpenes with DPPH radical scavenging activity from Cameroonian propolis. Nat Prod Res. 31(12):1379–1389. doi:10.1080/14786419.2016.1253077.
Tamfu NA, Ceylan O, Cârâc G, Talla E, Dinica MR., 2022. Antibiofilm and anti-quorum sensing potential of cycloartane-type triterpene acids from cameroonian Grassland Propolis: phenolic profile and antioxidant activity of crude extract. Molecules. 27(15):4872. doi:10.3390/molecules27154872.
Tran TD, Ogbourne SM, Brooks PR, Sánchez-Cruz N, Medina-Franco JL, Quinn RJ., 2020. Lessons from exploring chemical space and chemical diversity of propolis components. Int J Mol Sci. 21(14):4988.
Trusheva B, Trunkova D, Bankova V., 2007. Different extraction methods of biologically active components from propolis: a preliminary study. Chem Cent J. 1(1):13. doi:10.1186/1752-153X-1-13.
Vázquez LH, Palazon J, Navarro-Ocaña A., 2012. The pentacyclic triterpenes α, β-amyrins: a review of sources and biological activities, phytochemicals - a global perspective of their role in nutrition and health. Dr Venketeshwer Rao (Ed.), ISBN: 978-953-51-0296-0. www.intechopen.com. doi:10.5772/27253.
WHO. 2017. Global priority list of Antibiotic-resistant Bacteria to guide research, Discovery, and Development of New Antibiotics. https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf.
WHO. 2019. Critically important antimicrobials for human medicine 6th revision 2018. Ranking of medically important antimicrobials for risk management of antimicrobial resistance due to non-human use. Cataloguing-in-Publication (CIP) data. CIP data are available at http://apps.who.int/iris.
Woźniak M, Mrówczyńska L, Waśkiewicz A, Rogoziński T, Ratajczak I., 2019. Phenolic profile and antioxidant activity of propolis extracts from Poland. Nat Prod Com. 14:1–7.
Zayyanu UU, Mohamed M., 2015. Analysis of phytochemical compounds in water and ethanol extracts of malaysian propolis. Int J Pharm Biol Sci. 6:374–380.
