Antimicrobial Activity of Propolis from the Brazilian Stingless Bees Melipona quadrifasciata anthidioides and Scaptotrigona depilis (Hymenoptera, Apidae, Meliponini)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of the Ethanol Extract of Propolis
2.2. Analyses by High-Performance Liquid Chromatography Coupled to Diode Array Detector and Mass Spectrometry (HPLC-DAD-MS)
2.3. Antimicrobial Activity
2.4. Statistical Analysis
3. Results
3.1. Chemical Composition by HPLC-DAD-MS
3.2. Antimicrobial Activity
4. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- Camargo, J.M.F.; Pedro, S.R.M.; Melo, G.A.R. Meliponini Lepeletier, 1836. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region-Online Version. Moure, J.S., Urban, D., Melo, G.A.R., Eds.; 2013. Available online: http://moure.cria.org.br/catalogue (accessed on 12 February 2021).
- Slaa, E.J.; Chaves, L.A.S.; Malagodi-Braga, K.S.; Hofstede, F.E. Stingless bees in applied pollination: Practice and perspectives. Apidologie 2006, 37, 293–315. [Google Scholar] [CrossRef] [Green Version]
- Lavinas, F.C.; Macedo, E.H.B.; Sá, G.B.; Amaral, A.C.F.; Silva, J.; Azevedo, M.; Vieira, B.A.; Domingos, T.F.S.; Vermelho, A.B.; Carneiro, C.S.; et al. Brazilian stingless bee propolis and geopropolis: Promising sources of biologically active compounds. Rev. Bras. Farm. 2018, 29, 389–399. [Google Scholar] [CrossRef]
- Sforcin, J.M. Biological Properties and Therapeutic Applications of Propolis. Phytother. Res. 2016, 30, 894–905. [Google Scholar] [CrossRef] [PubMed]
- Zabaiou, N.; Fouache, A.; Trousson, A.; Baron, S.; Zellagui, A.; Lahouel, M.; Lobaccaro, J.-M.A. Biological properties of propolis extracts: Something new from an ancient product. Chem. Phys. Lipids 2017, 207, 214–222. [Google Scholar] [CrossRef]
- Popova, M.; Trusheva, B.; Bankova, V. Propolis of stingless bees: A phytochemist’s guide through the jungle of tropical biodiversity. Phytomedicine 2019, 86, 153098. [Google Scholar] [CrossRef]
- Osés, S.M.; Marcos, P.; Azofra, P.; De Pablo, A.; Fernández-Muíño, M.Á.; Sancho, M.T. Phenolic Profile, Antioxidant Capacities and Enzymatic Inhibitory Activities of Propolis from Different Geographical Areas: Needs for Analytical Harmonization. Antioxidants 2020, 9, 75. [Google Scholar] [CrossRef] [Green Version]
- Bankova, V. Chemical diversity of propolis and the problem of standardization. J. Ethnopharmacol. 2005, 100, 114–117. [Google Scholar] [CrossRef]
- Przybyłek, I.; Karpiński, T.M. Antibacterial Properties of Propolis. Molecules 2019, 24, 2047. [Google Scholar] [CrossRef] [Green Version]
- Salatino, A.; Teixeira, E.; Negri, G.; Message, D. Origin and Chemical Variation of Brazilian Propolis. Evid. -Based Complement. Altern. Med. 2005, 2, 33–38. [Google Scholar] [CrossRef] [Green Version]
- Bankova, V.; Popova, M.; Trusheva, B. Propolis volatile compounds: Chemical diversity and biological activity: A review. Chem. Cent. J. 2014, 8, 28. [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, 19610–19632. [Google Scholar] [CrossRef] [Green Version]
- Velikova, M.; Bankova, V.; Tsvetkova, I.; Kujumgiev, A.; Marcucci, M. Antibacterial ent-kaurene from Brazilian propolis of native stingless bees. Fitoterapia 2000, 71, 693–696. [Google Scholar] [CrossRef]
- Sawaya, A.C.H.F. Composition and antioxidant activity of propolis from three species of Scaptotrigona stingless bees. J. ApiProduct ApiMedical Sci. 2009, 1, 37–42. [Google Scholar] [CrossRef]
- Bonamigo, T.; Campos, J.F.; Alfredo, T.M.; Balestieri, J.B.P.; Cardoso, C.A.L.; Paredes-Gamero, E.J.; de Picoli Souza, K.; Dos Santos, E.L. Antioxidant, Cytotoxic, and Toxic Activities of Propolis from Two Native Bees in Brazil: Scaptotrigona depilis and Melipona quadrifasciata anthidioides. Oxidative Med. Cell. Longev. 2017, 2017, 1038153. [Google Scholar] [CrossRef] [Green Version]
- Silva, J.C.; Rodrigues, S.; Feás, X.; Estevinho, L.M. Antimicrobial activity, phenolic profile and role in the inflammation of propolis. Food Chem. Toxicol. 2012, 50, 1790–1795. [Google Scholar] [CrossRef]
- Reichert, C.L.; Silva, D.; Carollo, C.A.; Weffort-Santos, A.M.; Santos, C. Metabolic profiling and correlation analysis for the determination of killer compounds of proliferating and clonogenic HRT-18 colon cancer cells from Lafoensia pacari. J. Ethnopharmacol. 2018, 224, 541–552. [Google Scholar] [CrossRef]
- Dutra, R.P.; Abreu, B.V.D.B.; Cunha, M.S.; Batista, M.C.A.; Torres, L.M.B.; Nascimento, F.R.F.; Ribeiro, M.N.S.; Guerra, R.N.M. Phenolic Acids, Hydrolyzable Tannins, and Antioxidant Activity of Geopropolis from the Stingless Bee Melipona fasciculata Smith. J. Agric. Food Chem. 2014, 62, 2549–2557. [Google Scholar] [CrossRef]
- Silva, D.B.; Okano, L.T.; Lopes, N.P.; de Oliveira, D.C. Flavanone glycosides from Bidens gardneri Bak. (Asteraceae). Phytochemistry 2013, 96, 418–422. [Google Scholar] [CrossRef]
- Jin, W.; Wang, Y.-F.; Ge, R.-L.; Shi, H.-M.; Jia, C.-Q.; Tu, P.-F. Simultaneous analysis of multiple bioactive constituents inRheum tanguticum Maxim. ex Balf. by high-performance liquid chromatography coupled to tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2007, 21, 2351–2360. [Google Scholar] [CrossRef]
- Cisilotto, J.; Sandjo, L.P.; Faqueti, L.G.; Fernandes, H.; Joppi, D.; Biavatti, M.W.; Creczynski-Pasa, T.B. Cytotoxicity mechanisms in melanoma cells and UPLC-QTOF/MS2 chemical characterization of two Brazilian stingless bee propolis: Uncommon presence of piperidinic alkaloids. J. Pharm. Biomed. Anal. 2018, 149, 502–511. [Google Scholar] [CrossRef]
- Rubinho, M.P.; de Carvalho, P.L.N.; Reis, A.L.L.E.; Ern; Reis, E.; de Alencar, S.M.; Ruiz, A.L.T.G.; de Carvalho, J.E.; Ikegaki, M. A comprehensive characterization of polyphenols by LC-ESI–QTOF-MS from Melipona quadrifasciata anthidioides geopropolis and their antibacterial, antioxidant and antiproliferative effects. Nat. Prod. Res. 2019, 34, 3139–3144. [Google Scholar] [CrossRef] [PubMed]
- Biluca, F.C.; da Silva, B.; Caon, T.; Mohr, E.T.B.; Vieira, G.N.; Gonzaga, L.V.; Vitali, L.; Micke, G.; Fett, R.; Dalmarco, E.M.; et al. Investigation of phenolic compounds, antioxidant and anti-inflammatory activities in stingless bee honey (Meliponinae). Food Res. Int. 2019, 129, 108756. [Google Scholar] [CrossRef] [PubMed]
- Campos, J.F.; dos Santos, H.F.; Bonamigo, T.; Domingues, N.L.C.; de Picoli Souza, K.; Dos Santos, E.L. Stingless Bee Propolis: New Insights for Anticancer Drugs. Oxidative Med. Cell. Longev. 2021, 2021, 2169017. [Google Scholar] [CrossRef] [PubMed]
- Cornara, L.; Biagi, M.; Xiao, J.; Burlando, B. Therapeutic Properties of Bioactive Compounds from Different Honeybee Products. Front Pharmacol. 2017, 8, 412. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Torres, A.R.; Sandjo, L.P.; Friedemann, M.T.; Tomazzoli, M.M.; Maraschin, M.; Mello, C.F.; Santos, A.R.S. Chemical characterization, antioxidant and antimicrobial activity of propolis obtained from Melipona quadrifasciata quadrifasciata and Tetragonisca angustula stingless bees. Brazilian J. Med. Biol. Res. 2018, 51, e7118. [Google Scholar] [CrossRef]
- Negri, G.; Salatino, A.; Pereira, L.L.R.; Salatino, M.L.F.; Nascimento, R.M.; Mendonça, R.Z. A highly complex stingless bee propolis: Composition and influence of the period of collection. JSFA Rep. 2022, 2, 64–80. [Google Scholar] [CrossRef]
- Popova, M.P.; Chinou, I.B.; Marekov, I.N.; Bankova, V.S. Terpenes with antimicrobial activity from Cretan propolis. Phytochemistry 2009, 70, 1262–1271. [Google Scholar] [CrossRef]
- Chimshirova, R.; Popova, M.; Chakir, A.; Valcheva, V.; Dimitrov, S.; Trusheva, B.; Romane, A.; Bankova, V. Antimicrobial Triterpenoids and Ingol Diterpenes from Propolis of Semi-Arid Region of Morocco. Molecules 2022, 27, 2206. [Google Scholar] [CrossRef]
- Islam, M.T.; da Mata, A.M.; de Aguiar, R.P.; Paz, M.F.; de Alencar, M.V.; Ferreira, P.M.; de Carvalho Melo-Cavalcante, A.A. Therapeutic Potential of Essential Oils Focusing on Diterpenes. Phytother. Res. 2016, 30, 1420–1444. [Google Scholar] [CrossRef]
- Grecka, K.; Kuś, P.M.; Okińczyc, P.; Worobo, R.W.; Walkusz, J.; Szweda, P. The Anti-Staphylococcal Potential of Ethanolic Polish Propolis Extracts. Molecules 2019, 24, 1732. [Google Scholar] [CrossRef]
- Cushnie, T.P.T.; Lamb, A.J. Recent advances in understanding the antibacterial properties of flavonoids. Int. J. Antimicrob. Agents 2011, 38, 99–107. [Google Scholar] [CrossRef]
- Corradini, E.; Foglia, P.; Giansanti, P.; Gubbiotti, R.; Samperi, R.; Lagana, A. Flavonoids: Chemical properties and analytical methodologies of identification and quantitation in foods and plants. Nat. Prod. Res. 2011, 25, 469–495. [Google Scholar] [CrossRef]
- Seleem, D.; Pardi, V.; Murata, R.M. Review of flavonoids: A diverse group of natural compounds with anti-Candida albicans activity in vitro. Arch. Oral Biol. 2017, 76, 76–83. [Google Scholar] [CrossRef]
- Haghdoost, N.S.; Salehi, T.Z.; Khosravi, A.; Sharifzadeh, A. Antifungal activity and influence of propolis against germ tube formation as a critical virulence attribute by clinical isolates of Candida albicans. J. Mycol. Med. 2016, 26, 298–305. [Google Scholar] [CrossRef]
- Gucwa, K.; Kusznierewicz, B.; Milewski, S.; Van Dijck, P.; Szweda, P. Antifungal Activity and Synergism with Azoles of Polish Propolis. Pathogens 2018, 7, 56. [Google Scholar] [CrossRef]
Microorganisms | Reference | Origin |
---|---|---|
Bacteria | ||
Staphylococcus aureus | ATCC® 6538™ | Reference culture |
Methicillin-resistant Staphylococcus aureus | ESA 175 | Pus |
Methicillin-resistant Staphylococcus aureus | ESA 159 | Expectoration |
Enterococcus faecalis | ATCC® 43300™ | Reference culture |
Vancomycin-resistant Enterococcus faecalis | ESA 201 | Urine |
Vancomycin-resistant Enterococcus faecalis | ESA 361 | Rectal swabs |
Escherichia coli | ATCC® 29998™ | Reference culture |
Cephalosporin-resistant Escherichia coli | ESA 37 | Urine |
Cephalosporin-resistant Escherichia coli | ESA 54 | Hemoculture |
Pseudomonas aeruginosa | ATCC® 15442™ | Reference culture |
Imipenem-resistant Pseudomonas aeruginosa | ESA 22 | Expectoration |
Imipenem-resistant Pseudomonas aeruginosa | ESA 23 | Gingival exudates |
Fungi | ||
Cryptococcus neoformans | ATCC® 32264 | Reference culture |
Amphotericin B-resistant Cryptococcus neoformans | ESA 211 | Blood |
Amphotericin B-resistant Cryptococcus neoformans | ESA 105 | Skin biopsy |
Candida albicans | ATCC® 10231™ | Reference culture |
Amphotericin B-resistant Candida albicans | ESA 100 | Feces |
Amphotericin B-resistant Candida albicans | ESA 97 | Urine |
Peak | RT (min) | UV (nm) | Molecular Formula | [M-H]- (m/z) | MS/MS (m/z) | Compound | EEP-M | EEP-S |
---|---|---|---|---|---|---|---|---|
1 | 1.2 | 270 | C13H16O10 | 331.0677 | 169 | O-galloyl hexoside | + | - |
2 | 1.2 | 270 | C20H20O14 | 483.0781 | 169 | di-O-galloyl hexoside | + | - |
3 | 1.2 | 270 | C27H22O18 | 633.0749 | 301, 275, 249, 169 | O-galloyl-HHDP hexoside | + | - |
4 | 1.3 | 270 | C20H20O14 | 483.0782 | 169 | di-O-galloyl hexoside | + | - |
5 | 2.2 | 269 | C7H6O5 | 169.0127 | - | Gallic acid st | + | - |
6 | 16.4 | 254, 366 | C14H6O8 | 300.9990 | 245, 229 | Ellagic acid st | + | - |
7 | 17.5 | 283, 310 | C22H22O12 | 477.1038 | 331, 313, 271, 241, 169 | O-coumaroyl O-galloyl hexoside | + | - |
8 | 18.3 | 290, 310 | C22H22O12 | 477.1054 | 331, 313, 265, 205, 169 | O-coumaroyl O-galloyl hexoside | + | - |
9 | 18.9 | 289, 333 (sh) | C15H12O6 | 287.0571 | 259, 277, 173 | Eriodictyol | + | - |
10 | 19.3 | 286, 310 | C29H26O16 | 629.1166 | 465, 459, 316, 295, 271, 211, 169 | O-coumaroyl di-O-galloyl hexoside | + | - |
11 | 20.1 | 278 | C20H20O11 | 435.0950 | 169 | Gallic acid derivative | + | - |
12 | 22.9 | 281, 308 (sh) | C20H24O6 | 359.1502 | 329, 159 | Unknown | + | - |
13 | 24.9 | 282 | C22H22O11 | 461.1088 | 313, 253, 211, 189, 169, 161 | O-cinnamoyl O-galloyl hexoside | + | - |
14 | 26.1 | 279 | C29H26O15 | 613.1214 | 465, 313, 271, 211, 169 | O-cinnamoyl di-O-galloyl hexoside | + | - |
15 | 26.3 | 281, 308 | C43H34O24 | 933.1368 | 615, 169 | O-coumaroyl tetra-O-galloyl hexoside | + | - |
16 | 26.5 | 300, 312 | C24H24O10 | 471.1292 | 307, 265, 205, 187, 163, 145 | di-O-coumaroyl hexoside | + | - |
17 | 27.1 | 288, 325 (sh) | C15H12O5 | 271.0607 | 151 | Naringenin | + | - |
18 | 28.5 | 290, 311 | C31H28O14 | 623.1412 | 477, 459, 313, 271, 169 | di-O-coumaroyl O-galloyl hexoside | + | - |
19 | 29.3 | 292, 310 | C29H26O13 | 581.1310 | 417, 187, 169, 163 | O-coumaroyl O-galloyl O-benzoyl hexoside | + | - |
20 | 29.4 | 288, 310 | C22H22O9 | 429.1196 | 187, 163, 145 | Coumaric acid derivative | + | - |
21 | 29.5 | 290, 335 (sh) | C16H14O6 | 301.0726 | 273, 258, 179, 165 | O-methyl eriodictyol | + | - |
22 | 29.8 | 286 | C23H20O7 | 407.1141 | 313, 285, 245, 201, 177 | Unknown | + | - |
23 | 30.5 | 288, 320 (sh) | C31H30O13 | 609.1642 | 581, 441, 307, 283, 273, 179 | Unknown | + | - |
24 | 30.8 | 280, 320 (sh) | C22H26O7 | 401.1615 | 326, 205, 190 | Unknown | + | - |
25 | 31.1 | 284, 315 | C24H24O9 | 455.1369 | 187, 163, 145 | O-coumaroyl O-cynamoyl hexoside | + | - |
26 | 31.4 | 292 | C23H20O7 | 407.1161 | 313, 285, 245, 203, 177, 151 | Unknown | + | - |
27 | 31.7 | 281, 312 | C31H28O13 | 607.1485 | 461, 443, 313, 271, 211, 169 | O-coumaroyl O-cinnamoyl O-galloyl hexoside | + | - |
28 | 32.9 | 286, 328 (sh) | C16H14O5 | 285.0788 | 165 | O-methyl naringenin | + | - |
29 | 33.1 | 289 | C24H22O7 | 421.1320 | 393, 363, 299, 271, 165 | Unkown | + | - |
30 | 33.7 | 295 | C24H22O7 | 421.1328 | 393, 363, 299, 285, 271, 179, 165 | Unkown | + | - |
31 | 35.9 | 272 | C20H32O3 | 319,2313 | - | Diterpene | + | - |
32 | 36.2 | 275 | C20H32O3 | 319.2314 | - | Diterpene | + | - |
33 | 36.2 | 275 | C20H32O3 | 319.2314 | - | Diterpene | + | - |
34 | 38.1 | 284 | C20H28O2 | 299.2037 | - | Diterpene | + | - |
35 | 39.2 | - | C22H34O4 | 365.2405 | 301 | Unknown | + | - |
36 | 39.4 | 284 | C21H28O3 | 327.1987 | 312, 297, 201 | Unknown | + | - |
37 | 40.0 | - | C30H48O4 | 471.3494 | 453, 441, 427, 407 | Triterpene | + | + |
38 | 41.1 | - | C30H46O4 | 469.3337 | 451, 439, 421, 407 | Triterpene | + | + |
39 | 41.7 | 254 | C20H30O2 | 301.2184 | 283, 229 | Abietic acid | + | - |
40 | 42.2 | 275 | C23H34O2 | 341.2499 | 299, 191 | Unknown | + | + |
41 | 42.7 | - | C30H48O4 | 471.3467 | 425, 357 | Triterpene | + | + |
42 | 43.4 | 276 | C23H36O2 | 343.2653 | 301, 285 | Unknown | + | + |
43 | 44.5 | - | C31H50O3 | 469.3676 | - | Unknown | + | + |
44 | 44.8 | 275 | C21H36O2 | 319.2649 | 277 | Unknown | + | + |
46 | 44.9 | - | C24H34O3 | 369.2421 | 325 | Unknown | + | + |
47 | 48.3 | 275 | C23H38O2 | 345.2801 | 303 | Unknown | + | + |
Microorganisms (Bacteria) | EEP-M (mg/mL) | EEP-S (mg/mL) | Gentamicin (μg/mL) | |||
---|---|---|---|---|---|---|
MIC | MBC | MIC | MBC | MIC | MBC | |
Staphylococcus aureus ATCC® 6538™ | 3.00 ± 0.14 a | 4.33 ± 0.22 A | 1.67 ± 0.17 b | 2.25 ± 0.14 B | 1.67 ± 0.17 c | 2.00 ± 0.29 C |
Methicillin-resistant Staphylococcus aureus ESA 175 | 3.58 ± 0.30 a | 5.00 ± 0.14 A | 2.00 ± 0.29 b | 3.08 ± 0.08 B | 1.83 ± 0.17 c | 2.67 ± 0.17 C |
Methicillin-resistant Staphylococcus aureus ESA 159 | 3.92 ± 0.08 a | 5.50 ± 0.28 A | 2.67 ± 0.17 b | 4.17 ± 0.17 B | 2.00 ± 0.29 c | 2.50 ± 0.29 C |
Enterococcus faecalis ATCC® 43300™ | 4.75 ± 0.54 a | 6.92 ± 0.22 A | 3.00 ± 0.29 b | 3.75 ± 0.14 B | 2.17 ± 0.17 c | 2.83 ± 0.30 C |
Vancomycin-resistant Enterococcus faecalis ESA 201 | 5.33 ± 0.16 a | 7.17 ± 0.44 A | 3.50 ± 0.29 b | 5.17 ± 0.17 B | 2.33 ± 0.17 c | 3.25 ± 0.14 C |
Vancomycin-resistant Enterococcus faecalis ESA 361 | 5.83 ± 0.44 a | 7.50 ± 0.52 A | 4.67 ± 0.17 a | 6.5 ± 0.29 A | 2.67 ± 0.17 b | 3.33 ± 0.17 B |
Escherichia coli ATCC® 29998™ | 6.00 ± 0.30 a | 9.83 ± 0.44 A | 3.50 ± 0.29 b | 6.33 ± 0.17 B | 4.09 ± 0.08 c | 4.58 ± 0.30 C |
Cephalosporin-resistant Escherichia coli ESA 37 | 7.25 ± 0.14 a | 10.50 ± 0.29 A | 5.75 ± 0.14 b | 8.33 ± 0.33 B | 4.67 ± 0.17 c | 4.67 ± 0.22 C |
Cephalosporins-resistant Escherichia coli ESA 54 | 7.75 ± 0.14 a | 11.17 ± 0.22 A | 6.50 ± 0.29 b | 8.83 ± 0.44 B | 4.42 ± 0.08 c | 4.92 ± 0.08 C |
Pseudomonas aeruginosa ATCC® 15442™ | 8.42 ± 0.30 a | 12.00 ± 0.50 A | 6.83 ± 0.17 b | 9.50 ± 0.38 B | 4.75 ± 0.14 c | 5.00 ± 0.29 C |
Imipenem-resistant Pseudomonas aeruginosa ESA 22 | 9.33 ± 0.33 a | 12.58 ± 0.30 A | 8.25 ± 0.38 a | 11.08 ± 0.08 B | 5.67 ± 0.17 b | 6.17 ± 0.17 C |
Imipenem-resistant Pseudomonas aeruginosa ESA 23 | 9.92 ± 0.68 a | 13.08 ± 0.30 A | 8.75 ± 0.43 a | 12.00 ± 0.29 A | 6.67 ± 0.33 b | 6.50 ± 0.29 B |
Microorganisms (Fungi) | EEP-M (mg/mL) | EEP-S (mg/mL) | Amphotericin B (μg/mL) | |||
---|---|---|---|---|---|---|
MIC | MFC | MIC | MFC | MIC | MFC | |
Cryptococcus neoformans ATCC® 32264 | 11.42 ± 0.30 a | 14.33 ± 0.44 A | 7.00 ± 0.29 b | 10.50 ± 0.29 B | 0.55 ± 0.03 c | 0.87 ± 0.07 C |
Amphotericin B-resistant Cryptococcus neoformans ESA 211 | 12.58 ± 0.30 a | 15.25 ± 0.14 A | 7.83 ± 0.17 b | 12.16 ± 0.17 B | 0.62 ± 0.06 c | 1.25 ± 0.14 C |
Amphotericin B-resistant Cryptococcus neoformans ESA 105 | 13.25 ± 0.14 a | 16.67 ± 0.54 A | 8.50 ± 0.57 b | 12.33 ± 0.17 B | 0.63 ± 0.02 c | 1.67 ± 0.22 C |
Candida albicans ATCC® 10231™ | 14.25 ± 0.14 a | 18.42 ± 0.30 A | 8.50 ± 0.29 b | 13.00 ± 0.76 B | 0.72 ± 0.04 c | 0.92 ± 0.16 C |
Amphotericin B-resistant Candida albicans ESA 100 | 15.75 ± 0.38 a | 19.58 ± 0.30 A | 10.50 ± 0.29 b | 14.83 ± 0.17 B | 0.82 ± 0.04 c | 1.67 ± 0.08 C |
Amphotericin B-resistant Candida albicans ESA 97 | 16.50 ± 0.28 a | 20.75 ± 0.14 A | 11.67 ± 0.17 b | 16.00 ± 0.29 B | 0.92 ± 0.02 c | 1.75 ± 0.14 C |
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Campos, J.F.; Bonamigo, T.; Rocha, P.d.S.d.; Paula, V.M.B.; Santos, U.P.d.; Balestieri, J.B.P.; Silva, D.B.; Carollo, C.A.; Estevinho, L.M.; de Picoli Souza, K.; et al. Antimicrobial Activity of Propolis from the Brazilian Stingless Bees Melipona quadrifasciata anthidioides and Scaptotrigona depilis (Hymenoptera, Apidae, Meliponini). Microorganisms 2023, 11, 68. https://doi.org/10.3390/microorganisms11010068
Campos JF, Bonamigo T, Rocha PdSd, Paula VMB, Santos UPd, Balestieri JBP, Silva DB, Carollo CA, Estevinho LM, de Picoli Souza K, et al. Antimicrobial Activity of Propolis from the Brazilian Stingless Bees Melipona quadrifasciata anthidioides and Scaptotrigona depilis (Hymenoptera, Apidae, Meliponini). Microorganisms. 2023; 11(1):68. https://doi.org/10.3390/microorganisms11010068
Chicago/Turabian StyleCampos, Jaqueline Ferreira, Thaliny Bonamigo, Paola dos Santos da Rocha, Vanessa Marina Branco Paula, Uilson Pereira dos Santos, José Benedito Perrella Balestieri, Denise Brentan Silva, Carlos Alexandre Carollo, Leticia M. Estevinho, Kely de Picoli Souza, and et al. 2023. "Antimicrobial Activity of Propolis from the Brazilian Stingless Bees Melipona quadrifasciata anthidioides and Scaptotrigona depilis (Hymenoptera, Apidae, Meliponini)" Microorganisms 11, no. 1: 68. https://doi.org/10.3390/microorganisms11010068
APA StyleCampos, J. F., Bonamigo, T., Rocha, P. d. S. d., Paula, V. M. B., Santos, U. P. d., Balestieri, J. B. P., Silva, D. B., Carollo, C. A., Estevinho, L. M., de Picoli Souza, K., & Santos, E. L. d. (2023). Antimicrobial Activity of Propolis from the Brazilian Stingless Bees Melipona quadrifasciata anthidioides and Scaptotrigona depilis (Hymenoptera, Apidae, Meliponini). Microorganisms, 11(1), 68. https://doi.org/10.3390/microorganisms11010068