Characterization and assessment of the antimicrobial efficacy of Algerian propolis against American foulbrood and Nosema disease in honeybee
Abstract
Aim of study: Like all insects, honeybees (Apis mellifera) are vulnerable to infectious diseases. American foulbrood and nosemosis are among the most widespread diseases affecting this species worldwide. The present study aimed to evaluate the efficacy of propolis from different beehives in Algerian apiaries against these major honeybee diseases. Area of study: Propolis harvesting was conducted in three regions of M’sila province in Algeria: Bousaada, Ouled Madhi, and Maadid. Material and methods: The chemical characterization of Algerian propolis was performed by HPLC-DAD, a simple and highly effective technique for the identification of polyphenolic compounds. Paenibacillus larvae was isolated from hives showing clinical signs of infection. The antibacterial activity of ethanolic extracts of Algerian propolis was assessed according to the Mueller-Hinton disc diffusion method, using the antibiotic oxytetracycline (OT) as a positive control. Screening of infected individuals for Nosema spp. was conducted and infection intensity was determined by spore quantification. Main results: HPLC-DAD analysis of propolis revealed the presence of 13 phytochemical compounds, suggesting a high chemical quality. All tested ethanolic propolis extracts have shown a notable inhibitory activity against diseases affecting Apis mellifera. Concerning the antagonistic activity against Paenobacillus larvae, we found that the propolis extract from the Bousaada region (EEP3) showed the largest inhibition zones (45.05±3.40 mm) followed by extracts from Ouled Madhi (EEP1; 32.05±7.30 mm) and Maadid (EEP2; 22.16±8.51 mm). Moreover, propolis treatment resulted in a clear reduction on the activity of Nosema spp. spore counts, indicating its potential effectiveness against nosemosis. Research highlights: The study highlights the chemical composition of propolis and its potential benefits for bee health, aiming to exploit it in natural pest management strategies in apiculture.
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References
Abban S, Smith B, Corona M, Cook SC, Evans JD, Chen Y, Alburaki M, 2024. Prevalence and distribution of Varroa destructorand Nosema spp. in symptomatic honey bee colonies across the USA from 2015 to 2022.Sci Rep 14, 1726 https://doi.org/10.1038/s41598-024-51514-9
Abed F, Bachir-Bouiadjra B, Haddad A, Homrani A. Abdelkader H, 2022. Etat sanitaire de l’apiculture dans trois régions du Nord-Ouest algérien: Tiaret, Relizane et Mostaganem. Papers on Life Science, Marine & Environmental Research. (1)1:1-5.
Açık MN, Karagülle B, Yakut S, et al., 2024. Production, characterization and therapeutic efficacy of egg yolk antibodies specific to Nosema ceranae. PLOS ONE. 19(2): e0297864. https://doi.org/10.1371/journal.pone.029786
Afrouzan H, Tahghighi A, Zakeri S, Es-haghi A, 2018. Chemical Composition and Antimicrobial Activities of Iranian Propolis. Iranian Biomedical Journal. 22(1) https://doi.org/10.22034/ibj.22.1.50
Altuntaş Ü, Güzel İ, Özçelik B, 2023. Phenolic Constituents, Antioxidant and Antimicrobial Activity and Clustering Analysis of Propolis Samples Based on PCA from Different Regions of Anatolia. Molecules. 28(3): 1121. https://doi.org/10.3390/molecules28031121
Alvear M, Santos E, Cabezas F, Pérez-SanMartín A, Lespinasse M, Veloz J, 2021. Geographic Area of Collection Determines the Chemical Composition and Antimicrobial Potential of Three Extracts of Chilean Propolis. Plants. 10(8):1543. https://doi.org/10.3390/plants10081543
Ansari MJ, Al-Ghamdi A, Nuru A, Ahme AM, Ayaad TH, Khan KA, Al-Waili N, 2017. Diagnosis and molecular detection of Paenibacillus larvae, the causative agent of American foulbrood in honey bees in Saudi Arabia. International Journal of Tropical Insect Science. 37 (03):137-148. https://doi.org/10.1017/S1742758417000133
Ararso Z & Legesse G, 2016. Insecticidal action of honeybees propolis extract against larvae of lesser wax moth. Agriculture and biology journal of North America. 7(6):302-306. https://doi.org/10.5251/abjna.2016.7.6.302.306
Arismendi N, Vargas M, López MD, Barría Y, Zapata N, 2018. Promising antimicrobial activity against the honeybee parasite Nosema ceranae by methanolic extracts from Chilean native plants and propolis. Journal of Apicultural Research. 57(4):522-535. https://doi.org/10.1080/00218839.2018.1453006
Bakonyi T, Derakhshifar I, Grabensteiner E, Nowotny N, 2003. Development and Evaluation of PCR Assays for the Detection of Paenibacillus larvae in Honey Samples: Comparison with Isolation and Biochemical Characterization. Applied and Environmental Microbiology, 69(3):1504-1510. https://doi.org/10.1128/AEM.69.3.1504-1510.2003
Bastos EMAF, Simone M, Jorge DM, Soares AEE, Spivak M, 2008. In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. Journal of Invertebrate Pathology. 97(3):273-281. https://doi.org/10.1016/j.jip.2007.10.007
Bilikova K, Popova M, Trusheva B, Bankova V, 2013. New anti-Paenibacillus larvae substances purified from propolis. Apidologie. 44(3):278-285. https://doi.org/10.1007/s13592-012-0178-1
Bouhala Aissam DR 2012, Inventaire des plantes mellifères dans la région de Jijel (cas d’El Kennar). Magister thesis. University of Jijel, Algeria. 14-15.
Bouzahouane H, Ayari A, Guehria I, Riah O, 2021. Propolis: Antimicrobial activity and chemical composition analysis: Properties of propolis. Journal of Microbiology, Biotechnology and Food Sciences. 10(6):e3211. https://doi.org/10.15414/jmbfs.3211
Brahimi HA, Oulebsir-Mohandkaci H, Hendel N, Sarri M, 2025. Ethnobotanical knowledge and traditional uses of propolis among the Algerian population: a comparative and multivariate analysis. Ethnobotany Research and Applications 31:57. http://dx.doi.org/10.32859/era.31.57.1-18
Choi YM, Noh DO, Cho SY, Suh HJ, Kim KM, Kim JM, 2006. Activités antioxydantes et antimicrobiennes de la propolis de plusieurs régions de Corée. LWT. 39(7):756-761. https://doi.org/10.1016/j.lwt.2005.05.015
Choukri Barour DR, 2012. Analyse de la Biodiversité des Populations d’Abeilles Mellifères Apis mellifera intermissa (Buttell-Reepen, 1906) (Hymenoptera: Apidea) dans le Nord Algérien: Morphométrie Moderne Basée sur la Configuration des Points-Repères (Landmarks). Doctoral thesis. University of Badji Mokhtar Annaba, Algeria. 17-18.
Dadoun Nedjma DR, 2021. Effets combinés de la Varroase (Varroa destructor) et de la Nosémose (Nosema sp) sur le déclin de l’abeille saharienne Apis mellifera sahariensis. Doctoral thesis. University of M’hamed Bougara Boumerdes, Algeria.44-45.
Debab M & Toumi-Benali F, 2022. Activités antimicrobienne et anthelminthique de la propolis de l’Ouest algérien. Phytothérapie. (20):224-229. https://doi.org/10.3166/phyto-2021-0288
Dos Santos FF, Morais-Urano RP, Cunha WR, De Almeida SG, Cavallari PSDSR, Manuquian, HA, Pereira HDA, Furtado R, Santos MFC, Amdrade E, Silva ML, 2022. A review on the anti-inflammatory activities of Brazilian green, brown and red propolis. Journal of Food Biochemistry. 46(10) https://doi.org/10.1111/jfbc.14350
Domínguez-Rebolledo, Á, Lemus-Flores C, Salgado Moreno S, Dzib-Cauich D, Chi-Maas D, Loeza-Concha H, 2023. Variación de la prevalencia de Varroa, Nosema y Acarapis en dos regiones del estado de Campeche, México. Abanico Veterinario. (13):1-12 https://dx.doi.org/10.21929/abavet2023
Dumitru A, Chioveanu G, Ionita M, Dobre G, Mitrea, IL, 2017. In vitro studies on using natural essential oils in treatement on Nosemosis in honey bees: determination of the therapeutic dose. Scientific Works. Series C. Veterinary Medicine. (2):165-170.
Ecem Bayram N, Gerçek YC, Bayram S, Toğar B, 2020. Effects of processing methods and extraction solvents on the chemical content and bioactive properties of propolis. Journal of Food Measurement and Characterization. 14(2):905-916. https://doi.org/10.1007/s11694-019-00340-z
El-Seedi HR, El-Wahed AAA, Naggar YA, Saeed A, Xiao J, Ullah H, Musharraf SG, Boskabady MH, Cao W, Guo Z, Daglia M, Wakil AE, Wang K, Khalifa, SAM, 2022. Insights into the Role of Natural Products in the Control of the Honey Bee Gut Parasite (Nosema spp.). Animals. (12):3062. https://doi.org/10.3390/ani12213062
Fangio MF, Orallo DE, Gende LB, Churio MS, 2019. Chemical characterization and antimicrobial activity against Paenibacillus larvae of propolis from Buenos Aires province, Argentina. Journal of Apicultural Research. 58(4):626-638. https://doi.org/10.1080/00218839.2019.1601318
Formato G, Rivera-Gomis J, Bubnic J, Martín-Hernández R, Milito M, Croppi S, Higes, M, 2022. Nosemosis Prevention and Control. Applied Sciences (12):783. https://doi.org/10.3390/app12020783
Genersch E, Forsgren E, Rauch S, Kilwinski J, Fries I, 2006. Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. International Journal of Systematic and Evolutionary Microbiology. (56): 501–511.
Giménez-Martínez P, Cugnata N, Alonso-Salces RM, Arredondo D, Antúnez K, Castro RD, Castro D, Fuselli SR, 2019. Natural molecules for the control of Paenibacillus larvae, causal agent of American foulbrood in honey bees (Apis mellifera L.). Spanish Journal of Agricultural Research. 17(3). https://doi.org/10.5424/sjar/2019173-14740
Giménez-Martínez P, Zúñiga F, Medici S, Fuselli S, Martínez J, 2024. Spent coffee grounds extract: Antimicrobial activity against Paenibacillus larvae and its effect on the expression of antimicrobial peptides in Apis mellifera. Veterinary Research Communications. 48(2):889-899. https://doi.org/10.1007/s11259-023-10256-1
Gómez-Moracho T, Durand T, Pasquaretta C, Heeb P, Lihoreau M, 2021. Artificial Diets Modulate Infection Rates by Nosema ceranae in Bumblebees. Microorganisms. 9(1):158 https://doi.org/10.3390/microorganisms9010158
Graaf DC, Alippi AM, Antúnez K, Aronstein KA, Budge G, De Koker D, De Smet L, Dingman DW, Evans JD, Foster LJ, Fünfhaus A, 2013. Standard methods for American foulbrood research. Journal of Apicultural Research. 52(1):1–28. https://doi.org/10.3896/ibra.1.52.1.11
Grubbs KJ, May DS, Sardina JA, Dermenjian RK, Wyche TP, Pinto-Tomás AA, Clardy J, Currie CR, 2021. Pollen Streptomyces Produce Antibiotic That Inhibits the Honey Bee Pathogen Paenibacillus larvae. Frontiers in Microbiology. 12:632-637. https://doi.org/10.3389/fmicb.2021.632637
Haghdoost NS, Salehi TZ, Khosravi A, Sharifzadeh A, 2016. Antifungal activity and influence of propolis against germ tube formation as a critical virulence attribute by clinical isolates of Candida albicans. Journal de Mycologie Médicale. 26(4):298-305. https://doi.org/10.1016/j.mycmed.2015.11.004
Hamdi C, Essanaa J, Sansonno L, Crotti E, Abdi K, Barbouche N, Balloi A, Gonella E, Alma A, Daffonchio D, Boudabous A, Cherif A, 2013. Genetic and Biochemical Diversity of Paenibacillus larvae Isolated from Tunisian Infected Honey Bee Broods. BioMed Research International. 1:9. https://doi.org/10.1155/2013/479893
Isidorov VA, Buczek K, Zambrowski G, Miastkowski K, Swiecicka I, 2017. In vitro study of the antimicrobial activity of European propolis against Paenibacillus larvae. Apidologie. 48(3):411-422. https://doi.org/10.1007/ s13592-16-0485-z
Kalia P, Kumar NR, Harjai K, 2013. Phytochemical Screening and Antibacterial activity of different extracts of propolis. International Journal of Pharmaceutical and Biological Research (IJPBR). 3(6).
Kappagoda S, Singh U, Blackburn BG, 2011. Antiparasitic Therapy. Mayo Clinic Proceedings. 86(6):561-583. https://doi.org/10.4065/mcp.2011.0203
Khosravi AR, Shokri H, Sohrabi N, 2014. Potential effects of Trachyspermum copticum essential oil and propolis alcoholic extract on Mep3 gene expression of Microsporum canis isolates. Journal de Mycologie Médicale. 24(3):e101-e107. https://doi.org/10.1016/j.mycmed.2014.03.003
Koc AN, Silici S, Mutlu-Sariguzel F, Sagdic O, 2007. Antifungal Activity of Propolis in Four Different Fruit Juices. Food Technology and Biotechnology. 45(1):57–61.
Kochansky J, Knox DA, Feldlaufer M, Pettis JS, 2001. Screening alternative antibiotics against oxytetracycline-susceptible and -resistant Paenibacillus larvae. Apidologie. 32(3):215-222. https://doi.org/10.1051/apido:2001123
Martín-Hernández R, Botías C, Barrios L, Martínez-Salvador A, Meana A, Mayack C, Higes M, 2011. Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema Apis infection of honeybees (Apis mellifera). Parasitology Research. 109(3):605 612. https://doi.org/10.1007/s00436-011-2292-9
Moon TD, Oberhelman RA, 2005. Antiparasitic Therapy in Children. Pediatric Clinics of North America. 52(3):917-948. https://doi.org/10.1016/j.pcl.2005.02.012
Mura A, Pusceddu M, Theodorou P, Angioni A, Floris I, Paxton RJ, Satta, A, 2020. Propolis Consumption Reduces Nosema ceranae Infection of European Honey Bees (Apis mellifera). Insects. 11(2):124. https://doi.org/10.3390/insects11020124
Murray KD & Aronstein KA, 2006. Oxytetracycline-resistance in the honeybee pathogen Paenibacillus larvae is encoded on novel plasmid pMA67. Journal of Apicultural Research. (45):207-214. https://doi.org/10.1080/00218839.2006.11101349
Ngenge TA, Emmanuel T, Maurice TF, Joseph MT, 2017. A New Spinastane-type Triterpenoid from a Cameroonian Propolis sample and Evaluation of Antibacterial and Anti-inflammatory Potential of Extracts. Journal of Chemistry and Chemical Sciences. 7(10):763-770.
Nichitoi MM, Josceanu AM, Isopescu RD, Isopencu GO, Geana EI, Ciucure CT, Lavric V, 2021. Polyphenolics profile effects upon the antioxidant and antimicrobial activity of propolis extracts. Scientific Reports. 11(1):20113. https://doi.org/10.1038/s41598-021-97130-9
Nsiangani Lusambo N, Kaimbo Wa Kaimbo D, Ngoyi Mumba DM, de-la-Torre A, 2023. Outcomes of trimethoprim/ sulfamethoxazole treatment for ocular toxoplasmosis in Congolese patients. BMC Ophthalmology. 23(1):440. https://doi.org/10.1186/s12886-023-03183-x
Obshta O, Zabrodski MW, Soomro T, Wilson G, Masood F, Thebeau J, Silva MCB, Biganski S, Kozii IV, Koziy RV, Raza MF, Jose MS, Simko E, Wood SC, 2023. Oxytetracycline-resistant Paenibacillus larvae identified in commercial beekeeping operations in Saskatchewan using pooled honey sampling. Journal of Veterinary Diagnostic Investigation. 35(6):645-654. https://doi.org/10.1177/10406387231200178
Ory F, Dietemann V, Guisolan A, Von Ah U, Fleuti C, Oberhaensli S, Charrière JD, Dainat B, 2023. Paenibacillus melissococcoides sp. Nov, isolated from a honeybee colony affected by European foulbrood disease. International Journal of Systematic and Evolutionary Microbiology. 73(4). https://doi.org/10.1099/ijsem.0.005829
Oulebsir-Mohand Kaci H, Talbi-Khemili S, Gana-Kebbouche S, Doumandji-Mitiche B, 2016. Antagonistic Activity of two-bacillus sp. Strains isolated from an Algerian soil towards the migratory locust Locusta migratoria (LINNAEUS 1758). The Journal «Agriculture and Forestr ». 62(1). https://doi.org/10.17707/AgricultForest.62.1.17
Oumani Abdelati DR, 2021. Contribution à l’étude de l’activité anti oxydante et anti microbienne de la propolis d’origine marocaine. Doctoral thesis. University of Hassan 1er Doctoral Studies Centre, Algeria. 33-34.
Ożarowski M, Karpiński TM, Alam R, Łochyńska M, 2022. Antifungal Properties of Chemically Defined Propolis from Various Geographical Regions. Microorganisms. 10(2):364. https://doi.org/10.3390/microorganisms10020364
Özkırım A, Çelemli ÖG, Schiesser A, Charistos L, Hatjina F, 2014. A comparison of the activities of Greek and Turkish propolis against Paenibacillus larvae. Journal of Apicultural Research. 53(5):528-536. https://doi.org/10.3896/IBRA.1.53.5.01
Özüı̇Çlı̇ M, Gı̇Rı̇Şgı̇N AO, Dı̇Ker Aİ, Baykalir Y, Kisadere İ, Aydin L, 2023. The Efficacy of Thyme, Peppermint, Eucalyptus Essential Oils, and Nanoparticle Ozone on Nosemosis in Honey Bees. Kafkas Universitesi Veteriner Fakultesi Dergisi. https://doi.org/10.9775/kvfd.2023.29167
Pellati F, Orlandini G, Pinetti D, Benvenuti S, 2011. HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts. Journal of Pharmaceutical and Biomedical Analysis. 55(5):934-948. https://doi.org/10.1016/j.jpba.2011.03.024
Plavša N, Stojanovi D, Stojanov I, Puva N, 2011. Evaluation of oxytetracycline in the prevention of American foulbrood in bee colonies. African Journal of Agricultural Research. 6(6):1621-1626. https://doi.org/10.5897/AJAR10.1060
Poppinga L, Janesch B, Fünfhaus A, Sekot G, Garcia-Gonzalez E, Hertlein G, Hedtke K, Schäffer C, Genersch E, 2012. Identification and Functional Analysis of the S-Layer Protein SplA of Paenibacillus larvae, the Causative Agent of American Foulbrood of Honey Bees. Plop Pathogens, 8(5):e1002716. https://doi.org/10.1371/journal.ppat.1002716
Porrini LP, Porrini MP, Garrido PM, Principal J, Suarez CJB, Bianchi B, Iriarte PJF, Eguaras MJ, 2017. First Identification of Nosema Ceranae (Microsporidia) Infecting Apis Mellifera in Venezuela. Journal of Apicultural Science. 61(1):149 152. https://doi.org/10.1515/jas-2017-0010
Porrini MP, Fernández NJ, Garrido PM, Gende LB, Medici SK, Eguaras MJ, 2011. In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia). Apidologie. 42(6):700 707. https://doi.org/10.1007/s13592-011-0076-y
Porrini MP, Garrido PM, Gende LB, Rossini C, Hermida L, Marcángeli JA, Eguaras MJ, 2017. Oral administration of essential oils and main components: Study on honey bee survival and Nosema ceranae development. Journal of Apicultural Research. 56(5):616 624. https://doi.org/10.1080/00218839.2017.1348714
Porrini MP, Garrido PM, Umpiérrez ML, Porrini LP, Cuniolo A, Davyt B, González A, Eguaras MJ, Rossini C, 2020. Effects of Synthetic Acaricides and Nosema ceranae (Microsporidia: Nosematidae) on Molecules Associated with Chemical Communication and Recognition in Honey Bees. Veterinary Sciences. 7(4):199. https://doi.org/10.3390/vetsci7040199
Pratami DK, Indrawati T, Istikomah I, Farida S, Pujianto P, Sahlan M, 2020. Antifungal activity of microcapsule propolis from Tetragonula spp. to Candida albicans. Communications in Science and Technology. 5(1):16- 21. https://doi.org/10.21924/cst.5.1.2020.178
Rodríguez-García C, Heerman MC, Cook SC, Evans JD, DeGrandi-Hoffman G, Banmeke O, Zhang Y, Huang S, Hamilton M, Chen YP, 2021. Transferrin-mediated iron sequestration suggests a novel therapeutic strategy for controlling Nosema disease in the honeybee, Apis mellifera. PLOS Pathogens. 17(2): e1009270. https://doi.org/10.1371/journal.ppat.1009270
Saleh S, Salama A, Ali AM, Saleh AK, Elhady BA, Tolba E, 2023. Egyptian propolis extract for functionalization of cellulose nanofiber/poly (vinyl alcohol) porous hydrogel along with characterization and biological applications. Scientific Reports. 13(1):7739. https://doi.org/10.1038/s41598-023-34901-6
Salomão K, Pereira PRS, Campos LC, Borba CM, Cabello PH, Marcucci MC, De Castro SL, 2008. Brazilian Propolis: Correlation between Chemical Composition and Antimicrobial Activity. Evidence-Based Complementary and Alternative Medicine. 5(3):317 324. https://doi.org/10.1093/ecam/nem058
Schüler V, Liu YC, Gisder S, Horchler L, Groth D, Genersch E, 2023. Significant, but not biologically relevant: Nosema ceranae infections and winter losses of honeybee colonies. Communications Biology. 6(1):229. https://doi.org/10.1038/s42003-023-04587-7
Segueni N, Akkal S, Benlabed K, Nieto G, 2022. Potential Use of Propolis in Phytocosmetic as Phytotherapeutic Constituent. Molecules. 27(18):5833. https://doi.org/10.3390/molecules27185833
Segueni Narimene DR, 2011. Contribution à l’étude de la composition chimique et des Propriétés biologiques de la propolis. Doctoral thesis. University of Mentouri, Constantine, Algeria. 78.
Sevim E, Bozdeveci A, Pınarbaş Çetin M, Kekeçoğlu M, Akpınar R, Keskin, M, Kolaylı S, Alpay Karaoğlu Ş, 2021. Antibacterial effects of anatolian propolis on Paenibacillus Larvae. Uludağ Arıcılık Dergisi. 21(2):177-186. https://doi.org/10.31467/uluaricilik.976536
Soltani ELkhamsa, 2017. Caractérisation et activités biologiques de substances naturelles, cas de la propolis. Doctoral thesis. University of Ferhat Abbas, Setif 1. Algeria. 27-35.
Sönmez E, 2023. Investigationofchemicalcontentandantimicrobial activitiesof different plantsourcesof Anatolian propolis samples. Uludağ Arıcılık Dergisi. 23(1):37 48. https://doi.org/10.31467/uluaricilik.1208667
Šulcerová H, Mihok M, Jůzl M, Haščík P, 2014. Effect of addition of pollen and propolis to feeding mixtures during the production of broiler chickens ROSS 308 to the colour of thigh and breast muscle and pH determination. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis. 59(6):359 366. https://doi.org/10.11118/actaun201159060359
Suwannapong G, Maksong S, Phainchajoen M, Benbow ME, Mayack C, 2018. Survival and health improvement of Nosema infected Apis florea (Hymenoptera: Apidae) bees after treatment with propolis extract. Journal of Asia-Pacific Entomology. 21(2):437-444. https://doi.org/10.1016/j.aspen.2018.02.006
Teggar N, Bakchiche B, Abdel-Aziz MES, Bardaweel SK, Ghareeb MA, 2023. Chemical Composition and Biological Evaluation of Algerian Propolis from Six Different Regions. Jordan Journal of Pharmaceutical Sciences. 184 197. https://doi.org/10.35516/jjps.v16i2.1319
Touzani S, Embaslat W, Imtara H, Kmail A, Kadan S, Zaid H, ElArabi I, Badiaa L, Saad B, 2019. In Vitro Evaluation of the Potential Use of Propolis as a Multitarget Therapeutic Product: Physicochemical Properties, Chemical Composition, and Immunomodulatory, Antibacterial, and Anticancer Properties. BioMed Research International. 1-11. https://doi.org/10.1155/2019/4836378
Vică ML, Glevitzky M, Dumitrel GA, Popa M, Glevitzky I, Teodoru CA, 2024. Antimicrobial Activity of Honey and Propolis from Alba County, Romania. Antibiotics. 13(10):952. https://doi.org/10.3390/antibiotics13100952
Widelski J, Okińczyc P, Suśniak K, Malm A, Paluch E, Sakipov A, Zhumashova G, Ibadullayeva G, Sakipova Z, Korona-Glowniak I, 2023. Phytochemical Profile and Antimicrobial Potential of Propolis Samples from Kazakhstan. Molecules. 28(7):2984. https://doi.org/10.3390/molecules28072984
Woźniak M, Sip A, Mrówczyńska L, Broniarczyk J, Waśkiewicz A, Ratajczak I. 2022, Biological Activity and Chemical Composition of Propolis from Various Regions of Poland. Molecules. 28(1):141. https://doi.org/10.3390/molecules28010141
Yılmaz F, Kuvancı A, Konak F, Öztürk SH, Şahin AE, 2020. The Effects of Some Essential Oils Against Nosemosis. Bee Studies- Apiculture Research Institute. 12(2):37-41. https://doi.org/10.51458/BSTD.2021.7
Zhang Q, Yang A, Tan W, Yang W, 2023. Development, Physicochemical Properties, and Antibacterial Activity of Propolis Microcapsules. Foods. 12 (17): 31
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