Introduction
Recently the resistance of microorganisms to antimicrobial drugs has become a health concern. Antimicrobial resistance has been implicated, but not confirmed, to not only come from use of antibiotics in animals but may predominately come from over-use in human medicine (Levy and Marshall, Reference LEVY and MARSHALL2004; Marshall and Levy, Reference MARSHALL and LEVY2011). Evidence has been accumulated that there is a strong correlation (but no direct link) between the uses of antibiotics as a growth enhancement in livestock production, especially in poultry, and the increase in the risk of antibiotic resistance (Thorsteinsdottir et al., Reference THORSTEINSDOTTIR, HARALDSSON, FRIDRIKSDOTTIR, KRISTINSSON and GUNNARSSON2010; Laxminarayan et al., Reference LAXMINARAYAN, DUSE, WATTAL, ZAIDI, WERTHEIM, SUMPRADIT, VLIEGHE, HARA, GOULD, GOOSSENS, GREKO, SO, BIGDELI, TOMSON, LEE, KIM, PARK, AHN, PARK, KWON, MORITA, SHIM and HER2013) and incidence of zoonotic disease (Smith and Fratamico, Reference SMITH and FRATAMICO2010) in humans and other animals. Therefore, it is critical to develop alternatives to the use of antibiotics as growth promoters to improve health and welfare with the growth and production ratios at or near the genetic potential of the modern broiler chickens, turkeys, and laying hens (Edens, Reference EDENS2003; Maisonneuve and Gerdes, Reference MAISONNEUVE and GERDES2014).
Propolis, also commonly named as bee glue, is a natural resinous substance collected by bees from plants buds and exudates. This resin is masticated by adding salivary enzymes, and then mixed with beeswax and other compounds (Banskota et al., Reference BANSKOTA, TEZUKA and KADOTA2001). Aromatic acids, diterpenic acids, flavonoids and phenolic compounds appear to be the principal components responding of the biological activities of propolis (Greenaway et al., Reference GREENAWAY, MAY, SCAYSBROOK and WHATLEY1991; Markham et al., Reference MARKHAM, MITCHEL, WILKINS, DALDY and LU1996). Propolis’ chemical composition is determined by the types of plants from which the bees collect the exudates and, as a result, its biological activity is closely related to geographical location which can affect the ability of the propolis to confer a biological and thus protective effect in the bird when supplemented in the diet (Bankova, Reference BANKOVA2005).
Propolis has received attention for improving human health and combating diseases such as cancer, cataracts, and diabetes (Farré et al., Reference FARRÉ, FRASQUET and SÁNCHEZ2004). Similar to human research, propolis has been used as a diet supplement in broilers, laying hens, quail, and ducks (Denli et al., Reference DENLI, CANKAYA, SILICI, OKAN and ULUOCAK2005; Ziaran et al., Reference ZIARAN, RAHMANI and POURREZA2005; Galal et al., Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008; Abdel-Rahman and Mosaad, Reference ABDEL-RAHMAN and MOSAAD2013). It is very difficult to adequately compare research with propolis as a feed additive due to many authors not including active compound analyses with their publications. In spite of this, this review includes published work with only dietary concentrations as a reference. This review article focuses on the effects of propolis on domesticated poultry species (broiler chickens, laying hens, quails, and ducks); and future research needs.
Growth performance and efficiency
Previous studies have indicated that propolis has a growth promoting function. Body weight has been shown to increase by 2.03% in broiler chickens fed with 0.1% propolis compared with unsupplemented controls (Zhi-jiang et al., Reference ZHI-JIANG, SAN-FENG, KE, HONG-XIANG and KAI-JIE2004). Dose response effect of propolis on body weight have been reported, where average body weight and weight gain of broiler chickens were significantly improved by an increasing degree when feeding propolis at 50, 100, 150, 200 or 250 mg/kg diet (Shalmany and Shivazad, 2006). Similar results have been reported in other poultry species. For example, quail (Coturnix coturnix japonica) had improved body weight after supplementation with 1 g propolis/kg diet between 14 to 35 days of age (Denli et al., Reference DENLI, CANKAYA, SILICI, OKAN and ULUOCAK2005), and ducks fed propolis at 2 g/kg feed were heavier at 12 weeks of age compared to unsupplemented controls (Abdel-Rahman and Mosaad, Reference ABDEL-RAHMAN and MOSAAD2013). Bonomi et al. (Reference BONOMI, BONOMI, QUARANTELLI, SABBIONI and SUPERCHI2002) reported that duck body weight gain was increased by 10.50 and 13.50% by supplementation with 20 or 40 mg propolis/kg diet respectively during a trial from day old to 60 days of age. These studies reported that these effects were due to higher feed intake, which was dose correlated, i.e. the higher dose of propolis, the heaver body weight with improved feed intake.
FCR and feed intake were improved in broiler chickens raised under recommended temperature conditions following supplementation with 250 mg propolis/kg diet (Shalmany and Shivazad, 2006), 400 mg propolis/kg (Hassan and Abdulla, Reference HASSAN and ABDULLA2011), and in broiler chickens exposed to 200 mg/kg lead toxicity but with 1 g propolis/kg in the diet (Seven et al., Reference SEVEN, AKSU and TATLI SEVEN2012). Similar results were reported in laying hens reared under chronic heat stress after feeding 2 or 5 g propolis/kg diet (Tatli Seven, Reference TATLI SEVEN2008) and 3 g propolis/kg diet (Seven et al., Reference SEVEN, TATLI SEVEN and SILICI2011). FCR was improved in Japanese quail fed 1 g propolis/kg diet (Denli et al., Reference DENLI, CANKAYA, SILICI, OKAN and ULUOCAK2005) and in ducks fed 2 g/kg (Abdel-Rahman and Mosaad, Reference ABDEL-RAHMAN and MOSAAD2013). Feed intake was increased by 17 and 23%, in ducks fed 20 or 40 mg propolis/kg diet respectively, from 1 to 60 days of age, (Bonomi et al., Reference BONOMI, BONOMI, QUARANTELLI, SABBIONI and SUPERCHI2002). The improvement in feed intake and FCR was attributed to enhanced flavour by the flavonoid content in propolis, and/or due to components such as benzoic and 4-hidoxibenzoic acid, which may improve the digestibility of nutrients such as protein and ash (Tatli Seven, Reference TATLI SEVEN2008; Seven et al., Reference SEVEN, AKSU and TATLI SEVEN2012). Conversely, others have reported that propolis supplementation did not affect FCR in broiler chickens exposed to chronic heat stress (Tatli Seven et al., Reference TATLI SEVEN, SEVEN, YILMAZ and SIMSEK2008) or under thermo-neutral temperatures (Açikgöz et al., 2005; Mahmoud et al., Reference MAHMOUD, ABDEL-RAHMAN and DARWISH2013).
Propolis has been documented to increase resistance to various stressors in poultry species. Dietary supplementation of propolis improved the weight gain in heat stressed broilers (5 g/kg diet; Tatli Seven et al., Reference TATLI SEVEN, SEVEN, YILMAZ and SIMSEK2008); in birds exposed to lead toxicity (1 g/kg diet; Seven et al., Reference SEVEN, AKSU and TATLI SEVEN2012) or in those infected with Eimeria (200 ml/200 kg diet; Biavatti et al., Reference BIAVATTI, BELLAVER, VOLPATO, COSTA and BELLAVER2003). Similarly, dietary supplementation at 2 or 5 g/kg propolis in feed significantly improved weight gain of laying hens exposed to heat stress (Tatli Seven, Reference TATLI SEVEN2008). This may be attributed to the antimicrobial (antibacterial, antifungal, antiviral and antiprotozoal) activity of its components, inducing the refinement of intestinal health and improvement of digestion and absorption as a result of prevention of subclinical infections. These results may be also related to other activities such as antioxidants (Tekeli et al., Reference TEKELI, KUTLU, CELIK and DORAN2010; Abdel-Mohsein et al., Reference ABDEL-MOHSEIN, MAHMOUD and MAHMOUD2014).
Egg production and egg quality
Egg production and quality (shape index, yolk index, albumen index, and Haugh unit) in laying hens was not reportedly affected by dietary supplementation of propolis (Galal et al., Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008; Ozkok et al., Reference OZKOK, ISCAN and ILICI2013); however, egg mass and eggshell quality were significantly increased after feeding 100 and 150 mg propolis/kg diet (Galal et al., Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008). In addition, shell thickness and eggshell weight for heat stressed layers fed propolis plus vitamin C, were significantly increased (Tali Seven, 2008). The positive effects of propolis on eggshell quality could be linked to increase in calcium digestibility and absorption due to its acid derivatives such as benzoic, 4-hydroxy-benzoic acids (Tatli Seven, Reference TATLI SEVEN2008; Seven et al., Reference SEVEN, TATLI SEVEN and SILICI2011).
Propolis has been reported to exhibit antibacterial and antifungal activities in embryonated eggs, as it positively affects the microbiological quantity and quality of eggshells and the internal contents of the eggs. Thus, propolis could be an alternative hatching egg disinfectant versus chemical compounds currently used, having the benefit of not adversely affecting hatchability and performance of broiler chicks and quail (Aygun et al., Reference AYGUN, SERT and COPUR2012; Vilela et al., Reference VILELA, VARGAS, FISCHER, LADEIRA, DE FARIA, NUNES, DE LIMA, HÜBNER, LUZ, OSÓRIO and ANCIUTI2012).
Mortality
Broilers fed diets supplemented with propolis showed reduced mortality, decreasing by 3 to 7% (Omar et al., Reference OMAR, MAHMOUD, KAROUSA and RANDA2004; Shalmany and Shivazad, 2006; Tatli Seven et al., Reference TATLI SEVEN, SEVEN, YILMAZ and SIMSEK2008; Tatli Seven and Seven, Reference TATLI SEVEN and SEVEN2008). Similarly, mortality rate was reduced by 3.34% in heat stressed laying hens treated with 2 or 5 g propolis/kg diet (Tatli Seven, Reference TATLI SEVEN2008; Seven et al., Reference SEVEN, TATLI SEVEN and SILICI2011). The effects of propolis on reducing mortality may be explained by its functions in food digestion, nutrient absorption, and metabolism; leading to changes in blood concentrations of cholesterol, total protein, and amino acid (Tekeli et al., Reference TEKELI, KUTLU and CELIK2011; Abdel-Rahman and Mosaad, Reference ABDEL-RAHMAN and MOSAAD2013; Attia et al., Reference ATTIA, ABDAL-HAMID, IBRAHIM, AL-HARTHI, BOVERA and ELNAGGAR2014). It may also relate to the ability of propolis to stimulate and improve immunological function, such as macrophage activity and the functions of the lymphatic tissues (Çetin et al., Reference ÇETIN, SILICI, ÇETIN and GÜÇLÜ2010; Freitas et al., Reference FREITAS, VANAT, PINHEIRO, BALARIN, SFORCIN and VENANCIO2011; Shihab and Ali, Reference SHIHAB and ALI2012). Several previous studies on animals have showed that propolis or its flavonoids activate macrophages, increasing phagocytic capability and the release of microbicidal agents, such as nitric oxide and tumour necrosis factor-α (TNF-α) (Orsi et al., Reference ORSI, FUNARI, SOARES, CALVI, OLIVEIRA, SFORCIN and BANKOVA2000; Sforcin, Reference SFORCIN2007).
Behaviour
Adding propolis to the diet of Ross 708 chicks reared under heat stress (32°C) or Sasso chicks and ducks reared under regular management temperature (21°C) did not affect their feeding and drinking behaviour, but standing and walking activities were increased, while panting and feather pecking were reduced significantly (Omar et al., Reference OMAR, MAHMOUD, KAROUSA and RANDA2004; Abdel-Rahman and Mosaad, Reference ABDEL-RAHMAN and MOSAAD2013; Mahmoud et al., Reference MAHMOUD, ABDEL-RAHMAN, DARWISH, APPLEGATE and CHENG2015). These changes have been attributed to the high nutritive values if propolis as a growth promoting agent to improve birds’ health status and activity. In addition, Mahmoud et al. (Reference MAHMOUD, ABDEL-RAHMAN, DARWISH, APPLEGATE and CHENG2015) indicted that such behavioural changes were associated with the antioxidative effects of propolis due to its high content of flavonoids, caffeic acid and polyephnols.
Carcass characteristics
Haščík et al. (Reference HAŠČÍK, GARLÍK, ELIMAM, KAČÁNIOVÁ, POCHOP, BOBKO, KROČKO and BENCZOVÁ2011) reported that propolis (200 mg/kg) increased the aroma, taste, juiciness and softness properties of breast and thigh muscles of Ross 308 broiler, without influencing other meat quality score indicators, including: pH, colour, shear force or cooking losses. Bonomi et al. (Reference BONOMI, BONOMI, QUARANTELLI, SABBIONI and SUPERCHI2002) reported that propolis supplementation (20 or 40 mg/kg from day 1 to day 60) improved meat digestibility, tenderness and skin pigmentation in ducks.
Propolis supplementations have been shown to increase carcass weight, yield and dressing percentage in broiler chickens, quails, and ducks (Bonomi et al., Reference BONOMI, BONOMI, QUARANTELLI, SABBIONI and SUPERCHI2002; Tatli Seven et al., Reference TATLI SEVEN, SEVEN, YILMAZ and SIMSEK2008; Hassan and Abdulla, Reference HASSAN and ABDULLA2011). Conversely, Babińska et al. (Reference BABIŃSKA, KLECZEK, SZAREK and MAKOWSKI2012) reported that the meat-to-bone ratio in elements of carcasses was reduced in broiler chickens fed with 0.025% propolis during the first two weeks of fattening.
The relative weight of the small intestine, proventriculus, gizzard, liver, heart, thighs, spleen, bursa, pancreas dorsal and chest parts, legs, neck, wings, abdominal fat and chilled percentage were not affected by propolis treatment in either broiler chickens or quail (Denli et al., Reference DENLI, CANKAYA, SILICI, OKAN and ULUOCAK2005; Tatli Seven et al., Reference TATLI SEVEN, SEVEN, YILMAZ and SIMSEK2008; Babińska et al., Reference BABIŃSKA, KLECZEK, SZAREK and MAKOWSKI2012; Mahmoud et al., Reference MAHMOUD, ABDEL-RAHMAN and DARWISH2013). However, Hassan and Abdulla (Reference HASSAN and ABDULLA2011) demonstrated that the proportional weight of the liver was significantly higher in broiler chickens fed 400 mg propolis/kg diet than that of the control group.
Propolis supplementation at 0.025% of the diet fed to broiler chickens for the first two weeks of age did not affect the weight and length of tibial bones or their percentage shares of total body weight; and did not affect the geometric parameters of the tibia and its biomechanical properties. Dry matter content and phosphorus concentrations of the tibial bones of chickens were not affected; however, the concentration of calcium in bone ash was significantly reduced (Kleczek et al., Reference KLECZEK, MAJEWSKA, MAKOWSKI and MICHALIK2012).
Haematological parameters
Red blood cell (RBCs) counts were increased in broiler chickens fed propolis at 2 or 3 g/kg diet (Shihab and Ali, Reference SHIHAB and ALI2012); in laying hens at 3 g/kg (Çetin et al., Reference ÇETIN, SILICI, ÇETIN and GÜÇLÜ2010); and in ducks at 2 g/kg (Abdel-Rahman and Mosaad, Reference ABDEL-RAHMAN and MOSAAD2013). These results indicate that propolis may have a stimulatory effect on the synthesis and release of these cells from the bone marrow of various poultry species.
Çetin et al. (Reference ÇETIN, SILICI, ÇETIN and GÜÇLÜ2010) recorded a slight increase in haemoglobin and haematocrit values in laying hens receiving 3 g/kg of propolis in the diet. In another trial, Abdel-Rahman and Mosaad (Reference ABDEL-RAHMAN and MOSAAD2013) found that ducks from the propolis fed group had significantly higher haemoglobin concentrations than the controls; however, packed cell volume was not affected. These results suggest that propolis improves the digestive utilisation of iron and reduces the regeneration efficiency of haemoglobin. Dietary propolis supplementation may help prevention of anaemia in poultry.
Propolis dietary supplementation induced a significant increase in lymphocyte percentage and a significant decrease in heterophils and H/L ratio in both broiler chickens and laying hens (Ziaran et al., Reference ZIARAN, RAHMANI and POURREZA2005; Galal et al., Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008). These finding were refuted by another study, where Eyng et al. (Reference EYNG, MURAKAMI, PEDROSO, SILVEIRA, LOURENCO and GARCIA2013) reported no differences in the number of lymphocytes, heterophils and H/L ratio in broiler chicken supplemented with propolis.
The addition of 3 g propolis/kg in the diet of broiler chickens and laying hens resulted in significant increases in the serum IgG and IgM levels and significant decreases in the peripheral blood T-lymphocytes compared with those of the controls (Çetin et al., Reference ÇETIN, SILICI, ÇETIN and GÜÇLÜ2010; Shihab and Ali, Reference SHIHAB and ALI2012). The increased levels of IgG in birds treated with propolis may be related to the stimulation of B lymphocytes by increasing macrophage activity and increasing concentrations of cytokines such as interleukin-1, interleukin-2, and interleukin-4 (Park et al., Reference PARK, LEE, KIM, CHUNG, EOM, KIM, CHUNG, PAIK and OH2004). These cytokines further stimulate B lymphocytes to become plasma cells, producing immunoglobulins (Dimov et al., Reference DIMOV, IVANOVSKA, MANOLOVA, BANKOVA, NIKOLAV and POPOV1991). These effects could be attributed to the benzene and flavonoids constituents of propolis.
Propolis supplementation increased the antibody response to Newcastle disease virus, infectious bursal disease, and avian influenza (Taheri et al., Reference TAHERI, RAHMANI and POURREZA2005; Ziaran et al., Reference ZIARAN, RAHMANI and POURREZA2005), but had no effect on infectious bronchitis (Taheri et al., Reference TAHERI, RAHMANI and POURREZA2005). Similarly, Freitas et al. (Reference FREITAS, VANAT, PINHEIRO, BALARIN, SFORCIN and VENANCIO2011) stated that supplementation of propolis in laying hen feed (50 mg/kg) increased the production of IgG specifically to sheep red blood cells and natural antibodies; indicating that propolis could be used to increase antigen-specific antibody responses to vaccines.
Abdel-Rahman and Mosaad (Reference ABDEL-RAHMAN and MOSAAD2013) demonstrated that serum total protein and globulin levels were significantly increased in propolis (2 g/kg) fed Muscovy ducks kept at 21°C. In addition, serum total protein and globulin levels were significantly increased in Sasso chickens fed with 2% propolis from three to eight weeks of age (Omar et al., Reference OMAR, MAHMOUD, KAROUSA and RANDA2004) and in laying hens fed 100 or 150 mg propolis from week 46 to 54 (Galal et al., Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008) under thermo-neutral temperatures.
Blood cholesterol and triglyceride levels were significantly reduced in propolis-fed laying hens (100 or 150 mg/kg diet; Galal et al., Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008); and in broiler chickens (300 mg/kg fed throughout the fattening period; Attia et al., Reference ATTIA, ABDAL-HAMID, IBRAHIM, AL-HARTHI, BOVERA and ELNAGGAR2014). This due to its anti-oxidising properties, where propolis is considered to improve lipid metabolism, liver morphological structures and biological functions (Matsui et al., Reference MATSUI, EBUCHI, FUJISE, ABESUNDARA, DOI, YAMADA and MATSUMOTO2004; Babińska et al., Reference BABIŃSKA, KLECZEK, MAKOWSKI and SZAREK2013).
Petruška et al. (Reference PETRUŠKA, TUŠIMOVÁ, KALAFOVÁ, HAŠČÍK, KOLESÁROVÁ and CAPCAROVÁ2012) reported that propolis at 450 mg/kg caused a significant decrease of serum phosphorus concentrations in broiler chickens. Moreover, Petruška et al. (Reference PETRUŠKA, TUŠIMOVÁ, KALAFOVÁ, HAŠČÍK, KOLESÁROVÁ and CAPCAROVÁ2012) reported that 150, 450, 600 or 800 mg propolis/kg feed significantly reduced the serum magnesium content of broiler chickens. They suggested that propolis inclusion in the diet of broiler chickens may increase absorption of phosphorus and magnesium from the blood to the bone, resulting in reductions of these elements in the blood.
Enzymes
Attia et al. (Reference ATTIA, ABDAL-HAMID, IBRAHIM, AL-HARTHI, BOVERA and ELNAGGAR2014) stated that dietary supplementation of 300 mg propolis/kg diet significantly reduced aspartate aminotransferase activity in broiler chickens. Also, propolis supplementation for broiler chicks exposed to heat stress or lead toxicity significantly reduced superoxide dismutase, malondialdehyde, catalase activities and glutathione peroxidase levels, reflecting that propolis may regulate liver metabolism (Tatli Seven et al., Reference TATLI SEVEN, YILMAZ, SEVEN, CERCI, AZMAN and YILMAZ2009; Seven et al., Reference SEVEN, AKSU and TATLI SEVEN2010). Galal et al. (Reference GALAL, ABD EL-MOTAAL, AHMED and ZAKI2008) reported that supplemental propolis at 100 or 150 mg/kg diet for laying hens significantly reduced aspartate aminotransferase and alanine amino transferase concentrations compared to control birds. Denli et al. (Reference DENLI, CANKAYA, SILICI, OKAN and ULUOCAK2005) showed a significant decrease in serum alanine transaminase activity in Japanese quail given 1 g/kg of propolis compared with birds treated with flavomycin. Reduced enzyme activity could indicate that propolis is able to reduce tissue damage and prevent the leakage of enzymes through cellular membranes due to its antioxidative function (Newairy and Abdou, Reference NEWAIRY and ABDOU2013).
Hormones
Stress is a serious problem in the modern intensified poultry industry, resulting in an increase of abnormal behaviour and disease incidence, causing high economic losses. Stress acts through the central nervous system to trigger the release of neurotransmitters and stress hormones, such as dopamine and corticosterone from the sympathoadrenal and hypothalamic-pituitary-adrenal axes (Cheng et al., Reference CHENG, SINGLETON and MUIR2002). Propolis reduced the response of the hypothalamic-pituitary-adrenal axis to various stressors in mice and rats (Orsatti and Sforcin, Reference ORSATTI and SFORCIN2012; Lee et al., Reference LEE, KIM, PARK, AHN, PARK, KWON, MORITA, SHIM and HER2013). Propolis attenuated blood corticosterone levels, reduced the c-fos immunoreactive neurons and increased glucocorticoid receptor expression in the hippocampus (Lee et al., Reference LEE, KIM, PARK, AHN, PARK, KWON, MORITA, SHIM and HER2013; Sameni et al., Reference SAMENI, FATEMEH, HASSAN, REZA, BEHPOUR and ALI.2014). In birds, Mahmoud et al. (2014a) reported that serum corticosterone levels were not affected in heat stressed broiler chickens when 250 mg/kg propolis was added to the diet.
Tri-iodiothyronine (T3) and thyroxin (T4) perform important roles in controlling metabolism and thermoregulation in chickens (Tao et al., Reference TAO, ZHANG, DONG, ZHANG and XIN2006). Mahmoud et al. (2014a) reported that 250 mg propolis per kg diet did not affect serum T3 and T4 level and T3/T4 ratio in broiler chickens exposed to chronic heat stress.
Histopathological effects
Propolis supplementation in broilers has been shown to protect hepatic tissue against adverse effects of various hepatotoxic factors which can lead to both regressive (various types of degeneration and necrosis) and progressive lesions due to its high phenolic components (Babińska et al., Reference BABIŃSKA, KLECZEK, SZAREK and MAKOWSKI2012; Reference BABIŃSKA, KLECZEK, MAKOWSKI and SZAREK2013). Babińska et al. (Reference BABIŃSKA, KLECZEK, SZAREK and MAKOWSKI2012) stated that such histopathological results demonstrated that broiler chickens receiving propolis had less damage to the organs caused by Salmonella enteritidis infection compared with controls.
Eyng et al. (Reference EYNG, MURAKAMI, DUARTE and SANTOS2014) reported that inclusion of propolis at different levels (1, 2, 3, 4 or 5 g/kg) had no effect on broiler chickens’ crypt depth and the villus height: crypt ratio in the jejunum and ileum, or the villus height in the duodenum, jejunum and ileum. Contrary to this, Tekeli et al. (Reference TEKELI, KUTLU, CELIK and DORAN2010) reported that the intestinal villi length was significantly longer in chickens supplemented with 1000 mg propolis compared to controls. Further work is required to elucidate any reproducible effects of propolis on gut structures.
Microbiota of gastrointestinal tract
Mahmoud et al. (2014b) and Abdel-Mohsein et al. (Reference ABDEL-MOHSEIN, MAHMOUD and MAHMOUD2014) clarified that supplementation of propolis (100, 250, 500 or 750 mg/kg diet) had a significant stimulating effect on the numbers of Lactobacillus spp. and Bifidobacteria spp. in the broiler gut under both recommended temperature and chronic heat stress conditions. Conversely, dietary supplementation of propolis at 1000 mg/kg diet (Tekeli et al., Reference TEKELI, KUTLU, CELIK and DORAN2010) or 400 or 800 mg/kg diet (Kročko et al., Reference KROČKO, ČANIGOVÁ, BEZEKOVÁ, LAVOVÁ, HAŠČÍK and DUCKOVÁ2012) in broilers was reported not to influence the numbers of intestinal lactic acid bacteria. Supplementation of propolis has not been shown to affect caecal numbers of total coliforms, E. coli and Enterococcus spp. in chickens (Tekeli et al., Reference TEKELI, KUTLU, CELIK and DORAN2010; Mahmoud et al., 2014b). On the contrary, Abdel-Mohsein et al. (Reference ABDEL-MOHSEIN, MAHMOUD and MAHMOUD2014) reported that diets mixed with propolis (250, 500 or 750mg/kg diet) significantly reduced total anaerobes and coliform bacteria within the gut of broilers reared under heat stress.
Factors affecting bird responses to propolis dietary supplement
There are several factors that could affect the birds’ response to propolis dietary supplementations such as the qualities of the propolis itself (type, dose, form, collected location, and season), experimental birds (species, age, and gender, stress, heat and management) and other factors (time point and duration of propolis application). The origin of propolis affects its effects on birds’ productivity and health status. For example, Turkish propolis improves the productivity of broiler chickens and laying hens under both normal and stressed conditions (Tatli Seven, Reference TATLI SEVEN2008; Tatli Seven and Seven, Reference TATLI SEVEN and SEVEN2008; Seven et al., Reference SEVEN, AKSU and TATLI SEVEN2012). On the contrary, Chinese propolis negatively affects these parameters in broiler chickens (Mahmoud et al., Reference MAHMOUD, ABDEL-RAHMAN and DARWISH2013).
Propolis source can relay differing functions according to bird strain and/or stage of production. For example, Turkish propolis supplementation at 3g/kg diet improved body weight gain in broiler chickens (Tatlı Seven et al., 2008) but not in laying hens exposed to the same heat stress conditions (Seven et al., Reference SEVEN, TATLI SEVEN and SILICI2011).
The effect of propolis is also affected by the bird's age and the duration of supplementation. Açıkgöz et al. (2005) stated that 4000 mg/kg of propolis in the diet reduced weight gain and feed intake in broilers in later production phases (six weeks of age) if it was administered from day old to three weeks of age, but not from four to six weeks. No reports are available which fully discuss the effect of propolis on bird health and welfare affected by gender. One study, conducted by Santos et al. (Reference SANTOS, TEIXEIRA, RODRIGUES, FREITAS, GUIMARAES and GIACOMETTI2003), reported that male broiler chickens consumed 4.5% more food supplied with propolis than females from day old to 21 days of age but not from 22 to 42 days. However, the reasons for the difference were not discussed in the study. In addition, the type of stressor can affect the function of propolis in preventing the negative effect of the stressor-associated oxidative damage, e.g. 1 g/kg Turkish propolis appears sufficient to control 200 ppm lead toxicity in Ross 308 broilers (Seven et al., Reference SEVEN, AKSU and TATLI SEVEN2012), while a higher dose, 3 or 5 g/kg, is needed to control heat stress (34°C) in the same broiler strain (Tatli Seven et al., Reference TATLI SEVEN, SEVEN, YILMAZ and SIMSEK2008; Tatli Seven and Seven, Reference TATLI SEVEN and SEVEN2008; Tatli Seven et al., Reference TATLI SEVEN, YILMAZ, SEVEN, CERCI, AZMAN and YILMAZ2009).
Conclusions
Previous studies have indicated that the effects of propolis on poultry performance, health and welfare are affected by multiple factors, such as its type and dosage, active component levels, feeding duration and physiological factors (i.e. age, weight and/or breed) and animal species. The available literature, and its varying results with propolis suggests its efficiency is affected by trial conditions (stressed or unstressed and the types of stressors). However, the positive findings for propolis on performance and health of poultry support its stated biological functions as an antioxidant, antibacterial, immune-stimulant and growth promoter; and indicate that the use of propolis as a natural feed additive is promising. Further research on the best techniques for its application on poultry farms is still required. However, comparison across sources of propolis is difficult in the literature when researchers do not publish concentrations of the active compounds from the propolis source used. For this reason, researchers in the future must include these analyses to adequately compare and contrast results.
