Introduction
Common feed additives used in poultry diets include antimicrobials, antioxidants, emulsifiers, binders, pH control agents, and enzymes. These are included in feed beyond the absolute needs of nutrition of primary importance, and provide protection against continuous microbial threats that may escalate in intensive production, causing disease and poor performance in poultry. Other feed additives potentially used are those intended to preserve nutrition levels, nutrient availability, relieve costs and to improve the quality of the resulting meat (Mead, Reference MEAD2004). The use of antibiotics as growth promoters for poultry production has been banned in the European Union since 2006. This caused a prohibition of using them as protective agents against the emergence of infectious diseases, which consequently increased the economic losses of the poultry industry. Therefore, many researchers have focused to evaluate natural feed additives, such as bee products (Castanon, Reference CASTANON2007; Allen et al., Reference ALLEN, LEVINE, LOOFT, BANDRICK and CASEY2013).
Bee pollen
Bee pollen is an agglomerate of flower pollen collected by honey bees (Apis mellifera L.) from various botanical sources (Oliveira et al., Reference OLIVEIRA, SILVA, LOCH, MARTINS, DIAS and SIMON2013; Attia et al., Reference ATTIA, ABD AL-HAMID, IBRAHIM, AL-HARTHI, BOVERA and ELNAGGAR2014). Bees mix pollen with a small amount of saliva or nectar and, in the form of pollen loads, carry it to the hive on their rear legs. Pollen in the form of such loads is obtained using traps and, following drying, becomes a raw material for pharmaceutical, cosmetic or nutritional use (Rzepecka-Stojko et al., Reference RZEPECKA-STOJKO, STOJKO, KUREK-GÓRECKA, GÓRECKI, KABAŁA-DZIK, KUBINA, MOŹDZIERZ and BUSZMAN2015). Due to its nutritional and therapeutic properties, preparations made of bee pollen are used as dietary supplements (Rzepecka-Stojko et al., Reference RZEPECKA-STOJKO, STOJKO, KUREK-GÓRECKA, GÓRECKI, KABAŁA-DZIK, KUBINA, MOŹDZIERZ and BUSZMAN2015). Brindza et al. (Reference BRINDZA, GRÓF, BACIGÁLOVÁ, FERIANC and TÓTH2010) reported that bee pollen has a considerable potential to be used in increasing quantities as a food and/or in animal feed, and may be appreciated even in human nutrition. Bee pollen is promoted as a health-promoting food with a wide range of properties, among which antimicrobial, antifungal, antioxidant, anti-radiation, hepatoprotective, chemoprotective, chemopreventive, and anti-inflammatory activities are the most prominent (Cocan et al., Reference COCAN, MARGHITAS, DEZMIREAN and LASLO2005; Hamamoto et al., Reference HAMAMOTO, ISHIYAMA and YAMAGUCHI2006; Yamaguchi et al., Reference YAMAGUCHI, HAMAMOTO, UCHIYAMA, ISHIYAMA and HASHIMOTO2006; Pascoal et al., Reference PASCOAL, RODRIGUES, TEIXEIRA, FEAS and ESTEVINHO2014).
Chemical composition of bee pollen
Bee pollen is a heterogenous plant product rich in biologically active substances. More than 200 substances are found in pollen grains collected from different plant species. The major chemical substances are proteins (10-40%), carbohydrates (13-55%), and lipids (1-10%). Other minor components include amino acids, fatty acids, phenolic compounds, flavonoids, sterols, terpenes, enzymes and coenzymes, as well as vitamins, carotenoids and minerals (Kędzia and Hołderna-Kędzia, Reference KĘDZIA and HOŁDERNA-KĘDZIA2005; Reference KĘDZIA and HOŁDERNA-KĘDZIA2012; Marchini et al., Reference MARCHINI, REIS and MORETI2006; Campos et al., Reference CAMPOS, BOGDANOV, DE ALMEIDA-MURADIAN, SZCZESNA, MANCEBO, FRIGERIO and FERREIRA2008; Reference CAMPOS, FIRGERIO, LOPES and BOGDANOV2010; Feás et al., Reference FEÁS, VÁZQUEZ-TATO, ESTEVINHO, SEIJAS and IGLESIAS2012; El-Asely et al., Reference EL-ASELY, ABBASS and AUSTIN2014; Pascoal et al., Reference PASCOAL, RODRIGUES, TEIXEIRA, FEAS and ESTEVINHO2014). Bee pollen is varying in its chemical composition depending on the flora present in various climate zones (Nogueira et al., Reference NOGUEIRA, IGLESIAS, FEÁS and ESTEVINHO2012).
The average level of proteins in bee pollen is 22.7%, including 10.4% essential amino acids (Szczesna, Reference SZCZESNA2006). It constitutes a rich source of exogenous amino acids with branched chains, i.e. leucine, isoleucine, and valine (Rzepecka-Stojko et al., Reference RZEPECKA-STOJKO, STOJKO, KUREK-GÓRECKA, GÓRECKI, KABAŁA-DZIK, KUBINA, MOŹDZIERZ and BUSZMAN2015). Moreover, there are significant amounts of nucleic acids, especially ribonucleic acid. Among the most notable lipids, which constitute about 5.1% of bee pollen, are essential fatty acids (Szczesna, Reference SZCZESNA2006). The fatty acid content in bee pollen ranges between 1 and 20%, depending on the plant species (Brodschneider and Crailsheim, Reference BRODSCHNEIDER and CRAILSHEIM2010). Bee pollen contains, on average, 30.8% digestible carbohydrates out of which reducing sugars, fructose and glucose in particular, make up 25.7% (Roulston and Cane, Reference ROULSTON and CANE2000; Almeida-Muradian et al., Reference ALMEIDA-MURADIAN, PAMPLONA, COIMBRA and BARTH2005; Kędzia and Hołderna-Kędzia, Reference KĘDZIA and HOŁDERNA-KĘDZIA2005; Reference KĘDZIA and HOŁDERNA-KĘDZIA2012). Apart from nutritional components such as proteins, carbohydrates and lipids, bee pollen is also a rich source of vitamins, with a content of around 0.7%. It contains significant amounts of group B vitamins and ascorbic acid. Vitamins soluble in lipids represent only 0.1%, and β-carotene is present in the greatest amount, followed by other carotenoids, vitamin E and calciferol (Komosinska-Vassev et al., Reference KOMOSINSKA-VASSEV, OLCZYK, KAFMIERCZAK, MENCNER and OLCZYK2015).
The beneficial effects of bee pollen on health may be attributed to the presence of phenolic compounds (Sarić et al., Reference SARIĆ, BALOG, SOBOCANEC, KUSIĆ, SVERKO, RUSAK, LIKIĆ, BUBALO, PINTO, REALI and MAROTTI2009; Omar et al., Reference OMAR, AZHAR, FADZILAH and KAMAL2016), including flavonoids (1.6%) with high antioxidant capacity (Kroyer and Hegedus, Reference KROYER and HEGEDUS2001; Campos et al., Reference CAMPOS, WEBBY, MARKHAM, MITCHELL and CUNHA2003; Komosinska-Vassev et al., Reference KOMOSINSKA-VASSEV, OLCZYK, KAFMIERCZAK, MENCNER and OLCZYK2015; Zhou et al., Reference ZHOU, QI, RITHO, ZHANG, ZHENG, WU, LI and SUN2015) and antimicrobial properties (García et al., Reference GARCÍA, PÉREZ-ARQUILLUE, JUAN, JUAN and HERRERA2001; Basim et al., Reference BASIM, BASIM and OZCAN2006). In addition, polyphenols present in bee pollen have antiproliferative activities able to regulate cell proliferation and to induce apoptosis (Premratanachai and Chanchao, Reference PREMRATANACHAI and CHANCHAO2014). Wang et al. (Reference WANG, DIAO, ZHANG, LIU, GAO, ZHOU and LI2013) demonstrated that bee pollen has the ability to inhibit tumour growth and to alleviate pain following chemotherapy in cancer patients. Other phenolic compounds include leukotrienes, catechins, and phenolic acids (Komosinska-Vassev et al., Reference KOMOSINSKA-VASSEV, OLCZYK, KAFMIERCZAK, MENCNER and OLCZYK2015).
The effect of bee pollen in broiler chickens
Several studies have emphasised the positive effects of bee pollen on the growth, performance and internal functions of broiler chickens (Villanueva et al., Reference VILLANUEVA, MARQUINA, SERRANO and ABELLÁN2002; Wang et al., Reference WANG, LI, WANG, XIN and WANG2007; Cheng, Reference CHENG2009; Hashmi et al., Reference HASHMI, HAŠČÍK, ELIMAN, GARLÍK, BOBKO and KAČÁNIOVÁ2012; Haščík et al., Reference HAŠČÍK, ELIMAM, GARLÍK, KAČÁNIOVÁ, ČUBOŇ, BOBKO, VAVRIŠINOVÁ and ARPÁŠOVÁ2013; Kačániová et al., Reference KAČÁNIOVÁ, ROVNÁ, ARPÁŠOVÁ, HLEBA, PETROVÁ, HAŠČÍK, ČUBOŇ, PAVELKOVÁ, CHLEBO, BOBKOVÁ and STRIČÍK2013). Wang et al. (Reference WANG, LI, WANG, XIN and WANG2007) demonstrated that the small intestinal villi of the duodenum, jejunum, and ileum in chickens supplemented with pollen were longer and thicker when compared with the control group. This difference was more significant during early development, particularly through the first two weeks. Bee pollen increased the length of the villi by 37.1% and 29.4% in the duodenum, 28.1% and 33.7% in the jejunum, and 18.6% and 16.2% in the ileum during the first two weeks of age (weeks one and two respectively). Furthermore, the small intestinal glands developed at a higher density in the pollen-fed group, and the depth of the glands was significantly increased following bee pollen administration in the first two weeks. These findings suggest that bee pollen could promote the early development of the digestive system and could thus be a potentially beneficial food supplement for certain developmental problems seen in young chicks, or hatchlings.
Kročko et al. (Reference KROČKO, ČANIGOVÁ, BEZEKOVÁ, LAVOVÁ, HAŠČÍK and DUCKOVÁ2012) evaluated the effects of bee pollen as a dietary supplement on the bacterial colonization pattern in the gastrointestinal tract of broiler chickens. Higher doses of bee pollen supplemented in feed significantly reduced the count of the Enterobacteriaceae family isolates from chicken's crops. The ileum and caecum of broiler chickens fed pollen had the lowest count of Enterobacteriaceae family isolates. According to Basim et al. (Reference BASIM, BASIM and OZCAN2006) and Kumova et al. (Reference KUMOVA, KORKMAZ, AVCI and CEYRAN2002), the decline of the Enterobacteriaceae family counts in the chicken's crops may be associated with the antibacterial activity of bee pollen.
Angelovičová et al. (Reference ANGELOVIČOVÁ, ŠTOFAN, MOČÁR and LIPTAIOVÁ2010) evaluated the biological effects of bee pollen from Brassica napus L. in the diet of broiler chickens and found that the body weight at the end of the feeding period for supplemented broiler chickens was higher than that in the control group. Babaei et al. (Reference BABAEI, RAHIMI, TORSHIZI, TAHMASEBI and MIRAN2016) evaluated the effects of bee pollen on the growth performance and immune system of Japanese quails. Results of this experiment indicated that the supplementation with 5 g.kg-1 bee pollen could be beneficial in improving the quail chicks’ performance.
Haščík et al. (Reference HAŠČÍK, ELIMAM, GARLÍK, KAČÁNIOVÁ, ČUBOŇ, BOBKO and ABDULLA2012) reported that bee pollen extract added at levels of either 400 and 800 mg.kg-1 into feed mixtures for broiler chickens increased the body weight compared to an unsupplemented control group. Similarly, Attia et al. (Reference ATTIA, AL-HANOUN and BOVERA2011) and Eyng et al. (Reference EYNG, MURAKAMI, DUARTE and SANTOS2014) observed positive effects of bee pollen on the body weight of broilers.
Haščík et al. (Reference HAŠČÍK, TREMBECKÁ, BOBKO, KAČÁNIOVÁ, BUČKO, TKÁČOVÁ and KUNOVÁ2015a) evaluated the effect of bee pollen extract on the meat quality of broiler chickens. Results of this study indicated that bee pollen supplementation, when fed alongside probiotics, was effective in reducing meat weight losses caused by cooling and freezing. These losses were lower than those achieved by Haščík et al. (Reference HAŠČÍK, TREMBECKÁ, BOBKO, ČUBOŇ, BUČKO and TKÁČOVÁ2015b) when bee pollen was administered alone.
Such findings are not consistent with other researchers, such as Šulcerova et al. (Reference ŠULCEROVA, MIHOK, JŮZL and HAŠČIK2011) who reported only a small impact of various doses of bee pollen in poultry diets on meat quality, with some effects found in the group supplemented with 400 mg.kg-1 bee pollen. The pH of raw breast meat was significantly lower than that of thigh muscle in all measurement times. Furthermore, bee pollen supplementation of 400 and 800 mg.kg-1 in feed had a positive effect on the breast colour.
Another report (Haščík et al., Reference HAŠČÍK, ELIMAM, GARLÍK, KAČÁNIOVÁ, ČUBOŇ, BOBKO and ABDULLA2012) revealed that the use of 400 mg.kg-1 bee pollen as a dietary supplement in broilers led to an increase in the live body weight, carcass weight, giblets weight and carcass yield in males, but it had a negative impact on females, as it decreased the body weight of the hens. Seven et al. (Reference SEVEN, ARSLAN, SEVEN and GÖKÇE2016) recorded positive effects of dietary bee pollen (1 g.kg-1) with respect to the fatty acids composition of Japanese quails meat. The results of this study suggested that bee pollen supplementation had potential protective effects on the fatty acid composition of quails reared under high stocking density. In all groups, bee pollen supplementation increased the polyunsaturated fatty acids levels (PUFA), particularly the n-6 PUFA content. Hosseini et al. (Reference HOSSEINI, VAKILI AZGHANDI, AHANI and NOURMOHAMMADI2016) investigated the effects of bee pollen on the performance, intestinal morphometry and haematological profile of broilers reared under high ambient temperature.
Published data indicated that the dietary use of bee pollen may offer a practical nutritional strategy in a high temperature environment to prevail the harmful effects of the heat stress in broilers. The mechanism of bee pollen action may be attributed to its strong antibacterial action, coupled with a high content of micronutrients with positive effects on health and metabolism (Viuda-Martos et al., Reference VIUDA-MARTOS, RUIZ-NAVAJAS, FERNÁNDEZ-LÓPEZ and PÉREZ-ÁLVAREZ2008). It has been revealed that the positive effects of dietary bee pollen on the broiler growth could be related to an optimal composition of nutrients found in bee pollen. In addition, the inclusion of bee pollen into diet may improve selected blood parameters, i.e. increasing the haemoglobin concentration, red and white blood cell counts, and lymphocytes, as well as decreasing the concentrations of serum uric acid, creatinine, triglycerides and cholesterol (Attia et al., Reference ATTIA, ABD AL-HAMID, IBRAHIM, AL-HARTHI, BOVERA and ELNAGGAR2014; Farag and El-Rayes, Reference FARAG and EL-RAYES2016). Similar results were observed in the study of Hosseini et al. (Reference HOSSEINI, VAKILI AZGHANDI, AHANI and NOURMOHAMMADI2016), in which the creatine kinase level in broiler breast muscle was decreased after bee pollen supplementation. Moreover, it has been shown that bee pollen can enhance immunity (Popiela-Pleban et al., Reference POPIELA-PLEBAN, ROMAN, DOBRZANSKI, POGODA-SEWERNIAK, OPALINSKI and KORCZYNSKI2012), which is likely related to the presence of minerals, flavonoids and vitamins. This is reflected in work that shows that supplementation with bee pollen in chickens was favourable in respect to oxidative stability of meat (Bobko et al., Reference BOBKO, HAŠČÍK, BOBKOVÁ, PAVELKOVÁ, TKÁČOVÁ and TREMBECKÁ2015). A similar trend has been observed in Japanese quail meat in the study of Seven et al. (Reference SEVEN, ARSLAN, SEVEN and GÖKÇE2016).
Conclusions
Based on the research papers focused on the dietary use of bee pollen, it can be assumed that this natural feed additive may be a promising alternative to antibiotics and coccidiostats. Nevertheless, further investigations are needed to assess the dietary potential of bee pollen supplementation to establish and verify the levels of bee pollen in chicken diet which could lead to improvements in meat performance, carcass traits, meat quality, immunity, and blood parameters of broiler chickens. In addition, the relative costs and return on investment of such supplementation needs to be assessed.
