Honey Bees/Honey as Probiotic and Prebiotic Products

Version	Summary	Created by	Modification	Content Size	Created at	Operation
1		Suraiami Mustar	--	2648	2022-08-19 03:59:58	\|
2	Reference format revised.	Lindsay Dong	-3 word(s)	2645	2022-08-22 05:12:58	\|

This entry is adapted from the peer-reviewed paper 10.3390/foods11142102

Honey bees come from the family of Apidae and the genus Apis. A. dorsata, A. mellifera, A. cerana, A. laboriosa, A. florea, A. andreniformis, A. koschevnikovi, and A. nigrocincta are eight known species that can be found around the world. Honey bees are significant pollinators for cultivating crops for food production, ensuring the continuity of almost all life in this world. The honey bee’s gut contains many microorganisms as its normal microbiota. Most are probiotics, made up of lactic acid bacteria (LAB) and Bifidobacterium, which are widely distributed in their digestive tract system. Probiotics were first described in 2013 by the International Scientific Association for Probiotics and Prebiotics (ISAPP) as “live microorganisms that, when administered in adequate amounts, confer a health benefit on the host”. The scientific definition has been extensively applied around the globe. Probiotics enhance intestinal health and increase immune reaction by producing biological antimicrobial substances that can inhibit pathogens which caused digestive system imbalances in humans and animals.

probiotic prebiotic honey bee honey

1. Introduction

Many products produced by honey bees are useful to humans, including honey, ^[1]^[2] which is the most important and widely consumed bee product worldwide. Honey, a “natural sweet substance produced by Apis mellifera L. bees from the nectar of plants, secretions of living parts of plants, or excretions of plant-sucking insects on the living parts of plants, which the bees collect, transform by combining with specific substances of their own, deposit, dehydrate, store and leave in the honeycomb to ripen and mature” ^[3], comes in two varieties namely: blossom/nectar honey and honeydew honey. Blossom honey is made from flowering plant nectar, whereas honeydew honey is manufactured from honeydew collected from various parts of a plant or other sap-producing plants and insects ^[4]. Honey can be divided into two categories: unifloral (monofloral) and polyfloral (multifloral). Unifloral honey is made primarily from one type of plant nectar and is identified through pollen analysis, which reveals dominant pollen from a single plant species. Polyfloral honey does not have dominant pollen from one plant species but has a mixture of pollen from several plants ^[5]. Due to its refined, one-of-a-kind, and distinct flavor, unifloral honey typically commands a higher market price than polyfloral honey. The premium quality of unifloral honey mostly depends on the exclusive geographical area or the special plant species, for example, the Manuka honey from New Zealand ^[6]. Honey may contain probiotics that have been transmitted from the guts of honey bees during the process of making honey and may remain alive for a certain period ^[7]. Thus, both honey bees and honey may provide potential probiotics for future use. The health benefits of honey concerning its probiotic bacteria are that the probiotics will help to revitalize and strengthen the immune system of the host against harmful environmental factors and pathogens, aid in digestion, detoxify harmful substances and provide essential nutrients ^[8].

Honey is mostly made up of sugars or carbohydrates such as fructose (32–44%), glucose (23–38%), and some other complex sugars (5–15%) including sucrose, maltose, lactose, raffinose, trehalose, erlose, gentiobiose, turanose, panose, melezitose, and kojibiose amongst others ^[9]. Besides carbohydrates, the quality and health advantages of honey are also ascribed to the various components it possesses, such as protein, organic acids, amino acids, vitamins, minerals, enzymes, and polyphenols ^[10]. Different varieties of honey may vary in their content due to the different sources derived, such as geographical area, botanical origin, and bee species ^[9]. Blossom or nectar honey can be distinguished from honeydew honey by analyzing its carbohydrate concentration. Blossom honey contains higher concentrations of monosaccharides but is lower in trisaccharides (mainly melezitose, erlose, raffinose, and maltotriose) and other oligosaccharides compared to honeydew honey ^[11]. The honey’s prebiotic properties are known to come from its indestructible carbohydrates that cannot be fermented by digestive enzymes in humans and are not taken up in the upper intestinal tract system. They are capable of improving and enhancing health in general and intestinal health in particular by stimulating the development and promoting metabolic activity of the typical residents of the colon ^[12]. Honey’s prebiotic qualities can help probiotic microorganisms to flourish by supplying adequate nutrients. An increased number of probiotics may help to alleviate the total surface area for nutrient absorption, thus improving the health of the digestive system and enhancing resistance to pathogen infections ^[13]. These findings have sparked some ideas for conducting studies for further research on the natural microbiota of the bees’ gut with probiotic properties as a disease defense mechanism to be used as prophylaxis to treat not only bees themselves but also other animals and humans ^[8].

2. Probiotic Properties of Honey Bees and Honey

Table 1 highlights the studies that have been performed in several countries on honey bees’ guts and honey as the origin of potential probiotics. The majority of honey bee probiotics have been identified from A. mellifera spp., with a few from the A. cerana spp., and A. dorsata spp. Probiotics isolated from the honey bee gut were composed of diverse microorganisms including Bifidobacterium and lactic acid bacteria (LAB), as well as Fructophilic lactic acid bacteria (FLAB) which is a subgroup of LAB, yeasts, and other types of bacteria such as the Bacillus spp.

Table 1. Potential probiotics in the bees’ gut and honey.

Probiotic	Source	Origin/Country	Reference
Bifidobacterium spp.	Apis cerana japonica gut	Tsukuba, Japan	^[14]
Bifidobacterium spp., Lactobacillus spp., Bacillus spp.	Apis cerana indica gut	Samut-Songkhram, and Chumphon, Thailand	^[15]
Lactobacillus spp.	Apis cerana indica gut	Karnataka, India	^[16]
Lactobacillus plantarum, Lactobacillus pentosus, Lactobacillus fermentum	Apis dorsata gut	Terengganu, Malaysia	^[17]
Lactobacillus kunkeei strains	Yigilca honey bee gut	Duzce, Turkey	^[18]
Lactobacillus plantarum, Lactobacillus paraplantarum, Lactobacillus plantarum strains	Apis mellifera gut	Menoua, Cameroon	^[19] ^[20]
Lactobacillus plantarum strains	Apis cerana indica gut	Kerala, India	^[21]
Lactic Acid Bacteria (LAB) genera: Enterococcus, Lactobacillus, Micrococcus, Lactococcus, Streptococcus, Pediococcus, Leconostoc	Apis cerana indica Fabricius, Apis mellifera Linnaeus, Apis florea Fabricius, & Apis dorsata Fabricius guts and honey	Tamil Nadu, India	^[22]
Enterococcus faecalis strains, Lactobacillus brevis, Lactobacillus casei	Apis mellifera gut	Cairo, Egypt	^[23]
Fructobacillus fructossus strains, Lactobacillus kunkeei strains	Apis mellifera mellifera, Apis mellifera ligustica and hybridized bee guts, larvae and honey	Aland Island, Finland	^[24]
Lactobacillus kunkeei strains (sixty-six strains), Lactobacillus casei (one strain), Lactobacillus spp. (five unidentified strains), Fructobacillus fructosus strains (eight strains), Enterococcus (five strains), Bifidobacterium asteroids	Apis mellifera gut	The Caucasus Mountains, and Kolkheti Valley, Georgia	^[25]
Lactobacillus kunkeei strains, Lactobacillus fructosus strains	Apis mellifera gut	Lublin, Poland	^[26]
Lactobacillus kunkeei strains, Fructobacillus fructossus strains	Apis mellifera Linnaeus gut	Pulawy, Poland	^[27]
Fructobacillus fructossus, Proteus mirabilis, Bacillus subtilis, Bacillus licheniformis, Lactobacillus kunkeei, Enterobacter kobei, Morganella morganii	Apis mellifera jemenitica gut	Riyadh, Saudi Arabia	^[28]
Apilactobacillus kunkeei strains	Apis mellifera Linnaeus gut	N/A	^[29]
Bacillus spp.	Apis cerana japonica gut	Tsukuba, Japan	^[30]
Bacillus subtilis strains	Honey bee gut and honey	N/A	^[31]
Bacillus licheniformis, Paenibacillus polymyxa (Bacillus polymyxa), Wickerhamomyces anomalus, Lachancea thermotolerans, Zygosaccharomyces mellis,	Apis mellifera carnica gut Apis mellifera ligustica gut	Giza, Egypt	^[32]
Lactobacillus kunkeei strains, Lactobacillus spp.	Honey (Apis dorsata)	Kedah, Malaysia	^[33]
Leuconostoc mesenteroides strains	Honey (Apis mellifera)	Algeria	^[34]
Lactic Acid Bacteria (Species and subspecies not mentioned)	Honey (Apis mellifera)	Indonesia	^[35]
Bacillus spp.	Commercial honey (Libya, Saudi Arabia and Egypt)	N/A	^[36]
Bacillus subtilis, Brevibacillus brevis, Bacillus megaterium strains, Lactobacillus acidophilus	Local honey	Iran	^[37]
Bacillus subtilis strains Bacillus endophyticus	Mountain honey Persimmon honey (commercial)	Nigeria Egypt	^[38]
Bacillus spp.	Honey	China	^[39]
Bacillus subtilis, Bacillus mycoides, Bacillus thuringiensis, Bacillus amyloliquefaciens, Bacillus velezensis	Raw honey (Polyfloral)	Romania	^[40]
Gluconobacter oxydans	Honey (Apis cerana indica)	Tamil Nadu, India	^[41]
Saccharomyces cerevisiae strains, Meyerozyma guilliermondiii	Raw honey (Apis dorsata fabricius)	Ratchaburi, Thailand	^[42]

N/A = not available.

Bifidobacterium was less commonly discovered in the honey bees’ gut compared to the LAB. One study has shown the isolation of several Bifidobacterium species from the Japanese honey bee (Apis cerana japonica) gut. The isolates were shown to be strongly linked to bifidobacteria obtained from the European honey bees, implying that these bacteria are peculiar to the honey bee species.

LAB is the most common probiotic isolated from the guts of honey bees, as shown in many studies conducted earlier (refer to Table 1). Various strains of LAB were harvested from the guts of A. mellifera, A. cerana, A. dorsata, and A. florea species. In most of the studies, the microorganisms were identified using the PCR technique with gene sequencing. Lactobacillus spp. was recovered from the digestive tract of A. cerana indica in various Karnataka locales ^[16]. Other Lactobacillus species such as L. plantarum, L. pentosus, and L. fermentum were prevalent within the gut of Apis dorsata with L. plantarum accounting for 51.02%. The study was the first to highlight the presence of Lactobacillus spp. in the Malaysian wild honey bees’ gut (A. dorsata). The quantity of LAB microbiota members discovered in the honey bee gut was found to be dependent on the season, origin, and volume of nectar ^[17].

There have also been findings of the presence of Bacillus sp., in honey. Earlier in 2012, Esawy and colleagues ^[36] isolated Bacillus spp. from spores found in honey from three Gulf countries (Libya, Saudi Arabia, and Egypt). They exhibited good tolerance to pH 3 and pH 9 for up to 6 h with varying degrees of viability, resistance to 0.3% bile and pancreatic enzyme (except for one isolate), and negative results for hemolytic testing. The isolates also demonstrated antioxidant and antimicrobial properties, suggesting that they could flourish in the intestinal tract and function as potential antibiotic producers ^[36].

A. cerana indica honey becomes a carrier for Gluconobacter oxydans, a gram-negative bacterium from the Acetobacteraceae family which exhibits a probiotic quality ^[41]. G. oxydans isolated from freshly harvested honey was found to possess siderophorogenic potential and non-hemolytic activity which assure security as a possible probiotic microorganism. The probiotic’s capability to persist in the adverse conditions of the human gastrointestinal tract is revealed by its acid and bile tolerance characteristics of which the G. oxydans manage to endure a 2% bile salt concentration. The percentage of isolates that are auto-aggregated was found to be linearly related to incubation time, with notable % adherence to xylene being more than to ethyl acetate and chloroform.

3. Prebiotic Properties of Honey

Earlier research indicated that the prebiotic properties of honey are mainly due to the oligosaccharides and low molecular weight polysaccharides attached by the β-glycosidic linkages ^[12]. Prebiotics are hydrolyzed by the native intestinal microflora as human digestive enzymes do not possess β-glycosidases. Inulin, fructose-oligosaccharides (FOS), pyrodextrins, lactulose, and xylooligosaccharide are among the well-known prebiotics ^[43]. Several investigations into the possible prebiotic characteristics of honey have been undertaken in various regions of the world. Table 2 summarizes the different types of honey as a source of prebiotics and their effects on probiotics commonly found in the human intestinal system.

Table 2. Prebiotic potential of honey.

Probiotic	Sources of Prebiotic	Country	Key Findings	Reference
Lactobacillusacidophilus strains	Honey	India	- Honey enhanced the coaggregation of E. coli with L. acidophilus NCDC 291 more than with L. acidophilus NCDC 13. - Both strains showed a higher capability of autoaggregation and hydrophobicity, and reduced autolytic activity with inulin compared to honey.	^[44]
Lactobacillus acidophilus, Bifidobacterium bifidum	Sesame honey (Sesamum indicum)	India	- Sesame honey (5%) exhibited selective and significant growth-supporting properties of the probiotics.	^[45]
Lactobacillus acidophilus, Lactobacillus rhamnosus	Chestnut honey	Turkey	- Chestnut honey has positively impacted probiotic bacteria by increasing growth and modulating probiotic properties such as auto-aggregation and surface hydrophobia.	^[46]
Lactobacillus plantarum strain	Wild honey (Polyfloral)	Cameroon	- L. plantarum 29 V can survive for 28 days at 4 °C and 25 °C due to their ability to resist lower pH and the presence of oligosaccharides (fructo- and gluco-oligosaccharides) in honey recognized as prebiotics. - Hypercholesterolemic rats treated with honey containing L. plantarum 29 V showed an increase in HDL-cholesterol level and lowers total cholesterol, LDL-cholesterol, triglycerides and atherosclerosis index in serum.	^[47]
Lactobacillus acidophilus, Lactobacillus gasseri, Lacticaseibacillus casei, Lacticaseibacillus rhamnosus, Lactiplantibacillus plantarum	Fir, strawberry tree, ivy, tree of heaven, sulla, cardoon, rhododendron honey (Commercial, organic, monofloral honey)	Italy	- Fir, ivy, and sulla honey (1% and 2%) stimulate the growth of all the probiotics tested with various actions compared to more specific cardoon honey.	^[48]
Bifidobacterium longum strains, Bifidobacterium breve, Bifidobacterium bifidum	Agmark grade honey	India	- Honey showed a prebiotic effect on all isolates, especially on B. longum at 3% and 5% honey.	^[49]
Bifidobacterium bifidum and Lactobacilli	Clover honey (Unprocessed and sterilised)	Egypt	- Increased B. bifidum colony counts were observed in all honey-supplied group (Group A-5 g, B-10 g, and C-15 g honey), with group B, showing a significant rise in comparison with the control.	^[50]
Bifidobacteria	Buckwheat honey	China	- Buckwheat honey assists in propagating native Bifidobacteria and prohibits the growth of the pathogenic bacterium in the gut system.	^[51]
N/A	Manuka honey (MGO™)	Ireland	- Honey-containing oligosaccharides inhibited P. aeruginosa (52%), E. coli O157:H7 (40%) and S. aureus (30%) in the cancer cells.	^[52]
Microbiota of the mice gut	Jarrah honey	China	- Honey helps to retain more water in the faecal and relieves constipation and suppresses the growth of Desulfovibri.	^[53]
N/A	Giant Willow Aphid honeydew honey (Tuberolachnus salignus)	New Zealand	- A high concentration of melezitose can act as a prebiotic for the human digestive system since it is not hydrolysed by acid and is only partially hydrolysed by α-glucosidase.	^[54]
Limosilactobacillus reuteri	Manuka honey (Drapac DrKiwi AMF5, AMF10, AMF15 and AMF20)	New Zealand	- High sugar and oligosaccharides contributed to higher probiotic cell biomass of AMF20, but no obvious pattern in biomass with a decrease in AMF concentration.	^[55]

N/A = not available.

The probiotic ability to co-aggregate with the pathogens increased with the addition of honey, while the self-digestion reaction was greatly reduced when inulin was present. Co-aggregation capabilities allow probiotics to create a barrier that stops colonization by pathogens. Cell surface hydrophobicity is the probiotics’ capacity to attach to the gut endothelium. Inulin significantly increased cell membrane hydrophobicity in comparison to honey. Autolysis occurs when bacteria cell naturally deteriorates due to maturity or adverse biological factors, causing the autolysin enzymes to hydrolyse the cell wall peptidoglycan. It was found that L. acidophilus showed better attributes in prebiotics inulin than honey ^[44]. The viable count of L. acidophilus and B. bifidum were much higher when cultured in carbohydrate-free MRS broth fortified with sesame honey compared to the unfortified broth. At the same time, sesame honey also promotes antibacterial activity against several pathogens such as E. coli, V. cholerae, E. coli, S. typhi, and S. typhimurium with the lowest minimum inhibitory concentration (12.5%) toward S. typhi and S. typhimurium ^[45]. Chestnut honey was discovered to promote the flourishing of L. acidophilus LA-5 and L. rhamnosus GG, displaying probiotic features such as autoaggregation and surface hydrophobicity. Furthermore, as compared to probiotics or honey alone, probiotics grown with honey were more cytotoxic to cancer cell types ^[46].

Both types of honey, either monofloral or polyfloral, can serve as good prebiotic sources in foods. Honey is combined with dairy products derived from the fresh milk of cows ^[56]^[57]^[58]^[59]^[60], goats ^[61]^[62], camels ^[57], and buffalos ^[63] to produce yogurt. Some researchers also utilized skimmed milk powder to produce yogurt ^[64]^[65]^[66]. As for the non-dairy products, kefir ^[67], soy milk ^[68]^[69], and hydrolyzed soybean extract ^[67] were chosen to replace the animal’s milk. The most common starter culture probiotics used to produce yogurt are the S. thermophilus and L. delbrueckii ssp. bulgaricus. The findings of numerous investigations revealed that the number of probiotics in honey-containing foods is significantly enhanced. Monofloral honey (chestnut, acacia, lime honey) and polyfloral honey (eucalyptus, greenbrier) in yogurt were found to be good prebiotic sources for cultivating Bifidobacteria strains of diverse subspecies ^[64]^[68]. Saudi Arabian raw honey ^[56], black locust honey ^[57], Kerala natural honey ^[58], African commercial honey ^[66], marjoram honey ^[62], and pine honey ^[59] were all found to be suitable for cultivating Lactobacillus and Bifidobacterium species in the dairy and non-dairy goods. It was revealed in 2020 that Manuka honey of the brand AMF™ 15+ fortified in yogurt significantly increased the viable count of L. reuteri surpassing the recommended value of 7 log CFU/mL compared to the other brands tested (Manuka Blend and UMF™ 18+) ^[60]. A clinical trial in postmenopausal women treated with L. plantarum-fermented soymilk-honey for 90 days disclosed a notable reduction in the levels of osteocalcin in the participants’ blood serum, implying that honey as a source of prebiotics can assist probiotics in surviving longer for treatment purposes ^[69].

References

Paspuleti, V.R.; Sammugam, L.; Ramesh, N.; Gan, S.H. Honey, propolis and royal jelly: A comprehensive review of their biological actions and health benefits. Oxidative Med. Cell. Longev. 2017, 2017, 1259510.
Sforcin, J.M.; Bankova, V.; Kuropatnicki, A.K. Medical benefits of honeybee products. Evid. Based Complement. Altern. Med. 2017, 2017, 2702106.
Codex Alimentarius. International Food Standards. Standard for Honey CXS 12-19811. Adopted in 1981. Revised in 1987, 2001. Amended in 2019. Available online: https://www.fao.org/fao-who-codexalimentarius/shproxy/es/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCXS%2B12-1981%252FCXS_012e.pdf (accessed on 10 June 2021).
Bogdanov, S. Honey types. In Book of Honey; Scribners: Hunter, NY, USA, 2011; Chapter 6; pp. 1–5.
Ajibola, A. Novel insights into the health importance of natural honey. Malays J. Med. Sci. 2015, 22, 7–22.
Johnston, M.; McBride, M.; Dahiya, D.; Owusu-Apenten, R.; Nigam, P.S. Antibacterial activity of Manuka honey and its components: An overview. AIMS Microbiol. 2018, 4, 655–664.
Luchese, R.H.; Prudencio, E.R.; Guerra, A.F. Honey as a functional food. In Honey Analysis; INTECH Open Science: London, UK, 2017; Chapter 13; pp. 287–307.
Kechagia, M.; Basoulis, D.; Konstantopoulou, S.; Dimitriadi, D.; Konstantina, G.; Skarmoutsou, N.; Fakiri, E.M. Health benefits of probiotics: A review. ISRN Nutr. 2013, 2013, 481651.
Meo, S.A.; Al-Asiri, S.A.; Mahesar, A.L.; Ansari, M.J. Role of honey in modern medicine. Saudi J. Biol. Sci. 2017, 24, 975–978.
Bobisa, O.; Moisea, A.R.; Ballesterosb, I.; Reyes, E.S.; Sánchez-Duránc, S.; Sánchez-Sánchezc, J.; Cruz-Quintanae, S.; Giampierif, F.; Battino, M.; Alvarez-Suarez, J.M. Eucalyptus honey: Quality parameters, chemical composition and health-promoting properties. Food Chem. 2020, 325, 126870.
De-Melo, A.A.M.; De Almeida-Muradian, L.B.; Sancho, M.T.; Pascual-Maté, A. Composition and properties of Apis mellifera honey: A review. J. Apic. Res. 2017, 57, 5–37.
Mohan, A.; Quek, S.Y.; Gutierrez-Maddox, N.; Gao, Y.; Shu, Q. Effect of honey in improving the gut microbial balance. Food Qual. Saf. 2017, 1, 107–115.
Pătruică, S.; Dumitrescu, G.; Popescu, R.; Filimon, N.M. The effect of prebiotic and probiotic products used in feed to stimulate the bee colony (Apis mellifera) on intestines of working bees. J. Food Agric. Environ. 2013, 11, 2461–2464.
Wu, M.; Sugimura, Y.; Takaya, N.; Takamatsu, D.; Kobayashi, M.; Taylor, D.; Yoshiyama, M. Characterization of bifidobacteria in the digestive tract of the Japanese honeybee, Apis cerana japonica. J. Invertebr. Pathol. 2013, 112, 88–93.
Nonthapa, P.; Chanchao, C. Pathogen detection and gut bacteria identification in Apis cerana indica in Thailand. Afr. J. Biotechnol. 2015, 14, 3235–3247.
Pattabhiramaiah, M.; Reddy, M.S.; Brueckner, D. Detection of novel probiotic bacterium Lactobacillus spp. in the workers of Indian honeybee, Apis cerana indica. Int. J. Environ. Sci. 2012, 2, 1135–1143.
Tajabadi, N.; Mardan, M.; Manap, M.Y.A.; Mustafa, S. Molecular identification of Lactobacillus spp. isolated from the honey comb of the honey bee (Apis dorsata) by 16s rRNA gene sequencing. J. Apic. Res. 2013, 52, 235–241.
Uğras, S. Isolation, identification and characterization of probiotic properties of bacterium from the honey stomachs of Yigilca honeybees in Turkey. Türk. Entomol. Derg. 2017, 41, 253–261.
Kenfack, C.H.M.; Kaktcham, P.M.; Ngoufack, F.Z.; Wang, Y.R.; Yin, L.; Zhu, T. Screening and characterization of putative probiotic lactobacillus strains from honey bee gut (Apis mellifera). J. Adv. Microb. 2018, 10, 1–18.
Kenfack, C.H.M.; Kaktcham, P.M.; Ngoufack, F.Z.; Wang, Y.R.; Yin, L.; Zhu, T. Safety and antioxidant properties of five probiotic Lactobacillus plantarum strains isolated from the digestive tract of honey bees. Am. J. Microbiol. Res. 2018, 6, 1–8.
Honey, C.C.; Keerthi, T.R. Probiotic potency of Lactobacillus plantarum kx519413 and kx519414 isolated from honey bee gut. FEMS Microbiol. Lett. 2018, 365, fnx285.
Mathialagan, M.; Johnson, Y.S.; Edward, T.; David, P.M.M.; Senthilkumar, M.; Srinivasan, M.R.; Mohankumar, S. Isolation, characterization and identification of probiotic lactic acid bacteria (lab) from honey bees. Int. J. Curr. Microbiol. Appl. Sci. 2018, 7, 894–906.
Elzeini, H.M.; Ali, A.A.; Nasr, N.F.; Elenany, Y.E.; Hassan, A.A.M. Isolation and identification of lactic acid bacteria from the intestinal tracts of honey bees, Apis mellifera L., in Egypt. J. Apic. Res. 2020, 60, 349–357.
Endo, A.; Salminen, S. Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Syst. Appl. Microbiol. 2013, 36, 444–448.
Janashia, I.; Carminati, D.; Rossetti, L.; Zago, M.; Fornasari, M.E.; Haertlé, T.; Chanishvili, N.; Giraffa, G. Characterization of fructophilic lactic microbiota of Apis mellifera from the Caucasus Mountains. Ann. Microbiol. 2016, 66, 1387–1395.
Pachla, A.; Wicha, M.; Ptaszyńska, A.A.; Borsuk, G.; Laniewska –Trokenheim, L.; Małek, W. The molecular and phenotypic characterization of fructophilic lactic acid bacteria isolated from the guts of Apis mellifera L. derived from a Polish apiary. J. Appl. Genet. 2018, 59, 503–514.
Pachla, A.; Ptaszyn’ska, A.A.; Wicha, M.; Kunat, M.; Wydrych, J.; Olen´ska, E.; Małek, W. Insight into probiotic properties of lactic acid bacterial endosymbionts of Apis mellifera L. derived from the Polish apiary. Saudi J. Biol. Sci. 2021, 28, 1890–1899.
Al-Ghamdi, A.; Khan, K.A.; Ansari, M.J.; Al-Masaudi, S.B.; Al-Kahtani, S. Effect of gut bacterial isolates from Apis mellifera Jemenitica on Paenibacillus larvae infected bee larvae. Saudi J. Biol. Sci. 2017, 25, 383–387.
Vergalito, F.; Testa, B.; Cozzolino, A.; Letizia, F.; Succi, M.; Lombardi, S.J.; Tremonte, P.; Pannella, G.; Di Marco, R.; Sorrentino, E.; et al. Potential application of Apilactobacillus kunkeei for human use: Evaluation of probiotic and functional properties. Foods 2020, 9, 1535.
Wu, M.; Sugimura, Y.; Iwata, K.; Takaya, N.; Takamatsu, D.; Kobayashi, M.; Taylor, D.; Kimura, K.; Yoshiyama, M. Inhibitory effect of gut bacteria from the Japanese honey bee, Apis cerana japonica, against Melissococcus plutonius, the causal agent of European foulbrood disease. J. Insect Sci. 2014, 14, 129.
Hamdy, A.A.; Esawy, M.A.; Elattal, N.A.; Amin, M.A.; Ali, A.E.; Awad, G.E.A.; Connerton, I.; Mansour, N.M. Complete genome sequence and comparative analysis of two potential probiotics Bacillus subtilis isolated from honey and honeybee microbiomes. J. Genet. Eng. Biotechnol. 2020, 18, 34.
Khalafalla, M.S.; Sadik, M.W.; Ali, M.A.; Mohamed, R.S. Novel potential probiotics from gut microbiota of honeybees (Apis mellifera) in clover feeding season in Egypt. Plant Arch. 2019, 19, 3381–3389.
Tajabadi, N.; Mardan, M.; Saari, N. Identification of Lactobacillus plantarum, Lactobacillus pentosus and Lactobacillus fermentum from honey stomach of honeybee. Braz. J. Microbiol. 2013, 44, 717–722.
Zarour, K.; Prieto, A.; Perez-Ramos, A.; Kihal, M.; Lopez, P. Analysis of technological and probiotic properties of Algerian L. mesenteroides strains isolated from dairy and non-dairy products. J. Funct. Foods 2018, 49, 351–361.
Putri, I.; Jannah, S.N.; Purwantisari, S. Isolation and characterization of lactic acid bacteria from Apis mellifera and their potential as antibacterial using in vitro test against growth of Listeria monocytogenes and Escherichia coli. NICHE J. Trop. Biol. 2020, 3, 26–34.
Esawy, M.A.; Awad, G.E.A.; Ahmed, E.F.; Danial, E.N.; Mansour, N.M. Evaluation of honey as a new reservoir for probiotic bacteria. Adv. Food Sci. 2012, 34, 72–81.
Razmgah, N.; Mojgani, N.; Torshizi, M. Probiotic potential and virulence traits of Bacillus and Lactobacillus species isolated from local honey sample in Iran. J. Pharm. Biol. Sci. 2017, 11, 87–95.
Abdel Wahab, W.A.; Saleh, S.A.A.; Karam, E.A.; Mansour, N.M.; Esawy, M.A. Possible correlation among osmophilic bacteria, levan yield, and the probiotic activity of three bacterial honey isolates. Biocatal. Agric. Biotechnol. 2018, 14, 386–394.
Jia, L.; Kosgey, J.C.; Wang, J.; Yang, J.; Nyamao, R.M.; Zhao, Y.; Teng, X.; Gao, L.; Cheteu Wabo, M.T.; Vasilyeva, N.V.; et al. Antimicrobial and mechanism of antagonistic activity of Bacillus sp. A2 against pathogenic fungus and bacteria: The implication on honey’s regulatory mechanism on host’s microbiota. Food Sci. Nutr. 2020, 8, 4857–4867.
Pașca, C.; Mărghitaș, L.A.; Matei, I.A.; Bonta, V.; Mărgăoan, R.; Copaciu, F.; Bobiș, O.; Campos, M.G.; Dezmirean, D.S. Screening of some romanian raw honeys and their probiotic potential evaluation. Appl. Sci. 2021, 11, 5816.
Begum, S.B.; Roobia, R.R.; Karthikeyan, M.; Murugappan, R. Validation of nutraceutical properties of honey and probiotic potential of its innate microflora. LWT-Food Sci. Technol. 2015, 60, 743–750.
Zahoor, F.; Sooklim, C.; Songdech, P.; Duangpakdee, O.; Soontorngun, N. Selection of potential yeast probiotics and a cell factory for xylitol or acid production from honeybee samples. Metabolites 2021, 11, 312.
Wang, S.; Xiao, Y.; Tian, F.; Zhao, J.; Zhang, H.; Zhai, Q.; Chen, W. Rational use of prebiotics for gut microbiota alterations: Specific bacterial phylotypes and related mechanisms. J. Funct. Foods 2020, 66, 103838.
Saran, S.; Bisht, M.S.; Singh, K.; Teotia, U.V.S. Comparing adhesion attributes of two isolates of Lactobacillus acidophilus for assessment of prebiotics, honey and inulin. Int. J. Sci. Res. Publ. 2012, 2, 2250–3153.
Das, A.; Datta, S.; Mukherjee, S.; Bose, S.; Ghosh, S.; Dhar, P. Evaluation of antioxidative, antibacterial and probiotic growth stimulatory activities of Sesamum indicum honey containing phenolic compounds and lignans. LWT-Food Sci. Technol. 2015, 61, 244–250.
Celebioglu, H.U. Probiotic bacteria grown with chestnut honey enhance in vitro cytotoxicity on breast and colon cancer cells. Arch. Biol. Sci. 2020, 72, 329–338.
Bemmo, U.L.; Kenfack, C.H.; Bindzi, J.M.; Barry, R.B.; Ngoufack, F.Z. Viability and in vivo hypocholesterolemic effect of Lactobacillus plantarum 29V in local honey. J. Adv. Biol. Biotechnol. 2021, 24, 24–33.
Fratianni, F.; Ombra, M.N.; d’Acierno, A.; Caputo, L.; Amato, G.; De Feo, V.; Coppola, R.; Nazzaro, F. Polyphenols content and in vitro α-glycosidase activity of different Italian monofloral honeys, and their effect on selected pathogenic and probiotic bacteria. Microorganisms 2021, 9, 1694.
Narayanan, R.; Subramonian, B.S. Effect of prebiotics on bifidobacterial species isolated from infant faeces. Indian J. Tradit. Knowl. 2015, 14, 285–289.
Aly, H.; Said, R.N.; Wali, I.E.; Elwakkad, A.; Soliman, Y.; Awad, A.R.; Shawky, M.A.; Abu Alam, M.S.; Mohamed, M.A. Medically graded honey supplementation formula to preterm infants as a prebiotic: A randomized controlled trial. JPGN 2017, 64, 966–970.
Jiang, L.; Xie, M.; Chen, G.; Qiao, J.; Zhang, H.; Zeng, X. Phenolics and carbohydrates in Buckwheat honey regulate the human intestinal microbiota. Evid. Based Complement. Altern. Med. 2020, 2020, 6432942.
Lane, A.J.; Calonne, J.; Slattery, H.; Hickey, R.M. Oligosaccharides Isolated from MGO™ Manuka Honey Inhibit the Adhesion of Pseudomonas aeruginosa, Escherichia Coli O157:H7 and Staphylococcus Aureus to Human HT-29 Cells. Foods 2019, 8, 446.
Li, Y.; Long, S.; Liu, Q.; Ma, H.; Li, J.; Wei, X.; Yuan, J.; Li, M.; Hou, B. Gut microbiota is involved in the alleviation of loperamide-induced constipation by honey supplementation in mice. Food Sci. Nutr. 2020, 8, 4388–4398.
Swears, R.M.; Manley-Harris, M. Composition and potential as a prebiotic functional food of a Giant Willow Aphid (Tuberolachnus salignus) honeydew honey produced in New Zealand. Food Chem. 2021, 345, 128662.
Mohan, A.; Gutierrez-Maddox, N.; Meng, T.; He, N.; Gao, Y.; Shu, Q.; Quek, S.Y. Manuka honey with varying levels of active manuka factor (AMF) ratings as an anaerobic fermentation substrate for Limosilactobacillus reuteri DPC16. Fermentation 2021, 7, 128.
Rayes, A.A.H. Enhancement of probiotic bioactivity by some prebiotics to produce bio-fermented milk. Life Sci. J. 2012, 9, 2246–2253.
Varga, L.; Süle, J.; Nagy, P. Short communication: Viability of culture organisms in honey-enriched Acidophilus-bifidus-thermophilus (ABT)-type fermented camel milk. J. Dairy Sci. 2014, 97, 6814–6818.
Honey, C.C.; Meenu, D.M.; Keerthi, T.R. Effect of prebiotics on synbiotic fermented milk. World J. Pharm. Pharm. Sci. 2016, 5, 1557–1566.
Coskun, F.; Dirican, K.L. Effects of pine honey on the physicochemical, microbiological and sensory properties of probiotic yogurt. Food Sci. Technol. 2019, 39, 616–625.
Mohan, A.; Hadi, J.; Gutierrez-Maddox, N.; Li, Y.; Leung, I.K.H.; Gao, Y.; Shu, Q.; Quek, S.Y. Sensory, Microbiological and physicochemical characterisation of functional manuka honey yogurts containing probiotic Lactobacillus reuteri DPC162020. Foods 2020, 9, 106.
Ismail, M.; Hamad, M.; Elraghy, E.M. Quality of rayeb milk fortified with tamr and honey. Br. Food J. 2018, 120, 499–514.
Elenany, Y.E. Effect of incorporation of marjoram honey on the sensory, rheological and microbiological properties of goat yogurt. J. Entomol. 2019, 16, 9–16.
Mohamed, T.H.; Tammam, A.A.; Ali Bakr, I.; El-gazzar, F.E.S. Antioxidant, phenolic compounds and antimicrobial activity of yoghurt and bioyoghurt fortified with sedr honey. PAK J. Food Sci. 2016, 26, 161–172.
Riazi, A.; Ziar, H. Effect of honey and starter culture on growth, acidification, sensory properties and bifidobacteria cell counts in fermented skimmed milk. Afr. J. Microbiol. Res. 2012, 6, 486–498.
Rashid, A.; Thakur, E.S.N. Studies on quality parameters of set yoghurt prepared by the addition of honey. Int. J. Sci. Res. Publ. 2012, 2, 1–10.
Caldeira, L.A.; Alves, É.E.; Ribeiro, A.; Júnior, V.R.; Antunes, A.B.; Reis, A.F.; Gomes, J.; Carvalho, M.R.; Martínez, R. Viability of probiotic bacteria in bioyogurt with the addition of honey from Jataí and Africanized bees. Pesq. Agropec. Bras. Brasília 2018, 53, 206–211.
Fiorda, F.A.; de Melo Pereira, G.V.; Thomaz-Soccol, V.; Medeiros, A.P.; Rakshit, S.K.; Soccol, C.R. Development of kefir-based probiotic beverages with DNA protection and antioxidant activities using soybean hydrolyzed extract, colostrum and honey. LWT-Food Sci. Technol. 2016, 68, 690–697.
Slačanac, V.; Lučan, M.; Hardi, J.; Krstanović, V.; Koceva-Komlenić, D. Fermentation of honey-sweetened soymilk with Bifidobacterium lactis Bb-12 and Bifidobacterium longum Bb-46: Fermentation activity of bifidobacteria and in vitro antagonistic effect against Listeria monocytogenes FSL N1-017. Czech J. Food Sci. 2012, 30, 321–329.
Sri Desfita, W.S.; Yusmarini, Y.; Pato, U.; Zakłos-Szyda, M.; Budryn, G. Effect of fermented soymilk-honey from different probiotics on osteocalcin level in menopausal women. Nutrients 2021, 13, 3581.

© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.

Upload a video for this entry

Information

Subjects: Food Science & Technology

Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :

Suraiami Mustar

Nurliayana Ibrahim

View Times: 1.0K

Update Date: 22 Aug 2022

Table of Contents

Video Upload Options

Confirm

1. Introduction

2. Probiotic Properties of Honey Bees and Honey

3. Prebiotic Properties of Honey

References