Evaluation of Antioxidant and Antibacterial Activities of Apis florea Fabricius (Hymenoptera: Apidae) Honey on Helicobacter pylori

Document Type : Research Article-en

Authors

• Shabnam Parichehreh ¹
• Gholamhossein Tahmasbi ¹
• Mohammad Eslampanah ²
• Pejvak Khaki ²

¹ Department of Honeybee, Animal Science Research Institute of Iran, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

² Department of Microbiology, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

https://doi.org/10.22067/ifstrj.2023.81933.1248

Abstract

Iranian men are at risk of developing gastrointestinal cancer caused by H. pylori. It is very imperative to find effective methods to control this bacterium as there are currently no very effective treatments for it. Honey has been shown to have antimicrobial properties against various pathogens. This study analyzed 15 honey samples from A. florea bees, collected from different floral and geographical origins, for their antimicrobial efficacy against H. pylori. Using atomic absorption measurements, the honey samples were also tested for their phenolic and flavonoid content, protein concentration, and mineral content. Antioxidant activity was determined using the FRAP, DPPH, and ABTS methods. The antibacterial activity of honey samples was investigated both in-vitro and in-vivo in the gastrointestinal tract of mice. Statistical analysis revealed a significant positive correlation between antioxidant activity and antibacterial activity. All honey samples showed antimicrobial activity in-vitro, among which jujube honey from Bushehr exhibiting the highest activity. Differences in antioxidant and antimicrobial activities were likely due to the flora of the plants and the geographic region from which the honey was harvested. Based on these results, A. florea honey may be used in the prevention and treatment of H. pylori-associated infections and inflammation of the gastrointestinal tract. This feature can be applied to the control of Helicobacter pylori along with other available measures. 

Keywords

• Antioxidant activity
• Antimicrobial activities
• Honey
• H. pylori

Main Subjects

• Food Biotechnology

References

1. Al Somal, N., Coley, K.E., Molan, P.C., & Hancock, B.M. (1994). Susceptibility of Helicobacter pylori to the antibacterial activity of manuka honey. Journal of the Royal Society of Medicine, 87(1), 9. https://doi.org/10.1177/014107689408700106
2. Aliyazicioglu, R., & Boukraa, L. (2015). Honey: the natural inhibine”. Anti-Infective Agents, 13(1), 42-49.
3. Amaral, T.Y., Padilha, I.G., Presídio, G.A., Silveria, E.A.A.S.D., Duarte, A.W.F., Barbosa, A.P.F., & López, A.M. Q. (2017). Antimicrobial and anti-inflammatory activities of Apis mellifera honey on the Helicobacter pylori infection of Wistar rats gastric mucosa. Food Science and Technology, 37, 34-41. https://doi.org/10.1590/1678-457X.31016
4. Benzie, I.F., & Strain, J.J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical Biochemistry, 239(1), 70-76. https://doi.org/10.1006/abio.1996.0292
5. Bogdanov, S., Haldimann, M., Luginbühl, W., & Gallmann, P. (2007). Minerals in honey: environmental, geographical and botanical aspects. Journal of Apicultural Research, 46(4), 269-275. https://doi.org/10.1080/00218839.2007.11101407
6. .Boldt, M.S., Pereira, R.D., & Barbosa, A.J. (2015). Histological identification of pylori stained by hematoxylin-eosin and Giemsa: review for quality control. Jornal Brasileiro de Patologia e Medicina Laboratorial, 51(2), 108-112.
7. Bonacorsi, C., Raddi, M.S.G., Carlos, I.Z., Sannomiya, M., & Vilegas, W. (2009). Anti-Helicobacter pylori activity and immunostimulatory effect of extracts from Byrsonima crassa (Malpighiaceae). BMC Complementary and Alternative Medicine, 9(2), 2-7. https://doi.org/10.1186/1472-6882-9-2
8. Boyanova, L., Ilieva, J., Gergova, G., Vladimirov, B., Nikolov, R., & Mitov, I., 2015. Honey and green/black tea consumption may reduce the risk of Helicobacter pylori Diagnostic Microbiology and Infectious Disease, 82(1), 85-86. http://dx.doi.org/10.1016/j.diagmicrobio.2015.03.001
9. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
10. Cheung, Y., Meenu, M., Yu, X., & Xu, B. (2019). Phenolic acids and flavonoids profiles of commercial honey from different floral sources and geographic sources. International Journal of Food Properties, 22(1), 290-308. https://doi.org/10.1080/10942912.2019.1579835
11. de Queiroz Pimentel, R.B., da Costa, C.A., Albuquerque, P.M., & Junior, S.D. (2013). Antimicrobial activity and rutin identification of honey produced by the stingless bee Melipona compressipes manaosensis and commercial honey. BMC Complementary and Alternative Medicine, 13(1), 1-14.
12. Estevinho, L., Pereira, A.P., Moreira, L., Dias, L.G., & Pereira, E. (2008). Antioxidant and antimicrobial effects of phenolic compounds extracts of Northeast Portugal honey. Food and Chemical Toxicology, 46(12), 3774-3779. https://doi.org/10.1016/j.fct.2008.09.062
13. Gośliński, M., Nowak, D., & Kłębukowska, L. (2020). Antioxidant properties and antimicrobial activity of manuka honey versus Polish honeys. Journal of Food Science and Technology, 57, 1269-1277.
14. Graham, D.Y. (2015). Helicobacter pylori update: gastric cancer, reliable therapy, and possible benefits. Gastroenterology, 148(4), 719-731. https://doi.org/10.1053/j.gastro.2015.01.040
15. Grego, E., Robino, P., Tramuta, C., Giusto, G., Boi, M., Colombo, R., Serra, G., Chiadò-Cutin, S., Gandini, M., & Nebbia, P. (2016). Evaluation of antimicrobial activity of Italian honey for wound healing application in veterinary medicine. Band, 158, 521–527. http://hdl.handle.net/2318/1611345
16. Hernández, O.M., Fraga, J.M.G., Jiménez, A.I., Jiménez, F., & Arias, J.J. (2005). Characterization of honey from the Canary Islands: determination of the mineral content by atomic absorption spectrophotometry. Food Chemistry, 93(3), 449-458. https://doi.org/10.1016/j.foodchem.2004.10.036
17. Hussein, S.Z., Yusoff, K.M., Makpol, S., & Yusof, Y.A.M. (2011). Antioxidant capacities and total phenolic contents increase with gamma irradiation in two types of Malaysian honey. Molecules, 16(8), 6378-6395. https://doi.org/10.3390/molecules16086378
18. Jones, N.L., Day, A.S., Jennings, H., Shannon, P.T., Galindo-Mata, E., & Sherman, P.M. (2002). Enhanced disease severity in Helicobacter pylori-infected mice deficient in Fas signaling. Infection and Immunity, 70(5), 2591-2597. https://doi.org/10.1128/iai.70.5.2591-2597.2002
19. Khalil, M.I., Motallib, M.A., Anisuzzaman, A.S.M., Sathi, Z.S., Hye, M.A., & Shahjahan, M. (2001). Biochemical analysis of different brands of unifloral honey available at the northern region of Bangladesh. Sciences, 1(6), 385-338.
20. Khatun, S. (2014). Evaluation of helicobacter pyloristool antigen detection test (Doctoral dissertation, BRAC University).
21. Kolayli, S., Palabiyik, I., Atik, D.S., Keskin, M., Bozdeveci, A., Karaologu, S.A. (2020). Comparison of antibacterial and antifungal effects of different varieties of honey and propolis samples. Acta Aliment, 49, 515–523. https://doi.org/10.1556/066.2020.49.4.18
22. Manyi-Loh, C.E., Clarke, A.M., Munzhelele, T., Green, E., Mkwetshana, N.F., & Ndip, R.N. (2010). Selected South African honeys and their extracts possess in-vitro anti-Helicobacter pylori Archives of Medical Research, 41(5), 324-331. https://doi.org/10.1016/j.arcmed.2010.08.002
23. Marín, L., Miguélez, E.M., Villar, C.J., & Lombó, F. (2015). Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. BioMed Research International, 2, 12-25. https://doi.org/10.1155/2015/905215
24. Mello, B.C.B.S., Petrus, J.C.C., & Hubinger, M.D. (2010). Concentration of flavonoids and phenolic compounds in aqueous and ethanolic propolis extracts through nanofiltration. Journal of Food Engineering, 96(4), 533-539. https://doi.org/10.1016/j.jfoodeng.2009.08.040
25. Molan, P.C. (1992). The antibacterial activity of honey: 1. The nature of the antibacterial activity. Bee World, 73(1), 5-28. https://doi.org/10.1080/0005772X.1992.11099109
26. Molan, P.C. (2002) Re-introducing honey in the management of wounds and ulcers theory and practice. Ostomy/Wound Management 4811, 28-40.
27. Nakamura, M., Haruma, K., Kamada, T., Mihara, M., Yoshihara, M., Sumioka, M., & Chayama, K. (2002). Cigarette smoking promotes atrophic gastritis in Helicobacter pylori-positive subjects. Digestive Diseases and Sciences, 47(3), 675-681.
28. Parichehreh, S., Tahmasbi, G., Khaki, P., & Babaei, M. (2021). Evaluation of physicochemical characteristics of Apis florea honey in some southern provinces of Iran. Veterinary Researches and Biological Products, 34(2), 135-121. https://doi.org/10.22092/VJ.2020.128700.1668
29. Parichehreh, S., Tahmasbi, G., Sarafrazi, A., Tajabadi, N., & Solhjouy-Fard, S. (2020). Distribution modeling of Apis florea Fabricius (Hymenoptera, Apidae) in different climates of Iran. Journal of Apicultural Research, 1-12. https://doi.org/10.1080/00218839.2020.1775962
30. Pohl, P. (2009). Determination of metal content in honey by atomic absorption and emission spectrometries. TrAC Trends in Analytical Chemistry, 28(1), 117-128. https://doi.org/10.1016/j.trac.2008.09.015
31. Rahimifard, N., Hosseinzadeh Shanjani, B., & Shoeibi, S. (2019). The comparative study of antibacterial effects of Royal Jelly and Honey and the combination of them against standard strain of Helicobacter pylori. Journal of Food Microbiology, 6(2), 1-10.
32. Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9-10), 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
33. Saha, A., Hammond, C.E., Beeson, C., Peek, R.M., & Smolka, A.J. (2010). Helicobacter pylori represses proton pump expression and inhibits acid secretion in human gastric mucosa. Gut, 59(7), 874-881. http://dx.doi.org/10.1136/gut.2009.194795
34. Selahvarzian, A., Abdolahpour, F., Sepahvand. F., & Azadpour, M. (2015). Anti-oxidant and anti-microbial activities of two types of honey by change in bees, diet in comparison with other honey products in Abestan region of Khorramabad province. Yafte, 17(3): 115-125.
35. Shamala, T.R., Shri Jyothi, Y.P., & Saibaba, P. (2002). Antibacterial effect of honey on the in-vitro and in-vivo growth of Escherichia coli. World Journal of Microbiology and Biotechnology, 18(9), 863-865.
36. Silva, L.R., Videira, R., Monteiro, A.P., Valentão, P., & Andrade, P.B. (2009). Honey from Luso region (Portugal): Physicochemical characteristics and mineral contents. Microchemical Journal, 93(1), 73-77. https://doi.org/10.1016/j.microc.2009.05.005
37. Singleton, V.L., Orthofer, R., & Lamuela- Raventos, R.M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymology, 299, 152–178.
38. Snowdon, J.A., & Cliver, D.O. (1996). Microorganisms in honey. International Journal of Food Microbiology, 31(1-3), 1-26. https://doi.org/10.1016/0168-1605(96)00970-1
39. Stagos, D., Soulitsiotis, N., Tsadila, C., Papaeconomou, S., Arvanitis, C., Ntontos, A., & Mossialos, D. (2018). Antibacterial and antioxidant activity of different types of honey derived from Mount Olympus in Greece. International Journal of Molecular Medicine, 42(2), 726-734. https://doi.org/10.3892/ijmm.2018.3656
40. Tajik, H., Shokouhi, F., & Valehi, S. (2007). Evaluation of antimicrobial potential of commercial honey produced in Urmia. Journal of Food, Science, and Technology, 4(2), 39-45. https://doi.org/10.22067/ifstrj.2023.81933.1248
41. Take, S., Mizuno, M., Ishiki, K., Hamada, F., Yoshida, T., Yokota, K., & Yamamoto, K. (2015). Seventeen-year effects of eradicating Helicobacter pylori on the prevention of gastric cancer in patients with peptic ulcer; a prospective cohort study. Journal of Gastroenterology, 50(6), 638-644.
42. Tosic, S., Stojanovic, G., Mitic, S., Pavlovic, A., & Alagic, S. (2017). Mineral composition of selected Serbian propolis samples. Journal of Apicultural Science, 61(1), 5-15.
43. Von Gadow, A., Joubert, E., & Hansmann, CF. (1997). Comparison of antioxidant activity of aspalathin with that of other plant phenols of Rooibosed tea (Aspalathon linearis), atocopherol, BHT, and BHA. Journal of Agricultural and Food Chemistry, 45, 632–638. https://doi.org/10.22067/ifstrj.2023.81933.1248
44. Weston, R.J. (2000). The contribution of catalase and other natural products to the antibacterial activity of honey: a review. Food Chemistry, 71(2), 235-239. https://doi.org/10.1016/S0308-8146(00)00162-X
45. Wroblewski, L.E., Peek Jr, R.M., & Wilson, K.T. (2010). Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clinical Microbiology Reviews, 23(4), 713-739. https://doi.org/10.1128/cmr.00011-10
46. Yaoa, L., Jiang, Y., Singanusong, R., Datta, N., & Raymont, K. (2005). Phenolic acids in Australian Melaleuca, Guioa, Lophostemon, Banksia and Helianthus honeys and their potential for floral authentication. Food Research International, 38(6), 651-658. https://doi.org/10.1016/j.foodres.2005.01.002