Propolis: Its Role and Efficacy in Human Health and Diseases
Abstract
:1. Introduction
2. Chemical Constituents
3. Pharmaceutical and Therapeutic Properties of Propolis
3.1. Autoimmune Diseases
3.1.1. Diabetes Mellitus (Type 2)
3.1.2. Rheumatoid Arthritis
3.1.3. Anticancer
3.2. Cardiovascular Disease
3.3. Coronavirus Disease
Medical Disorder | Propolis Active Components | Type of Diseases | Outcomes | Ref. |
---|---|---|---|---|
Auto-immune disease | Apigenin, chrysin, galangin, genistein, kaempferol, luteolin, naringin, pinocembrin, and quercetin |
|
| [18,22] |
Apigenin, caffeic acid, CAPE, galangin, hesperidin, and quercetin |
|
| [22,23,24,27,28] | |
Cancer | Apigenin, artepillin C, caffeic acid, CAPE, chrysin, galangin, kaempferol, luteolin, myricetin, pinocembrin, and quercetin |
|
| [50,53,79,80] |
Cardiovascular diseases | CAPE, chrysin, kaempferide, luteolin, pinocembrin, pinostrobin, and quercetin |
|
| [57,63,64] |
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) | Artepillin C, baccharin, caffeic acid, CAPE, drupanin, myricetin, and quercetin |
|
| [69,70,71,72,73,74,75] |
Gastrointestinal disorder | Artepillin C, CAPE, coumaric acid, galangin, kaempferide, 4-methyl ester, and aromadendrin |
|
| [81] |
Neurological disorders | Apigenin, CAPE, chrysin, kaempferol, pinocembrin, and quercetin |
|
| [24,82,83,84,85] |
Respiratory tract-related diseases | Artepillin C, baccharin, CAPE, chrysin, galangin, kaempferide, kaempferol, naringenin, pinocembrin, benzyl caffeate, geranyl caffeate, and 3-methyl-2-butenyl caffeate |
|
| [85,86,87] |
Caffeic acid, CAPE, cinnamic acid, aromandendrin, N-acetylcysteine, p-coumaric acid, |
|
| [88,89,90,91] |
3.4. Gastrointestinal Disorder
3.5. Neurological Disorders
3.6. Respiratory Tract-Related Disease
3.6.1. Asthma
3.6.2. Chronic Obstructive Pulmonary Disease
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Atanasov, A.G.; Zotchev, S.B.; Dirsch, V.M.; Supuran, C.T. Natural products in drug discovery: Advances and opportunities. Nat. Rev. Drug Discov. 2021, 20, 200–216. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Kismali, G.; Gupta, S. Natural products for the prevention and treatment of chronic inflammatory diseases: Integrating traditional medicine into modern chronic diseases care. Evid. Based Complement. Altern. Med. 2018, 2018, 9837863. [Google Scholar] [CrossRef] [PubMed]
- Wagh, V.D. Propolis: A wonder bees product and its pharmacological potentials. Adv. Pharmacol. Sci. 2013, 2013, 308249. [Google Scholar] [CrossRef] [PubMed]
- Salatino, A.; Salatino, M.L.F.; Negri, G. How diverse is the chemistry and plant origin of Brazilian propolis? Apidologie 2021, 52, 1075–1097. [Google Scholar] [CrossRef] [PubMed]
- Pascoal, A.; Feás, X.; Dias, T.; Dias, L.G.; Estevinho, L.M. Chapted 13—The role of honey and propolis in the treatment of infected wounds. In Microbiology for Surgical Infections Diagnosis, Prognosis and Treatment; Academic Press: Cambridge, MA, USA, 2014; pp. 221–234. [Google Scholar]
- Anjum, S.I.; Ullah, A.; Khan, K.A.; Attaullah, M.; Khan, H.; Ali, H.; Bashir, M.A.; Tahir, M.; Ansari, M.J.; Ghramh, H.A.; et al. Composition and functional properties of propolis (bee glue): A review. Saudi J. Biol. Sci. 2019, 26, 1695–1703. [Google Scholar] [CrossRef] [PubMed]
- Marcucci, M.C. Propolis: Chemical composition, biological properties and therapeutic activity. Apidologie 1995, 26, 83–99. [Google Scholar] [CrossRef]
- Shanahan, M.; Spivak, M. Resin use by stingless bees: A review. Insects 2021, 12, 719. [Google Scholar] [CrossRef]
- Kuropatnicki, A.K.; Szliszka, E.; Krol, W. Historical aspects of propolis research in modern times. Evid. Based Complement. Altern. Med. 2013, 2013, 964149. [Google Scholar] [CrossRef]
- Fokt, H.; Pereira, A.; Ferreira, A.M.; Cunha, A.; Aguiar, C. How do bees prevent hive infections? The antimicrobial properties of propolis. Curr. Res. Technol. Educ. Top. Appl. Microbiol. Microb. Biotechnol. 2010, 2, 481–493. [Google Scholar]
- Toreti, V.C.; Sato, H.H.; Pastore, G.M.; Park, Y.K. Recent progress of propolis for its biological and chemical compositions and its botanical origin. Evid. Based Complement. Altern. Med. 2013, 2013, 697390. [Google Scholar] [CrossRef]
- Ahangari, Z.; Naseri, M.; Vatandoost, F. Propolis: Chemical composition and its applications in endodontics. Iran. Endod. J. 2018, 13, 285–292. [Google Scholar] [PubMed]
- Pasupuleti, V.R.; Sammugam, L.; Ramesh, N.; Gan, S.H. Honey, propolis, and royal jelly: A comprehensive review of their biological actions and health benefits. Oxid. Med. Cell. Longev. 2017, 2017, 1259510. [Google Scholar] [CrossRef] [PubMed]
- Abdullah, N.A.; Ja’afar, F.; Yasin, H.M.; Taha, H.; Petalcorin, M.I.R.; Mamit, M.H.; Kusrini, E.; Usman, A. Physicochemical analyses, antioxidant, antibacterial, and toxicity of propolis particles produced by stingless bee Heterotrigona itama found in Brunei Darussalam. Heliyon 2019, 5, e02476. [Google Scholar] [CrossRef]
- Abdullah, N.A.; Zullkiflee, N.; Zaini, S.N.Z.; Taha, H.; Hashim, F.; Usman, A. Phytochemicals, mineral contents, antioxidants, and antimicrobial activities of propolis produced by Brunei stingless bees Geniotrigona thoracica, Heterotrigona itama, and Tetrigona binghami. Saudi J. Biol. Sci. 2020, 27, 2902–2911. [Google Scholar] [CrossRef]
- Bankova, V. Chemical diversity of propolis and the problem of standardization. J. Ethnopharmacol. 2005, 100, 114–117. [Google Scholar] [CrossRef]
- Huang, S.; Zhang, C.P.; Wang, K.; Li, G.Q.; Hu, F.L. Recent advances in the chemical composition of propolis. Molecules 2014, 19, 19610–19623. [Google Scholar]
- Devequi-Nunes, D.; Machado, B.A.S.; Barreto, G.A.; Silva, J.R.; da Silva, D.F.; da Rocha, J.L.C.; Brandão, H.N.; Borges, V.M.; Umsza-Guez, M.A. Chemical characterization and biological activity of six different extracts of propolis through conventional methods and supercritical extraction. PLoS ONE 2018, 13, e0207676. [Google Scholar] [CrossRef] [PubMed]
- Bonvehi, J.S.; Coll, F.V.; Jorda, R.E. The composition, active components and bacteriostatic activity of propolis in dietetics. J. Am. Oil Chem. Soc. 1994, 71, 529–532. [Google Scholar] [CrossRef]
- Kalogeropoulos, N.; Konteles, S.J.; Troullidou, E.; Mourtzinos, I.; Karathanos, V.T. Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus. Food Chem. 2009, 116, 452–461. [Google Scholar] [CrossRef]
- Nedjia, N.; Loucif-Ayad, W. Antimicrobial activity of Algerian propolis in foodborne pathogens and its quantitative chemical composition. Asian Pacific J. Trop. Dis. 2014, 4, 433–437. [Google Scholar] [CrossRef]
- Kurek-Górecka, A.; Keskin, Ş.; Bobis, O.; Felitti, R.; Górecki, M.; Otręba, M.; Stojko, J.; Olczyk, P.; Kolayli, S.; Rzepecka-Stojko, A. Comparison of the antioxidant activity of propolis samples from different geographical regions. Plants 2022, 11, 1203. [Google Scholar] [CrossRef] [PubMed]
- Santos, V.R. Chapter 5—Propolis: Alternative medicine for the treatment of oral microbial diseases. In Alternative Medicine; Sakagami, H., Ed.; IntechOpen: Vienna, Austria, 2012; Volume 11, pp. 133–169. [Google Scholar]
- Sawicka, D.; Car, H.; Borawska, M.H.; Nikliński, J. The anticancer activity of propolis. Folia Histochem. Cytobiol. 2012, 50, 25–37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maciejewicz, W.; Daniewski, M.; Bal, K.; Markowski, W. GC-MS identification of the flavonoid aglycones isolated from propolis. Chromatographia 2001, 53, 343–346. [Google Scholar] [CrossRef]
- Banskota, A.H.; Tezuka, Y.; Kadota, S. Recent progress in pharmacological research of propolis. Phyther. Res. 2001, 15, 561–571. [Google Scholar] [CrossRef]
- Wolska, K.; Górska, A.; Antosik, K.; Ługowska, K. Immunomodulatory effects of propolis and its components on basic immune cell functions. Indian J. Pharm. Sci. 2019, 81, 575–588. [Google Scholar] [CrossRef]
- Ansorge, S.; Reinhold, D.; Lendeckel, U. Propolis and some of its constituents down-regulate DNA synthesis and inflammatory cytokine production but induce TGF-Beta1 production of human immune cells. Z. Naturforsch. 2003, 58, 580–589. [Google Scholar] [CrossRef]
- Nattagh-Eshtivani, E.; Pahlavani, N.; Ranjbar, G.; Navashenaq, J.G.; Salehi-Sahlabadi, A.; Mahmudiono, T.; Shalaby, M.N.; Jokar, M.; Nematy, M.; Barghchi, H.; et al. Does propolis have any effect on rheumatoid arthritis? A review study. Food Sci. Nutr. 2021, 10, 1003–1020. [Google Scholar] [CrossRef]
- Bankova, V.S.; De Castro, S.L.; Marcucci, M.C. Propolis: Recent advances in chemistry and plant origin. Apidologie 2000, 31, 3–15. [Google Scholar] [CrossRef]
- Filippin, L.I.; Vercelino, R.; Marroni, N.P.; Xavier, R.M. Redox signalling and the inflammatory response in rheumatoid arthritis. Clin. Exp. Immunol. 2008, 152, 415–422. [Google Scholar] [CrossRef]
- Farooqui, T.; Farooqui, A.A. Beneficial effects of propolis on human health and neurological diseases. Front. Biosci. 2012, 4, 779–793. [Google Scholar] [CrossRef]
- Zullkiflee, N.; Taha, H.; Abdullah, N.A.; Hashim, F.; Usman, A. Antibacterial and antioxidant activities of ethanolic and water extracts of stingless bees Tetrigona binghami, Heterotrigona itama, and Geniotrigona thoracica propolis found in Brunei. Philipp. J. Sci. 2022, 151, 1455–1462. [Google Scholar]
- Rivera-Yañez, N.; Rodriguez-Canales, M.; Nieto-Yañez, O.; Jimenez-Estrada, M.; Ibarra-Barajas, M.; Canales-Martinez, M.M.; Rodriguez-Monroy, M.A. Hypoglycaemic and antioxidant effects of propolis of Chihuahua in a model of experimental diabetes. Evid. Based Complement. Altern. Med. 2018, 2018, 4360356. [Google Scholar] [CrossRef] [PubMed]
- Matsui, T.; Ebuchi, S.; Fujise, T.; Abesundara, K.J.; Doi, S.; Yamada, H.; Matsumoto, K. Strong antihyperglycemic effects of water-soluble fraction of Brazilian propolis and its bioactive constituent, 3,4,5-tri-o-caffeoylquinic acid. Biol. Pharm. Bull. 2004, 27, 1797–1803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fuliang, H.U.; Hepburn, H.R.; Xuan, H.; Chen, M.; Daya, S.; Radloff, S.E. Effects of propolis on blood glucose, blood lipid and free radicals in rats with diabetes mellitus. Pharmacol. Res. 2005, 51, 147–152. [Google Scholar] [CrossRef]
- Zhang, X.; Wang, G.; Gurley, E.C.; Zhou, H. Flavonoid apigenin inhibits lipopolysaccharide-induced inflammatory response through multiple mechanisms in macrophages. PLoS ONE 2014, 9, e107072. [Google Scholar] [CrossRef]
- Ramos, A.; Miranda, J. Propolis: A review of its anti-inflammatory and healing actions. J. Venom. Anim. Toxins Incl. Trop. Dis. 2007, 13, 697–710. [Google Scholar] [CrossRef]
- Kurek-Górecka, A.; Rzepecka-Stojko, A.; Górecki, M.; Stojko, J.; Sosada, M.; Swierczek-Zieba, G. Structure and antioxidant activity of polyphenols derived from propolis. Molecules 2014, 19, 78–101. [Google Scholar] [CrossRef]
- Zakerkish, M.; Jenabi, M.; Zaeemzadeh, N.; Hemmati, A.A.; Neisi, N. The effect of Iranian propolis on glucose metabolism, lipid profle, insulin resistance, renal function and inflammatory biomarkers in patients with type 2 diabetes mellitus: A randomized double-blind clinical trial. Sci. Rep. 2019, 9, 7289. [Google Scholar] [CrossRef]
- Daleprane, J.B.; Abdalla, D.S. Emerging roles of propolis: Antioxidant, cardioprotective, and antiangiogenic actions. Evid. Based Complement. Altern. Med. 2013, 2013, 175135. [Google Scholar] [CrossRef]
- Samadi, N.; Mozaffari-Khosravi, H.; Rahmanian, M.; Askarishahi, M. Effects of bee propolis supplementation on glycemic control, lipid profile and insulin resistance indices in patients with type 2 diabetes: A randomized, double-blind clinical trial. J. Integr. Med. 2017, 15, 124–134. [Google Scholar] [CrossRef]
- Pahlavani, N.; Malekahmadi, M.; Firouzi, S.; Rostami, D.; Sedaghat, A.; Moghaddam, A.B.; Ferns, G.A.; Navashenaq, J.G.; Reazvani, R.; Safarian, M.; et al. Molecular and cellular mechanisms of the effects of propolis in inflammation, oxidative stress and glycemic control in chronic diseases. Nutr. Metab. 2020, 17, 65. [Google Scholar] [CrossRef] [PubMed]
- Roy, J.; Galano, J.M.; Durand, T.; Le Guennec, J.Y.; Lee, J.C. Physiological role of reactive oxygen species as promoters of natural defenses. FASEB J. 2017, 31, 3729–3745. [Google Scholar] [CrossRef] [PubMed]
- Matsumoto, Y.; Takahashi, K.; Sugioka, Y.; Inui, K.; Okano, T.; Mandai, K.; Yamada, Y.; Shintani, A.; Koike, T. Double-blinded randomized controlled trial to reveal the effects of Brazilian propolis intake on rheumatoid arthritis disease activity index; BeeDAI. PLoS ONE 2021, 16, e0252357. [Google Scholar] [CrossRef]
- Karikas, G.A. Anticancer and chemopreventing natural products: Some biochemical and therapeutic aspects. J. BUON 2010, 15, 627–638. [Google Scholar] [PubMed]
- Elumalai, P.; Muninathan, N.; Megalatha, S.T.; Suresh, A.; Kumar, K.S.; Jhansi, N.; Kuppuswamy Kalaivani, K.; Krishnamoorthy, G. An Insight into anticancer effect of propolis and its constituents: A review of molecular mechanisms. Evid. Based Complement. Altern. Med. 2022, 2022, 5901191. [Google Scholar] [CrossRef]
- Demir, S.; Aliyazicioglu, Y.; Turan, I.; Misir, S.; Mentese, A.; Yaman, S.O.; Akbulut, K.; Kilinc, K.; Deger, O. Antiproliferative and proapoptotic activity of Turkish propolis on human lung cancer cell line. Nutr. Cancer. 2016, 68, 165–172. [Google Scholar] [CrossRef]
- Reed, J.C. Mechanisms of apoptosis. Am. J. Pathol. 2000, 157, 1415–1430. [Google Scholar] [CrossRef]
- Masadah, R.; Ikram, D.; Rauf, S. Effects of propolis and its bioactive components on breast cancer cell pathways and the molecular mechanisms involved. Breast Dis. 2021, 40, S15–S25. [Google Scholar] [CrossRef]
- Turan, I.; Demir, S.; Misir, S.; Kilinc, K.; Mentese, A.; Aliyazicioglu, Y.; Deger, O. Cytotoxic effect of Turkish propolis on liver, colon, breast, cervix and prostate cancer cell lines. Trop. J. Pharm. Res. 2015, 14, 777. [Google Scholar] [CrossRef]
- Vatansever, H.S.; Sorkun, K.; Gurhan, S.I.D.; Ozdal-Kurt, F.; Turkoz, E.; Gencay, O.; Salih, B. Propolis from Turkey induces apoptosis through activating caspases in human breast carcinoma cell lines. Acta Histochem. 2010, 112, 546–556. [Google Scholar] [CrossRef]
- Benguedouar, L.; Lahouel, M.; Gangloff, S.C.; Durlach, A.; Grange, F.; Bernard, P.; Antonicelli, F. Ethanolic extract of Algerian propolis and galangin decreased Murine melanoma tumor progression in mice. Anticancer Agents Med. Chem. 2016, 16, 1172–1183. [Google Scholar] [CrossRef] [PubMed]
- Frión-Herrera, Y.; Díaz-García, A.; Ruiz-Fuentes, J.; Rodríguez-Sánchez, H.; Sforcin, J.M. Brazilian green propolis induced apoptosis in human lung cancer A549 cells through mitochondrial-mediated pathway. J. Pharm. Pharmacol. 2015, 67, 1448–1456. [Google Scholar] [CrossRef] [PubMed]
- Brihoum, H.; Maiza, M.; Sahali, H.; Boulmeltout, M.; Barratt, G.; Benguedouar, L.; Lahouel, M. Dual effect of Algerian propolis on lung cancer: Antitumor and chemopreventive effects involving antioxidant activity. Braz. J. Pharm. Sci. 2018, 54, 1–12. [Google Scholar] [CrossRef]
- Tao, L.; Chen, X.; Zheng, Y.; Wu, Y.; Jiang, X.; You, M.; Li, S.; Hu, F. Chinese propolis suppressed pancreatic cancer Panc-1 cells proliferation and migration via Hippo-YAP pathway. Molecules 2021, 26, 2803. [Google Scholar] [CrossRef] [PubMed]
- Ahn, M.R.; Kunimasa, K.; Kumazawa, S.; Nakayama, T.; Kaji, K.; Uto, Y.; Hori, H.; Nagasawa, H.; Ohta, T. Correlation between antiangiogenic activity and antioxidant activity of various components from propolis. Mol. Nutr. Food Res. 2009, 53, 643–651. [Google Scholar] [CrossRef] [PubMed]
- Silva, H.; Francisco, R.; Saraiva, A.; Francisco, S.; Carrascosa, C.; Raposo, A. The cardiovascular therapeutic potential of propolis-A comprehensive review. Biology 2021, 10, 27. [Google Scholar] [CrossRef] [PubMed]
- Ebeid, S.A.; El Moneim, N.A.A.; El-Benhawy, S.A.; Hussain, N.G.; Hussain, M.I. Assessment of the radioprotective effect of propolis in breast cancer patients undergoing radiotherapy. New perspective for an old honey bee product. J. Radiat. Res. Appl. Sci. 2016, 9, 431–440. [Google Scholar] [CrossRef]
- Piredda, M.; Facchinetti, G.; Biagioli, V.; Giannarelli, D.; Armento, G.; Tonini, G.; De Marinis, M.G. Propolis in the prevention of oral mucositis in breast cancer patients receiving adjuvant chemotherapy: A pilot randomised controlled trial. Eur. J. Cancer Care 2017, 26, e12757. [Google Scholar] [CrossRef]
- Darvishi, N.; Yousefinejad, V.; Akbari, M.E.; Abdi, M.; Moradi, N.; Darvishi, S.; Mehrabi, Y.; Ghaderi, E.; Jamshidi-Naaeinii, Y.; Ghaderi, B.; et al. Antioxidant and anti-inflammatory effects of oral propolis in patients with breast cancer treated with chemotherapy: A randomized controlled trial. J. Herb. Med. 2020, 23, 100385. [Google Scholar] [CrossRef]
- Benjamin, E.J.; Blaha, M.J.; Chiuve, S.E.; Cushman, M.; Das, S.R.; Deo, R.; de Ferranti, S.D.; Floyd, J.; Fornage, M.; Gillespie, C.; et al. Heart disease and stroke statistics-2017 update: A report from the American Heart Association. Circulation 2017, 135, e146–e603. [Google Scholar] [CrossRef]
- Hadi, A.; Rafie, N.; Arab, A. Bee products consumption and cardiovascular diseases risk factors: A systematic review of interventional studies. Int. J. Food Prop. 2021, 24, 115–128. [Google Scholar] [CrossRef]
- Olas, B. Bee products as interesting natural agents for the prevention and treatment of common cardiovascular diseases. Nutrients 2022, 14, 2267. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, R.; Tanvir, E.M.; Hossen, M.S.; Afroz, R.; Ahmmed, I.; Rumpa, N.E.; Paul, S.; Gan, S.H.; Sulaiman, S.A.; Khalil, M.I. Antioxidant properties and cardioprotective mechanism of Malaysian propolis in rats. Evid. Based Complement. Altern. Med. 2017, 2017, 5370545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vazhappilly, C.G.; Ansari, S.A.; Al-Jaleeli, R.; Al-Azawi, A.M.; Ramadan, W.S.; Menon, V.; Hodeify, R.; Siddiqui, S.S.; Merheb, M.; Matar, R.; et al. Role of flavonoids in thrombotic, cardiovascular, and inflammatory diseases. Inflammopharmacology 2019, 27, 863–869. [Google Scholar] [CrossRef] [PubMed]
- Cucinotta, D.; Vanelli, M. WHO declares COVID-19 a pandemic. Acta Bio-Med. 2020, 91, 157–160. [Google Scholar]
- Shi, Y.; Wang, G.; Cai, X.P.; Deng, J.W.; Zheng, L.; Zhu, H.H.; Zheng, M.; Yang, B.; Chen, Z. An overview of COVID-19. J. Zhejiang Univ. 2020, 21, 343–360. [Google Scholar] [CrossRef]
- Dilokthornsakul, W.; Kosiyaporn, R.; Wuttipongwaragon, R.; Dilokthornsakul, P. Potential effects of propolis and honey in COVID-19 prevention and treatment: A systematic review of in silico and clinical studies. J. Integr. Med. 2022, 20, 114–125. [Google Scholar] [CrossRef]
- Berretta, A.A.; Silveira, M.A.D.; Cóndor Capcha, J.M.; De Jong, D. Propolis and its potential against SARS-CoV-2 infection mechanisms and COVID-19 disease. Biomed. Pharmacother. 2020, 131, 110622. [Google Scholar] [CrossRef]
- Ripari, N.; Sartori, A.A.; da Silva Honorio, M.; Conte, F.L.; Tasca, K.I.; Santiago, K.B.; Sforcin, J.M. Propolis antiviral and immunomodulatory activity: A review and perspectives for COVID-19 treatment. J. Pharm. Pharmacol. 2021, 73, 281–299. [Google Scholar] [CrossRef]
- Scorza, C.A.; Gonçalves, V.C.; Scorza, F.A.; Fiorini, A.C.; de Almeida, A.G.; Fonseca, M.; Finsterer, J. Propolis and coronavirus disease 2019 (COVID-19): Lessons from nature. Complement. Ther. Clin. Pract. 2020, 41, 101227. [Google Scholar] [CrossRef]
- Fiorini, A.C.; Scorza, C.A.; Almeida, A.G.; Fonseca, M.C.; Finsterer, J.; Fonseca, F.L.; Scorza, F.A. Antiviral activity of Brazilian green propolis extract against SARS-CoV-2 (severe acute respiratory syndrome—Coronavirus 2) infection: Case report and review. Clinics 2021, 76, e2357. [Google Scholar] [CrossRef] [PubMed]
- Sahlan, M.; Irdiani, R.; Flamandita, D.; Aditama, R.; Alfarraj, S.; Ansari, M.J.; Khayrani, A.C.; Pratami, D.K.; Lischer, K. Molecular interaction analysis of Sulawesi propolis compounds with SARS-CoV-2 main protease as preliminary study for COVID-19 drug discovery. J. King Saudi Univ. 2021, 33, 101234. [Google Scholar] [CrossRef]
- Mani, J.S.; Johnson, J.B.; Steel, J.C.; Broszczak, D.A.; Neilsen, P.M.; Walsh, K.B.; Naiker, M. Natural product-derived phytochemicals as potential agents against coronaviruses: A review. Virus Res. 2020, 284, 197989. [Google Scholar] [CrossRef]
- Silveira, M.A.D.; De Jong, D.; Berretta, A.A.; dos Santos Galvão, E.B.; Ribeiro, J.C.; Cerqueira-Silva, T.; Amorim, T.C.; da Conceição, L.F.M.R.; Dantas-Gomes, M.M.; Teixeira, M.B.; et al. Efficacy of Brazilian green propolis (EPP-AF®) as an adjunct treatment for hospitalized COVID-19 patients: A randomized, controlled clinical trial. Biomed. Pharmacother. 2021, 138, 111526. [Google Scholar] [CrossRef] [PubMed]
- Yildirim, A.; Duran, G.G.; Duran, N.; Jenedi, K.; Bolgul, B.S.; Miraloglu, M.; Muz, M. Antiviral activity of Hatay propolis against replication of herpes simplex virus type 1 and type 2. Med. Sci. Monit. 2016, 22, 422–430. [Google Scholar] [CrossRef] [PubMed]
- Debiaggi, M.; Tateo, F.; Pagani, L.; Luini, M.; Romero, E. Effects of propolis flavonoids on virus infectivity and replication. Microbiologica 1990, 13, 207–213. [Google Scholar]
- Forma, E.; Bryś, M. Anticancer activity of propolis and its compounds. Nutrients 2021, 13, 2594. [Google Scholar] [CrossRef]
- Xuan, H.; Li, Z.; Yan, H.; Sang, Q.; Wang, K.; He, Q.; Wang, Y.; Hu, F. Antitumor activity of Chinese propolis in human breast cancer MCF-7 and MDA-MB-231 cells. Evid. Based Complement. Altern. Med. 2014, 2014, 280120. [Google Scholar] [CrossRef]
- Ruiz-Hurtado, P.A.; Garduño-Siciliano, L.; Domínguez-Verano, P.; Balderas-Cordero, D.; Gorgua-Jiménez, G.; Canales-Álvarez, O.; Canales-Martínez, M.M.; Rodríguez-Monroy, M.A. Propolis and its gastroprotective effects on NSAID-induced gastric ulcer disease: A systematic review. Nutrients 2021, 13, 3169. [Google Scholar] [CrossRef]
- Altuğ, M.E.; Serarslan, Y.; Bal, R.; Kontaş, T.; Ekici, F.; Melek, I.M.; Aslan, H.; Duman, T. Caffeic acid phenethyl ester protects rabbit brains against permanent focal ischemia by antioxidant action: A biochemical and planimetric study. Brain Res. 2008, 1201, 135–142. [Google Scholar] [CrossRef]
- Choi, D.; Han, J.; Lee, Y.; Choi, J.; Han, S.; Hong, S.; Jeon, H.; Kim, Y.M.; Jung, Y. Caffeic acid phenethyl ester is a potent inhibitor of HIF prolyl hydroxylase: Structural analysis and pharmacological implication. J. Nutr. Biochem. 2010, 21, 809–817. [Google Scholar] [CrossRef] [PubMed]
- Machado, C.S.; Mokochinski, J.B.; de Lira, T.O.; de Oliveira, F.C.; Cardoso, M.V.; Ferreira, R.G.; Sawaya, A.C.H.F.; Ferreira, A.G.; Pessoa, C.; Cuesta-Rubio, O.; et al. Comparative study of chemical composition and biological activity of yellow, green, brown, and red Brazilian propolis. Evid. Based Complement. Altern. Med. 2016, 2016, 6057650. [Google Scholar] [CrossRef] [PubMed]
- Liu, R.; Li, J.Z.; Song, J.K.; Sun, J.L.; Li, Y.J.; Zhou, S.B.; Zhang, T.T.; Du, G.H. Pinocembrin protects human brain microvascular endothelial cells against fibrillar amyloid-β(1-40) injury by suppressing the MAPK/NF-ΚB inflammatory pathways. Biomed. Res. Int. 2014, 2014, 470393. [Google Scholar] [CrossRef] [PubMed]
- Liew, K.Y.; Kamise, N.I.; Ong, H.M.; Aw Yong, P.Y.; Islam, F.; Tan, J.W.; Tham, C. Anti-allergic properties of propolis: Evidence from preclinical and clinical studies. Front. Pharmacol. 2022, 12, 785371. [Google Scholar] [CrossRef] [PubMed]
- Martins, N.S.; de Campos Fraga-Silva, T.F.; Correa, G.F.; Boko, M.M.M.; Ramalho, L.N.Z.; Rodrigues, D.M.; Hori, J.I.; Costa, D.L.; Bastos, J.K.; Bonato, V.L.D. Artepillin C reduces allergic airway inflammation by induction of monocytic myeloid-derived suppressor cells. Pharmaceutics 2021, 13, 1763. [Google Scholar] [CrossRef]
- Szliszka, E.; Mertas, A.; Czuba, Z.P.; Król, W. Inhibition of inflammatory response by artepillin C in activated RAW264.7 macrophages. Evid. Based Complement. Altern. Med. 2013, 2013, 735176. [Google Scholar] [CrossRef]
- Machado, J.L.; Assunção, A.K.; da Silva, M.C.; Dos Reis, A.S.; Costa, G.C.; Arruda Dde, S.; Rocha, B.A.; Vaz, M.M.; Paes, A.M.; Guerra, R.N.; et al. Brazilian green propolis: Anti-inflammatory property by an immunomodulatory activity. Evid. Based Complement. Altern. Med. 2012, 2012, 157652. [Google Scholar] [CrossRef]
- Kolarov, V.; Kotur Stevuljević, J.; Ilić, M.; Bogdan, M.; Tušek, B.; Agic, A.; Dugajlić, M.; Tot Vereš, K.; Kutlešić Stević, S.; Zvezdin, B. Factorial analysis of N-acetylcysteine and propolis treatment effects on symptoms, life quality and exacerbations in patients with chronic obstructive pulmonary disease (COPD): A randomized, double-blind, placebo-controlled trial. Eur. Rev. Med. Pharmacol. Sci. 2022, 26, 3192–3199. [Google Scholar]
- Barroso, M.V.; Cattani-Cavalieri, I.; de Brito-Gitirana, L.; Fautrel, A.; Lagente, V.; Schmidt, M.; Porto, L.C.; Romana-Souza, B.; Valença, S.S.; Lanzetti, M. Propolis reversed cigarette smoke-induced emphysema through macrophage alternative activation independent of Nrf2. Bioorganic Med. Chem. 2017, 25, 5557–5568. [Google Scholar] [CrossRef]
- Jones, S.L.; Blikslager, A.T. Disorders of the gastrointestinal system. Equine Intern. Med. 2009, 2004, 769–949. [Google Scholar]
- Miryan, M.; Soleimani, D.; Alavinejad, P.; Abbaspour, M.; Ostadrahimi, A. Effects of propolis supplementation on irritable bowel syndrome with constipation (IBS-C) and mixed (IBS-M) stool pattern: A randomized, double-blind clinical trial. Food Sci. Nutr. Nutr. 2022, 10, 1899–1907. [Google Scholar] [CrossRef] [PubMed]
- Xue, M.; Liu, Y.; Xu, H.; Zhou, Z.; Ma, Y.; Sun, T.; Liu, M.; Zhang, H.; Liang, H. Propolis modulates the gut microbiota and improves the intestinal mucosal barrier function in diabetic rats. Biomed. Pharmacother. Pharmacother. 2019, 118, 109393. [Google Scholar] [CrossRef] [PubMed]
- Farooqui, A.A.; Horrocks, L.A.; Farooqui, T. Glycerophospholipids in brain: Their metabolism, incorporation into membranes, functions, and involvement in neurological disorders. Chem. Phys. Lipids 2000, 106, 1–29. [Google Scholar] [CrossRef]
- Walker, P.; Crane, E. Constituents of propolis. Apidologie 1987, 18, 327–334. [Google Scholar] [CrossRef]
- Parmar, S.K.; Sharma, T.P.; Airao, V.B.; Bhatt, R.; Aghara, R.; Chavda, S.; Rabadiya, S.; Gangwal, A. Neuropharmacological effects of triterpenoids. Phytopharmacology 2013, 4, 354–372. [Google Scholar]
- Noelker, C.; Bacher, M.; Gocke, P.; Wei, X.; Klockgether, T.; Du, Y.; Dodel, R. The flavanoide caffeic acid phenethyl ester blocks 6-hydroxydopamine-induced neurotoxicity. Neurosci. Lett. 2005, 383, 39–43. [Google Scholar] [CrossRef]
- Zulhendri, F.; Perera, C.O.; Tandean, S. Can propolis be a useful adjuvant in brain and neurological disorders and injuries? A systematic scoping review of the latest experimental evidence. Biomedicines 2021, 9, 1227. [Google Scholar] [CrossRef]
- Nakamura, R.; Nakamura, R.; Watanabe, K.; Oka, K.; Ohta, S.; Mishima, S.; Teshima, R. Effects of propolis from different areas on mast cell degranulation and identification of the effective components in propolis. Int. Immunopharmacol. 2010, 10, 1107–1112. [Google Scholar] [CrossRef]
- He, S.H.; Zhang, H.Y.; Zeng, X.N.; Chen, D.; Yang, P.C. Mast cells and basophils are essential for allergies: Mechanisms of allergic inflammation and a proposed procedure for diagnosis. Acta Pharmacol. Sin. 2013, 34, 1270–1283. [Google Scholar] [CrossRef]
- Stone, K.D.; Prussin, C.; Metcalfe, D.D. IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 2010, 125, S73–S80. [Google Scholar] [CrossRef]
- Lloyd, C.M.; Hessel, E.M. Functions of T cells in asthma: More than just T(H)2 cells. Nat. Rev. Immunol. 2013, 10, 838–848. [Google Scholar] [CrossRef] [PubMed]
- Khayyal, M.T.; El-Ghazaly, M.A.; El-Khatib, A.S.; Hatem, A.M.; de Vries, P.J.; El-Shafei, S.; Khattab, M.M. A clinical pharmacological study of the potential beneficial effects of a propolis food product as an adjuvant in asthmatic patients. Fundam. Clin. Pharmacol. 2003, 17, 93–102. [Google Scholar] [CrossRef]
- Tani, H.; Hasumi, K.; Tatefuji, T.; Hashimoto, K.; Koshino, H.; Takahashi, S. Inhibitory activity of Brazilian green propolis components and their derivatives on the release of cys-leukotrienes. Bioorganic Med. Chem. 2010, 18, 151–157. [Google Scholar] [CrossRef] [PubMed]
- Hausen, B.M. Evaluation of the main contact allergens in propolis (1995 to 2005). Dermatitis 2005, 16, 127–129. [Google Scholar] [PubMed]
- Wang, L.C.; Lin, Y.L.; Liang, Y.C.; Yang, Y.H.; Lee, J.H.; Yu, H.H.; Wu, W.M.; Chiang, B.L. The effect of caffeic acid phenethyl ester on the functions of human monocyte-derived dendritic cells. BMC Immunol. 2009, 10, 39. [Google Scholar] [CrossRef] [PubMed]
- Cukic, V.; Lovre, V.; Dragisic, D.; Ustamujic, A. Asthma and chronic obstructive pulmonary disease (COPD)—Differences and similarities. Mater. Sociomedia 2012, 24, 100–105. [Google Scholar] [CrossRef]
- Guo, R.; Pittler, M.H.; Ernst, E. Herbal medicines for the treatment of COPD: A systematic review. Eur. Respir. J. 2006, 28, 330–338. [Google Scholar] [CrossRef]
- Brierley, S.M.; Kelber, O. Use of natural products in gastrointestinal therapies. Curr. Opin. Pharmacol. 2011, 11, 604–611. [Google Scholar] [CrossRef]
- Zulhendri, F.; Perera, C.O.; Tandean, S.; Abdulah, R.; Herman, H.; Christoper, A.; Chandrasekaran, K.; Putra, A.; Lesmana, R. The potential use of propolis as a primary or an adjunctive therapy in respiratory tract-related diseases and disorders: A systematic scoping review. Biomed. Pharmacother. 2022, 146, 112595. [Google Scholar] [CrossRef]
- Lofty, M. Biological activity of bee propolis in health and disease. Asian Pacific J. Cancer Prev. 2006, 7, 22–31. [Google Scholar]
- Catchpole, O.; Mitchell, K.; Bloor, S.; Davis, P.; Suddes, A. Antiproliferative activity of New Zealand propolis and phenolic compounds vs human colorectal Adenocarcinoma cells. Fitoterapia 2015, 106, 167–174. [Google Scholar] [CrossRef] [PubMed]
- Asfaram, S.; Fakhar, M.; Keighobadi, M.; Akhtari, J. Promising anti-protozoan activities of propolis (bee glue) as natural product: A review. Acta Parasitol. 2021, 66, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Ullah, A.; Munir, S.; Badshah, S.L.; Khan, N.; Ghani, L.; Poulson, B.G.; Emwas, A.H.; Jaremko, M. Important flavonoids and their role as a therapeutic agent. Molecules 2020, 25, 5243. [Google Scholar] [CrossRef] [PubMed]
- De Moura, S.A.; Ferreira, M.A.; Andrade, S.P.; Reis, M.L.; Noviello Mde, L.; Cara, D.C. Brazilian green propolis inhibits inflammatory angiogenesis in a Murine sponge model. Evid. Based Complement. Altern. Med. 2011, 2011, 182703. [Google Scholar] [CrossRef]
- Hwu, Y.J.; Lin, F.Y. Effectiveness of propolis on oral health: A meta-analysis. J. Nurs. Res. 2014, 22, 221–229. [Google Scholar] [CrossRef]
- Dodwad, V.; Kukreja, B. Propolis mouthwash: A new beginning. J. Indian Soc. Periodontol. 2011, 15, 121–125. [Google Scholar]
- Ellis, R.D.; Goodlad, J.R.; Limb, G.A.; Powell, J.J.; Thompson, R.P.H.; Punchard, N.A. Activation of nuclear factor Kappa B in Crohn’s disease. Inflamm. Res. 1998, 47, 440–445. [Google Scholar] [CrossRef]
Chemical Compositions | Bioactive Compounds | Ref. |
---|---|---|
Aromatic acids | Benzoic acids, caffeic acid, cinnamic acid, coumaric acid, ferulic acid, and gallic acid | [12,15,22,23,24,25] |
Alcohols | Glycerol, erythritol, α-cedrol, xylitol | |
Esters | Caffeic acid phenethyl ester, 2-propenoic acid methyl ester, 4,3-acetyloxycaffeate, 3,4 dimethoxy-trimethylsilyl esters, and 3-methoxy-4-cinnamate | |
Fatty and aliphatic acids | Isoferulic acid, glutamic acid, phosphoric acid, malic acid, tartaric acid, propanoic acid, butanedoic acid, and stearic acid | |
Flavonoids | Apigenin, acacetin, chrysin, galangin, genistein, hesperetin, kaempferol, kaempferide, luteolin, naringenin, pinobanksin, pinocembrin, quercetin, and tetrochrysin | |
Microelements | Aluminium (Al), copper (Cu), magnesium (Mg), zinc (Zn), silicon (Si), tin (Sn), manganese (Mn), nickel (Ni), and chrome (Cr) | |
Sugars | d-Altrose, d-glucose, maltose, and d-fructose | |
Vitamins | Vitamin A (retinol), vitamin B1 (thiamine), vitamin B2 (riboflavin), vitamin B3 (nicotinamide), vitamin B6 (pyridoxine), vitamin B9 (folic acid), vitamin C (ascorbic acid), and vitamin E (tocopherol) | |
Others | Butane, cyclohexane, cyclopentene, and guanidine |
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Zullkiflee, N.; Taha, H.; Usman, A. Propolis: Its Role and Efficacy in Human Health and Diseases. Molecules 2022, 27, 6120. https://doi.org/10.3390/molecules27186120
Zullkiflee N, Taha H, Usman A. Propolis: Its Role and Efficacy in Human Health and Diseases. Molecules. 2022; 27(18):6120. https://doi.org/10.3390/molecules27186120
Chicago/Turabian StyleZullkiflee, Nadzirah, Hussein Taha, and Anwar Usman. 2022. "Propolis: Its Role and Efficacy in Human Health and Diseases" Molecules 27, no. 18: 6120. https://doi.org/10.3390/molecules27186120