SavedAdd your journal

Journals / Journal of Agricultural Sciences / 2026 / Volume: 29 Issue: 2

Does Dry or Fresh Bee Bread Contain Clinically Significant, and Antimicrobial Agents Resistant Microorganisms?

Fatma Mutlu Sarıguzel(Department of Medical Microbiology, Faculty of Medicine, Erciyes University, Kayseri, Turkey)0000-0003-2747-0208
Sibel Silici(Department of Agricultural Biotechnology, Faculty of Agriculture, Erciyes University, Nutral Therapy Co. Erciyes Technopark Kayseri, Turkey)0000-0003-2810-2917
Ayşe Nedret Koç(Department of Medical Microbiology, Faculty of Medicine, Erciyes University, Kayseri, Turkey)0000-0002-1736-9707
Pınar Sağıroğlu(Department of Medical Microbiology, Faculty of Medicine, Erciyes University, Kayseri, Turkey)0000-0001-6742-0200
Bedia Dinç(Clinic of Medical Microbiology, Ankara Training and Research Hospital, Ankara, Turkey)0000-0001-8318-2556
Pages
—
Publication Date
2023-03-31
🏛️Bibliographic metadata and full text access for this article are provided via DergiPark.
DergiPark Record ↗
✨

AI Summary & Key Takeaways

AI Insight
⚡ TL;DR(Too Long; Didn't Read)

In addition, it was concluded that yeast, mold, and bacteria isolated in fresh bee bread samples may be resistant to antibiotics and antifungal drugs.

📌 3 Key Takeaways

🎯
Objective & Hypothesis:Bee bread is fermented and naturally preserved pollen that is enriched with digestive enzymes and organic acids from both honey and the salivary gland secretions of honeybees.
📊
Key Findings & Data:Fresh and dry bee bread samples were obtained from 8 different colonies that were cultivated in suitable medium to reproduction the aerobic microorganisms, anaerobic microorganisms, and fungi.
💡
Conclusion & Impact:In addition, it was concluded that yeast, mold, and bacteria isolated in fresh bee bread samples may be resistant to antibiotics and antifungal drugs.
🔬Design:Research Article
📍Scope:Comprehensive Sample
⚙️Variables:Perga · Bacteria · Yeast

Abstract

Bee bread is fermented and naturally preserved pollen that is enriched with digestive enzymes and organic acids from both honey and the salivary gland secretions of honeybees. As yet, there is insufficient information concerning which bacteria and yeasts are involved in the fermentation. This study seeks to determine the contents of microorganisms in fresh and dry bee bread samples and to ascertain the antimicrobial resistance of these isolated microorganisms. Fresh and dry bee bread samples were obtained from 8 different colonies that were cultivated in suitable medium to reproduction the aerobic microorganisms, anaerobic microorganisms, and fungi. The isolated strains in bee bread samples were identified by conventional and MALDI-TOF MS methods. The minimal inhibitory concentrations (MIC) of the antimicrobial agents for strains were determined according to the Clinical and Laboratory Standards Institute (CLSI). The 34 strains were isolated from fresh bee bread samples. There were no microrganisms reproduced in the dried bee bread samples. The 34 isolated strains were; Aspergillus spp. (12), Rhizopus oryzae (6), Mucor circinelloides (1), Bipolaris (2), Trichoderma (3), Paecilomyces variotii (1), Penicillium chrysogenum (1), Kodamaea ohmeri (1), Bacillus altitudinis/pumilus (3), Bacillus licheniformis (1), B. megaterium (1), Micrococcus luteus (1) and Serratia marcescens (1). The MIC values of itraconazole (IT), voriconazole, anidulafungin (AND), and caspofungin (CS) for Mucor and Rhizopus strains were higher (≥32 μg/mL), with the exception of amphamphotericin B posaconazole. All antifungal agents had lower MIC values compared to the Aspergillus, Bipolaris, P. variotii, and K. ohmeri strains. The trichoderma strains had low MIC values (≤0.50 μg/mL), with the exception of IT. The P. chrysogenum strains were found to have low MIC value (≤0.25 μg/mL) compared to posaconazole, AND, and CS. In this study, there were no microorganisms reproduce in the dried bee bread samples stored under suitable conditions. In addition, it was concluded that yeast, mold, and bacteria isolated in fresh bee bread samples may be resistant to antibiotics and antifungal drugs.

🔖

Cite This Article

Sarıguzel, F. M., Silici, S., Koç, A. N., Sağıroğlu, P., Dinç, B. (2023). Does Dry or Fresh Bee Bread Contain Clinically Significant, and Antimicrobial Agents Resistant Microorganisms?. Journal of Agricultural Sciences, Volume: 29 Issue: 2. https://doi.org/10.15832/ankutbd.1067297

📄 Full Text PDF Viewer

📄

PDF görüntüleyici hazırlanıyor...

References (57)

  1. Audisio M C, Terzolo H R & Apella M C (2005). Bacteriocin from honeybee beebread Enterococcus avium, active against Listeria monocytogenes. Applied and Environmental Microbiology 71(6): 3373-3375. doi.org/10.1128/AEM.71.6.3373-3375.2005
  2. Anderson K E, Carroll M J, Sheehan T, Mott B M, Maes P, Corby-Harris V (2014). Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol Ecol 23: 5904-5917. doi.org/10.1111/mec.12966
  3. Ares A M, Valverde S, Bernal J, Nozal M J & Bernal J (2018). Extraction and determination of bioactive compounds from bee pollen. Journal of Pharmaceutical and Biomedical Analysis 147: 110-124. doi.org/10.1016/j.jpba.2017.08.009
  4. Bang L M, Buntting C & Molan P (2003). The effect of dilution on the rate of hy- drogen peroxide production in honey and its implications for wound healing. J Altern Complement Med 9(2): 267-273. doi.org/10.1089/10755530360623383
  5. Bakour M, Fernandes A, Barros L, Sokovic M, Ferreir I C F R & Lyoussi B (2019). Bee bread as a functional product: Chemical composition and bioactive properties. LWT 109: 276-282. doi.org/10.1016/j.lwt.2019.02.008
  6. Barene I, Daberte I & Siksna S (2015). Investigation of bee bread and development of its dosage forms. Medicinos Teorija Ir Praktika 21(1): 16-22. doi.org/10.15591/mtp.2015.003
  7. Belina-Aldemita M D, Opper C, Schreiner M & D’Amico S (2019). Nutritional composition of pot-pollen produced by stingless bees (Tetragonula biroi Friese) from the Philippines. Journal of Food Composition and Analysis 82: 103215. doi.org/10.1016/j.jfca.2019.04.003
  8. Bobis O, Marghitas L A, Dezmirean D, Morar O, Bonta V & Chirila F (2010). Quality parameters and nutritional value of different commercial bee products. Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj–Napoca. Animal Science and Biotechnologies 67: 1-2.
  9. Bonvehi J S & Escola R (1997). Nutrient composition and microbiological quality of honeybee-collected pollen in Spain. J Agric Food Chem 45(3): 725-732. doi.org/10.1021/jf960265q
  10. Burnside C E (1929). Saprophytic fungi associated with the honey bee. Bee World 10: 42. doi.org/10.1080/0005772X.1929.11092782
  11. Čadež N, Fülöp L, Dlauchy D, Péter G (2015). Zygosaccharomyces favi sp. nov., an obligate osmophilic yeast species from bee bread and honey. Antonie Van Leeuwenhoek 107(3): 645-654. doi.org/10.1007/s10482-014-0359-1
  12. Campos M G R, Bogdanov S, Almeida-Muradian L B, Szczesna T, Mancebo Y, Frigerio C & Ferreira F (2008). Pollen composition and standardisation of analytical methods. Journalof Apicultural Research 47: 156-163. doi.org/10.1080/00218839.2008.11101443
  13. Carpes S T, Begnini R, de Alencar S M &Masson M L (2007). Study of preparations of bee pollen extracts, antioxidant and antibacterial activity. Cienc Agrotec 31(6): 1818-1825. doi.org/10.1590/S1413-70542007000600032
  14. Chen S C A, Sorrell T C & Meyer W (2015). Aspergillus and Penicillium. Manual of Clinical Microbiology, 11th Edition. Jorgensen J H, Carroll K C, Funke G, Pfaller M A, Landry M L, Richter S S, Warnock D W (eds.) Warnock. pp. 2030-2056
  15. Clinical and Laboratory Standards Institute (2008). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi: approved standard, 2nd ed. CLSI document M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA.
  16. Clinical and Laboratory Standards Institute (2017). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: 4th Informational Supplement. CLSI document M27-S4. Clinical and Laboratory Standards Institute, Wayne, PA.
  17. Clinical and Laboratory Standards Institute Guidelines (2015). M02-A12: Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard-12th Edition. Clinical and Laboratory Standards Institute, Wayne, PA.
  18. De-Melo A A M, Estevinho M L M F & Almeida-Muradian L B (2015). A diagnosis of the microbiological quality of dehydrated bee-pollen produced in Brazil. Lett Appl Microbiol 61(5): 477-483. doi.org/10.1111/lam.12480
  19. Deveza M V, Keller K M, Lorenzon M C A, Nunes L M T, Sales É O & Barth O M (2015). Mycotoxicological and palynological profiles of commercial brands of dried bee pollen. Braz J Microbiol 46(4): 1171-1176. doi.org/10.1590/S1517-838246420140316
  20. DeGrandi-Hoffman G, Chen Y & Simonds R (2013). The effects of pesticides on queen rearing and virus titers in honey bees (Apis mellifera L.). Insects 4(1): 71-89. doi.org/10.3390/insects4010071
  21. Detry R, Simon-Delso N, Bruneau E & Daniel H M (2020). Specialization of yeast genera in different phases of bee bread maturation. Microorganisms 8: 1789. doi.org/10.3390/microorganisms8111789
  22. Di Cagno R, Filannino P, Cantatore V & Gobbetti M (2019). Novel solid-state fermentation of bee-collected pollen emulating the natural fermentation process of bee bread. Food Microbiol 82: 218-230. doi.org/10.1016/j.fm.2019.02.007
  23. Disayathanoowat T, Yoshiyama M, Kimura K & Chantawannakul P (2012). Isolation andcharacterization of bacteria from the midgut of the Asian honey bee (Apis cerana indica). Journal of Apicultural Research 51(4): 312-319. doi.org/10.3896/IBRA.1.51.4.04
  24. Egorova A L (1971). Preservative microflora in stored pollen. Veterinariya 8: 40-41.
  25. Fatrcovaa-Sramkovaa K, Noozzkova J, Maariaassyova M & Kaccaniova M (2016). Biologically active antimicrobial and antioxidant substances in the Helianthus annuus L. bee pollen. J Environ Sci Health B 51(3): 176-181. doi.org/10.1080/03601234.2015.1108811
  26. Forsgren E, Olofsson T C, Vásquez A & Fries I (2010). Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41(1): 99-108. doi.org/10.1051/apido/2009065
  27. Garcia-Hermoso D, Alanio A, Lortholary O & Dromer F (2015). Agents of Systemic and subcutaneous Mucormycosis and Entomophthoromycosis. Manual of Clinical Microbiology, 11th Edition. Versalovic J, Carroll K C, Funke G, Jorgensen J H, Landry M L, Warnock D W. Warnock. pp. 2087-2108.
  28. Gilliam M, Morton H L, Prest D B, Martin R D & Wickerham L (1977). The mycoflora of adult worker honeybees, Apis mellifera: E ects of 2,4,5-T and caging of bee colonies. The Journal of Invertebrate Pathology 30: 50-54. doi.org/10.1016/0022-2011(77)90036-2
  29. Gilliam M (1979a). Microbiology of pollen and bee bread: The yeasts. Apidologie 10(1): 43-53. doi.org/10.1051/apido:19790106
  30. Gilliam M (1979b). Microbiology of pollen and bee bread: The genus Bacillus. Apidologie 10(3): 269-274. doi.org/10.1051/APIDO:19790304
  31. Gilliam M, Prest D B & Lorenz B J (1989). Microbiology of pollen and bee bread: taxonomy and enzymology of moulds. Apidologie 20: 53-68. doi.org/10.1051/apido:19890106
  32. Habryka C, Kruczek M & Drygas B (2016). Bee products used in apitherapy. WSN 48: 254-258.
  33. Haydak M H (1958). Pollen-pollen subtitutes- bee bread. American Bee Journal 98: 145-146.
  34. Human H & Nicolson S W (2006). Nutritional content of fresh, bee–collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67(14): 1486-1492. doi.org/10.1016/j.phytochem.2006.05.023
  35. Kaplan M, Karaoglu O, Eroglu N & Silici S (2016). Fatty acid and proximate composition of bee bread. Food Technology and Biotechnology 54(4): 497-504. doi.org/10.17113/ftb.54.04.16.4635
  36. Kieliszek M, Piwowarek K, Kot A M, Błażejak S, Chlebowska-Śmigiel A & Wolska I (2018). Pollen and bee bread as new health-oriented products: a review. Trends in Food Science & Technology 71: 170-180. doi.org/10.1016/j.tifs.2017.10.021
  37. Maes PW, Rodrigues PA, Oliver R, Mott BM, Anderson KE (2016). Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Mol Ecol 25(21): 5439-5450. d doi.org/10.1111/mec.13862
  38. Matthews K R, Kniel K E & Montville T J (2017). Food Microbiology: An Introduction, 4th Edition. WILEY, New Jersey.
  39. Mutlu Sariguzel F, Berk E, Nedret Koc A, Sav H, Aydemir G (2016). Erratum: Evaluation of CHROMagar Candida, VITEK2 YST and VITEK® MS for identification of Candida strains isolated from blood cultures. Infez Med 24(1): 90. Erratum for (2015): Infez Med 23(4): 318-322.
  40. Nagai T, Nagashima T, Suzuki N & Inoue R (2005). Antioxidant activity and an- giotensin I–converting enzyme inhibition by enzymatic hydrolysates from bee bread. Z Naturforsch C J Biosci 60(1-2): 133-138. doi.org/10.1515/znc-2005-1-224
  41. Nogueira C, Iglesia A, Feás X & Estevinho L M (2012). Commercial bee pollen with different geographical origins: a comprehensive approach. Int J Mol Sci 13(9): 11173-11187. doi.org/10.3390/ijms130911173
  42. Pascoal A, Rodrigues S, Teixeira A, Feas X & Estevinho L M (2014). Biological activities of commercial bee pollens: antimicrobial, antimutagenic, antioxidant and anti-inflammatory. Food Chem Toxicol 63: 233-239. doi.org/10.1016/j.fct.2013.11.010
  43. Podriznik B & Bozic J (2015). Maturation and stratification of antibacterial activity and total phenolic content of bee bread in honey comb cells. Journal of Apicultural Research 54: 81-92. doi.org/10.1080/00218839.2015.1090774
  44. Sabino R, Carolino E, Veríssimo C, Martinez M, Clemons K V, Stevens D A (2016). Antifungal susceptibility of 175 Aspergillus isolates from various clinical and environmental sources. Med Mycol 54(7): 740-756. doi.org/10.1093/mmy/myw024
  45. Salminen S, Deighton M, Benno Y & Gorbach L (1998). Lactic acid bacteria in health and disease. In: Salminen S, Von Wright A. Lactic acid bacteria: microbiology and functional aspects. 2nd ed. 1998. New York: Marcel Dekker Inc pp. 211-254.
  46. Sağıroğlu P, Koc A N, Atalay M A, Altinkanat Gelmez G, Canöz O & Mutlu Sarıgüzel F (2019). Mucormycosis experience through the eyes of the laboratory. Infect Dis (Lond) 51(10):730-737. doi.org/10.1080/23744235.2019.1645962
  47. Schallmey M, Singh A & Ward O P (2004). Developments in the use of Bacillus species for industrial production. Canadian Journal of Microbiology 50: 1-17. doi.org/10.1139/w03-076
  48. Stanciu O G, Marghitas L A& Dezmirean D (2009). Macro and oligo-mineral elements from honeybee-collected pollen and beebread harvested from Transylvania (Romania). Bulletin UASVM Animal Science and Biotechnologies 66(1-2): 276-281. doi.org/10.15835/BUASVMCN-ASB:66:1-2:3368
  49. Sinpoo C, Williams G R & Chantawannakul P (2017). Dynamics of fungal communities in corbicular pollen and bee bread. Chiang Mai J Sci 44(4): 1244-1256.
  50. Tomas A, Falcao SI, Russo-Almeida P& Vilas-Boas M (2017). Potentialities of beebread as a food supplement and source of nutraceuticals: botanical origin, nutritional composition and antioxidant activity. Journal of Apicultural Research 56(3): 219-230. doi.org/10.1080/00218839.2017.1294526
  51. Urcan A C, Criste A D, Dezmirean D S, Margaoan R, Caeiro A & Campos M G (2018). Similarity of data from bee bread with the same taxa collected in India and Romania. Molecules 23: 2491. doi.org/10.3390/molecules23102491
  52. vanEngelsdorp D, Evans JD, Donovall L, Mullin C, Frazier M, Frazier J, Tarpy DR, Hayes J Jr & Pettis JS (2009). “Entombed Pollen”: A new condition in honey bee colonies associated with increased risk of colony mortality. J Invertebr Pathol 101(2): 147-149. doi.org/10.1016/j.jip.2009.03.008
  53. Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L & Olofsson TC (2012). Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7(3): e33188. doi.org/10.1371/journal.pone.0033188
  54. Vaasquez A & Olofsson T C (2009). The lactic acid bacteria involved in the production of bee pollen and bee bread. Journal of Apicultural Research 48(3): 189-195. doi.org/10.3896/IBRA.1.48.3.07
  55. Villanueva M O, Marquina A D, Serrano R B & Abellán G B (2002). The importance of bee–collected pollen in the diet: A study of its composition. Int J Food Sci Nutr 53(3): 217-224. doi.org/10.1080/09637480220132832
  56. Wasko A, Kieliszek M & Targoński Z (2012). Purification and characterization of a proteinase from the probiotic Lactobacillus rhamnosus OXY. Prep Biochem Biotechnol 42(5): 476-488. doi.org/10.1080/10826068.2012.656869
  57. Yoder Y A, Jajack A J, Rosselot A E, Smith T J, Yerke M C & Sammataro D (2013). Fungicide contamination reduces beneficial fungi in bee bread based on an area-wide field study in honeybee, Apis mellifera, colonies. J Toxicol Environ Health A 76: 587-600. doi.org/10.1080/15287394.2013.798846