Journal of Food and Nutrition Research
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Journal of Food and Nutrition Research. 2019, 7(10), 725-735
DOI: 10.12691/jfnr-7-10-6
Open AccessArticle

A Great Concern Regarding the Authenticity Identification and Quality Control of Chinese Propolis and Brazilian Green Propolis

Shengwei Sun1, Jian He1, Meijuan Liu1, Guangling Yin1 and Xuguang Zhang1,

1Science and Technology Centre, By-Health Co. Ltd, No. 3 Kehui 3rd Street, No. 99 Kexue Avenue Central, Science City, Luogang District, Guangzhou 510000, China

Pub. Date: October 23, 2019

Cite this paper:
Shengwei Sun, Jian He, Meijuan Liu, Guangling Yin and Xuguang Zhang. A Great Concern Regarding the Authenticity Identification and Quality Control of Chinese Propolis and Brazilian Green Propolis. Journal of Food and Nutrition Research. 2019; 7(10):725-735. doi: 10.12691/jfnr-7-10-6

Abstract

Propolis (bee glue) is a natural resin mixture produced by honey bees and it is composed of substances collected from parts of plants, buds and exudates. The composition of propolis varies primary on the geographical locations of the ingredients obtained by the bees. A series of biological properties of propolis including anti-microbial, immunostimulatory, anti-inflammatory, anti-tumor and anti-oxidation activities have been reported in relation to their chemical composition, plant origin and geographical area. This review collates the scientific literature regarding Chinese propolis and Brazilian green propolis, specifically focusing on their different constituents and biological activities. While there are known differences in composition of these two kinds of propolis, they share considerable similarity in their overall chemical composition. Importantly, techniques such as principal component analysis (PCA) and fingerprint are viable options for authenticity identification and quality control of propolis. Many of the molecular mechanisms driving various biological activities of propolis have been determined. We have also found that the biological activity of propolis mainly depends on its constituents, such as flavonoids or phenolic compounds. Each activity is regulated by a variety of biological pathways. The compounds in both Chinese propolis and Brazilian green propolis were found to participate in different biological pathways through distinct molecular mechanisms due to their diverse chemical compositions and unique structures. With the growing market interest of Brazilian green propolis in China, an evaluation between the chemical diversity and biological activity of Chinese propolis and Brazilian green propolis are in need of a review.

Keywords:
Chinese propolis Brazilian green propolis chemical diversity biological activity

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References:

[1]  Zakerkish, M., Jenabi, M., Zaeemzadeh, N., Hemmati, A. A., and Neisi, N. (2019) The Effect of Iranian Propolis on Glucose Metabolism, Lipid Profile, Insulin Resistance, Renal Function and Inflammatory Biomarkers in Patients with Type 2 Diabetes Mellitus: A Randomized Double-Blind Clinical Trial, Scientific reports 9.
 
[2]  Burdock, G. (1998) Review of the biological properties and toxicity of bee propolis (propolis), Food and Chemical toxicology 36, 347-363.
 
[3]  Sforcin, J. M., and Bankova, V. (2011) Propolis: is there a potential for the development of new drugs?, Journal of ethnopharmacology 133, 253-260.
 
[4]  Wu, Y.-W., Sun, S.-Q., Zhao, J., Li, Y., and Zhou, Q. (2008) Rapid discrimination of extracts of Chinese propolis and poplar buds by FT-IR and 2D IR correlation spectroscopy, Journal of Molecular Structure 883, 48-54.
 
[5]  Toreti, V. C., Sato, H. H., Pastore, G. M., and Park, Y. K. (2013) Recent progress of propolis for its biological and chemical compositions and its botanical origin, Evidence-based complementary and alternative medicine 2013.
 
[6]  Rubiolo, P., Casetta, C., Cagliero, C., Brevard, H., Sgorbini, B., and Bicchi, C. (2013) Populus nigra L. bud absolute: a case study for a strategy of analysis of natural complex substances, Analytical and bioanalytical chemistry 405, 1223-1235.
 
[7]  Kai, W., Shun, P., Shuai, H., Lin, H., Hongzhuan, X., Cuiping, Z., and Fuliang, H. (2013) Molecular mechanisms underlying the in vitro anti-inflammatory effects of a flavonoid-rich ethanol extract from chinese propolis (poplar type), Evidence-Based Complementray and Alternative Medicine,2013,(2013-1-15) 2013, 127672.
 
[8]  Krol, W., ., Czuba, Z., ., Scheller, S., ., Gabrys, J., ., Grabiec, S., ., and Shani, J., . (1990) Anti-oxidant property of ethanolic extract of propolis (EEP) as evaluated by inhibiting the chemiluminescence oxidation of luminol, Biochemistry International 21, 593.
 
[9]  Mirzoeva, O. K., and Calder, P. C. (1996) The effect of propolis and its components on eicosanoid production during the inflammatory response, Prostaglandins Leukotrienes & Essential Fatty Acids 55, 441.
 
[10]  Wei, Z., Ying-Hua, L., Min-Li, C., and Fu-Liang, H. (2011) Protective effects of Chinese and Brazilian propolis treatment against hepatorenal lesion in diabetic rats, Human & Experimental Toxicology 30, 1246-1255.
 
[11]  Xuan, H., Zhu, R., Li, Y., and Hu, F. (2010) Inhibitory effect of chinese propolis on phosphatidylcholine-specific phospholipase C activity in vascular endothelial cells, Evid Based Complement Alternat Med 2011, 985278.
 
[12]  Missima, F., Filho, A. A. d. S., Nunes, G. A., Bueno, P. C. P., De Sousa, J. P. B., Bastos, J. K., and Sforcin, J. M. (2007) Effect of Baccharis dracunculifolia DC (Asteraceae) extracts and its isolated compounds on macrophage activation, Journal of Pharmacy and Pharmacology 59, 463-468.
 
[13]  Cestari, S. H., Bastos, J. K., and Di Stasi, L. C. (2011) Intestinal anti-inflammatory activity of Baccharis dracunculifolia in the trinitrobenzenesulphonic acid model of rat colitis, Evidence-Based Complementary and Alternative Medicine 2011.
 
[14]  dos Santos, D. A., Fukui, M. d. J., Nanayakkara, N. D., Khan, S. I., Sousa, J. P. B., Bastos, J. K., Andrade, S. F., da Silva Filho, A. A., and Quintão, N. L. (2010) Anti-inflammatory and antinociceptive effects of Baccharis dracunculifolia DC (Asteraceae) in different experimental models, Journal of Ethnopharmacology 127, 543-550.
 
[15]  Paulino, N., Abreu, S. R. L., Uto, Y., Koyama, D., Nagasawa, H., Hori, H., Dirsch, V. M., Vollmar, A. M., Scremin, A., and Bretz, W. A. (2008) Anti-inflammatory effects of a bioavailable compound, Artepillin C, in Brazilian propolis, European Journal of Pharmacology 587, 296-301.
 
[16]  Lemos, M., De Barros, M. P., Sousa, J. P. B., Filho, A. A. d. S., Bastos, J. K., and De Andrade, S. F. (2007) Baccharis dracunculifolia, the main botanical source of Brazilian green propolis, displays antiulcer activity, Journal of Pharmacy and Pharmacology 59, 603-608.
 
[17]  da Silva Filho, A. A., de Sousa, J. P., Soares, S., Furtado, N. A., e Silva, M. L. A., Cunha, W. R., Gregório, L. E., Nanayakkara, N. D., and Bastos, J. K. (2008) Antimicrobial activity of the extract and isolated compounds from Baccharis dracunculifolia DC (Asteraceae), Zeitschrift für Naturforschung C 63, 40-46.
 
[18]  Guimarães, N. S., Mello, J. C., Paiva, J. S., Bueno, P. C., Berretta, A. A., Torquato, R. J., Nantes, I. L., and Rodrigues, T. (2012) Baccharis dracunculifolia, the main source of green propolis, exhibits potent antioxidant activity and prevents oxidative mitochondrial damage, Food and Chemical Toxicology 50, 1091-1097.
 
[19]  da Silva Filho, A., Resende, D., Fukui, M., Santos, F., Pauletti, P., Cunha, W., Silva, M., Gregório, L., Bastos, J., and Nanayakkara, N. (2009) In vitro antileishmanial, antiplasmodial and cytotoxic activities of phenolics and triterpenoids from Baccharis dracunculifolia DC (Asteraceae), Fitoterapia 80, 478-482.
 
[20]  Munari, C. C., Resende, F. A., Alves, J. M., de Sousa, J. P. B., Bastos, J. K., and Tavares, D. C. (2008) Mutagenicity and antimutagenicity of Baccharis dracunculifolia extract in chromosomal aberration assays in Chinese hamster ovary cells, Planta medica 74, 1363-1367.
 
[21]  Bankova, V. (2005) Chemical diversity of propolis and the problem of standardization, Journal of ethnopharmacology 100, 114-117.
 
[22]  Bankova, V. (2005) Recent trends and important developments in propolis research, Evidence-based complementary and alternative medicine 2, 29-32.
 
[23]  Banskota, A. H., Tezuka, Y., and Kadota, S. (2001) Recent progress in pharmacological research of propolis, Phytotherapy research 15, 561-571.
 
[24]  Bankova, V. S., de Castro, S. L., and Marcucci, M. C. (2000) Propolis: recent advances in chemistry and plant origin, Apidologie 31, 3-15.
 
[25]  Guo, X., Chen, B., Luo, L., Zhang, X., Dai, X., and Gong, S. (2011) Chemical compositions and antioxidant activities of water extracts of Chinese propolis, Journal of agricultural and food chemistry 59, 12610-12616.
 
[26]  Ahn, M.-R., Kumazawa, S., Usui, Y., Nakamura, J., Matsuka, M., Zhu, F., and Nakayama, T. (2007) Antioxidant activity and constituents of propolis collected in various areas of China, Food Chemistry 101, 1383-1392.
 
[27]  Zhou, J., Li, Y., Zhao, J., Xue, X., Wu, L., and Chen, F. (2008) Geographical traceability of propolis by high-performance liquid-chromatography fingerprints, Food Chemistry 108, 749-759.
 
[28]  Park, Y. K., Alencar, S. M., and Aguiar, C. L. (2002) Botanical origin and chemical composition of Brazilian propolis, Journal of Agricultural and Food Chemistry 50, 2502-2506.
 
[29]  Szliszka, E., Zydowicz, G., Mizgala, E., and Krol, W. (2012) Artepillin C (3, 5-diprenyl-4-hydroxycinnamic acid) sensitizes LNCaP prostate cancer cells to TRAIL-induced apoptosis, International Journal of Oncology 41, 818-828.
 
[30]  Moura, S. A. L. d., Negri, G., Salatino, A., Lima, L. D. d. C., Dourado, L. P. A., Mendes, J. B., Andrade, S. P., Ferreira, M. A. N. D., and Cara, D. C. (2011) Aqueous extract of Brazilian green propolis: primary components, evaluation of inflammation and wound healing by using subcutaneous implanted sponges, Evidence-Based Complementary and Alternative Medicine 2011.
 
[31]  Nakajima, Y., Shimazawa, M., Mishima, S., and Hara, H. (2007) Water extract of propolis and its main constituents, caffeoylquinic acid derivatives, exert neuroprotective effects via antioxidant actions, Life sciences 80, 370-377.
 
[32]  Szliszka, E., Kucharska, A. Z., Sokół-Łętowska, A., Mertas, A., Czuba, Z. P., and Król, W. (2013) Chemical composition and anti-inflammatory effect of ethanolic extract of Brazilian green propolis on activated J774A. 1 macrophages, Evidence-Based Complementary and Alternative Medicine 2013.
 
[33]  Cui-ping, Z., Shuai, H., Wen-ting, W., Shun, P., Xiao-ge, S., Ya-jing, L., and Fu-liang, H. (2014) Development of high-performance liquid chromatographic for quality and authenticity control of Chinese propolis, Journal of food science 79, C1315-C1322.
 
[34]  Szliszka, E., Zydowicz, G., Janoszka, B., Dobosz, C., Kowalczyk-Ziomek, G., and Krol, W. (2011) Ethanolic extract of Brazilian green propolis sensitizes prostate cancer cells to TRAIL-induced apoptosis, International Journal of Oncology 38, 941-953.
 
[35]  Alencar, S., Oldoni, T., Castro, M., Cabral, I., Costa-Neto, C., Cury, J., Rosalen, P., and Ikegaki, M. (2007) Chemical composition and biological activity of a new type of Brazilian propolis: red propolis, Journal of ethnopharmacology 113, 278-283.
 
[36]  Kalogeropoulos, N., Konteles, S. J., Troullidou, E., Mourtzinos, I., and Karathanos, V. T. (2009) Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus, Food chemistry 116, 452-461.
 
[37]  de Funari, C. S., de Oliveira Ferro, V., and Mathor, M. B. (2007) Analysis of propolis from Baccharis dracunculifolia DC. (Compositae) and its effects on mouse fibroblasts, Journal of ethnopharmacology 111, 206-212.
 
[38]  Lima, B., Tapia, A., Luna, L., Fabani, M. P., Schmeda-Hirschmann, G., Podio, N. S., Wunderlin, D. A., and Feresin, G. E. (2009) Main flavonoids, DPPH activity, and metal content allow determination of the geographical origin of propolis from the province of San Juan (Argentina), Journal of agricultural and food chemistry 57, 2691-2698.
 
[39]  Cao, Y., Wang, Y., and Yuan, Q. (2004) Analysis of flavonoids and phenolic acid in propolis by capillary electrophoresis, Chromatographia 59, 135-140.
 
[40]  Jiang, L., Fang, G., Zhang, Y., Cao, G., and Wang, S. (2008) Analysis of flavonoids in propolis and Ginkgo biloba by micellar electrokinetic capillary chromatography, Journal of agricultural and food chemistry 56, 11571-11577.
 
[41]  Campo Fernández, M., Cuesta-Rubio, O., Rosado Perez, A. s., Montes De Oca Porto, R., Márquez Hernández, I., Piccinelli, A. L., and Rastrelli, L. (2008) GC-MS determination of isoflavonoids in seven red Cuban propolis samples, Journal of agricultural and food chemistry 56, 9927-9932.
 
[42]  Gardana, C., Scaglianti, M., Pietta, P., and Simonetti, P. (2007) Analysis of the polyphenolic fraction of propolis from different sources by liquid chromatography–tandem mass spectrometry, Journal of Pharmaceutical and Biomedical Analysis 45, 390-399.
 
[43]  Lu, Y., Wu, C., and Yuan, Z. (2004) Determination of hesperetin, cinnamic acid and nicotinic acid in propolis with micellar electrokinetic capillary chromatography, Fitoterapia 75, 267-276.
 
[44]  Pellati, F., Orlandini, G., Pinetti, D., and Benvenuti, S. (2011) HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts, Journal of Pharmaceutical and Biomedical Analysis 55, 934-948.
 
[45]  Sun, S., Liu, M., He, J., Li, K., Zhang, X., and Yin, G. (2019) Identification and Determination of Seven Phenolic Acids in Brazilian Green Propolis by UPLC-ESI-QTOF-MS and HPLC, Molecules 24, 1791.
 
[46]  Jiang, X., Tian, J., Zheng, Y., Zhang, Y., Wu, Y., Zhang, C., Zheng, H., and Hu, F. (2019) A New Propolis Type from Changbai Mountains in North-east China: Chemical Composition, Botanical Origin and Biological Activity, Molecules 24, 1369.
 
[47]  Chang, R., Piló-Veloso, D., Morais, S. A., and Nascimento, E. A. (2008) Analysis of a Brazilian green propolis from Baccharis dracunculifolia by HPLC-APCI-MS and GC-MS, Revista Brasileira de Farmacognosia 18, 549-556.
 
[48]  Castaldo, S., and Capasso, F. (2002) Propolis, an old remedy used in modern medicine, Fitoterapia 73, S1-S6.
 
[49]  Xu, L., Yan, S.-M., Cai, C.-B., and Yu, X.-P. (2013) Untargeted detection and quantitative analysis of poplar balata (PB) in Chinese propolis by FT-NIR spectroscopy and chemometrics, Food chemistry 141, 4132-4137.
 
[50]  Nunes, C. A., and Guerreiro, M. C. (2012) Characterization of Brazilian green propolis throughout the seasons by headspace GC/MS and ESI-MS, Journal of the Science of Food and Agriculture 92, 433-438.
 
[51]  Huang, S., Zhang, C.-P., Li, G., Sun, Y.-Y., Wang, K., and Hu, F.-L. (2014) Identification of catechol as a new marker for detecting propolis adulteration, Molecules 19, 10208-10217.
 
[52]  Zhang, C.-p., Zheng, H.-q., Liu, G., and Hu, F.-l. (2011) Development and validation of HPLC method for determination of salicin in poplar buds: Application for screening of counterfeit propolis, Food Chemistry 127, 345-350.
 
[53]  Stan, L., Mărghitaş, L. A., and Dezmirean, D. (2011) Quality criteria for propolis standardization, Scientific Papers Animal Science and Biotechnologies 44, 137-140.
 
[54]  Sawaya, A. C., Cunha, I. B., Marcucci, M. C., de Oliveira Rodrigues, R. F., and Eberlin, M. N. (2006) Brazilian propolis of Tetragonisca angustula and Apis mellifera, Apidologie 37, 398-407.
 
[55]  Sawaya, A. C., Tomazela, D. M., Cunha, I. B., Bankova, V. S., Marcucci, M. C., Custodio, A. R., and Eberlin, M. N. (2004) Electrospray ionization mass spectrometry fingerprinting of propolis, Analyst 129, 739-744.
 
[56]  Abdi, H., and Williams, L. J. (2010) Principal component analysis, Wiley interdisciplinary reviews: computational statistics 2, 433-459.
 
[57]  Wold, S., Esbensen, K., and Geladi, P. (1987) Principal component analysis, Chemometrics and intelligent laboratory systems 2, 37-52.
 
[58]  Yang, C., Luo, L., Zhang, H., Yang, X., Lv, Y., and Song, H. (2010) Common aroma-active components of propolis from 23 regions of China, Journal of the Science of Food and Agriculture 90, 1268-1282.
 
[59]  Cheng, H., Qin, Z., Guo, X., Hu, X., and Wu, J. (2013) Geographical origin identification of propolis using GC–MS and electronic nose combined with principal component analysis, Food research international 51, 813-822.
 
[60]  Sawaya, A. C. H. F., da Silva Cunha, I. B., Marcucci, M. C., Aidar, D. S., Silva, E. C. A., Carvalho, C. A. L., and Eberlin, M. N. (2007) Electrospray ionization mass spectrometry fingerprinting of propolis of native Brazilian stingless bees, Apidologie 38, 93-103.
 
[61]  Sawaya, A. C., Abdelnur, P. V., Eberlin, M. N., Kumazawa, S., Ahn, M.-R., Bang, K.-S., Nagaraja, N., Bankova, V. S., and Afrouzan, H. (2010) Fingerprinting of propolis by easy ambient sonic-spray ionization mass spectrometry, Talanta 81, 100-108.
 
[62]  Volpi, N., and Bergonzini, G. (2006) Analysis of flavonoids from propolis by on-line HPLC–electrospray mass spectrometry, Journal of Pharmaceutical and Biomedical Analysis 42, 354-361.
 
[63]  Corrêa, W. R., López, B. G.-C., Prado, S. C. d., Cunha, I. B. d. S., Sawaya, A. C. H. F., and Salvador, M. J. (2016) ESI-MS fingerprinting of residues of green propolis, and evaluation of their antioxidant and antimicrobial activities, Journal of Apicultural Research 55, 1-7.
 
[64]  Milojković Opsenica, D., Ristivojević, P., Trifković, J., Vovk, I., Lušić, D., and Tešić, Ž. (2016) TLC fingerprinting and pattern recognition methods in the assessment of authenticity of poplar-type propolis, Journal of chromatographic science 54, 1077-1083.
 
[65]  Tang, T. x., Guo, W. y., Xu, Y., Zhang, S. m., Xu, X. j., Wang, D. m., Zhao, Z. m., Zhu, L. p., and Yang, D. p. (2014) Thin-layer chromatographic identification of Chinese propolis using chemometric fingerprinting, Phytochemical analysis 25, 266-272.
 
[66]  de Groot, A. C. (2013) Propolis: a review of properties, applications, chemical composition, contact allergy, and other adverse effects, Dermatitis 24, 263-282.
 
[67]  Król, W., Bankova, V., Sforcin, J. M., Szliszka, E., Czuba, Z., and Kuropatnicki, A. K. (2013) Propolis: properties, application, and its potential, Evidence-Based Complementary and Alternative Medicine 2013.
 
[68]  Silva-Carvalho, R., Baltazar, F., and Almeida-Aguiar, C. (2015) Propolis: a complex natural product with a plethora of biological activities that can be explored for drug development, Evidence-Based Complementary and Alternative Medicine 2015.
 
[69]  Kujumgiev, A., Tsvetkova, I., Serkedjieva, Y., Bankova, V., Christov, R., and Popov, S. (1999) Antibacterial, antifungal and antiviral activity of propolis of different geographic origin, Journal of ethnopharmacology 64, 235-240.
 
[70]  Sforcin, J. M. (2016) Biological properties and therapeutic applications of propolis, Phytotherapy research 30, 894-905.
 
[71]  Kuropatnicki, A. K., Szliszka, E., and Krol, W. (2013) Historical aspects of propolis research in modern times, Evidence-Based Complementary and Alternative Medicine 2013.
 
[72]  Noori, A., Al-Ghamdi, A., Ansari, M. J., Al-Attal, Y., and Salom, K. (2012) Synergistic effects of honey and propolis toward drug multi-resistant Staphylococcus aureus, Escherichia coli and Candida albicans isolates in single and polymicrobial cultures, International journal of medical sciences 9, 793.
 
[73]  Ahuja, V., and Ahuja, A. (2011) Apitherapy-A sweet approach to dental diseases. Part II: Propolis, Journal of Advanced Oral Research 2, 1-8.
 
[74]  Takaisi-Kikuni, N. B., and Schilcher, H. (1994) Electron microscopic and microcalorimetric investigations of the possible mechanism of the antibacterial action of a defined propolis provenance, Planta Medica 60, 222-227.
 
[75]  Orsi, R., Sforcin, J., Rall, V., Funari, S., Barbosa, L., and Fernandes, J. (2005) Susceptibility profile of Salmonella against the antibacterial activity of propolis produced in two regions of Brazil, Journal of Venomous Animals and Toxins including Tropical Diseases 11, 109-116.
 
[76]  Nolkemper, S., Reichling, J., Sensch, K. H., and Schnitzler, P. (2010) Mechanism of herpes simplex virus type 2 suppression by propolis extracts, Phytomedicine 17, 132-138.
 
[77]  Schnitzler, P., Neuner, A., Nolkemper, S., Zundel, C., Nowack, H., Sensch, K. H., and Reichling, J. (2010) Antiviral activity and mode of action of propolis extracts and selected compounds, Phytotherapy Research 24, S20-S28.
 
[78]  Serkedjieva, J., Manolova, N., and Bankova, V. (1992) Anti-influenza virus effect of some propolis constituents and their analogues (esters of substituted cinnamic acids), Journal of Natural Products 55, 294-297.
 
[79]  Sforcin, J. (2007) Propolis and the immune system: a review, Journal of ethnopharmacology 113, 1-14.
 
[80]  Murad, J. M., Calvi, S. A., Soares, A. M. V. C., Bankova, V., and Sforcin, J. M. (2002) Effects of propolis from Brazil and Bulgaria on fungicidal activity of macrophages against Paracoccidioides brasiliensis, Journal of Ethnopharmacology 79, 331-334.
 
[81]  Oršolić, N., and Bašić, I. (2003) Immunomodulation by water-soluble derivative of propolis: a factor of antitumor reactivity, Journal of Ethnopharmacology 84, 265-273.
 
[82]  Dimov, V., Ivanovska, N., Bankova, V., and Popov, S. (1992) Immunomodulatory action of propolis: IV. Prophylactic activity against gram-negative infections and adjuvant effect of the water-soluble derivative, Vaccine 10, 817-823.
 
[83]  Meltzer, M. S., Tucker, R. W., Sanford, K. K., and Leonard, E. J. (1975) Interaction of BCG-activated macrophages with neoplastic and nonneoplastic cell lines in vitro: quantitation of the cytotoxic reaction by release of tritiated thymidine from prelabeled target cells, Journal of the National Cancer Institute 54, 1177-1184.
 
[84]  Orsatti, C., Missima, F., Pagliarone, A., Bachiega, T. F., Búfalo, M., Araújo Jr, J., and Sforcin, J. (2010) Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice, Phytotherapy Research 24, 1141-1146.
 
[85]  Oršolić, N., Šaranović, A. B., and Bašić, I. (2006) Direct and indirect mechanism (s) of antitumour activity of propolis and its polyphenolic compounds, Planta medica 72, 20-27.
 
[86]  Chang, H., Wang, Y., Yin, X., Liu, X., and Xuan, H. (2017) Ethanol extract of propolis and its constituent caffeic acid phenethyl ester inhibit breast cancer cells proliferation in inflammatory microenvironment by inhibiting TLR4 signal pathway and inducing apoptosis and autophagy, BMC complementary and alternative medicine 17, 471.
 
[87]  Omene, C., Kalac, M., Wu, J., Marchi, E., Frenkel, K., and O’Connor, O. A. (2013) Propolis and its active component, caffeic acid phenethyl ester (CAPE), modulate breast cancer therapeutic targets via an epigenetically mediated mechanism of action, Journal of cancer science & therapy 5, 334.
 
[88]  Sawicka, D., Car, H., Borawska, M. H., and Nikliński, J. (2012) The anticancer activity of propolis, Folia Histochemica et Cytobiologica 50, 25-37.
 
[89]  Uzel, A., Önçağ, Ö., Çoğulu, D., and Gençay, Ö. (2005) Chemical compositions and antimicrobial activities of four different Anatolian propolis samples, Microbiological research 160, 189-195.
 
[90]  Sigal, L. H., and Ron, Y. (1994) Immunology and inflammation. Basic mechanisms and clinical consequences, McGaw-Hill, Inc., New York, 583.
 
[91]  Massaro, F. C., Brooks, P. R., Wallace, H. M., and Russell, F. D. (2011) Cerumen of Australian stingless bees (Tetragonula carbonaria): gas chromatography-mass spectrometry fingerprints and potential anti-inflammatory properties, Naturwissenschaften 98, 329-337.
 
[92]  Park, E.-H., Kim, S.-H., and Park, S.-S. (1996) Anti-inflammatory activity of propolis, Archives of Pharmacal Research 19, 337-341.
 
[93]  Woo, K. J., Jeong, Y.-J., Inoue, H., Park, J.-W., and Kwon, T. K. (2005) Chrysin suppresses lipopolysaccharide-induced cyclooxygenase-2 expression through the inhibition of nuclear factor for IL-6 (NF-IL6) DNA-binding activity, FEBS letters 579, 705-711.
 
[94]  Kao, T.-K., Ou, Y.-C., Raung, S.-L., Lai, C.-Y., Liao, S.-L., and Chen, C.-J. (2010) Inhibition of nitric oxide production by quercetin in endotoxin/cytokine-stimulated microglia, Life sciences 86, 315-321.
 
[95]  Wang, K., Ping, S., Huang, S., Hu, L., Xuan, H., Zhang, C., and Hu, F. (2013) Molecular mechanisms underlying the in vitro anti-inflammatory effects of a flavonoid-rich ethanol extract from Chinese propolis (poplar type), Evidence-Based Complementary and Alternative Medicine 2013.
 
[96]  Amic, D., Davidovic-Amic, D., Beslo, D., Rastija, V., Lucic, B., and Trinajstic, N. (2007) SAR and QSAR of the antioxidant activity of flavonoids, Current medicinal chemistry 14, 827-845.
 
[97]  Zhang, J., Cao, X., Ping, S., Wang, K., Shi, J., Zhang, C., Zheng, H., and Hu, F. (2015) Comparisons of ethanol extracts of Chinese propolis (poplar type) and poplar gums based on the antioxidant activities and molecular mechanism, Evidence-Based Complementary and Alternative Medicine 2015.
 
[98]  Nakanishi, I., Uto, Y., Ohkubo, K., Miyazaki, K., Yakumaru, H., Urano, S., Okuda, H., Ueda, J.-I., Ozawa, T., and Fukuhara, K. (2003) Efficient radical scavenging ability of artepillin C, a major component of Brazilian propolis, and the mechanism, Organic & biomolecular chemistry 1, 1452-1454.
 
[99]  Lotito, S. B., and Frei, B. (2006) Dietary flavonoids attenuate tumor necrosis factor α-induced adhesion molecule expression in human aortic endothelial cells structure-function relationships and activity after first pass metabolism, Journal of Biological Chemistry 281, 37102-37110.
 
[100]  Wu, W.-M., Lu, L., Long, Y., Wang, T., Liu, L., Chen, Q., and Wang, R. (2007) Free radical scavenging and antioxidative activities of caffeic acid phenethyl ester (CAPE) and its related compounds in solution and membranes: a structure–activity insight, Food Chemistry 105, 107-115.