Next Article in Journal
A Novel Principal Component Analysis Integrating Long Short-Term Memory Network and Its Application in Productivity Prediction of Cutter Suction Dredgers
Next Article in Special Issue
Health Promoting Effect of Phyllanthus emblica and Azadiractha indica against Advanced Glycation End Products Formation
Previous Article in Journal
Predictive Ability of Fahrenheit, a Hand Motion Recording System for Assessing Hand Motor Function in Patients with Hemiplegia Post-Cerebrovascular Disease—A Pilot Study
Previous Article in Special Issue
Basic Chemical Composition and Concentration of Selected Bioactive Compounds in Leaves of Black, Red and White Currant
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Applied Sciences
Volume 11
Issue 17
10.3390/app11178156
applsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Addition of Bee Products in Diverse Food Sources: Functional and Physicochemical Properties

by
Gloria Isabel Camacho-Bernal
1,
Nelly del Socorro Cruz-Cansino
1,*,
Esther Ramírez-Moreno
1,
Luis Delgado-Olivares
1,
Quinatzin Yadira Zafra-Rojas
1,
Araceli Castañeda-Ovando
2 and
Ángela Suárez-Jacobo
3
1
Instituto de Ciencias de la Salud, Universidad Autónoma del Estado de Hidalgo, Circuito Ex Hacienda La Concepción S/N, Carretera Pachuca-Actopan, San Agustín Tlaxiaca 42160, Hidalgo, Mexico
2
Instituto de Ciencias Básicas e Ingeniería, Universidad Autónoma del Estado de Hidalgo, Carretera Pachuca-Tulancingo Km. 4.5, Mineral de la Reforma 42184, Hidalgo, Mexico
3
Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco A.C., Biotecnología Industrial, Camino Arenero 1227, el Bajío del Arenal, Zapopan 45019, Jalisco, Mexico
*
Author to whom correspondence should be addressed.
Appl. Sci. 2021, 11(17), 8156; https://doi.org/10.3390/app11178156
Submission received: 29 July 2021 / Revised: 25 August 2021 / Accepted: 28 August 2021 / Published: 2 September 2021
(This article belongs to the Special Issue New Perspectives in Chemical and Functional Properties of Natural Products)
Review Reports Versions Notes

Abstract

:
The growing interest of consumers to find products with greater health benefits has led to multiple research works focused on product developments with antioxidant-rich foods by creating safe, acceptable, and high-value nutrition, even in those foods susceptible to deterioration, in order to replace synthetic preservatives with natural ones. Bee products are an alternative addition for food products (dairy and meat products, coating fruits, and alcoholic and non-alcoholic drinks), which can improve the final quality of the food for the benefit of the consumer. The aim of this review was to provide detailed information on the main findings of innovative food products based on the addition of bee products by highlighting their physicochemical and functional properties and their behavior throughout storage.

1. Introduction

The history of bee products dates back to ancient times; for example, the Greeks believed that pollen and honey were responsible for giving youth and life to kings, and as a result, it was highly valued. Further, it also performed an important role in religious rites [1,2].
Honey is the main product generated by bees and recognized for its sweet flavor derived from the nectar of flowers that bees collect, transform, and combine with specific substances of their own, and is then stored in the honeycomb to mature. It is essentially composed of sugars, predominantly fructose and glucose, in addition to other substances such as organic acids and enzymes [3]. Another apiary product is pollen, which is a natural product of great biological value obtained from hives.
The composition of bee products have been widely discussed depending on the geographical origin, as well as the importance of quality through the years [4]. In general, they are constituted by proteins, lipids, and vitamins, (mainly vitamin D), flavonoids, minerals (iron and zinc), dietary fiber, and carotenoids; however, this depends on drying techniques and storage conditions of the pollen [5]. In dairy products (yogurt, milk, and cheese), amins, pigments (chlorophylls, carotenoids), and aminoacids can act together as antioxidants [2,6].
Propolis is a solid collected by bees from the buds and exudates of plants, mixed with bee enzymes, pollen, and wax. It has been recognized in alternative medicine for its antimicrobial, anti-inflammatory, antitumor, immunomodulatory, and antioxidant activities [7,8]. Finally, there is the royal jelly, which is a thick, milky discharge produced by the hypopharyngeal and mandibular glands of bees. It serves as food for the larvae during the first three days and for the queen bee [9].
In recent years, multiple scientific research works maintain that dietary patterns have specific effects on the health–disease binomial, related to lifestyles, malnutrition and sedentary behavior, resulting in an increase in mortality [10]. As a consequence, the industrialized world faces new challenges, where researchers place emphasis on improving scientific knowledge about alternatives to achieve “optimal nutrition”, which can be defined as a nutrition model with nutrients or bioactive compounds to prevent disease and protect health, derived from the growing consumer demand for high-quality life standards [11]; therefore, enrichment is an option to provide micronutrients and health-promoting compounds in processed foods [12].
This approach has generated interest in taking advantage of the properties of apiary products in the food industry. In this paper, our objective was to present an overview of new food product developments with bee-related products added (honey, pollen, royal jelly, and propolis) and their impact on the food’s physicochemical characteristics and functional value. The review has been prepared considering six food product categories: dairy, fruits, drinks, meat, bakery and related products enriched with apiary products.

2. Dairy Products

The effect of apiary products content on the survival of yogurt starter bacteria, storage time, temperature, nutritional and functional composition, and sensory properties of dairy products (yogurt, milk, and cheese) is shown in Table 1.
There is significant interest in adding honey to dairy products because, in addition to being considered a sweetener, it produces changes in several characteristics (bacterial survival, nutritional composition, antioxidant content, antioxidant activity, and sensory properties). A similar effect has been observed in pollen, royal jelly, and propolis addition; thus, these changes are described below:

2.1. Bacterial Survival

The maintenance of bifidobacteria survival in milk is a challenge for the food industry due to the high nutrient demands of bacteria as well as proteolytic and glycolytic reactions [36]. It is reported that the oligosaccharides present in honey exhibit a potential prebiotic effect, stimulating the probiotic bacterial growth, thus producing an increase in bifidobacteria and lactobacilli counts [15,37]. A formulation with 5% of honey maintains the viability and average counts for L. acidophilus, even during storage (21 days) [17]. Likewise, in a yogurt powder, the incorporation of honey (2.5%) did not affect the lactic acid bacteria counts, finding similar CFU (Colony Forming Units) values to the control (3.1 × 108 and 2.8 × 108 CFU/g, respectively) [22]. Further, bee pollen has a positive effect on bacterial survival for L. acidophilus in fermented milk beverages; in contrast, when pollen was incorporated at high concentrations (20 mg/mL) [24]. This difference in results may be due to the L. acidophilus surviving in acid conditions [38].

2.2. Nutritional Composition

In general, the chemical composition of dairy products is determined by the bacteria metabolic activity that interacts with the environment during their growth, generating certain components as result of their metabolism [39]. The honey addition to yogurt samples causes changes during storage, resulting in an increase of 7% in fat and 25% in protein content [13].
There is a possible explanation for the protein increase, as it has been reported that honey contains a small concentration of protein [40,41]; however, this depends on the amount of honey added as well as its quality. With respect to fat, there is some controversy over whether honey leads to an increase in fat content; because other studies maintain that adding honey to yogurt leads to a decrease in fat content [30], and that honey has a low or even no fat content [42].
Regarding mineral profile, the honey incorporation between 2–9% showed high mineral content in comparison to control because apiary products are considered a rich source of minerals [21].
When added to cheese samples, pollen significantly increased the amount of protein in cheese samples [25]. Further, the ash concentration in yogurt increased considerably, which was related to its high dry matter concentration [32]. In relation to aminoacids and fatty acids content, yogurt with 5% honey added, as well as coconut milk, causes a decrease in saturated fatty acid content, but in medium and long-chain fatty acids, the content was similar to the control yogurt [16].
When pollen (0.6%) is present in yogurt, it provides a significant amount of valuable amino acid content (isoleucine, histidine, lysine, valine, methionine, threonine, arginine, proline, and cysteine). Furthermore, this addition resulted in a product with high amounts of fatty acids, except for butyric acid [34]. This effect could be due to the diversity of aminoacids (threonine, phenylalanine, and leucine) [43] and fatty acids (palmitic acid, stearic acid, oleic acid, linoleic acid, linoleic acid, and eicosenoic acid) contained in pollen [44], both fatty acids and aminoacids are important compounds for human health. Finally, the addition of propolis into yogurt generated similar fatty acid content compared to the control [29].

2.3. Physicochemical Properties

Some authors have dedicated efforts to determine how apiary products modify the pH and titratable acidity in yogurt; they affirm that 2% to 7% of added honey causes a decrease in acidity [14,17]. It is possible that the fructooligosaccharides contained in honey are responsible for this effect, where its addition could modify the pH of the products [37]. In other research work regarding acidity, the incorporation of pollen into yogurt leads to low levels of titratable acidity, even at minimal proportions of 0.4, 0.6, and 0.8% [35]. This is probably caused by the antimicrobial effect of pollen on S. thermophilus and L. bulgaricus, leading to a harmful effect on lactic acid bacteria [45]. On the other hand, the propolis extract in raw milk resulted in significantly high acidity values, which could be attributed to the improvement of lactic acid bacteria action, leading to a greater decomposition of sugars in the milk and an increase in acidity [28]. Numerous studies concluded that honey generates changes in total soluble solid content when it is added to dairy products [14,16,17,24]. It can be due to the fact that honey is composed mostly of sugars (they comprise approximately 95% of the dry weight), resulting in a high concentration [46].
Color is an important quality attribute of yogurt related to its acceptability, and it is considered one of the first attributes perceived by consumers [47]. The brightness (L*) of yogurt is related to the size of the fat and protein particles, which can affect their ability to disperse and reflect light [48]. In this way, the incorporation of honey into dairy products produces an increase in the a* values; however, these values depend on the amount of honey added. In yogurt, a 7% honey content generates a reduction in the brightness (L*) values [17].
With respect to rheological properties, the addition of honey caused an increase in the viscosity values (up to 126%) [17]. In comparison, the propolis addition promoted a non-Newtonian and pseudoplastic behavior [30]. In fermented beverages, the addition of pollen also allowed a significantly high viscosity [24].
Regarding the microstructure of dairy products, a yogurt formulation with added pollen resulted in a product with an uniform distribution and size of the casein micelles, giving rise to a product with more consistency and syneresis control during its storage [33].

2.4. Antioxidants Content and Antioxidant Properties

The addition of honey into yogurt significantly increases the total phenolic content, maintaining the differences with respect to the control yogurt during 4 weeks of storage [13]. Furthermore, 5% of honey in yogurt caused high values of antioxidant activity (5 more times) compared to the control [21]. Further, propolis extract caused a considerable increase in phenolic, flavonoids content, and antioxidant activity (aproximately 52%, 51%, and 4.54% more, respectively) than control yogurt [49]. Likewise, in buffalo milk powder with 20% of honey added, the phenolic compounds and flavonoids content were 5 and 28 times higher, respectively, as well as the antioxidant activity increased up to 12.61%, in comparison with the control sample [50]. Finally, a process of milk with pollen added was optimized, where the optimal pollen amount to preserve the functional properties was 13.72%, with a processing temperature of 26.84 °C, and 23.37 in Hg pressure [27]. The increase in polyphenol content and antioxidant activity is due to the fact that apiary products are rich sources of antioxidants [51], generating a high content when they are added to yogurt and milk.

2.5. Sensory Evaluation

Honey is recognized for its sweet taste, so when it is incorporated into other foods, it is necessary to evaluate whether it really improves the sensory properties. A level of 5% honey in yogurt promoted better acceptance in terms of taste, texture, and consequently in the sensory attributes of yogurt, even after being stored for 14 days [13]. Further, with honey levels between 5%, and 7%, it does not affect the level of acceptance, consistency, nor sweetness [17]. When pollen was added to yogurt (0.5%), it resulted in a product with a high acceptance level; however, when the total levels were higher than 1%, the flavor and taste were affected [26]. On the other hand, in fermented beverages, the addition of pollen between 2.5–20 mg/mL negatively influenced the taste, but on the contrary, a positive impact was observed in the texture scores. This effect could be due to the increase in viscosity by increasing the dry matter content, causing an improvement of the structural and sensory properties [24].
The addition of royal jelly into yogurt (0.6%) resulted in a product with good sensory quality, without a negative effect on the survival of lactic acid bacteria [21,32]. The propolis (1% and 2% in ethanolic extract) mixed with raw milk produced better characteristics in terms of aroma, body, texture, flavor, and general acceptability [28]. Further, a yogurt with 0.05% of royal jelly generated pleasant sensory characteristics. Nevertheless, formulations contained corn syrup and flavorings, and this could have favored the result [30].
Bee products have also led to several beneficial effects on products susceptible to alteration during storage. These results are directly related to each bee product; the honey and bee pollen provide sweetness and fruity taste [52,53], royal jelly provides a spicy taste [54], and the propolis adds a toasted, sweet, nutty taste [55]; however, these results depend on the amount added.
Their implementation in fruits can protect the fruits against deterioration; this implementation is described in the following section.

3. Fruits

Propolis also has a diversity of applications in food technology, highlighting its use in the improvement of some attributes of fruits through the generation of biodegradable coatings, which can be another option for the production of films [56,57]. Artepillin C is a compound of propolis that has beneficial effects, such as the preservation of fruits and a powerful antifungal activity [58].
For example, banana is a climacteric fruit that ripens quickly, losing quality and sensory attributes over time [59]. In response to this, the food industry has implemented new alternatives that allow regulating their deterioration. Propolis extract has been incorporated (2.5%) in bananas to prevent weight losses during a storage period of 12 days, although negative changes in the acceptance of the product were found [60]; however, when 5% of propolis extract was applied in orange peel, as a protective coating, the storage period was extended up to ten weeks [61]. The incorporation of 40% of honey in amla papaya jam generated a product with a high content of total soluble solids, carbohydrates, and ashes, and also increased their acceptability [62].
Another important application of bee products is in beverages; this is described in the following section.

4. Enriched Drinks

On a global scale, fruit juices are a versatile option that consumers find as an important part of the modern diet for their nutritional properties and sweet taste. Hence, their preservation is an important subject for food researchers [63]. The propolis addition (0.02 mg/mL) to juices shows an ability to maintain pH and titratable acidity in a period of 5 weeks, maintaining the carotenes and the color (measured as luminosity parameter) stability. It can also be an alternative to preserve the vitamin C content against degradation during storage (the propolis generates 13.12% less oxidation of vitamin) [64].
Likewise, in citrus juice samples, the addition of pollen (0.25 and 0.60%) increases the total phenols content (26.7% more), as well as the antioxidant activity. In contrast, in a sensory evaluation, its presence modifies the color and produces a sensation of powder on the tongue, identified by some panelists as unpleasant. Despite these changes, more than 70% of the panelists indicated that they would buy the product [65].
In malt beverages, pollen addition increases the content of phenols and flavonoids by 45.7% and 211.6%, respectively [66]. Finally, pollen in drinks improves not only the antioxidant properties but also its sensory characteristics. In wines with pollen concentrations of 0.1 and 0.25 g/L, it promotes better aromatic and taste characteristics; however, a high proportion is related to a lower aroma score due to a typical or similar odor of nuts or vegetables, accompanied by notes of bitter taste [53].
On the other hand, the quality and durability of meat products are a challenge in the food industry; therefore, bee products have shown interesting effects on their properties; this is described in the following section.

5. Meat Products

Meat products and all foods of animal origin are considered very susceptible to being affected by microorganisms. The addition of propolis ensures microbial stability and food quality during storage [67].
In general, the fat content and composition profile in hams and sausages play a fundamental role in their technofunctional characteristics; however, during processing, lipids are vulnerable to oxidation affecting their structure and generating the presence of various harmful volatile compounds, such as aldehydes, which are responsible for meat products becoming rancid. Lipid oxidative stability is a challenge for the food industry [68]. The main findings regarding the effects of bee pollen and propolis addition regarding lipid oxidation, physicochemical composition, microbiological characteristics, and sensory quality are described in Table 2.
The addition of propolis extract (0.06%) in cured ham is an alternative method to control lipid oxidation, producing a decrease in odor [69]. A similar protective effect was found in salami samples (0.05% propolis extract) in comparison to the positive control by using BHT (butylated hydroxytoluene) after 35 days of aging [73]. Further, burger meat with microencapsulated propolis (0.1 g/kg) added showed a better lipid oxidative stability than the use of a commercial additive (sodium erythorbate). The burger meat with added propolis showed a lower TBA (thiobarbituric acid) value than control during storage. The maximum malonaldehyde value was reached in 14 days, whereas in the control sample, it was reached at 7 days. This could be due to the gradual release of propolis bioactive compounds; however, for this product, the sensory characteristics and the general consumer acceptance were negatively affected [74].
Similarly, in fish burger meat with 5% propolis, changes affecting the odor were observed [70]. This effect was also observed with 1% propolis extract addition in fish sausages; however, in this research, it was concluded that the addition of propolis extract increases the shelf life of fish sausages by up to 3 weeks [75].
Definitively, the lower acceptance scores for meat with propolis addition could be related to their own taste and odor characteristics affecting the final product acceptance [74]. Although a perception of astringency caused by phenolic compounds is possible, depending not only on the amount added, but also on the composition of the enriched food [79].
On the other hand, 0.2% bee pollen in pork sausages shows a greater antioxidant effect and a better lipid peroxidation control during 30 days of storage by inhibiting the oxidation in 13.37% when compared to the control [77]. Further, in meatballs with added pollen, the lowest values of malonaldehyde were found at 90 days of storage. These results indicate that pollen is effective in delaying lipid oxidation in meatballs [76]; this mechanism could be associated with the presence of cinnamic acid derivatives and flavonoid content [80].
Some additives such as nitrate (antioxidant and preservative) are used in meat products; however, it is known that it has detrimental effects, e.g., reacting with the biogenic amines by the decarboxylation of some aminoacids [81], and it produces nitrogenous compounds known as cancer precursors [82]. Thus, propolis is a promising natural substitute with antimicrobial agents. When propolis was added in chorizo samples at 0.8 mg/mL, the growth of some bacteria, such as Staphylococcus aureus, Escherichia coli, Salmonella subsp., and Clostridium subsp., was inhibited. Furthermore, the addition does not cause any modification in the sensory attributes [71]. A 0.8% of propolis extract was used on fish fillet samples, resulting in a similar effect against the same bacteria previously described; an improved color score was also observed [72], where phenolic acids, anthraquinones, and flavonoid content [83], are thought to be responsible.
Currently, research has focused on the incorporation of bee products for the nutritional improvement or substitution of ingredients in formulations of baked products. This addition is considered to be a reasonable alternative to traditional additions, has better characteristics, and has a high acceptance rate by consumers; the addition of bee products to baked goods is described in the following section.

6. Bakery and Related Products

Bakery products are among the most popular ready-to-eat food products in the world [84]. Currently, a large proportion of people suffer intestinal malabsorption and gluten is often excluded from their diet [85]. Researchers have designed some gluten-free bakery products as an option; however, these products have a lower nutritional quality. To counter the lower nutritional quality, they must be fortified with other ingredients, e.g., amaranth, quinoa, and other seeds with high protein content [86,87,88]. Adding pollen in the range of 5% to gluten-free bread increased the content of protein by 0.54%, the potassium by 20%, and the calcium by 37%. The addition also improved the bioaccessibility of antioxidant compounds with an increase of 36% and the concentration of phenolic compounds by up to 11.2% [89].
In cookies with formulations containing 5.0%, 7.5%, and 10% of pollen, a significant increase in the protein content was obtained (0.6% more), a high percentage of ashes (up to 0.59%), and lower L* values. The lower L* values can be explained by the darkening caused by the pollen; however, it results in an increase in the total phenolics content by up to 2.9 and 2.3 more times that of the antioxidant activity. Finally, a positive effect on the maintenance of sensory parameters, by adding a concentration of 5%, since a greater amount produces changes in the taste, making it bitter and with a less pleasant consistency [90].
On the other hand, the mineral profile of a 15% honey enriched bread showed a calcium and iron content up to 12.53% and 35.34% more, respectively [91].
In cookie samples, with the addition of pollen in 16% and 32% (equivalent to 1 or 2 g), the protein content ranged from 7.18–9%; regarding ash, the sample with 16% contained the maximum antiradical activity with 69.91%, which leads to a pleasant taste, since high amounts (proportion higher than 16%) caused a decrease in acceptance, odor, and flavor with a predominance of cabbage notes [92].
Finally, the propolis addition (1%) in a croissant with honey (25%) caused an improvement in the color scores, without generating significant changes in the odor; however, an addition greater than 1% impairs the acceptance, decreases the moisture, but increased the ash and protein content (up to 1.17% and 19.79%, respectively) [93].

7. Enrichment of Apiary Products

Bee products have been used since ancient times in popular medicine due to their wide variety of beneficial health properties [94,95,96,97]. The number of bioactive compounds could be the basis for the attention, particularly for formulation development and food innovation [98]. Studies on the physico-chemical properties of apiary products with mixture of other bee products are scarce; due to most studies focus on the addition of honey, polen, propolis or royal jelly to other food matrices. Honey enriched with propolis at 0.1–1% intervals no generates changes in humidity, fructose, glucose, or sucrose content. It was observed that propolis added in the largest amount (1%) leads to an increase in the total phenolic, flavonoids, total phenolic acids, anthocyanins, and carotenoid content of 4.34, 5.37, 3.98, 2.61, and 1.37 more times, respectively. Further, in the same research, the same addition exhibited chrysin and p-cumaric acid as major compounds, reaching levels of 775 and 179 more times, respectively, compared to the control. Finally, regarding sensory properties, the propolis did not present changes in acceptance, except in a proportion higher than 0.3%, which results in low acceptability (unpleasant sensation and bitter taste), and the presence of an aftertaste as well as a change in the color and odor [99].
Other evidence establishes that honey enriched with propolis extract (0.3% and 0.5%, with 90% ethanol and 48 h of maceration) is promising, as it can maintain a good acceptance level in consumers. Furthermore, it showed a total phenolic compound and high flavonoids content (270.08 mg/100 g and 15.68 mg/100 g, respectively) compared to honey; however, the mixture with more than 0.5% of the extract was perceived as unpleasant, bitter, and intense [100].
A mixture of honey with dry cherries (40%) had better acceptability scores, even when stored for 3 months. Moreover, the total phenolic and flavonoid content increase up to 2.17 and 2.81 more times, respectively; this could be due to the fact that cherries are a rich source of antioxidants [101]. Similarly, a combination of honey with bee bread (10–60%) resulted in a product with a significant total of phenolic, flavonoids content, and an antioxidant activity of 3.99, 0.3, and 4.08 more times, respectively, than the control sample [102]. Furthermore, a mixture of honey with propolis extract (1%) and bee bread (15%) resulted in a product with a high phenolic compounds content (150 mg/100 g) and a high antioxidant activity (6.5 more times) as evaluated by DPPH•+ [103].

8. Conclusions

Given the importance of bee products described in this review (honey, pollen, propolis, and royal jelly) and the great variability of food matrices to which they can be incorporated, it is important to highlight the potential benefits as food ingredients. In dairy products, honey improves sensory attributes such as taste and texture, and results in an increase in phenolic compounds and antioxidant activity; however, viscosity increases and luminosity values decrease, which is seen as unfavorable. Propolis is an effective ingredient for the production of edible fruit films, and in sausages and meat products, it generates protective effects similar to synthetic preservatives due to its antimicrobial activity. Pollen addition in cookies leads to a significant increase in some micronutrients, as well as fiber, protein, phenolic compounds, and antioxidant activity. With respect to royal jelly, its incorporation into dairy products improves the physical and chemical characteristics during storage; it also allows for a uniform distribution of the casein micelles.
We recommend that future research for the food industry should be to find the optimal concentration of bee product additives (as ingredients) for different food matrices, without forgetting that, for every food product development, e.g., antioxidant-rich foods, it is necessary to have a safe final product, which provides health benefits to consumers, as well as good sensory properties.

Author Contributions

Investigation, G.I.C.-B.; Writing—Original Draft Preparation, G.I.C.-B., N.d.S.C.-C., and E.R.-M.; Writing—Review and Editing, N.d.S.C.-C., E.R.-M., A.C.-O., Q.Y.Z.-R., Á.S.-J., and L.D.-O. All authors have read and agreed to the published version of the manuscript.

Funding

The first author was supported by a fellowship from the Consejo Nacional de Ciencia y Tecnología (CONACYT) (No. 764080).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Campos, M.G.R.; Frigerio, C.; Lopes, J.; Bogdanov, S. What is the future of bee-pollen? J. ApiProd. ApiMed. Sci. 2010, 2, 131–144. [Google Scholar] [CrossRef]
  2. Kieliszek, M.; Piwowarek, K.; Kot, A.M.; Błażejak, S.; Chlebowska-Śmigiel, A.; Wolska, I. Pollen and bee bread as new health-oriented products: A review. Trends Food Sci. Technol. 2018, 71, 170–180. [Google Scholar] [CrossRef]
  3. Codex Alimentarius Commission. Codex Standard for Honey; Allinorm 1; FAO: Roma, Italy, 2001; pp. 19–26. [Google Scholar]
  4. Thakur, M.; Nanda, V. Composition and functionality of bee pollen: A review. Trends Food Sci. Technol. 2020, 98, 82–106. [Google Scholar] [CrossRef]
  5. Kostić, A.; Milinčić, D.D.; Barać, M.B.; Ali Shariati, M.; Tešić, Ž.L.; Pešić, M.B. The Application of Pollen as a Functional Food and Feed Ingredient-The Present and Perspectives. Biomolecules 2020, 10, 84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Komosinska-Vassev, K.; Olczyk, P.; Kazmierczak, J.; Mencner, L.; Olczyk, K. Bee pollen: Chemical composition and therapeutic application. Evid.-Based Complement. Altern. 2015, 2015, 297425. [Google Scholar] [CrossRef] [Green Version]
  7. Sforcin, J.M. Biological properties and therapeutic applications of propolis. Phyther. Res. 2016, 30, 894–905. [Google Scholar] [CrossRef] [PubMed]
  8. Toreti, V.C.; Sato, H.H.; Park, Y.K.; Pastore, G.M. Recent progress of propolis for its biological and chemical compositions and its botanical origin. Evid.-Based Complement. Altern. Med. 2013, 2013, 697390. [Google Scholar] [CrossRef]
  9. Isidorov, V.A.; Czyzewska, U.; Isidorova, A.G.; Bakier, S. Gas chromatographic and mass spectrometric characterization of the organic acids extracted from some preparations containing lyophilized royal jelly. J. Chromatogr. B. 2009, 877, 3776–3780. [Google Scholar] [CrossRef]
  10. WHO/FAO. Diet, Nutrition and the Prevention of Chronic Diseases. Report of a Joint WHO/FAO Expert Consultation; WHO Technical Report Series; WHO: Geneva, Switzerland, 2003; Available online: http://whqlipdoc.who.int/trs/who_trs_916.pdf (accessed on 14 May 2021).
  11. Ashwell, M. Concepts of Functional Foods [Internet]; ILSI Europe Concise Monograph Series; ILSI Press: Washington, DC, USA, 2002; 40p. [Google Scholar]
  12. Ahmed, A.; Anjum, F.; Ur Rehman, S.; Randhawa, M.; Farooq, U. Bioavailability of calcium, iron and zinc fortified whole wheat flour chapatti. Plant Foods Hum. Nutr. 2008, 63, 7–13. [Google Scholar] [CrossRef]
  13. Bakr, I.A.; Mohamed, T.H.; Tammam, A.A.; El-Gazzar, F.E. Characteristics of bioyoghurt fortified with fennel honey. Int. J. Curr. Microbiol. Appl. Sci. 2015, 4, 959–970. [Google Scholar]
  14. Ammar, E.T.M.A.; Ismail, M.M.; Khalil, A.E.-W.E.; Eid, M.Z. Impact of fortification with honey on some properties of bio-yoghurt. J. Microbiol. Biotechnol. Food Sci. 2015, 4, 503–508. [Google Scholar] [CrossRef] [Green Version]
  15. Mohamed, T.H.; Tammam, A.A.; Bakr, I.A.; El-Gazzar, F.E. Antioxidant, phenolic compounds and antimicrobial activity of yoghurt and bioyoghurt fortified with sedr honey. Pak. J. Food Sci. 2016, 26, 161–172. [Google Scholar]
  16. Hamad, M.N.F.; Ismail, M.M.; El-Kadi, S.M.L.; Zidan, M.S. Chemical composition, microbial properties and sensory evaluation of bio-yoghurt made from admixture of cow and coconut milk and honey. J. Food Dairy Sci. 2016, 2, 246–260. [Google Scholar] [CrossRef] [Green Version]
  17. Mercan, E.; Akın, N. Effect of different levels of pine honey addition on physicochemical, microbiological and sensory properties of set-type yoghurt. Int. J. Dairy Technol. 2016, 69, 1–8. [Google Scholar] [CrossRef]
  18. Rotar, A.M.; Semeniuc, C.; Bunghez, F.; Jimborean, M.; Pop, C. Effect of Different Storage Period on Lactic Acid Bacterias from Goji Yogurt and Goji Yogurt with Honey. Bull. UASVM Food Sci. Technol. 2014, 71, 75–76. [Google Scholar] [CrossRef] [Green Version]
  19. Machado, T.A.D.G.; de Oliveira, M.E.G.; Campos, M.I.F.; de Assis, P.O.A.; de Souza, E.L.; Madruga, M.S.; Pacheco, M.T.B.; Pintado, M.M.E.; do Egypto, R.D.C.R. Impact of honey on quality characteristics of goat yogurt containing probiotic Lactobacillus acidophilus. LWT-Food Sci. Technol. 2017, 80, 221–229. [Google Scholar] [CrossRef]
  20. Coskun, F.; Dirican, L.K. Effects of pine honey on the physicochemical, microbiological and sensory properties of probiotic yoghurt. Food Sci. Technol. 2019, 39, 616–625. [Google Scholar] [CrossRef] [Green Version]
  21. Metry, W.A.; Owayss, A.A. Influence of incorporating honey and royal jelly on the quality of yoghurt during storage. Egypt J. Food Sci. 2009, 37, 115–131. [Google Scholar]
  22. Kennas, A.; Amellal-Chibane, H.; Kessal, F.; Halladj, F. Effect of pomegranate peel and honey fortification on physicochemical, physical, microbiological and antioxidant properties of yoghurt powder. J. Saudi Soc. Agric. Sci. 2020, 19, 99–108. [Google Scholar] [CrossRef]
  23. Remenová, Z.; Canigová, M.; Krocko, M.; Ducková, V. Effect of added rape honey on chosen physicochemical and textural properties and antioxidant activity of yogurts during storage. J. Microbiol. Biotechnol. Food Sci. 2018, 8, 802–804. [Google Scholar] [CrossRef]
  24. Yerlikaya, O. Effect of bee pollen supplement on antimicrobial, chemical, rheological, sensorial properties and probiotic viability of fermented milk beverages. Mljekarstvo 2014, 64, 268–279. [Google Scholar] [CrossRef] [Green Version]
  25. Abd Elhamid, A.; Elbayoumi, M. Influence of bee pollen on the bioactive behavior, sensory and physicochemical properties of white cheese made from camel and cow milk mixture. J. Food Dairy Sci. 2017, 8, 419–424. [Google Scholar] [CrossRef] [Green Version]
  26. Karabagias, I.K.; Karabagias, V.K.; Gatzias, I.; Riganakos, K.A. Bio-functional properties of bee pollen: The case of “bee pollen yoghurt”. Coatings 2018, 8, 423. [Google Scholar] [CrossRef] [Green Version]
  27. Thakur, M.; Nanda, V. Process optimization of polyphenol-rich milk powder using bee pollen based on physicochemical and functional properties. J. Food Process. Eng. 2019, 42, 1–12. [Google Scholar] [CrossRef]
  28. El-Deeb, A. Utilization of propolis extract as a natural preservative in raw milk. J. Food Dairy Sci. 2017, 8, 315–321. [Google Scholar] [CrossRef]
  29. Santos, M.S.; Estevinho, L.M.; Carvalho, C.A.L.; Morais, J.S.; Conceição, A.L.S.; Paula, V.B.; Magalhães-Guedes, K.; Almeida, R.C.C. Probiotic yogurt with brazilian red propolis: Physicochemical and bioactive properties, stability, and shelf life. J. Food Sci. 2019, 84, 3429–3436. [Google Scholar] [CrossRef] [Green Version]
  30. Santos, M.S.; Estevinho, L.M.; de Carvalho, C.A.L.; da Silva Conceição, A.L.; de Castro Almeida, R.C. Rheological and sensorial evaluation of yogurt incorporated with red propolis. J. Food Sci. Technol. 2019, 57, 1080–1089. [Google Scholar] [CrossRef] [Green Version]
  31. Chon, J.-W.; Seo, K.-H.; Oh, H.; Jeong, D.; Song, K.-Y. Chemical and Organoleptic Properties of Some Dairy Products Supplemented with Various Concentration of Propolis: A Preliminary Study. J. Dairy Sci. Biotechnol. 2020, 38, 59–69. [Google Scholar] [CrossRef]
  32. Atallah, A. The production of bio-yoghurt with probiotic bacteria, royal jelly and bee pollen grains. J. Nutr. Food Sci. 2016, 06, 1–7. [Google Scholar] [CrossRef] [Green Version]
  33. Atallah, A.A.; Morsy, K.M. Effect of incorporating royal jelly and bee pollen grains on texture and microstructure profile of probiotic yoghurt. J. Food Process. Technol. 2017, 8, 8–11. [Google Scholar] [CrossRef]
  34. Atallah, A. Amino acids, fatty acids and volatile compounds of yoghurt supplemented with probiotic, royal jelly and pollen grain. Nutr. Food Sci. Int. J. 2018, 6, 1–6. [Google Scholar] [CrossRef]
  35. Zlatev, Z.; Taneva, I.; Baycheva, S.; Petev, M. A comparative analysis of physico-chemical indicators and sensory characteristics of yogurt with added honey and bee pollen. Bulg. J. Agric. Sci. 2018, 24, 132–144. [Google Scholar]
  36. Mohammadi, R.; Mortazavian, A.M. Review article: Technological aspects of prebiotics in probiotic fermented milks. Food Rev. Int. 2011, 27, 192–212. [Google Scholar] [CrossRef]
  37. Akalin, A.S.; Fenderya, S.; Akbulut, N. Viability and activity of bifidobacteria in yoghurt containing fructooligosaccharide during refrigerated storage. Int. J. Food Sci. Technol. 2004, 39, 613–621. [Google Scholar] [CrossRef]
  38. Kailasapathy, K.; Harmstorf, I.; Phillips, M. Survival of Lactobacillus acidophilus and Bifidobacterium animalis ssp. lactis in stirred fruit yogurts. LWT-Food Sci. Technol. 2008, 41, 1317–1322. [Google Scholar] [CrossRef]
  39. Collomb, M.; Schmid, A.; Sieber, R.; Wechsler, D.; Ryhänen, E.L. Conjugated linoleic acids in milk fat: Variation and physiological effects. Int. Dairy J. 2006, 16, 1347–1361. [Google Scholar] [CrossRef]
  40. Won, S.; Li, C.; Kim, J.; Rhee, H. Immunological characterization of honey major protein and its application. Food Chem. 2009, 113, 1334–1338. [Google Scholar] [CrossRef]
  41. Bueno-Costa, F.M.; Zambiazi, R.C.; Bohmer, B.W.; Chaves, F.C.; Silva WP da Zanusso, J.T.; Dutra, I. Antibacterial and antioxidant activity of honeys from the state of Rio Grande do Sul, Brazil. LWT-Food Sci. Technol. 2016, 65, 333–340. [Google Scholar] [CrossRef] [Green Version]
  42. Rashid, A. Thakur ESN. Studies on quality parameters of set yoghurt prepared by the addition of honey. Int. J. Sci. Res. Publ. 2012, 2, 1–10. [Google Scholar]
  43. Sommano, S.R.; Bhat, F.M.; Wongkeaw, M.; Sriwichai, T.; Sunanta, P.; Chuttong, B.; Burgett, M. Amino Acid Profiling and Chemometric Relations of Black Dwarf Honey and Bee Pollen. Front. Nutr. 2020, 7, 558579. [Google Scholar] [CrossRef]
  44. Mayda, N.; Özkök, A.; Ecem, N.; Yusuf, B.; Gerçek, C.; Sorkun, K. Bee bread and bee pollen of different plant sources: Determination of phenolic content, antioxidant activity, fatty acid and element profiles. J. Food Meas. Charact. 2020. [CrossRef]
  45. Lomova, N.; Narizhnyi, S.; Snizhko, O. Yoghurt enrichment with natural bee farming products. Ukr Food J. 2014, 3, 415–421. [Google Scholar]
  46. Da Silva, P.M.; Gauche, C.; Gonzaga, L.V.; Oliveira Costa, A.C.; Fett, R. Honey: Chemical composition, stability and authenticity. Food Chem. 2016, 196, 309–323. [Google Scholar] [CrossRef] [PubMed]
  47. Giusti, M.; Wrolstad, R. Acylated anthocyanins from edible sources and their application in food system. Biochem. Eng. J. 2003, 14, 217–225. [Google Scholar] [CrossRef]
  48. Ciron, C.; Gee, V.; Kelly, A.; Auty, M. Modifying the microstructure of low-fat yoghurt by microfluidisation of milk at different pressures to enhance rheological and sensory properties. Food Chem. 2012, 130, 510–519. [Google Scholar] [CrossRef]
  49. Mathias, T.R.; Carvalho Junior, I.; Carvalho, C. Rheological characterization of coffee- flavored yogurt with different types of thickener. Alim. Nutr. 2011, 22, 521–529. [Google Scholar]
  50. Bansal, V.; Premi, M.; Sharma, H.K.; Nanda, V. Compositional, physical, functional attributes and flow characterization of spray-dried skim milk powder enriched with honey. J. Food Meas. Charact. 2017, 11, 1474–1485. [Google Scholar] [CrossRef]
  51. Martinello, M.; Mutinelli, F. Antioxidant Activity in Bee Products: A Review. Antioxidants 2021, 10, 71. [Google Scholar] [CrossRef] [PubMed]
  52. Kivima, E.; Tanilas, K.; Martverk, K.; Rosenvald, S.; Timberg, L.; Laos, K. The Composition, Physicochemical Properties, Antioxidant Activity, and Sensory Properties of Estonian Honeys. Foods 2021, 10, 511. [Google Scholar] [CrossRef] [PubMed]
  53. Amores-Arrocha, A.; Roldán, A.; Cantizano, A.C.J.; Caro, I.; Palacios, V. Evaluation of the use of multiflora bee pollen on the volatile compounds and sensorial profile of Palomino fino and Riesling white young wines. Food Res. Int. 2018, 105, 197–209. [Google Scholar] [CrossRef]
  54. Kausar, S.H.; More, V.R. Royal Jelly: Organoleptic Characteristics and Physicochemical Properties. Pharm. Chem. J. 2019, 6, 20–24. [Google Scholar]
  55. Narbona, E.; García-García, E.; Vázquez-Araújo, L.; Carbolle-Barrachina, Á.A. Volatile composition of functional ‘a la Piedra’ turrón with propolis. Int. J. Food Technol. 2010, 45, 569–577. [Google Scholar] [CrossRef]
  56. Ali, A.; Chow, W.L.; Zahid, N.; Ong, M.K. Efficacy of propolis and cinnamon oil coating in controlling post-harvest anthracnose and quality of chilli (Capsicum annuum L.) during cold storage. Food Bioprocess. Technol. 2013, 7, 2742–2748. [Google Scholar] [CrossRef]
  57. Ali, A.; Wei, Y.Z.; Mustafa, M.A. Exploiting propolis as an antimicrobial edible coating to control post-harvest anthracnose of bell pepper. Packag. Technol. Sci. 2014, 28, 173–179. [Google Scholar] [CrossRef]
  58. Zahid, N.; Ali, A.; Siddiqui, Y.; Maqbool, M. Efficacy of ethanolic extract of propolis in maintaining postharvest quality of dragon fruit during storage. Postharvest Biol. Technol. 2013, 79, 69–72. [Google Scholar] [CrossRef]
  59. Chitarra, M.; Chitarra, A. Pós-Colheita de Frutas e Hortaliças: Fisiologia e Manuseio, 2nd ed.; UFLA: Lavras, Brazil, 2005; 785p. [Google Scholar]
  60. Passos, F.R.; Queiroz Mendes, F.; Crivelari da Cunha, M.; Teixeira Pigozzi, M.; Xavier de Carvalho, A.M. Propolis extract in postharvest consevation banana “prata”. Rev. Bras. Frutic. 2016, 38. [Google Scholar] [CrossRef] [Green Version]
  61. Badawy, I.F.M. Effect of ethanol-extracted propolis on fruit quality and storability of balady oranges during cold storage. Assiut J. Agric. Sci. 2016, 47, 156–166. [Google Scholar] [CrossRef]
  62. Srinu, D.; Suseela, K. Proximate and mineral composition of amla-papaya jam incorporated with honey. Int. J. Agric. Sci. Res. 2016, 6, 317–328. [Google Scholar] [CrossRef]
  63. Franke, A.; Cooney, R.; Henning, S.; Custer, L. Bioavailability and antioxidant effects of orange juice components in humans. J. Food Sci. Technol. 2005, 53, 5170–5178. [Google Scholar] [CrossRef] [Green Version]
  64. Yang, W.; Wu, Z.; Huang, Z.Y.; Miao, X. Preservation of orange juice using propolis. J. Food Sci. Technol. 2017, 54, 3375–3383. [Google Scholar] [CrossRef]
  65. Stan, L. Bee pollen as antioxidant ingredient in ready-to-serve citrus juice. Sci. Pap. Ser. D Anim. Sci. 2018, LXI, 312–317. [Google Scholar]
  66. Solgajová, M.; Ivanišová, E.; Nôžková, J.; Frančáková, H.; Tóth, Ž.; Dráb, Š. Antioxidant activity and polyphenol content of malt beverages enriched with bee pollen. J. Microbiol. Biotechnol. Food Sci. 2014, 3, 281–284. [Google Scholar]
  67. Ali, F.H.; Kassem, G.M.; Atta-Alla, O.A. Propolis as a natural decontaminant and antioxidant in fresh oriental sausage. Vet. Ital. 2010, 46, 167–172. [Google Scholar]
  68. Gandemer, G. Dry cured ham quality as related to lipid quality of raw material and lipid changes during processing: A review. Grasas Aceites 2009, 60, 297–307. [Google Scholar] [CrossRef]
  69. Kročko, M.; Bobko, M.; Bučko, O.; Čanigová, M.; Ducková, V. Sensory quality, colour and oxidative stability of cured cooked ham with propolis extract. Potravin. Slovak J. Food Sci. 2014, 8, 102–106. [Google Scholar] [CrossRef]
  70. Spinelli, S.; Conte, A.; Lecce, L.; Incoronato, A.L.; Del Nobile, M.A. Microencapsulated propolis to enhance the antioxidant properties of fresh fish burgers. J. Food Process. Eng. 2015, 38, 527–535. [Google Scholar] [CrossRef]
  71. Gutiérrez-Cortés, C.; Suarez Mahecha, H. Antimicrobial activity of propolis and its effect on the physicochemical and sensoral characteristics in sausages. Vitae Rev. Fac. Química Farm. 2014, 21, 90–96. [Google Scholar]
  72. Suarez, M.H.; Jiménez, T.Á.; Díaz, M.C. Determination of microbiological and sensory parameters of fish fillets with propolis preserved under refrigeration. Rev. MVZ Cordoba 2014, 19, 4214–4225. [Google Scholar] [CrossRef] [Green Version]
  73. Kunrath, C.A.; Savoldi, D.C.; Mileski, J.P.F.; Novello, C.R.; Da Trindade Alfaro, A.; Marchi, J.F.; Tonial, I.B. Application and evaluation of propolis, the natural antioxidant in Italian-type salami. Braz. J. Food Technol. 2017, 20, 1–10. [Google Scholar] [CrossRef] [Green Version]
  74. Reis, A.; Diedrich, C.; de Moura, C.; Pereira, D.; Almeida, J.F.; da Silva, L.D.; Plata-Oviedo, M.S.V.; Tavares, R.A.W.; Carpes, S.T. Physico-chemical characteristics of microencapsulated propolis co-product extract and its effect on storage stability of burger meat during storage at −15 °C. LWT-Food Sci. Technol. 2017, 76, 306–313. [Google Scholar] [CrossRef]
  75. Çoban, Ö.E.; Fadıoğlu, E.E.; Çoban, M.Z. Investigation of some quality characteristics of smoked common carp (Cyprinus carpio) sausages supplemented with propolis extract. Procedia Comput. Sci. 2018, 13, 196–203. [Google Scholar] [CrossRef] [Green Version]
  76. Turhan, S.; Saricaoglu, F.T.; Mortas, M.; Yazici, F.; Genccelep, H. Evaluation of color, lipid oxidation and microbial quality in meatballs formulated with bee pollen during frozen storage. J. Food Process. Preserv. 2017, 41, 1–8. [Google Scholar] [CrossRef]
  77. Almeida, J.F.; dos Reis, A.S.; Heldt, L.F.S.; Pereira, D.; Bianchin, M.; de Moura, C.; Plata-Oviedo, M.V.; Haminiuk, C.; Ribeiro, I.S.; Luz, C.F.P.; et al. Lyophilized bee pollen extract: A natural antioxidant source to prevent lipid oxidation in refrigerated sausages. LWT-Food Sci. Technol. 2017, 76, 299–305. [Google Scholar] [CrossRef]
  78. Fernanda, L.; Heldt, S.; Pereira, D.; Rodrigues Souza, B.; Almeida-Muradian, L.B.; Carpes, S.T. Fortification of beef burger with the addition of bee pollen from Apis mellifera L. Emir. J. Food Agric. 2019, 31, 895–901. [Google Scholar] [CrossRef]
  79. Çam, M.; Içyer, N.C.; Erdoǧan, F. Pomegranate peel phenolics: Microencapsulation, storage stability and potential ingredient for functional food development. LWT-Food Sci. Technol. 2014, 55, 117–123. [Google Scholar] [CrossRef]
  80. Leja, M.; Mareczek, A.; Wyzgolik, G.; Klepacz-Baniak, J.; Czekońska, K. Antioxidative properties of bee pollen in selected plant species. Food Chem. 2007, 100, 237–240. [Google Scholar] [CrossRef]
  81. Lv, F.; Liang, H.; Yuan, Q.; Li, C. In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res. Int. 2011, 44, 3057–3064. [Google Scholar] [CrossRef]
  82. Rojas-Graü, M.A.; Avena-Bustillos, R.J.; Olsen, C.; Friedman, M.; Henika, P.R.; Martín-Belloso, O.; Pan, Z.; McHugh, T.H. Effects of plant essential oils and oil compounds on mechanical, barrier and antimicrobial properties of alginate–apple puree edible films. J. Food Eng. 2007, 81, 634–641. [Google Scholar] [CrossRef]
  83. Duthoit, F.; Callon, C.; Tessier, L.; Montel, M.-C. Relationships between sensorial characteristics and microbial dynamics in “Registered Designation of Origin” Salers cheese. Int. J. Food Microbiol. 2005, 103, 259–270. [Google Scholar] [CrossRef]
  84. David, M. Nigeria, No 1 market for US Wheat; Potential for other grains and feeds. USAID Foreign Agric. Serv. Bull. 2006, 21, 1–2. [Google Scholar]
  85. Naik, R.; Seidner, D.; Adams, D. Nutritional consideration in celiac disease and nonceliac gluten sensitivity. Gastroenterol. Clin. N. Am. 2018, 47, 139–154. [Google Scholar] [CrossRef]
  86. Collar, C.; Conte, P.; Fadda, C.; Piga, A. Gluten-free dough-making of specialty breads: Significance of blended starches, flours and additives on dough behaviour. Food Sci. Technol. Int. 2015, 21, 523–536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  87. Haghayegh, G.; Ataye Salehi, S. Enrichment of gluten free cookie by quinoa, amaranth and buckwheat flour as semi cereal. Iran. J. Food Sci. Technol. 2017, 14, 47–56. [Google Scholar]
  88. Turkut, G.; Cakmak, H.; Kumcuoglu, S.; Tavman, S. Effect of quinoa flour on gluten-free bread batter rheology and bread quality. J. Cereal Sci. 2016, 69, 174–181. [Google Scholar] [CrossRef]
  89. Conte, P.; Del Caro, A.; Urgeghe, P.; Petretto, G.; Montanari, L.; Piga, A.; Fadda, C. Nutritional and aroma improvement of gluten-free bread: Is bee pollen effective? LWT-Food Sci. Technol. 2020, 118, 108711. [Google Scholar] [CrossRef]
  90. Krystyjan, M.; Gumul, D.; Ziobro, R.; Korus, A. The fortification of biscuits with bee pollen and its effect on physicochemical and antioxidant properties in biscuits. Food Sci. Technol. 2015, 63, 640–646. [Google Scholar] [CrossRef]
  91. Juhaimi, F.A.L.; Ghafoor, K.; Babiker, E.E.; Özcan, M.M.; Harmankaya, M. Mineral contents of traditional breads enriched with floral honey. Indian J. Tradit. Knowl. 2016, 15, 223–226. [Google Scholar]
  92. Solgajová, M.; Nozková, J.; Kadáková, M. Quality of durable cookies enriched with rape bee pollen. J. Cent. Eur. Agric. 2014, 15, 24–28. [Google Scholar] [CrossRef]
  93. Zeiny, A.; Shalaby, A.; Zemzemi, F.; Awad, O. Effect of croissant supplemented with honey and propolis on aspirin-induced stomach ulceration in rats. J Food Dairy Sci. 2015, 6, 177–191. [Google Scholar] [CrossRef]
  94. Kavanagh, S.; Gunnoo, J.; Marques Passos, T.; Stout, J.C.; White, B. Physicochemical properties and phenolic content of honey from different floral origins and from rural versus urban landscapes. Food Chem. 2019, 272, 66–75. [Google Scholar] [CrossRef]
  95. Kedzia, B.; Hołderna-Kedzia, E. Presence of phenolic compounds in bee honey. Phytother. Prog. 2008, 4, 225–232. [Google Scholar]
  96. Khalil, I.; Moniruzzaman, M.; Boukraâ, L.; Benhanifia, M.; Islam, A.; Islam, N.; Sulaiman, S.A.; Gan, S.H. Physicochemical and Antioxidant Properties of Algerian Honey. Molecules 2012, 17, 11199–11215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Wilczynska, A. Phenolic content and antioxidant activity of different types of Polish honey-A short report. Pol. J. Food Nutr. Sci. 2010, 60, 309–313. [Google Scholar]
  98. Socha, R.; Habryka, C.; Juszczak, L. Effect of bee bread additive on content of phenolic compounds and antioxidant activity of honey. Food Sci. Technol. Qual. 2018, 25, 108–119. [Google Scholar] [CrossRef]
  99. Habryka, C.; Socha, R.; Juszcak, L. The effect of enriching honey with propolis on the antioxidant activity, sensory characteristics, and quality parameters. Molecules 2020, 25, 1176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Osés, S.M.; Melgosa, L.; Pascual-Maté, A.; Fernández-Muiño, M.A.; Sancho, M.T. Design of a food product composed of honey and propolis. J. Apic. Res. 2016, 54, 461–467. [Google Scholar] [CrossRef]
  101. Vulić, J.J.; Čanadanović-Brunet, J.M.; Ćetković, G.S.; Djilas, S.M.; Tumbas Šaponjac, V.T.; Stajčić, S.M. Polyfloral, linden and acacia honeys with dried cherries after three months of storage—Antioxidant and sensory evaluation. Acta Period. Technol. 2015, 46, 103–114. [Google Scholar] [CrossRef] [Green Version]
  102. Juszczak, L.; Gałkowska, D.; Ostrowska, M.; Socha, R. Antioxidant activity of honey supplemented with bee products. Nat. Prod. Res. 2015, 30, 1436–1439. [Google Scholar] [CrossRef]
  103. Kowalski, S.; Makarewicz, M. Functional properties of honey supplemented with bee bread and propolis. Nat. Prod. Res. 2017, 31, 2680–2683. [Google Scholar] [CrossRef]
Table
Table 1. Effect of the concentration of bee products in dairy products, on bacterial cultures and physicochemical properties.
Table 1. Effect of the concentration of bee products in dairy products, on bacterial cultures and physicochemical properties.
Apiary ProductOriginBotanical OriginContent AddedType of ProductStorage Temperature (°C)Storage
Days		Bacterial CultureEffectReference
HoneyEgyptFennel honey5, 10, 15%Yogurt6 ± 20, 3, 7, 14ABT-5 cultures (Lactobacillus acidophilus, Bifidobacterium bifidum and Streptococcus thermophilus)Increase in Bifidobacteria counts during and at the end of storage time (until 54 × 106/g CFU), titratable acidity and total soluble solids were proportional to the honey content added and the storage time.[13]
HoneyEgypt----0, 2, 4, 6%Yogurt40, 7, 15S. thermophilus, L. delbrueckii subsp. bulgaricus (1:1) and ABT-5Bifidobacteria counts, acceptable to exhibit probiotic effect (1.7–3.5 × 106 CFU/g, at day 15), good sensory attributes, in particular, sample with 5% honey.[14]
HoneyEgyptSedr honey5, 10, 15, 20%Yogurt6 ± 20, 3, 7, 14L. delbrueckii ssp. bulgaricus, S. thermophilus and ABT-5Increases in B. bifidum and S. thermophilus and high protein proportion compared to the control,[15]
HoneyEgypt----5%Yogurt40, 7, 14S. thermophilus and L. delbrueckii subsp. bulgaricus (1:1) and ABT-5High L. bulgaricus and S. thermophilus counts, significant increase in ashes, unsaturated fatty acids content, improvement of consistency and flavor.[16]
HoneyTurkeyPine3, 5, 7%Yogurt40, 7, 14, 28S. thermophilus and L. delbrueckii subsp. bulgaricus (1:1)The addition of 7% honey presents the highest L. bulgaricus counts (8.27 log CFU/g). Better water retention capacity (led to lower syneresis), high viscosity than the control, low water activity, enhancement of antioxidant properties.[17]
Honey Romania----7% Yogurt --------S. thermophilus, and L. bulgaricusIncrease in S. thermophilus counts during storage, and a decrease in L. bulgaricus at the end of storage.[18]
HoneyBrazil----5, 10, 15%Yogurt4 ± 21, 7, 14, 21, 28S. salivarius subsp. thermophilus and L. delbrueckii subsp. bulgaricus and the probiotic culture of L. acidophilus La-05Honey as a growth-promoting probiotic ingredient (most evident between day 14 and before day 21 of storage). Odor characteristics, syneresis, viscosity, water retention capacity, sensory acceptance, and purchase intention were positively affected.[19]
Honey TurkeyPine2, 4, 6%Yogurt41, 7, 14, 21S. thermophilus, L. delbrueckii subsp. bulgaricus, L. rhamnosus, L. acidophilus, L. plantarum, B. animals subspL. acidophilus and L. delbrueckii counts were minor to the control. The presence of honey increases acidity, promote less syneresis and color modification with increasing concentration (L* values were affected).[20]
Honey and royal jellyEgyptEgyptian clover (honey)Honey: 2, 4, 6, 9%
Royal jelly: 0.2, 0.4, 0.6, 0.8, 1.0, 1.2, 1.5%		Yogurt5 ± 10, 3, 6, 9S. thermophilus and L. delbrueckii subsp. bulgaricusImproves viability of S. thermophilus with an addition of 4% honey, suggesting a prebiotic effect. An increase in viscosity and mineral content was observed.[21]
HoneyAlgeria MultifloralHoney: 0, 2.5, 5%
Pomegranate peel: 0, 2.5, 5, 10%		Yogurt powder4–6 ----S. thermophilus and L. delbrueckii subsp. bulgaricusNo significant differences in moisture content or particle sizes distribution and density values were affected. Fortified samples showed higher phenolic content and antioxidant activities than control samples.[22]
Honey SlovakiaRape honey1, 3, 5%Yogurt6 ± 11, 7, 14Laktoflora®The dry matter content increases gradually with the addition of honey, with a lower cohesion and firmness, but a high antioxidant activity.[23]
Apiary ProductOriginContent AddedType of ProductStorage Temperature (°C)Storage DaysBacterial CultureEffectReference
Bee pollenTurkey 2.5, 5.0, 7.5, 10, 20 mg/mLFermented milk beverages41, 7, 14, 21L. acidophilus, Bifidobacterium animalis subsp. lactis and S. thermophilus (ABT-1)Possible antimicrobial effect against B. Lactis, negative effect on sensory properties. Increase in soluble solids content, and viscosity, more proteolytic activity (first day). [24]
Bee pollen Egypt 0, 0.5, 1.0, 1.5, 2.0% White cheese (camel and cow milk) 100, 15, 30, 45-----Antibacterial activity (with 2%) for S. typhimurium and E. coli, 31 times high in total phenolic content (till 46.12 mg/g), detrimental effect on sensory attributes (texture, taste, acceptance, odor).[25]
Bee pollen Greece0.5, 1.0, 2.5, 3.0%Yogurt
(cow, goat and sheep)		4 ± 1----S. thermophilus and L. bulgaricusRadical inhibition around 100%, the potential effect of the surface material causing an improvement in appearance and cohesion.[26]
Bee pollen India 5, 10, 15%, with variations in temperature and pressureMilk powder 4--------Negative effect on solubility, apparent density within the limit for powdered foods, improvement of a lower molecular weight sugar concentration, resulting in a more hygroscopic powder.[27]
Propolis Egypt 1, 2, 3% (aqueous extract)Yogurt 5 ± 10, 7, 14L. delbrueckii subsp. bulgaricus and S. thermophilus (1:1)Variations in coagulation time were proportional to the aqueous extract of propolis added (synergistic effect); samples with 1 and 2% represented the highest sensory scores (fresh and during storage).[28]
PropolisBrazil0.05%Yogurt4 ± 20, 7, 14, 28L. acidophilus, Bifidobacterium and S. thermophilusAdequate concentrations of oleic and linoleic acid, without negative interactions in the survival of lactic acid bacteria, and high levels of antioxidant activity.[29]
PropolisBrazil0.05%Yogurt4 ± 20, 7, 14, 21, 28L. acidophilus, Bifidobacterium and S. thermophilusInhibitory effect for Salmonella spp., and E. coli., cohesion increases, good sensory acceptance.[30]
Propolis Brazil 0.5, 1.0, 1.5, 2.0%Commercial milk, yogurt and Kefir4----S. thermophilus, L. delbrueckii subsp. bulgaricus, L. acidophilus, and Bifidobacterium animalis subsp. lactisCommercial milk, yogurt, and Kefir supplemented with 0.5% of propolis resulted in best organoleptic characteristics for each product.[31]
Bee pollen and royal jellyEgyptRoyal jelly: 0.6%
Bee pollen: 0.8%		Yogurt~50, 7, 14, 21L. delbrueckii subsp. bulgaricus and S. thermophilus (1:1)Decrease of S. thermophilus and L. delbrueckii subsp. bulgaricus counts. Total content of solids, ash, fat, protein, and acidity increases significantly. Acceptability improving during storage (up to day 7).[32]
Royal jelly and bee pollenEgypt Royal jelly: 0.6%
Bee pollen: 0.8%		Yogurt 4 ± 10, 7, 14, 21L. delbrueckii spp. bulgaricus, S. thermophilus, Bifidobacterium angulatum, L. rhamnosus, and L. gasseriRefrigeration conditions increase hardness and chewiness in bee product added samples, resulting in a better texture and less syneresis.[33]
Royal jelly and bee pollen EgyptRoyal jelly: 0.6%
Bee pollen: 0.8% 		Yogurt4 ± 1----B. angulatum, L. gasseri and L. rhamnosusIncrease of amino acids and fatty acids content, high presence of acetaldehyde in treatment with 0.6% of royal jelly.[34]
Honey and bee pollenBulgaria Honey 5, 10, 15%
Bee Pollen: 0.4, 0.6, 0.8% 		Yogurt--------S. thermophilus and L. delbrueckii ssp. BulgaricusNo changes were observed in the organoleptic properties, with the incorporation of honey in 5% and pollen in 0.4%.[35]
Table
Table 2. Effect of the addition of bee products as natural antioxidants in storage conditions, on lipid oxidation, composition, microbiological, and sensory quality in meat products.
Table 2. Effect of the addition of bee products as natural antioxidants in storage conditions, on lipid oxidation, composition, microbiological, and sensory quality in meat products.
Apiary ProductOriginContent AddedType of ProductStorage Temperature (°C)Storage DaysEffectReference
Propolis Slovakia0.06% in extractCured cooked ham4 21 (sliced) and 20, 50, 100 (unsliced).Lower TBA values in unsliced hams after 100 days of storage. Hams sliced with propolis have a lower aroma intensity.[69]
Propolis ItalyPowdered to 5%Fish burgers--------Formulation with 5% spray-dried propolis and 10% potato flakes and 9% olive oil, shows an increase in antioxidant activity and better sensory quality.[70]
Propolis Colombia0.8%Sausages with 60% porcine meat, 20% bovine meat and 20% porcine fat50 0, 8, 16, 24TBA value similar to sausage with sodium nitrite, lower concentration of volatile nitrogenous bases in all storage, the propolis addition does not modify the consumer acceptance.[71]
PropolisColombia0.8, 1.2%Fish fillets 30, 4, 8, 12, 16, 20, 24Growth inhibition of bacterial pathogens (Clostridum sp., Salmonella, Escherichia coli, Staphylococcus aureus), acceptable microbiological load in storage with 0.8 mg/mL and 1.2 mg/mL (6.1 log CFU/g and 5.4 log CFU/g, respectively), color remained unchanged at 0.8% propolis added.[72]
PropolisBrazil0.01, 0.05% andcompared to TBHItalian-type salami (pork meat)181, 15, 35 No relevant changes in proximal composition, protective effect similar to BHT or TBAR with the extract of 0.05% propolis.[73]
Propolis Brazil 0.1 g/KgBurger meat (lean beef) −15 ± 0.6 0, 7, 14, 21, 28Effective protective agent to control TBA values similar to sodium erythorbate, aroma and flavor results below ideal. [74]
Propolis China 1%Fish sausages 263 (9 weeks)TBA values below the limit of 5 mg/kg in fish meat and lower than the control sample during storage, an improvement in shelf life is concluded, reduction in sensory attributes. Escherichia coli and Salmonella were not detected in any sample.[75]
Bee pollenTurkey0, 1.5, 3.0, 4.5, 6.0%Frozen meatballs−20 ± 10, 30, 60, 90Lower TBA values, total viable counts decreases. Chroma (C) and hue angle (h) values increases with 4.5 and 6.0%, respectively as the concentration of pollen is added.[76]
Bee pollenBrazil0.2 g/kgPork sausages40, 5, 10, 15, 20, 25, 30Control of lipid oxidation exhibiting lower TBA values, compared before (0.67 vs. 2.44 mg/kg) and after storage (4.08 vs. 4.71 mg/kg).[77]
Bee pollen Brazil0.1 g/KgBeef burger−120, 7, 14, 21, 28, 35 and 42Lower TBA values in the samples with pollen, suggesting an increase shelf life up to 42 days storage.[78]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Camacho-Bernal, G.I.; Cruz-Cansino, N.d.S.; Ramírez-Moreno, E.; Delgado-Olivares, L.; Zafra-Rojas, Q.Y.; Castañeda-Ovando, A.; Suárez-Jacobo, Á. Addition of Bee Products in Diverse Food Sources: Functional and Physicochemical Properties. Appl. Sci. 2021, 11, 8156. https://doi.org/10.3390/app11178156

AMA Style

Camacho-Bernal GI, Cruz-Cansino NdS, Ramírez-Moreno E, Delgado-Olivares L, Zafra-Rojas QY, Castañeda-Ovando A, Suárez-Jacobo Á. Addition of Bee Products in Diverse Food Sources: Functional and Physicochemical Properties. Applied Sciences. 2021; 11(17):8156. https://doi.org/10.3390/app11178156

Chicago/Turabian Style

Camacho-Bernal, Gloria Isabel, Nelly del Socorro Cruz-Cansino, Esther Ramírez-Moreno, Luis Delgado-Olivares, Quinatzin Yadira Zafra-Rojas, Araceli Castañeda-Ovando, and Ángela Suárez-Jacobo. 2021. "Addition of Bee Products in Diverse Food Sources: Functional and Physicochemical Properties" Applied Sciences 11, no. 17: 8156. https://doi.org/10.3390/app11178156

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop