2024 年 12 巻 p. 65-78
Bee pollen, also known as ‘life-giving dust’, is a treasure trove of nutrients and bioactive compounds. It is regarded as a valuable functional food ingredient owing to its various health-promoting effects. Thus, it can be incorporated into different food products for the development of functional foods. The nutritional and bioactive constituents of bee pollen contribute to its extensive health benefits, including its role against cancer, diabetes, liver disease, cardiovascular disorders, etc. Despite having numerous positive health implications, its utilization as a functional ingredient in food products needs to be critically evaluated in terms of clinical effects and safety profile. The exine layer of bee pollen limits its utilization and contributes to the low bioavailability of key nutrients. Processing techniques (chemical, physical, enzymatic) break down the robust outer coat, improves digestibility, and allow the diffusion of nutrients in the GI tract. In addition, 50 g of bee pollen is sufficient to fulfill 50% reference daily intake (RDI) of most vitamins and minerals. Overall, the use of bee pollen is safe and its use seems promising for coping with various nutritional inadequacies. This review focuses on the important aspects and specific considerations which are required to be taken into account before the development of bee pollen-based food products. Particular attention must be paid to nutritional adequacy, sensory attributes, health effects, allergenicity, digestibility, and compliance with regulatory bodies.
The primary role of diet is not only confined to hunger satisfaction or individual survival but rather also includes disease prevention and promoting the overall well-being of the consumer [1, 2]. Owing to the increased awareness of the population towards the importance of a healthy lifestyle, the current emphasis is laid on the role of functional foods in overall health promotion [2]. Thus, the functional food industry is considered to be one of the fastest-growing sectors which aims at the development of biologically active foods, beverages, and supplements by the addition of new components or increasing the amount of existing health-promoting components [3]. Functional foods are destined to have a physiological benefit and alleviate the risk factors responsible for causing chronic health problems besides providing the basic nutrients. Moreover, it should be considered that the functional foods must be similar to traditional/conventional foods and consumed as a part of a daily diet [3]. Along the same line, the current trend is the exploration of bee pollen as a functional ingredient due to its health-promoting effects as well as its rich nutritional profile [4].
Worker honeybees combine flower pollen with nectar and salivary secretions to produce bee pollen. The chemical and nutritional composition of different types of bee pollen is highly variable as it depends on multiple factors including the type of flower, season, geography, characteristics of soil, type of colony as well as the actions and handling of beekeepers [3]. Bee pollen can be considered a treasure-trove of nutrients due to the presence of various macro- and micronutrients viz., carbohydrates (40–60%), proteins (20–60%), lipids (1–32%), vitamins, minerals, phenolic compounds, carotenoids and other bioactive compounds [4]. It exhibits diverse pharmacological properties such as antioxidant, antimicrobial, anti-inflammatory, anticarcinogenic, antimutagenic, hepatoprotective, immunomodulatory as well as local analgesic action [3, 4].
Recent studies have demonstrated that bee pollen could be potentially used as a functional ingredient for the development of various fermented & non-fermented beverages, bakery, confectionery, and meat products [2]. Although bee pollen is an abundant source of nutrients, however, its consumption is also associated with allergic symptoms and cross-reactions with other allergens. Thus, there is a significant need to develop bee pollen-based products that are affordable, nutritionally balanced, and appealing to consumers. Special attention must be given to ensuring economical, nutritional, and organoleptic attributes as well as compliance with concerned regulatory bodies. The review at hand aims to throw light on the above-mentioned aspects to help researchers, industrialists, and manufacturers to develop bee pollen-based food products and beverages that are nutritious, safe for consumption, and meet the needs of different age groups. Bee pollen could be regarded as a viable functional food ingredient.
Bee pollen is considered a functional food ingredient due to its bioactive potential. Hence, the incorporation of bee pollen for developing different value-added food products will be a step forward to providing more nutrients via foods. It has been reported to be ‘the only perfectly complete food’ due to the presence of a significant amount of carbohydrates, fats, protein, phytosterols, phenolic compounds, carotenoids, enzymes, bio-elements, vitamins, nucleic acids, and triterpene acids [5]. The presence of these phytonutrients highlights the role of bee pollen in managing various health problems due to its extensive variety of pharmacological activities. It has been confirmed to exhibit antioxidant, antifungal, antimicrobial, anticancer, antidiabetic, antitoxic, antimutagenic, anti-inflammatory, antiradiation, chemo-preventive as well as hepatoprotective properties [3, 5]. The global burden of chronic health problems has increased tremendously as a result of environmental, genetic, behavioral as well as physiological factors [6]. The leading causes of death among the adult population are heart diseases, followed by cancer, respiratory tract problems and digestive disorders. Due to this increased burden, the pharmaceutical market has escalated remarkably to cure the aforementioned deadly diseases but at the same time, drug manufacturing companies are becoming extremely diverse, complex, less regulated, and less affordable [7]. Research studies have elucidated a strong interrelation between diet and health status of an individual. Consumers have developed a positive outlook on the consumption of a healthy diet instead of depending upon expensive drugs for disease prevention, which has further increased the demand for functional food products all across the globe. The size of the global functional food market was estimated to be $161.49 billion in the year 2018 and is projected to grow up to $529.66 billion by 2028 [8]. Based on increased consumer demand and interest in including functional foods as a part of their daily diet, manufacturers and health professionals have emphasized the development or incorporation of functional ingredients in conventional food products. Along the same line, bee pollen is considered to be a valuable front-runner among biologically active ingredients; therefore, its addition to foods will prove to be beneficial in the management of several medical as well as nutritional problems.
The essential amino acids present in bee pollen play a vital role in the optimal growth and development of an individual by monitoring gene expression and cell signaling pathways. Owing to its nutritionally-rich chemical composition, bee pollen can be utilized as a natural supplement that provides protection against many health problems such as diabetes, obesity [9], non-alcoholic fatty liver disease [10], acute myocardial infarction, atherosclerosis, hyperuricemia [11], oxidative damage, cancer [12], fluorosis [13], ovarian and testicular dysfunction, intestinal damage [14], food-borne mycotoxicity, prostatitis [12], amends cognitive dysfunction [15], regulates bone metabolism and acts as an immunostimulant [12, 16].
The presence of active metabolites in bee pollen, helps to improve cognitive function by converting pro-brain-derived neurotrophic factor (BDNF) to mature BDNF via Extracellular signal-regulated kinase (ERK)-response element-binding protein (CREB) pathway or protein kinase B (AKT)- glycogen synthase kinase-3β (GSK) signaling pathway [15]. The consumption of bee pollen leads to morphological changes in the small intestine including a relative increase in the epithelial volume, increased depth of Lieberkühn, and longer villi, which in turn increase the surface area for better absorption of nutrients in intestinal mucosa [14]. It inhibits the activity of intestinal enzymes which are responsible for the breakdown of polysaccharides into simple glucose molecules and raising the blood sugar levels [17]. Research studies have revealed the significant role of bee pollen in the amendment of testicular dysfunction by reducing oxidative stress, enhancing testicular antioxidant defense system, and increasing the levels of spermatids, spermatocytes, spermatogonia, and Sertoli cells [12]. It also contributes to the up-regulation of ovarian secretions (progesterone and estradiol) as well as pro-apoptotic and anti-apoptotic molecules, thus regulating ovarian functions. The phenolic compounds in bee pollen accelerates lipid metabolism, enhances nutrient absorption, and hence promotes weight loss [9]. Its consumption (1 g/kg body weight) is also linked with ameliorating degenerative changes in hepatocytes, hepatic steatosis and non-alcoholic fatty liver disease (NAFLD). Moreover, the consumption of high doses of bee pollen aids to decrease the activity of hepatic enzymes, blood urea nitrogen (BUN) as well as creatinine (Cr) levels [10].
Bee pollen causes a significant reduction in the levels of total serum cholesterol, low-density lipoprotein (LDL), asymmetric di-methylarginine (ADMA), angiotensin-II and angiotensin-converting enzyme (ACE) which would otherwise lead to the deposition of atherosclerotic plaques in blood capillaries. The flavonoids and other phenolic compounds have been reported to inhibit platelet aggregation, increase the synthesis of nitric oxide, inhibit xanthin oxidase, promote antioxidant activity and exhibit anti-hyperuricemic effect [11]. Furthermore, studies have also reported the utilization of bee pollen in ameliorating the signs of fluorine toxicity by decreasing malondialdehyde (MDA) levels, alkaline phosphatase (ALP) activity, BUN, sodium, potassium, and Cr levels [13]. Bee pollen poses anabolic effects on bone tissues (diaphyseal or metaphyseal) by increasing calcium deposition, maintaining calcium homeostasis and increasing the concentration of ALP which is very essential for bone mineralization [16].
Bee pollen boosts the immune system by increasing lymphocyte proliferation due to its amino acids, vitamins, minerals, phenolics and flavonoids. It also protects the immune system by increasing total serum protein, globulin, and neutrophil polymorphonuclear leukocyte (PMN)/lymphocyte ratio. Additionally, bee pollen has anti-allergic effects by inhibiting factors such as immunoglobulin E (Ig E) binding with mast cells, tumor necrosis factor (TNF) production, signal transduction pathway and inflammatory mediator production [18]. The various health benefits of bee pollen by different mechanisms are presented in Fig. 1.
Preparation of bee pollen-based food products is a difficult task for manufacturers with the main challenge being the exine layer which hampers its easy digestibility. Although it contains numerous health compounds, the utilization of bee pollen is limited due to its robust outer covering, exine. The removal of the outer tough coat is necessary to increase its nutritional quality and bioavailability. Various techniques including chemical treatments, high temperature, enzymatic hydrolysis, fermentation, and other physical treatments have been employed so far to destroy the exine layer which allows nutrients to flow freely [12]. Apart from this, another challenge faced by the manufacturers is the safety and acceptability of bee pollen as per the guidelines approved by various regulatory bodies [19]. Therefore, keeping all the above points in mind, several considerations need to be followed by manufacturers while developing any bee pollen-based food products.
4.1 Digestibility of bee pollenPollen cell walls are composed of stratified concentric layers, with the outermost layer referred to as exine. The pollen coat (exine) is characterized by its stability, flexibility, elasticity, strength, resistance and firmness, attributed to the presence of sporopollenin. Sporopollenin is composed of aliphatic compounds, phenolics and hydroxylated fatty acids. It is a strong and inert biopolymer known for its resistance against chemicals, high temperature, microbial action, and enzymatic treatment; which helps to protect the internal compounds of pollen. It consists of two layers, outer sexine and inner nexine (nexine I and nexine II). These biopolymers protect bee pollen from desiccation and unfavorable environmental conditions [20]. The extraordinary stability and tolerance of exine suggest that bee pollen has to be subjected to processing conditions to make it suitable for human consumption [21]. These processes serve two main purposes: first, to extend the shelf life of the product, and second, to enhance nutritional and functional quality indicators [20].
The use of chemical treatment to enhance digestibility is considered to be inappropriate while adding bee pollen to food supplements as it involves treatment with monoethanolamine (for 3 hours at 97 ºC), which is a chemical compound. Other chemical methods including acidic pretreatment and alkaline pretreatment (3% NaOH) are also employed to improve the digestibility and bioavailability of nutrients in bee pollen [20, 22]. Utilizing acidic solutions for incubation proves to be an effective pretreatment method for the industrial-scale enzymatic digestion of lignocellulosic materials [22]. The use of concentrated acids might lead to hydrolysis and elimination of additional pollen components, such as polysaccharides, proteins, and lipids found in the intine and pollen coat. This process leaves the sporopollenin-based exine unaffected [20]. Among the various options, diluted sulfuric acid stands out as the most extensively employed agent for acidic pretreatment, primarily due to its cost-effectiveness [22]. Physical methods like high temperature, ultrasound, and supercritical CO2 have also been used to disrupt the exine layer, however, these methods are not suitable on a small scale due to the associated cost of equipment as well as time [22]. Another method is the mechanical method which involves the action of shear forces leading to heat generation, which in turn result in the loss of heat-labile nutrients [23]. Some of the other suitable and affordable methods include fermentation and enzymatic treatment which have been proven to give more remarkable results. The former involves the use of bacteria (like Lactic acid bacteria, Apilactobacillus) for the dissolution of the exine layer; whereas, the latter involves the use of enzymes (protease, cellulase, pectinase, hemicellulase, papain) to breakdown the tough outer coat of pollen grain. Thus, these biotechnological processes may be employed to improve digestibility and aid in the easy diffusion of nutrients under controlled conditions in the gastrointestinal tract [12, 23, 24]. The average degree of carbohydrate and protein digestibility has been reported to be 4% and 53% respectively, which can be further increased by grinding and dissolving the bee pollen in warm water before consumption (Fig. 2). It helps to improve the functionality of pollen by increasing the accessibility of nutrients to 60–80% [25]. The application of such pre-treatments (acidic, alkaline, dry thermal, and wet thermal) helps to break the peptide bonds existing in complex protein structures, thereby increasing the digestibility up to as high as 85–98% [20].
Zuluaga et al. [25] made an attempt to examine the impact of both physical and biotechnological processing on the availability of nutrients and bioactive compounds in bee pollen. Their research revealed that subjecting bee pollen to thermal treatment at 121 ºC for 10 minutes, coupled with enzymatic hydrolysis, resulted in a comprehensive improvement in terms of digestibility (↑10%), total phenolics (↑14%), and antioxidant capacity (↑13%). Consequently, the modified bee pollen, particularly following thermal and enzymatic treatments, emerges as a potential complete food, due to increased nutritional and bioactive compounds, as compared to its already established nutritional composition.
The rising demand for natural products with health-promoting properties drives the increased consumption of bee pollen. Amid concerns about food safety, it is crucial for beekeepers to consistently monitor key stages in beekeeping, implementing good production and processing practices. Ensuring the quality of bee pollen involves prioritizing purity and microbiological safety. Neglecting hygienic standards during early production stages can lead to health risks for consumers. The critical step is pollen collection from traps, where prolonged storage may elevate humidity, fostering microbial growth [19, 25].
Despite having several beneficial properties as stated in the above-mentioned sections, bee pollen may either be primarily allergic to certain individuals or cross-react with other allergens. People having an intolerance to bee pollen might suffer from health problems such as diarrhea, abdominal pain, skin allergy, gastroenteritis, nausea, urticaria, malaise, cognitive impairment, rhinitis, dysphagia, myalgia, disorientation etc. [19]. Moreover, the presence of certain contaminants is another matter of concern that needs to be addressed before incorporating bee pollen into food products. Some of the most common contaminants present in bee-collected pollen include heavy metals, herbicides, ochratoxin A, mycotoxins, pesticides, pyrrolizidine alkaloids, bacteria etc. [26]. Bee pollen allergies result depending upon where the bee pollen comes from, i.e., plant variety. The possible reason for respiratory symptoms might be anemophilous plants containing water-soluble glycoproteins which evoke IgE antibody-mediated allergic reaction by either of the two mechanisms. The first mechanism involves the expulsion of allergenic particles from the cytoplasm by diffusion (in an isotonic medium) as a result of direct contact between pollen grain and mucosa. In the second mechanism, pollen grain gets hydrated rapidly in a hypotonic medium leading to the expulsion of small-sized inhalable allergic components which reach lower airways and cause asthma. In addition to this, other key factors like pH, time, temperature, and relative humidity may cause the secretion of a remarkable amount of eicosanoid-like substances which cross-react with prostaglandin E2 and leukotriene B4 to produce allergic reactions [27]. Allergy symptoms may also arise due to cross-reactivity between common epitopes on anemophilous and entomophilous pollens belonging to the same botanical family or reaction to honeybee antigens (derived from bee secretions) present in bee products (here, bee pollen). Some of the major allergen proteins found in different varieties of bee pollen include pollen-specific protein Bnm1, calmodulins, profilin, Sal k2, Sal k3, pollen allergen MetE (cobalamin-independent methionine synthase) and MRJPs (major royal jelly proteins). Moreover, the naturally present pollen enzymes may act as sensitizers that induce allergic symptoms such as rhinitis, sneezing and asthma in the human respiratory tract [28]. It has been suggested that the allergic symptoms are found to get resolved after treatment with diphenhydramine, epinephrine, chlorpheniramine and dexamethasone [29]. Various case studies on bee pollen-induced anaphylaxis have reported high levels of serum-specific IgE against pollens derived from Artemisia vulgaris (15.5 kU/L), Lolium perenne (4.9 kU/L), Cupressus arizonica (2.2 kU/L), Taraxacum officinalis (14.8 kU/L), Olea europaea (6.4 kU/L), Platanus acerifolia (3.4 kU/L), Cynodom dactylon, Plantago lanceolata, Dactylis glomerata, Poa pratensis, ragweed (25.2 kU/L), chrysanthemum (20.6 kU/L), dandelion (11.4 kU/L), sunflower, chamomile, mugwort, mesquite and willow. The bee pollen extracts of aforementioned varieties showed positive reactions in the skin-prick test [29, 30]. Thus, bee pollen and other bee products must be given very carefully to particularly children and older adults as they may cross-react with other allergens (like pollens and other bee products) [19].
4.3 Nutritional value and meeting Recommended Dietary Allowance (RDA) requirementsThe current trend is the replacement of conventional food ingredients with functional food ingredients having high nutritional significance to appeal the health-conscious consumers [31]. Bee pollen, also called the ‘life-giving dust’; is a rich source of nutritional components including carbohydrates, protein, lipids, fiber, fat-soluble vitamins (pro-vitamin A, D, E), water-soluble vitamins (B1, B2, B6, C), macro-minerals (Na, Mg, Ca, P, K), micro-minerals (Zn, Cu, Mn, Fe, Se), phospholipids, phytosterols, 1.6% phenolic compounds (catechins, leukotrienes), flavonoids (quercetin, isorhamnetin, kaempferol), nucleic acids, co-enzymes and other acids (folic acid, nicotinic acid, pantothenic, inositol, archaic, linoleic, γ-linoleic acid, chlorogenic acid) [12]. The chief bioactive compounds present in bee pollen are isorhamnetin, quercetin, kaempferol, quercetin-3-O-rutinoside, isorhamnetin-3-O-rutinoside, rhamnetin-3-O-neohesperidoside, quercetin-3-O-neohesperidoside, naringenin etc. [32].
Recommended Dietary Allowance (RDA) refers to the average daily nutrient intake adequate to meet the daily nutritional requirements of approximately 97–98% of individuals falling under a specific age group. Adhering to the RDA values provided by the Indian Council of Medical Research helps to fulfill the daily nutrient requirements of the body and aids in the control or prevention of various non-communicable as well as communicable diseases (hepatitis, influenza, etc.) [1]. Campos et al. [33] conducted a study to compare the average bee pollen composition and daily nutritional requirements of an individual as per Reference Daily Intake (RDI) and concluded that the contribution of macronutrients present in bee pollen viz., carbohydrates and fats were comparatively less than the other major nutritional components, i.e., protein and crude fiber which might contribute up to 60–70% of RDI. He further reported that the RDI is highly variable and is affected by the composition of bee pollen. The Spanish pollen variety (15 g) has been reported to adequately fulfill the daily requirement of free amino acids [34]. In addition to this, consumption of even 50 g of bee pollen is sufficient to meet 50% RDI of most of the essential vitamins as well as minerals except vitamins B5, B6 and calcium. A daily administration of 40 g bee pollen to cardiac patients helps to decrease total cholesterol, serum lipid content, blood viscosity, fibrinogen and fibrin concentration [31].
4.4 Anti-nutritional compounds in bee pollenBesides the nutritional components, bee pollen also possesses certain anti-nutritional compounds like pyrrolizidine alkaloids, mycotoxins, bacterial toxins, pesticides, metalloids and other toxic elements. The oral allergic reactions generally subside within 10–30 minutes after consuming bee pollen-based products. But these products are often tolerated by allergic individuals after employing certain cooking methods like boiling and baking. Bee-collected pollen derived from Echium and Senecio is prone to be hepatotoxic due to the presence of pyrrolizidine alkaloids; whereas, the improper and unhygienic handling of bee pollen increases the possibility of contamination of mycotoxins. Some of the potentially toxic elements present in bee pollen include aluminum, arsenic, cadmium, chromium, cobalt, iron, lead, mercury, nickel and strontium [25]. The acceptable contamination level or maximum tolerance level of these elements in bee pollen is 0.5 mg/kg for lead and arsenic, 0.1 mg/kg for cadmium, and 0.03 mg/kg for mercury. But there is no set recommendation for aluminum which is a potent neurotoxicant and can be present in a significant amount in pollen samples [33]. According to a research study conducted by Morgano et al. [35], the concentration of certain heavy metals (Al, As, Cd, Co, and Pb) and particulate matter were found to be higher in the dry season which is attributed to the air pollution during this period, hence favoring the contamination of bee pollen. Al toxicity in humans has been linked to clinical complications and neurological dysfunctions, including conditions like Alzheimer’s disease. The buildup of heavy metals within human body can result in serious health implications, such as carcinogenesis, mental disorders and various conditions that affect growth, development, metabolism and the nervous system. These inorganic pollutants vie with vital trace elements for available binding sites within biological systems, leading to adverse effects on the maintenance of homeostasis [36]. Furthermore, the nutritional composition and physicochemical properties of bee pollen favor the growth of several microbes including yeasts and mycotoxin-producing molds [36]. Aflatoxin B1, ochratoxin A, deoxynivalenol, neosolaniol, nivalenol, zearalenone, and fumonisins are among the most commonly occurring carcinogenic mycotoxins present in different pollen samples [33]. The maximum allowed concentration of aforementioned mycotoxins is 0.00–17.32 μg/kg, 0.00–10.98 μg/kg, 133.30–273.90 μg/kg, 22–30 μg/kg, 1 μg/kg, 115.60–361.30 μg/kg and 6.30–12.60 μg/kg, respectively. Aflatoxin contamination of bee pollen is influenced by factors like humidity, hygiene practices at the time of pollen harvesting, weather conditions and processing methods. Therefore, it must be suitably processed as well as properly stored followed by regular quality control before it is used for consumption [25, 33].
Airborne particulate matter is another pollutant that might contaminate bee pollen and cause a hazardous impact on the human cardiovascular, respiratory as well as gastrointestinal system. Apart from the negative impact on human health, it may also prove to be a major threat to the honeybee’s health by bringing about certain cytohistological modifications of the gut epithelium [37]. Papa et al. [37] attempted to identify the sources and potential risk of inorganic particulate matter in pollen grains obtained from honeybees residing in an industrial area. It was evident from the obtained results that pollen pellets were contaminated by airborne particulate matter such as iron compounds, barite, zinc, antimony oxides, silicon dioxide, lead, calcite, clay minerals, feldspars, quartz, etc. Studies have also suggested the presence of radioactive isotopes (137Cs, 40K) in bee products (bee pollen, honey, propolis) between 1986 and 1990 after the atomic power station accident on April 26, 1986, in Ukraine. Pesticide residue contamination of bee pollen is another area of study that has been widely investigated by several researchers. Furthermore, the most widely occurring active ingredients which serve as the major contaminants of bee pollen are carbendazim (169 µg/kg), thiacloprid (89 µg/kg), tebuconazole (30 µg/kg), acetamiprid (26 µg/kg), chlorpyrifos (16 µg/kg), fluvalinate (11 µg/kg) and thiametoxam (10 µg/kg) [36].
Over the past two decades, scientific research on bee pollen and associated food safety risks has increased, but some areas lack comprehensive information. Further studies are required, particularly on alternatives to banned pesticides found in bee pollen. Current literature is insufficient to make definitive conclusions about mycotoxin and mercury contamination. Bee pollen may contain heavy metals and pyrrolizidine alkaloids, posing potential health risks. Therefore, it is recommended to establish and monitor maximum limits for these substances in commercially available products [36, 37].
4.5 Processing of bee pollenWater concentration significantly influences the chemical constituents and storage life of a product, with water activity (aw) closely linked to quality. Higher aw favors microbial growth, potentially producing mycotoxins and ochratoxins. Fresh pollen pellets contain 20–30% moisture content, which is relatively high and favors the growth of various micro-organisms causing chemical as well as enzymatic reactions, further posing health risks and reduced shelf-life. To ensure safety and retain nutrients, dried pollen should have moisture content between 5% and 9%, with humidity levels ranging from 4% to 8%. Hence, ready-to-consume pollen should maintain a water activity between 0.261 and 0.280 which can be achieved by employing drying techniques like hot-air drying, vacuum drying, freeze-drying and microwave-assisted drying [25, 31]. Among all, freeze-drying is considered to be the most classic method for drying bee pollen as it helps to retain phenolic compounds, flavonoids and antioxidant activity when compared to other drying techniques viz., drying at 42 °C [25]. On the contrary, subjecting bee pollen to 60 °C results in reduced protein content and vitamin C content up to 43.7% and 31.5% respectively. In addition to this, there is a remarkable decrease in the physicochemical properties, morphological features as well as organoleptic attributes such as color, texture, and odor [38]. It has been suggested by Canale et al. [39] that microwave-assisted drying is a suitable technique when it comes to the preservation of bioactive constituents like rutin, but on the other hand, it also increases hydroxymethylfurfural levels by affecting diastasis activity. Castagna et al. [40] studied the effect of conventional drying on the bioactivity of chestnut pollen (an excellent source of phenolic compounds) and observed that it resulted in a substantial reduction in the concentration of total phenolic content.
Thakur et al. [41] attempted to optimize the spray drying technique for encapsulating bee pollen and developing functional milk powder. The study concluded that in comparison to fresh pollen, the total phenolic content was found to be decreased in developed powder. This might be attributed to the application of ultrasonication before spray drying leading to the release of phenolic compounds in the sample extract. Another research study aimed to encapsulate pollen pellets in hydrolyzed collagen and Arabic gum by using spray drying and lyophilization. The results confirmed that spray-dried pollens encapsulated with collagen and Arabic gum constitute high protein and fiber content; whereas, the lyophilized pollen samples had a more proportional chemical composition of carbohydrates, protein, lipids and fiber content [42].
Another processing method, i.e., baking might result in decarboxylation and depolymerization of phenolic acids and polyphenols, thereby causing a drastic reduction in the level of total phenolic compounds. Thus, fortification and enrichment of bakery products with bee pollen could be regarded as a useful option to overcome the losses of thermal treatment [43]. Researchers have investigated the effect of bee pollen enrichment in biscuits. The crude protein and ash content were increased remarkably with an increase in the concentration of bee pollen from 0 to 10%. Moreover, bee pollen substitution resulted in a statistically remarkable increase in total phenolic content as well as antioxidant activity [44]. Krystyjan et al. [43] suggested that an addition of 10% bee pollen in biscuits helps to increase the polyphenolic content and antioxidant activity remarkably. In terms of physical properties, bee pollen addition gives an intense color which is caused by a non-enzymatic reaction (Maillard browning) between reducing sugar and amino acids.
4.6 Storage of bee pollenThe overall quality of bee pollen gets largely affected by certain factors like cleaning, transportation, packaging, storage conditions and storage time. de Arruda et al. [45] stated that the functionality and nutritional value of bee pollen declines with time as storage allows the oxidation of phenolic compounds and Maillard reactions to occur. Thus, the concentration of β-carotene, vitamin B2, B6, B12, C and E decreases. The average loss of nutritional components like β-carotene, vitamin C and vitamin E has been reported to be 12%, 26% and 13% respectively in freezer storage conditions. To overcome these challenges, micro- and nano-encapsulation can be employed to prevent the degradation of sensitive phenolic compounds caused by exposure to air, O2, light, pH and heat processing techniques [25].
4.7 Techno-functional properties of bee pollenThe important techno-functional properties of bee pollen like hardness, chewiness, adhesiveness, gumminess, springiness, resilience and cohesiveness; have allowed its successful incorporation into various food products. An increase in the concentration of bee pollen leads to a decrease in gumminess, hardness, springiness and chewiness of meatballs and decreased hardness of biscuits as well as bread. Furthermore, it possesses good emulsifying properties and can therefore be added to natural emulsifiers used for the development of gluten-free bread [46]. On the other hand, it does not possess good foaming properties which limits its utilization in ice creams, toppings etc. [4].
Studies have revealed that bee collected pollen exhibits poor water absorption capacity which is a plus point because functional ingredients having high water absorption capacity might result in brittle and dry food products, particularly during storage. However, bee pollen possesses excellent oil-holding capacity which makes it an ideal ingredient in the formulation of food products for better retention of flavor and good mouthfeel [25, 46].
4.8 Compliance with FDA and FSSAI guidelinesCompliance with national as well as international standards and regulations is of utmost importance when it comes to the development of any food product. According to FDA (Food and Drug Administration) law, bee pollen can be marked as food because it does not pose any harmful effect on non-allergic individuals. However, FDA thwarts to mention any therapeutic claims regarding its consumption. To date, many promoters have made claims for bee pollen being ‘a giant germ killer’, ‘nature’s most perfect food’, ‘retards aging’, ‘the richest source of protein’, ‘relieves allergy’, ‘improves athletic performance’, but FDA invalidated and disapproved all these claims as there was no scientific evidence in favor of such statements. FDA states that bee pollen and its products must be prepared, packed, and held in a sanitary manner otherwise steps like injunction, seizure or criminal prosecution might be taken against the manufacturer [47]. According to Food Safety and Standards Authority of India (FSSAI) guidelines, the maximum moisture content in bee pollen should be 20% along with a 25,000/gram pollen count [48].
Bee pollen has widely been used as a functional food and feed ingredient. Numerous researchers have attempted to incorporate bee pollen for developing food products including fermented as well as non-fermented foods and beverages viz., Kombucha, mead, wines, yogurt, milk beverages, dietary supplements, white cheese, bee bread, gluten-free bread, biscuits, cookies, juices, sausages, meatballs, etc. (Supplementary Table 1). The deterioration of meat products primarily results from lipid oxidation, leading to a reduction in overall quality and potentially compromising the product's shelf life. To counteract this issue and mitigate damage caused by lipid oxidation, natural antioxidant compounds are commonly incorporated into food formulations [57]. The use of bee pollen in meat products is of great significance because its extract shows a strong antioxidative effect which has helped to solve the problems faced by manufacturers of meat products. Although these problems at large, are solved by the use of synthetic additives but consumer awareness has favored the use of additives of natural origin capable to cease microbial action and uncontrolled oxidation processes [60]. Bee pollen, rich in phenolic compounds, serves as a valuable source of antioxidants. The redox properties of these phenolic compounds enable them to function as reducing agents, hydrogen donors and scavengers of oxygen singlet, directly contributing to antioxidant action [57]. Thus, bee pollen has been considered to be a suitable contender to slow down lipid oxidation in meatballs and sausages, that not only extends shelf life but also enhances the diversity of food products offered. This, in turn, holds promise for future industrial advancements and contributes to a deeper understanding of bee pollen as a significant functional food [25, 57, 60].
Bee pollen is a natural ingredient having excellent nutritional value based on the geographic origin and floral species. Thus, it can be potentially incorporated into food products and accepted as a part of our daily diet. However, it is very important to acknowledge the other aspects related to pollen contamination, allergenicity, processing, health implications, digestibility as well as storage. The review of the literature has revealed that more emphasis should be laid on extending the existing guidelines and regulations for determining the acceptable upper levels of potentially harmful compounds in bee pollen before human consumption. Intensive research on the unexplored aspects will help in enriching the knowledge of researchers, industrialists and manufacturers to develop healthy, nutritious and safe bee pollen-based food products.
