Perspectives and advantages of using olive (Olea europaea) by-products as a dietary supplement for rabbit production and health

 

 

C. Losacco^I; V. Laudadio^I; M. Schiavitto^II; V. Tufarelli^{I, #}

^ISection of Veterinary Science and Animal Production, Department of Precision and Regenerative Medicine and Jonian Area, University of Bari 'Aldo Moro', Valenzano 70010, Italy
^IIItalian Rabbit Breeders Association (ANCI-AIA), 71030 Volturara Appula, Foggia, Italy

 

 

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ABSTRACT

Over the years, the olive oil market has increased considerably due to its organoleptic features and increasing awareness of the beneficial properties of olive products for human health. However, the olive oil production processes generate a variety of wastes and by-products that create serious environmental concerns because of their high phytotoxicity, but also represent an extraordinary potential source of functional compounds, such as polyphenols. This review explored the application of olive by-products as possible functional feed ingredient in rabbit nutrition. The available literature indicates that the manipulation of the rabbit diet is very reliable in producing "enriched meat" and that the bioactive fractions of olive by-products can be used to enhance meat microbial quality, fatty acid profile, and can increase the presence of compounds with natural antioxidant effect, which can exert beneficial effects on gut microbiota and animal welfare. Therefore, supplementing the diet of rabbits with olive by-products could present a sustainable option for valuable biomass, reduce the costs associated with animal feeding, and provide an "eco-green" improvement of meat quality.

Keywords: by-products, diet, nutrition, meat, olive, rabbit

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Introduction

Agro-industrial processing of food or non-food products generates a huge amount of by-products and residues that are rich in natural bioactive compounds (Kasapidou et al., 2015; Cappelli et al., 2021). The reports on global fruit and vegetable production show that residues with potential utilization after processing have been calculated in millions tons every year (Kowalska et al., 2017). Indeed, there is a great social, economic, and environmental concern about the effective reuse of these residues, which may have a negative impact on the environment and, on the other hand, represent a loss of valuable biomass rich in natural bioactive molecules and nutrients, which may be used for innovative food production (Santana-Meridas, 2012; Pfaltzgraff et al., 2013; Kasapidou et al., 2015; Kowalska et al., 2017; De Bruno et al., 2018). Vegetable residues constitute a valuable natural source of carbohydrates and polysaccharides; according to researchers, these by-products can present a very high content of bioactive molecules, such as proteins, vitamins, minerals, and antioxidants, such as polyphenols, flavonoids, and tannins (Grigoras et al., 2012; Correddu et al., 2020; Branciari et al., 2021 ; Vastolo et al., 2022). Therefore, although biomass residues produced along the food chain are not suitable for human consumption, they have considerable nutritional properties (Luciano et al., 2020) due to their appreciable bioactive components (Vastolo et al., 2022) that are useful for animal nutrition to improve animal health (Azizi et al., 2018; Correddu et al., 2020; Pinotti et al., 2020). As a sustainable alternative to traditional procedures, green approaches have recently been presented to recover bioactive compounds that safeguard human welfare, preserve the environment, and raise agro-industrial field competitiveness by a circular-green strategy. The 3R slogan "Reduce, Reuse, Recycle" should be assumed to revise the management of food waste and reduce the adverse effects on the environment of by-products (Memon et al., 2010; Sakai et al., 2011; Pinotti et al., 2020). Circular production models create more effective systems able to decrease both the consumption of natural resources and the amplification of wastes (Brunetti et al., 2022). Moreover, in the auspicious vision of the circular economy, the European Commission set the strategy "Farm to Fork Strategy - for a fair, healthy, and environmentally-friendly food system" (European Union Commission, 2020) with the intent of reducing the losses along the food chain and ensure the sustainability of food production, processing, and consumption (Vastolo et al., 2021).

Fruit and vegetable processing residues have historically been used in livestock feeding as main ingredients and their influence on animal performance has been extensively studied (Pfaltzgraff et al., 2013). Therefore, studies on the application of these by-products have attracted great interest, not only from an environmental point of view, but also from a human health perspective in producing functional foods that contain natural extracts (Cappelli et al., 2021).

The olive (Olea europea) cultivation and the olive oil industries play an important economic and social role in the Mediterranean basin (International Olive Council, 2017; Tufarelli et al., 2022a). Apart from the Mediterranean area, olive tree cultivation is also increasing in USA, Middle Eastern, and African countries (Selim et al., 2022). In recent years, the olive oil market has increased substantially due to organoleptic characteristics and rising awareness of the health benefits of olive products. However, cultivating olive trees and producing industrial and table olive oil generates enormous volumes of solid waste and dark liquid effluents, such as olive pomace, leaves, and olive oil mill wastewaters. Thus, these by-products cause an economic problem for producers and pose serious environmental concerns (Salomone et al., 2012).

Therefore, examining all the potential circular economic paths for the reuse of compounds from the olive oil supply chain is crucial (Stempfle et al., 2021). Olive by-products are rich in bioactive principles; indeed, they deliver a considerable amount of valuable organic acids, carbohydrates, proteins, fibre, and phenolic materials, which are characterized by a high variability in chemical composition between the various wastes and depend on the olive oil extraction method. Furthermore, innovative food applications and enhanced technological functions are now available to transfer these high value products in food directly or through the animal diets (Pinotti et al., 2020). Indeed, researchers have focused their interest on the production of new technologies for extracting and recovering bioactive chemicals from olive by-products and using them as functional feed ingredients in animal nutrition (Brunetti et al., 2022). Thus, the use of olive by-products as a part of animal diets can be a very effective strategy for recovering these healthy molecules and improving the functional value of meat and meat production.

Thus, using by-products in animal feed may ameliorate the technological quality of the final product and, on the other hand, constitute an economically and environmentally-friendly option in the livestock arena, raising productivity and sustainability (Berbel et al., 2018; Foti et al., 2021). Moreover, in recent decades, the European ban of the use of synthetic additives and antibiotic growth promoters (AGPs) in animal feed has emphasized the necessity to research alternative substances and additives that promote animal health, benefit growth performance, and improve meat quality (Bosetti et al., 2020; De Cara et al., 2023). This also considers the growing interest of the consumer on the link between diet and health, which has increased the demand for animal-derived functional foods for human consumption and a pressing requirement for 'clean label' foods that are safe and health-promoting.

Recent studies indicate that the use of natural feed additives (such as prebiotics, probiotics, synbiotics, organic acids, essential oils, antibodies, enzymes) affect the growth, function, and health of living organisms and they have been recognized as antimicrobials, antioxidants, antioxygenic, and antiparasitic (Madhupriya et al., 2018; Morshedy et al., 2021; Brunetti et al., 2022; Vastolo et al., 2022; Wickramasuriya et al., 2022). Moreover, when they are used as additives in animal diets, they can also act as growth promoters since they don't negatively affect animal health or the quality of animal products for human consumption (Falcao-e-Cunha et al., 2007; Akyildiz et al., 2016: Dalle Zotte et al., 2016; Brunetti et al., 2022). Owing to the rich rate of high value-added compounds, olive by-products can be employed to enrich other food products directly or indirectly, present lower toxicity, and are free of undesirable residues, compared to inorganic chemicals or antibiotics. Consequently, the bioactive molecules found in olive by-products, in particular, the fatty acids and polyphenols, can be used to make nutritional supplements and can represent an alternative natural dietary strategy based on plant-derived metabolites instead of synthetic products (Correddu et al., 2020; Oluwafemi et al., 2020).

Of the livestock products, rabbit meat is well appreciated for its high nutritional and dietetic properties that meet the favour of consumers. This animal-derived product is considered very healthy because it is lean, possesses a relatively high content of unsaturated fatty acids (60% of total FA), is rich in proteins (20-21%), and the amino acids are of high biological value; furthermore, it is low in cholesterol and sodium and rich in potassium, phosphorus, and magnesium (Bielanski et al., 2000; Dalle Zotte, 2002). Thus, rabbit meat could be a precious food in human nutrition, also considering that dietary fortification has been seen to be very effective in increasing the provision of the main nutrients. However, due to its significant concentrations of PUFA, rabbit meat presents a high susceptibility to lipid oxidation during storage, manifested by adverse changes in flavour, colour, texture, and nutritive value, with the possible production of toxic compounds (Trebusak et al., 2014).

Over the years, numerous studies have been conducted to determine how rabbit meat can be nutritionally enhanced and its shelf life extended to provide health-promoting effects for consumers. Studies involving humans and animals (in vivo and in vitro) have evidenced that dietary supplementation with olive oil and olive by-products has potentially advantageous biological effects resulting from their antioxidant, antimicrobial, and anti-inflammatory activities. Indeed, due to the high ratio of bioactive components, olive by-products represent a natural raw material for the recovery of valuable nutrients, such as polyphenols or aromatic oil; thus, their inclusion in rabbit diets could be a convenient strategy to increase the intrinsic quality and health conditions of the rabbits.

Based on these considerations, this review aimed to provide an overview of the recent knowledge on the application of olive by-products as a functional feed ingredient in the nutrition of growing rabbits for meat production. A brief description of the most represented bioactive molecules in the different olive by-products is also reported.

 

Rabbit meat: Main properties and perspectives for its improvement

The demand for functional foods has grown in recent years, also due to the increasing consumer knowledge of the link between health and diet. Consumers demand the production of "clean, natural, and eco-green"-label food products and pay attention on the major determinants of food quality such as sensory characteristics, shelf life, nutritional value, and health enhancers (Wenk, 2000; Kasapidou et al., 2015). Meat and meat products may be reputed as functional foods to the extent that they contain numerous compounds thought to be functional (Dalle Zotte et al., 2011).

Rabbit meat, per se, is characterized by a valuable nutritional composition and is thus appropriate for the modern consumer. This aspect represents the reason for promoting its consumption by nutritionists. Moreover, since the rabbit is a monogastric animal, dietary changes and/or supplementation with health-promoting ingredients are efficient strategies to further increase the nutritional quality of its meat (Dalle Zotte et al., 2011).

The rabbit is a highly specialized herbivore, being a monogastric hindgut fermenter. Due to its digestive physiology, rabbits effectively turn the proteins contained in cellulose-rich plants into food containing high-value animal proteins (Dalle Zotte, 2014; Cappelli et al., 2021). In fact, rabbit meat is rich in protein with a high essential amino acid content and it has a low fat content with an excellent proportion of saturated, monounsaturated, and polyunsaturated fatty acids. Rabbit meat also has a low cholesterol and sodium content. In addition, it is a good source of potassium, phosphorus, selenium, and B vitamins and is one of the richest sources of vitamin B12 (Cullere et al., 2018).

Moreover, manipulating rabbit diet is very effective in producing enriched meat and some bioactive compounds can be easily incorporated into the meat through the diet to obtain products considered functional (Dalle Zotte et al., 2011). One of the main aims of meat researchers for the nutritional improvement of meat is to reduce the saturated FA and increase the unsaturated FA in fat deposits. However, when the dietary manipulation enhances the content of unsaturated FA, this tends to increase the oxidative susceptibility of muscle tissue. Many investigations have shown that increasing the content of n-3 PUFA in diet has a positive effect on meat fatty acid composition (Dal Bosco et al., 2012; Trebusak et al., 2014; Branciari et al, 2021), but in return, this makes muscle tissue more susceptible to lipid oxidation (Bielanski et al., 2008; Zsédely et al., 2008; Trebusak et al, 2014). Thus, to prevent the oxidation, the addition of natural antioxidants in the rabbit diet seems to be an effective strategy to improve meat stability.

Therefore, appropriate dietary supplementation that is balanced in fat sources and antioxidant intake is fundamental to improving nutritional value and meat-product stability, shelf-life, and sensorial properties of rabbit meat. The dietary incorporation of olive by-products would satisfy both the requirements and the demands of the consumer since the biocompounds present in them can increase both the content of unsaturated fatty acids and the content of substances with antioxidant activity.

 

Use of olive by-products in animal production: Main goals and advantages

In recent years, researchers have focused their attention on applying olive by-products and/or their bioactive compounds to ameliorate the nutritional profile of food products, find novel natural additives, and reduce costs related to waste management and animal feeding.

Many generations attest to the fact that olive oil is an essential component of the healthy Mediterranean diet and represents the primary fat source in the MedDiet (Frankel et al., 2013; Pappas et al., 2019). In this context, olive oil consumption, in particular extra virgin olive oil (EVOO), plays an essential role as the main source of natural bioactive compounds, which exert the well-known beneficial health effects of the diet (European Union Reg EU 432/2012; Gaforio et al., 2019; Sarapis et al., 2022).

EVOO's ability to improve health conditions is due to several components, including its high content of monounsaturated fatty acids (MUFAs), in particular oleic acid, which can improve a-linolenic acid (ALA) conversion into longer-chain n-3 polyunsaturated fatty acids (PUFAs), leading to greater health benefits in terms of cardiovascular disease (CDV) (Wahle et al., 2004), metabolic diseases, inflammatory and autoimmune diseases, as well as the prevention of breast and colon cancer (Alarcon de la Lastra et al., 2001). The Food and Drug Administration (FDA) had recognized olive oil (23 g/day) as a qualified health claim to decrease the risk of coronary heart disease (FDA, 2004). To deliver benefits for human health, researchers recommend the absolute dietary intake of long chain n-3 PUFA and a decrease in the n-6/n-3 ratio to 5 as a maximum threshold value (Dalle Zotte et al., 2011; Cullere et al., 2018).

Numerous studies reported that olive oil health effects might also attributed to microconstituents, such as phenolic compounds or phenolic glycosides, such as oleuropein, hydroxityrosol, and tyrosol. In fact, their relevance has been recognized by the European Food Safety Authority (EFSA, 2011) with a 'health claim' related to specific EVOO phenolic compounds. According to the scientific opinion of EFSA (2011), a daily amount of 5 mg of hydroxytyrosol (3,4 dihydroxyphenylethanol; 3,4-DHPEA or HT) and its derivatives is responsible for the explicated health claim "protection of blood lipids from oxidative stress" (EFSA 2011). In an experimental study on humans, Colica et al. (2017) detected that the regular intake of 15 mg/kg HTyr resulted in the modification of body composition parameters and modulated the antioxidant profile and the expression of inflammation and oxidative stress-related genes in atherosclerosis (Finicelli et al., 2022). Moreover, the phenolic fraction of EVOO, except for oleic acid, also acts as promoting factor in the growth or survival of beneficial gut bacteria (mainly Lactobacillus strains) and inhibits the proliferation of some pathogenic bacteria (Martîn-Pelàez et al., 2017; Luisi et al., 2019). The available literature consistently emphasises that the diet influences the intestinal ecosystem and the functional capacity of the gut microbiota, which is recognized as a key factor in driving metabolic activity and is involved in the regulation of host immunity (Delzenne et al., 2011 ; Danneskiold-Samsøe et al., 2019).

Since the highest content (up to 70%) of these bioactive molecules is found in the unwrapped part and in the outer parts of the olive fruit, researchers have focused their attention on the use in animal feeding of olive processing by-products such as olive pomace, olive cake, olive mill waste waters, and olive leaves, the main characteristic and biocompounds of which are briefly described below (Contreras-Calderòn et al., 2011; Nunes et al., 2016; Sagar et al., 2018; Romeo et al., 2021; Foti et al., 2022).

Olive pomace (OP) is a heterogeneous biomass of semi-solid consistency remaining after olive oil extraction, with a considerable moisture and oil content that depends on the cultivation region, the ripening period, and the extraction system utilized (Meziane, 2011; Akay et al., 2015). Its major ingredients are sugars, proteins, fatty acids (oleic acid and other C2-C7 fatty acids), polyalcohols, polyphenols (Rodriguez et al., 2008; Mirabella et al., 2014), which can be gained using different extraction methods. OP chemical compounds, especially phenols, stand out as a promising valuable by-product. Several phenolic compounds have been detected: oleuropein, hydroxytyrosol and tyrosol derivatives, iridoid precursors, secoiridoids and derivates, flavonoids, lignans, and phenolic acids. In particular, the most abundant phenolic compound in olive fruit, namely oleuropein, has been found at high concentrations in OP (up to 0.9%) (Savournin, 2001; Sanchez de Medina et al., 2012).

Olive cake is constituted by the olive skin, crushed pulp, and kernel shell that come after oil extraction; it still contains some oil (9%) and ~25% water. The olive cake is also called "fatty olive cake" if the cake is not subjected to solvent extraction for oil separation. Generally, in animal feed, the olive cake is mixed with molasses (considering its lower palatability) and is utilized as a substitute for fibre because of its high cellulose content (Ferrer et al., 2021). The olive cake is characterized by a low crude protein content, a high crude fibre content, and up to 15% ether extract which is composed, principally, of monounsaturated fatty acids (mainly C18:1 cis-9 or oleic acid) (Molina-Alcaide et al., 2008). The use of olive cake in animal feeding constitutes a sustainable option to the disposal of biodegradable organic matter, decreasing dietary costs and permitting the rational utilization of this residual biomass. Furthermore, olive cake is a considerable source of phenolic and flavonoid compounds, so it has a wide range of biological properties. In accordance with several reports, olive cake contains phenolic compounds such as oleuropein, caffeic acid and hydroxytyrosol catechol (Selim et al., 2022). Allouche et al. (2004) identified tyrosol, rutin, vanillic acid, p-coumaric acid, verbascoside, and oleanolic acid.

Olive mill waste water (OMWW) is a liquid effluent derived mainly from the water used for the various stages of oil production and vegetable water from the fruit, and amounts to 0.5-3.25 m³ per 1000 kg of olives (Paraskeva et al., 2006; Kapellakis et al., 2012; Gerasopoulos et al., 2015b). The physicochemical features of OMWW are highly influenced by the conditions of soil and climate, cultivar, ripeness state and, above all, by oil extraction method. The OMWW is black and has a typical and intense aroma (Foti et al., 2021).

OMWW consists of 90% water, a minimal amount of organic compounds and mineral salts, and contains tannins, lignin, long chain fatty acids, reduced sugars, proteins, and phenolic compounds, which are toxic to microorganisms and plants (Paixao et al., 2002; Paraskeva et al., 2006). However, despite the toxicological effects on the environment, these compounds may have nutritional relevance in human diets owing the several health benefits, such as the inhibition of low-density lipoprotein oxidation, platelet aggregation, free radical reduction, production of leukotriene for human neutrophils, and in vitro antimicrobial activity (De Marco et al., 2007; Nunes et al., 2016). The OMWWs contain a substantial amount of bioactive compounds, namely phenols. Most of the phenolic portion present in olives is found in OMWW (>53%) and OP (45%), with only 2% of the initial content remaining in virgin olive oil (Rodis et al., 2002; Di Nunzio et al., 2019). The OMWW is a rich source of phenols, as it comprises 98 g/100 g of the total phenolic content of olive fruit and can therefore be considered to be of great potential (De Bruno et al., 2018).

The phenolic compounds present in OMWW are hydroxytyrosol, tyrosol, verbascoside, acids (such as caffeic, gallic, vanillic, and syringic), and polymeric substances (Obied et al., 2008a; Frankel et al., 2013; D'Antuono et al., 2014). Therefore, OMWW could be exploited as a possible cheap, starting matrix for the extraction of antioxidants in several fields, not least the food industry, where they could be used for fortifying and prolonging the shelf life of final products (De Marco et al., 2007; Obied et al., 2008b; Foti et al., 2021).

Olive leaves (OL) have been used for different purposes as food preservatives, additives in many products, cosmetics, and human health (Roselló-Soto et al., 2015). Olive leaves are mainly used to obtain olive leaf extract (OLE), tea, powder, and capsules (Ghanbari et al., 2012; Selim et al., 2022). Oleuropein is the most abundant phenolic compound in OL, followed by hydroxytyrosol (Benavente-Garcia et al., 2000; Dub et al., 2013; Nunes et al., 2016). Cavalheiro et al. (2015) determined OL fatty acids and showed that unlike olive oil, where the major unsaturated FA present is oleic acid, the predominant fatty acid in the OL lipid fraction was linolenic acid. Considering that linolenic acid, after metabolic pathways, results in long-chain PUFA of the n-3 series, OL can be considered a source of long-chain PUFA.

Several investigations have outlined the antioxidant, anti-inflammatory, immunomodulatory, analgesic, antimicrobial, antihypertensive, anticancer, and anti-hyperglycaemic activities of olive oil by-products (Foti et al., 2021). In recent decades, the valorization of these by-products in the food-chain represents a new challenge for olive mills and responds to the strong demand for innovation in food with a view to the creation of virtuous recycling (Foti et al., 2022). With this in mind, olive oil by-products can be used as feed supplements to improve animal reproductive and productive performance, health status, and welfare in order to obtain animal-derived functional foods containing natural extracts from the olive plant.

According to Ibrhaim et al. (2021) and Papadomichelakis et al. (2019), including olive oil by-products in the feed of growing animals has a positive impact for the following reasons. Firstly, olive by-products are considered as a low-cost complementary energy source due to their high oil content (Al-Harti, 2017). Secondly, they have more PUFAs, which account for meat fatty acid composition (Molina-Alcaide et al., 2008). Thirdly, their polyphenol content can be considered as an excellent source of natural antioxidants (King et al., 2014; Gerasopoulos et al., 2015a,b; Tufarelli et al., 2016), which help in delaying oxidative consequences in muscle tissues.

Thus, olive by-products may be considered a feed additive as per EFSA (2008) definition, because of the "favourable effects":

1- the sensory characteristics and acceptance of products (i.e., antioxidants and colorants);

2- the nutritional value of products (i.e., long chain PUFA, conjugated linoleic acid);

3- the microbial quality of products.

 

Effects of olive by-products on meat quality, oxidative status, and microbial spoilage

The advantage of using olive byproducts as feed supplements to improve performance, reduce oxidative stress, and fortify meat antioxidant status has been demonstrated in different production animals, such as lambs and goats (Luciano et al., 2013; Hukerdi et al., 2019), chickens (Gerasopoulos et al., 2015b; Tufarelli et al., 2016; De Cara et al., 2023), rabbits (Dal Bosco et al., 2012; Branciari et al., 2021), beef cattle (Branciari et al., 2015, Chiofalo et al., 2020), and pigs (Joven et al., 2014; Tsala et al., 2020). Furthermore, several studies have shown that dietary supplementation is effective also for the improvement of nutritional quality and quantity of animal products like milk, cheese (Abbeddou et al., 2011; Terramoccia et al., 2013; Vargas-Bello-Perez et al., 2013; Branciari et al., 2014; Roila et al., 2019; Chiofalo B. et al., 2020), and eggs (Abd El-Samee et al., 2011; Dedousi et al., 2022).

According to the available literature, dietary supplementation with by-products from olive oil processing might enrich the incorporation of bioactive compounds in rabbit muscle, influencing not only the microflora and the oxidative stability of meat, but also the nutritional profile of the products (Simitzis et al., 2018). In particular, the FA composition of olive by-products may have an advantageous influence on the intramuscular FA level (Molina-Alcaide et al., 2008). The olive by-products in rabbit diets influence meat quality, such as intramuscular fat and unsaturated FA contents. Indeed, the intramuscular FA profile of rabbit meat has an important role as MUFA, including oleic acid (18:1 n-9), have been shown to reduce plasma total cholesterol and low-density lipoprotein, and their consumption is highly recommended to prevent cardiovascular diseases (Gurr et al., 1989).

Many studies report that the inclusion of olive by-products in the diet of farm animals increases MUFA levels (especially oleic acid) in the meat of rabbits (Dal Bosco et al., 2012), broilers (Papadomichelakis et al., 2019), pigs (Tsala et al., 2020), lambs (Luciano et al., 2013), ewe milk (Vargas-Bello-Perez et al., 2013), and egg yolks (Dedousi et al., 2022). Dal Bosco et al. (2012) demonstrated that the content of intramuscular oleic acid and MUFA of rabbits fed different olive pomaces (OP) were proportional to oleic acid content of the by-product. The Authors also reported that dietary treatment with OP resulted in a modification of the fatty acid profile of meat with a marked increase in MUFA, and they concluded that feeding rabbits with OPs could enrich meat in precious FA that had beneficial effects on human health. Furthermore, rabbits fed supplemented diets had the greatest thiobarbituric acid reactive substances (TBARS) content and were therefore more susceptible to lipid peroxidation. Mattioli et al. (2018) reported that rabbits fed diets enriched with 10% olive leaves (OL) and 10% OL fortified with selenium (SeOL) showed a high amount of oleic acid and a positive trend for MUFA compared to the control group. Moreover, Papadomichelakis et al. (2019) found that in broiler chickens, dietary OP increased intramuscular oleic acid and MUFA in proportion to the inclusion in the finisher diet, as observed in prior studies (Sanz et al., 2000; Zhang et al., 2013a). In Japanese quail reared at different stocking densities, adding an OL extract with an oleuropein level of up to 400 ppm decreased the proportion of total SFA and increased total PUFA and n-3 and n-6 FA. Consequently, dietary oleuropein supplementation improved the quality of breast muscle lipids by lowering SFA proportions and enhancing PUFA content (Bahsi et al., 2016).

In finishing pigs, the increasing inclusion of olive cake linearly increased the oleic acid and MUFA levels in adipose, while meat SFA contents were decreased (Joven et al., 2014). An increase of MUFA concentration in the meat of pigs fed partially-defatted olive cake-supplemented diets (120 g/kg) was also observed without other side effects on growth performance, carcass quality, and microbial counts (Ferrer et al., 2020). Similarly, Chiofalo et al. (2020) found that the addition of between 7.5 and 15% OP influenced the performance of beef cattle by improving meat tenderness and modifying the meat quality index, including intramuscular fat and UFA.

Dietary olive cake supplementation of up to 5% in dairy cows increased UFA (mostly oleic acid, vaccenic acid, and CLA) and decreased SFA (short- and medium-chain FA) in derived cheese, suggesting a positive role of olive cake in increasing the nutritional and nutraceutical properties of the cheese (Chiofalo et al., 2020). Recently, Dedousi et al. (2022) reported that dietary supplementation with dried olive pulp reduced the content of total SFA, increased the percentage of PUFA, and improved the PUFA to SFA ratio in eggs.

Many trials have shown that enriching the content of n-3 PUFA has positive effect on FA content, but has a negative impact on lipid oxidation in rabbit meat, which might be improved by the implementation of antioxidants (Bielanski et al., 2008; Zsédely et al., 2008; Trebusak et al., 2014). Furthermore, many Authors (Rey et al., 2020; Xie et al., 2022) have focused on replacing synthetic additives with natural antioxidants; olive polyphenolic compounds seem to be an effective alternative to improving meat oxidative stability and microbial quality (Branciari et al., 2021 ; Foti et al., 2021). Studies both in vivo and in vitro were carried out to assess the antioxidant capacity of olive polyphenols to fortify meat and meat products through the addition of exogenous products after slaughter. Furthermore, these compounds have been also used for producing packaging materials (Bermúdez-Oria et al., 2018; Da Rosa et al., 2019; Khwaldia et al., 2022).

Through their antioxidant activity, olive by-products can provide multidimensional improvement in stored meat products, including colour retention, retardation of microbial growth, retardation of fat deterioration, and, ultimately, extended shelf-life (Foti et al., 2022). Galanakis et al. (2018) collected data related to the addition of an olive oil by-product (olive mill waste waters, OMWW) extract to fortify meat and meat products. Antioxidant supplementation improved hygienic conditions and rheological features of the final products. Hayes et al. (2009) tested aqueous phenolic extracts (100-300 mg/l) from olive leaves as well as lutein (100-300 mg/l), sesamol (500-2000 mg/l), and ellagic acid (300-900 mg/l) against oxymyoglobin oxidation and lipid oxidation in bovine and porcine muscle model systems. The lipid oxidation decreased following the addition of each of these natural antioxidants, suggesting that their application in meat products enhanced shelf-life characteristics (Gerasopoulos et al., 2015b; Galanakis et al., 2018). According to Foti et al. (2021), adding such compounds not only inhibits the growth of pathogens, reducing spoilage microorganisms in meat during storage, but also extends the shelf life through their antioxidant potential.

In particular, phenolic fractions of by-products have been shown to inhibit or delay the rate of growth of a vast range of gram-positive and gram-negative bacteria (Fasolato et al., 2015; Nazzaro et al., 2019; Branciari et al., 2021). In vivo assays showed that phenolic compounds from trees and leaves presented a potent antioxidant activity; the addition of only 5 g O. europaea leaves/kg in turkey diets markedly increased the oxidative stability of breast fillets during refrigerated storage and was equal to 150 mg/kg a-tocopherol acetate supplementation (Botsoglou et al., 2010). The inclusion of 6% linseed oil and 1% Ganoderma lucidum (Reishi mushrooms) or O. europaea leaves in rabbit diets both enhanced MUFA content and balanced the oxidative status of the treated meat. The supplemented group tended to have an increase in meat oxidative stability, as detected by modestly decreased MDA values in all stored and heat-treated conditions. The activity of O. europaea leaves was more efficient in cooked samples (Trebusak et al., 2014).

Recently, Branciari et al. (2021) demonstrated that rabbit dietary fortification with low (150 mg/kg) and high doses (280 mg/kg) of an extract of polyphenols derived from OMWW could influence the growth of meat microflora by enriching the level of these bioactive compounds in the muscle. The analytic determination of polyphenol content was conducted in both feed and meat (Longissimus lumborum muscle, LL) samples. The inclusion of OMWW in diets clearly influenced the total biophenol content in feed and muscle tissue. In the tested feeds, hydroxityrosol and verbascoside were the prevalent chemicals, followed by tyrosol and pinoresinol. As expected, the phenol metabolite contents were higher in the muscle of the treated than the control group. In particular, the hydroxityrosol sulphates (HT-3-S and HT-4-S) were ~three times higher in the muscle of animals fed with OMWW supplement at low concentration (0.60-1.25 mg/kg) than in rabbits that were fed the control diet (0.160.40 mg/kg). Furthermore, the content of these compounds was ~two-fold higher in rabbits fed with the highest concentration in the diet (1.11-2.52 mg/kg).

The microbiological determination was conducted on the cranial part of the LL at time 0 and after 3, 6, 9, and 12 days of storage. The microbial evolution of refrigerated LL muscle was carried out using the total viable count (TVC), psychrotrophic counts (TPC), lactic acid bacteria (LAB), and counts of Pseudomonas spp. and Enterobacteriaceae. The antimicrobial activity of phenolic compounds varied among the microbial populations and phenolic integration levels. The feeding strategy reduced Pseudomonas spp. growth starting from 6 d of storage in the group fed the highest concentration, but did not interfere with the growth of TVC, TVP, LAB, and Enterobacteriaceae. This is in contrast with previous studies that have referred to antimicrobial activity on TVC count, LAB count, and Enterobacteriaceae exerted by the addition of polyphenolic compounds through dietary supplementation with liquorice extract (Dal Bosco et al., 2019), oregano essential oils (Soultos et al., 2009), and onion and cranberry extracts (Konè et al., 2019) in rabbit diets.

Dal Bosco et al. (2012) evaluated the effects of a dietary supplementation by adding 5% of three types of olive pomace (OP) and a mixture of them derived from different olive cultivars (Coratina, Maraiolo, Frantoio, and Ogliarola), characterized by different phenolic contents. The three diets supplemented with 5% OPs yielded differences in the performance and meat quality of growing rabbits. The data demonstrated that meat quality could be seriously affected by the quality of the OP used in the rabbit diets and that the meat oxidation values tended to decrease in the OP-supplemented groups, compared to the control group. The rabbits fed the diet containing the cultivar with the highest phenolic concentration had the highest oxidative stability and nutritional value, as revealed by the low concentration of lipid peroxidation and the high nutritional indices, respectively. The lipid peroxidation level in the muscle, measured by the value of the absorbance of TBARs, revealed that, in the meat of OP-treated rabbits, the extent of peroxidation was less than in the control group. This suggests that the high polyphenol content of the supplemented diet prevented the oxidation of unsaturated lipids, contributing to the preservation of meat and resulting in a high nutritional index of meat from the treated rabbits. Furthermore, Dal Bosco et al. (2012) observed that rabbit meat from the group fed the diet supplemented with OP from the Coratina cultivar (50 g/kg), despite its relatively high hydroxytyrosol content, presented reduced oxidative stability and was more susceptible to lipid peroxidation. The Authors concluded that only olive by-products of high quality (in terms of pro-oxidant/antioxidant balance and high polyphenol content) could ensure an advantageous meat oxidative stability.

Oxidative stress also causes direct damage to proteins or leads to chemical modification of amino acids (Andreadou et al., 2006). Recent studies have shown that protein oxidation can induce protein polymerization and aggregation, affecting their digestibility and reducing the nutritional value of the meat (Zhang et al., 2013b; Gerasopoulos, 2015a). According to Tufarelli et al. (2022a), this reaction seems to be directly influenced by the level of lipid oxidation in meat. Moreover, Gerasopoulos et al. (2015a) reported that there was evidence that oxidation products from protein and lipids could further increase the oxidation (Faustamn et al., 2010). Protein oxidation increases the protein content in carbonyls, which then serve as biomarkers of general oxidative stress (Dalle-Donne et al., 2003). It was found by Gerasopoulos et al. (2015a) that incorporating 4% OMWW into broiler feed markedly decreased the protein carbonyl content in meat; TBARS content was also substantially decreased in groups that received OMWW by 50.70 and 13.60%, respectively, in muscle; by 33.5 and 11.8%, respectively, in heart; and by 23.0 and 17.9%, respectively, in the liver, compared to the control group.

Recently, De Cara et al. (2023) conducted a study to demonstrate a linear and negative correlation between plasma antioxidant biomarkers and meat lipid oxidation by including an olive leaf and grape-based by-product (2g/kg OLG-mix) in broiler diets. Meat from birds supplemented with the OLG-mix resulted in a tendency to have lower TBARS production compared to groups without supplementation; plasma SOD concentrations of treated groups showed a marked increase, confirming that the supplemented diet fortified oxidative status and meat stability.

 

Preservation of gut microbiota and antimicrobial activity for improving rabbit health and performance

The control of oxidative stress is relevant in achieving adequate growth and a good state of health (Forman et al., 2021). Under physiological conditions, all cells produce reactive oxygen species (ROS), which can cause cellular damage if not captured in time by the body's antioxidant systems (Evans et al., 1997). Therefore, an imbalance in the organism's antioxidant and oxidant capacity can lead to diseases and physiological alterations.

The diet can influence the oxidative processes in the body and may lead to biological damage, health disorders, lower growth rates, and economic losses (Tufarelli et al., 2016). Supplementing animal diets with antioxidants improves the plasma's redox status balance and prevents oxidative damage by protecting the body from free radicals (Puvaca et al., 2018; Tufarelli et al., 2023).

The fruit of the olive tree (Kalogeropoulos et al., 2014) and its by-products (Botsoglou et al., 2013; King et al., 2014; Gerasopoulos et al., 2015a,b) contain several antioxidants, namely phenols, which can potentially scavenge free radicals and provide antioxidant protection. These positive effects act on both plasma and meat oxidative status. Moreover, researchers report that the antioxidant action of these compounds can have beneficial effects on the gut microbiota.

The first requirement for a dietary compound to be an in vivo antioxidant in an organism is that it enters the blood circulation. Animal and human studies show that olive oil by-products are well absorbed. Many reports (Vissers et al., 2002; Tan et al., 2003) have shown that oleuropein is rapidly absorbed after oral administration, with maximum plasma concentration occurring 2 h after administration (Andreadou et al., 2006). Polyphenols are directly absorbed or metabolized in the intestine or transformed into active metabolites, where they might exert a local action in relation to their interaction with gut microbiota (Luisi et al., 2019). Branciari et al. (2021) demonstrated that olive-derived phenolic supplementation in rabbit diets produced mainly polyphenol sulphate metabolites, confirming that these molecules were absorbed in gut (Corona et al., 2009; Rubiò et al., 2014; Branciari 2021). Tufarelli et al. (2016) reported that the absorption of hydroxytyrosol, the most important metabolite of oleuropein, takes place in the small intestine and colon with an absorption rate that varies according to the animal species (Visioli et al., 2002). It has been reported that polyphenols in some environments may exert pro-oxidant effects or interact with the gut microbiota, where they potentially modulate the oxidative status of the intestinal barrier, inflammation, and immune response of the host (Lipinski et al., 2017; Deiana et al., 2018; Luisi et al., 2019; Abd El-Moneim et al., 2020; De Cara et al., 2023).

The addition of olive phenols to mixed feed of many livestock species may enhance the protective mechanism of gut microbiota against bacterial disease, promote digestion and absorption of nutrients and, as a result, improve performance (Sayehban et al., 2015; Tufarelli et al., 2016; Berbel et al., 2018; Mancini et al., 2018; Tzamaloukas et al., 2021; Tufarelli et al., 2022b). Tufarelli et al. (2016) reported a marked improvement in the growth performances in broilers fed extra-virgin olive oil over other dietary fat sources. In the same study, the intestinal histological features indicated that olive phenol supplementation increased the intestinal villus height and crypt depth, raising the absorption of nutrients and improving the performance score. The Authors postulated that the favourable results of the EVOO diet on growth performance of chickens could be explained by the positive impact of this oil on the reduced passage rate of the digesta through the gastrointestinal tract, facilitating better nutrient absorption and utilization (Poorghasemi et al., 2013, 2015; Tufarelli et al., 2016).

In a study conducted by Sayehban et al. (2016) the inclusion of olive pulp (OP) (100 g/kg) in broiler diets increased absolute and relative jejunum weights and length, resulting in an increase in lipid absorption and serum levels in comparison to other experimental groups. The jejunum is the main site of nutrient absorption in the gastrointestinal tract, and increasing its size is highly desirable and correlated with greater absorption of nutrients (Macari, 2008). Furthermore, considering that the gastrointestinal tract is the largest organ of the body's immune defence in animals, the presence of antioxidants and antimicrobial substances in this environment may influence immune organ size and weight, thus resulting in less inflammatory and chemotactic local reaction (Sayehban et al., 2016). Lastly, the antioxidant compounds may enhance the antioxidant enzyme activities, reducing the intensity of lipid peroxidation and the generation of free radicals (Sreelatha et al., 2009), thus, preventing morphological changes and oxidative damage of intestinal microflora. Al-Sagheer et al. (2017) examined the influence of supplemental dietary extra virgin olive oil (EVOO), gallic acid (GA), or lemongrass essential oil (LGEO) on growth performance, nutrient digestibility, carcass traits, lipid peroxidation, haematological, and antioxidative status in growing rabbits under heat stress conditions. In growing rabbits, studies confirm that heat-stress is the most remarkable cause of oxidative stress linked with a drastic formation of free radicals and ROS.

Oxidative stress has a detrimental effect on feed intake, body weight gain, feed efficiency, reproductive performance, and health of rabbits (Marai et al, 2002; Finzi et al., 2010; Al Sagheer et al., 2017). High environmental temperature decreases growth indices, probably due by the amplification ROS, which oxidize and destroy cellular structures and impair intestinal tissues (Al-Sagheer et al., 2017). Additionally, heat stress has been reported to suppress diverse components of the immune system, enhancing vulnerability to various pathologies (Aggarwal et al., 2013). Thus, antioxidant feed supplementation has been recommended for protecting and mitigating the impact of stress on health and productivity (Lykkesfeldt et al., 2007; Abuelo et al., 2015; Gerasopoulos et al., 2015a; Al Sagheer et al., 2017). In their study, Al-Sagheer et al. (2017) reported that dietary supplementation of EVOO, GA, or LGEO enhance growth performance, nutrient digestibility, lipid peroxidation, and antioxidative status of growing rabbits. In fact, rabbits supplemented with EVOO, GA, or LGEO showed substantially higher values of weight gain (14.57, 11.29, and 14.90%, respectively) throughout the experiment, compared with the non-supplemented rabbits. Al-Sagheer et al. (2017) reported that natural antioxidants can protect intestinal mucosa against oxidative damage and pathogens and limit peristaltic movement in digestive disorders, preventing diarrhoea and enhancing animal performance (Kermauner et al., 2008). Consequently, the Authors postulated that such improvements in growth performance in response to EVOO and LGEO could be linked to the antioxidant activity of their components. On the other hand, significant increases in WBC, lymphocyte, and heterophils counts have been reported in EVOO-supplemented rabbits. According to the Authors, such elevations might be due to activation of gut-associated lymphoid tissue in response to the diet supplemented with EVOO or its cytoprotective activity against free radical-induced injury during heat stress (Khalil et al., 2013).

In order to reduce the environmental stress caused by stocking density in Japanese quail, Bahsi et al. (2016) reported that the addition of oleuropein (440 ppm) in the diet increased the body weight gain, feed conversion ratio, and PUFA content, emphasizing that oleuropein was effective in mitigating the negative effects of oxidative stress, especially in a stressed state. This situation can be explained by the addition of essential oils to mixed feed, which then regulate the gastrointestinal tract of animals, increase feed intake, and act as protective agents against bacterial diseases (Dalle Zotte et al., 2016; Elazab et al., 2022). Moreover, intestinal microbial integrity is important in protecting the host from pathogen colonization through multiple mechanisms, including competition for epithelial binding sites, production of bacteriocins, and the strengthening of the intestinal immune response (Burkholder et al., 2008; El-Badawi et al., 2018).

In recent decades, in vitro and in vivo studies have provided clear evidence concerning the antimicrobial activity of compounds contained in olive, olive oil, leaves, and vegetation waters (Furneri et al., 2004). Thus, many studies have focused on the antimicrobial properties of plant-derived active compounds with the aim of finding and developing new antimicrobial agents that can be transferred to food through the animal diet (Fasolato et al., 2015; Branciari et al., 2016; Roila et al., 2019; Branciari et al., 2021). Studies have demonstrated that the olive-phenol fraction is able to inhibit or delay the rate of growth of a range of bacteria and fungi, and so it can be used effectively as an alternative natural additive in both human and animal diets (Branciari et al., 2021). Furneri et al. (2004) showed good antimicrobial activity of oleuropein and hydroxytyrosol against gram-positive and gram-negative bacteria (Salmonella sp., Vibrio sp., and Staphylococcus aureus) (Bisignano et al., 2001), as well as the ability of oleuropein to inhibit mycoplasmas (Furneri et al., 2002). Obied et al. (2008b) reported that the phenolic fraction of OMWW showed antibacterial activity against S. aureus, Bacillus subtilis, Escherichia coli, and Pseudomonas aeruginosa. These findings indicate that oleuropein and hydroxytyrosol can be considered an alternative antimicrobial agents for preventing or treating infections.

In growing rabbits, particularly weaners, digestive disturbances are the main cause of important economic losses for rabbit farmers (Marlier et al., 2006). The post-weaning period (from 5-8 w of age) is considered a crucial period in which the kits are removed from the mothers. Milk is substituted with solid feed while the kits' immune system and digestive systems (caecal microbiota) are still immature (Gidenne et al., 2005; Carabano et al., 2006; De Blas et al., 2012; Cullere et al., 2018).

Digestive disorders may be derived from infection, bacteria, or parasites or may be described under the term "non-specific enteritis", in which feeding and stress seem to be the principal agents that provoke different clinical symptoms, intestinal lesions, and diarrhoea (Dalle Zotte et al., 2016). Thus, preserving the integrity of gut microbiota and intestinal mucosa adequately through dietary strategies is an important target to reduce productive losses. It was observed by Younan et al. (2018) that the supplementation of olive leaf extract (OLE) of up to 1.5 ml/kg of rabbit diets improved the growth performance and increased the final body weight of animals. The Authors supposed that the improvement of rabbit performance may be due to the beneficial effects of OLE phenols in controlling the microbial infections (Aliabadi et al., 2012), thus enhancing nutrient digestibility and intestinal absorption. According to Sudjana et al. (2009), oleuropein plays a role in regulating the composition of the gastric flora by selectively reducing levels of C. jejuni and S. aureus. Markin et al. (2003) revealed that aqueous OLE 0.6% (w/v) in drinking water killed E. coli, P. aeruginosa, S. aureus, and K. pneumonia. Moreover, Dalle Zotte et al. (2016) refer that olive extract and its active compound, oleuropein, had an antimicrobial effect against pathogens such as B. cereus, S. aureus, S. enteritidis,and Listeria monocytogenes(Nychas et al., 1990). Polyphenolic compounds indirectly decrease the growth of pathogenic microorganisms by increasing the activity of digestive enzymes and reducing toxins within the feed (Wenk, 2002; Tufarelli et al., 2016; Younan et al., 2018). The overall effects on health and productive parameters of rabbits fed diets including olive by-products are summarized in Table 1.

 

Conclusions

Because of the increasing trends in consumer demands for functional foods and 'eco-green' products, researchers have directed their attention to the development of reasonable practices that can be adopted to improve the nutritional value and organoleptic properties of meat using bioactive molecules from natural products. Olive by-products represent a valuable source of functional compounds that can potentially be used in animal feeding for food product preservation and meat quality improvement. Furthermore, phenolic extracts from olive by-products could be used as an alternative to synthetic additives that have recently been banned. The reviewed literature, although scarce, confirms that dietary supplementation with olive by-products can satisfy rabbit nutritional requirements as the biocompounds may increase the content of unsaturated fatty acids and the content of substances with antioxidant and antimicrobial activity. Moreover, the literature demonstrates a negative, linear relationship between plasma redox status and the development of detrimental oxidative processes in the muscle, highlighting the influence of phenolic compounds on meat stability. Thus, it can be concluded that dietary supplementation with olive by-products can be a feasible approach in rabbit farming to support performance, reduce costs, and respond to the consumers request for high quality, healthy, safe, and friendly products. Further research is indicated to explore their biological action in organic systems and to produce alternative feeding strategies that enrich meat in precious compounds and improve the oxidative stability of meat products.

 

Acknowledgements

Authors acknowledge the Apulia Region for supporting the research work within the framework of the Program RIPARTI POC Puglia FESR-FSE 2014/2020 at the University of Bari "Aldo Moro" (Grant No. 31523dd2).

 

Author contributions

All the authors approved the final version of the manuscript. CL, MS, VL, and VT: conceptualization, writing-review & editing, writing-original draft.

 

Data availability

Data are contained within the article.

 

Conflict of Interest Declaration

The authors declare no conflicts of interest.

 

References

Abbeddou, S., Rischkowsky, B., Hilali, M.E.D., Hess, H.D., Kreuzer., M., 2011. Influence of feeding Mediterranean food industry by-products and forages to Awassi sheep on physicochemical properties of milk, yoghurt, and cheese. J. Dairy Res. 78, 426-435.         [ Links ]

Abd El-Moneim, A. E. M. E., Sabic, E. M., Mabu-Taleb, A., 2022. Influence of dietary supplementation of irradiated or non-irradiated olive pulp on biochemical profile, antioxidant status and immune response of Japanese quails. Biol. Rhythm Res. 53:519-534.         [ Links ]

Abd El-Samee, L.D., Hashish, S.M., 2011. Olive cake in laying hen diets for modification of yolk lipids. J. Agric. Sci. Technol. A1, 415-421.         [ Links ]

Abuelo, A., Hernandez, J., Benedito, J.L., Castillo, C., 2015. The importance of the oxidative status of dairy cattle in the periparturient period: Revisiting antioxidant supplementation. J. Anim. Physiol. Anim. Nutr. (Berl) 99(6): 1003-1016.         [ Links ]

Aggarwal A, Upadhyay R., 2013. Heat stress and immune function. In: Aggarwal, A., Upadhyay, R. (eds). Heat Stress and Animal Productivity. Springer India, New Delhi, pp 113-136.         [ Links ]

Akay, F., Kazan, A., Celiktas, M.S., Yesil-Celiktas, O., 2015. A holistic engineering approach for utilization of olive pomace. J Supercrit Fluids 99:1-7.         [ Links ]

Akyildiz, S., Denli, M., 2016. Application of plant extracts as feed additives in poultry nutrition. Anim. Sci. 59: 71-74        [ Links ]

Al Saagher, A.A., Daader, A.H., Gabr, H.A., Abd El-Moniem, E.A., 2017. Palliative effects of extra virgin olive oil, gallic acid, and lemongrass oil dietary supplementation on growth performance, digestibility, carcass traits, and antioxidant status of heat-stressed growing New Zealand White rabbits. Environ Sci Pollut Res 24:6807-6818.         [ Links ]

Alarcon de la Lastra, C., Barranco, M.D., Motilva, V., Herrerias, J.M., 2001. Mediterranean diet and health: Biological importance of olive oil. Current Pharmaceutical Design 7:933-950.         [ Links ]

Al-Harthi, M., 2017. The effect of olive cake, with or without enzymes supplementation, on growth performance, carcass characteristics, lymphoid organs and lipid metabolism of broiler chickens. Braz J Poult Sci. 19:83-90.         [ Links ]

Aliabadi, M.A., Darsanaki, R.K., Rokhi, M.L., Nourbakhsh, M., Raeisi, G., 2012. Antimicrobial activity of olive leaf aqueous extract. Ann. Biol. Res. 3(8): 4189-4191.         [ Links ]

Amro, B., Aburjai, T., Al-Khalil, S., 2002. Antioxidative and radical scavenging effects of olive cake extract. Fitoterapia 73: 456-461.         [ Links ]

Andreadou, I., Iliodromitis, E.K., Mikros, E., Constantinou, M., Agalias, A., Magiatis, P., Skaltsounis, A.L., Kamber, E., Tsantili-Kakoulidou, A., Kremastinos, D.T., 2006. The olive constituent oleuropein exhibits anti-ischemic, antioxidative, and hypolipidemic effects in anesthetized rabbits. J Nutr 136: 2213-2219.         [ Links ]

Azizi, M., Seidavi, A., Ragni, M., Laudadio, V., Tufarelli, V., 2018. Practical applications of agricultural wastes in poultry feeding in Mediterranean and Middle East regions. Part 1: Citrus, grape, pomegranate, and apple wastes. World's Poult. Sci. J. 74: 489-498.         [ Links ]

Bahsi, M., Çiftci, M., Şimsek, Ü.G., Azman, M.A., Özdemir, G., Yilmaz, Ö., Dalkilic, B., 2016. Effects of olive leaf extract (oleuropein) on performance, fatty acid levels of breast muscle, and some blood parameters in Japanese quail (Coturnix coturnix Japonica) reared in different stocking densities. Ankara. Üniv. Vet. Fak. Derg. 63: 61-68.         [ Links ]

Benavente-Garcia, O., Castillo, J., Lorente, J., Ortuno, A., Del Rio, J.A., 2000. Antioxidant activity of phenolics extracted from Olea europaea L. leaves. Food Chem. 68: 457-462.         [ Links ]

Berbel, J., Posadillo, A., 2018. Opportunities for the bioeconomy of olive oil byproducts. Biomed. J. Sci. Tech. Res. 2: 2094-2096.         [ Links ]

Bermúdez-Oria, A., Rodríguez-Gutiérrez, G., Rubio-Senent, F., Fernández-Prior, Á., Fernández-Bolaños, J., 2018. Effect of edible pectin-fish gelatin films containing the olive antioxidants, hydroxytyrosol and 3,4-dihydroxyphenylglycol, on beef meat during refrigerated storage. Meat Science 148: 213-218.         [ Links ]

Bielanski P., Zajac J., Fijal J., 2000. Effect of genetic variation of growth rate and meat quality in rabbits. Proceedings of the 7th World Rabbit Congress, Valencia, Spain, 4-7 July 2000. pp. 561-566.         [ Links ]

Bielanski, P., Kowalska, D., 2008. Use of linseed oil and antioxidant (vitamin E) in rabbit diets to improve dietetic traits of rabbit meat. 9th World Rabbit Congress. Verona, Italy, pp. 1319-1324.         [ Links ]

Bisignano, G., Lagana, M.G., Trombetta, D., Arena, S., Nostro, A., Uccella, N., Mazzanti, G., Saija. A., 2001. In vitro antibacterial activity of some aliphatic aldehydes from Olea europaea L. FEMS Microbiol. Lett. 198:9-13.         [ Links ]

Bosetti, G.E., Griebler, L., Aniecevski, E., Facchi, C.S., Baggio, C., Rossatto, G., Leite, F., Valentini, F.D.A., Santo, A.D., Pagnusatt, H., et al., 2020. Microencapsulated carvacrol and cinnamaldehyde replace growth-promoting antibiotics: Effect on performance and meat quality in broiler chickens. An. Acad. Bras. Cienc. 92: 1-14.         [ Links ]

Botsoglou E., Christaki E., Botsoglou, N., 2010. Effect of dietary olive leaves and/or a-tocopheryl acetate supplementation on microbial growth and lipid oxidation of turkey breast fillets during refrigerated storage. Food Chemistry 121: 17-22.         [ Links ]

Botsoglou, E.N., Govaris, A.K., Ambrosiadis, I.A., Fletouris, D.J., 2013. Olive leaves (Olea europaea L.) versus a-tocopheryl acetate as dietary supplements for enhancing the oxidative stability of eggs enriched with very-long-chain n-3 fatty acids. J Sci Food Agric. 93: 2053-2060.         [ Links ]

Bouaziz, M., Fki, I., Jemai, H., Ayadi, M., Sayadi, S., 2008. Effect of storage on refined and husk olive oils composition: Stabilization by addition of natural antioxidants from Chemlali olive leaves. Food Chem. 108: 253-262.         [ Links ]

Branciari, R., Galarini, R., Trabalza-Marinucci, M., Miraglia, D., Roila, R., Acuti, G., Giusepponi, D., Dal Bosco, A., Ranucci, D., 2021. Effects of olive mill vegetation water phenol metabolites transferred to muscle through animal diet on rabbit meat microbial quality. Sustainability. 13 (8): 4522.         [ Links ]

Branciari, R., Ranucci, D., Miraglia, D., Urbani, S., Esposto, S., Servili, M., 2015. Effect of dietary treatment with olive oil by-product (olive cake) on physicochemical, sensory, and microbial characteristics of beef during storage. Ital. J. Food Saf. 4: 225-229.         [ Links ]

Branciari, R., Ranucci, D., Ortenzi, R., Roila, R., Trabalza-Marinucci, M., Servili, M., Papa, P., Galarini, R., Valiani, A., 2016. Dietary administration of olive mill wastewater extract reduces Campylobacter spp. Prevalence in broiler chickens. Sustainability. 8: 837.         [ Links ]

Branciari, R., Ranucci, D., Trabalza-Marinucci, M., Codini, M., Orru, M., Ortenzi, R., Valiani, A., 2014. Evaluation of the antioxidant properties and oxidative stability of Pecorino cheese made from the raw milk of ewes fed Rosmarinus officinalis L. leaves. Int. J. Food Sci. Technol. 50: 558-565.         [ Links ]

Brunetti, L., Leuci, R., Colonna, M.A., Carrieri, R., Celentano, F.E., Bozzo, G., Loiodice, F., Selvaggi, M., Tufarelli, V., Piemontese, L., 2022. Food industry byproducts as starting material for innovative, green feed formulation: A sustainable alternative for poultry feeding. Molecules. 27: 4735.         [ Links ]

Burkholder, K.M., Thompson, K.L., Einstein, M.E., Applegate, T.J., Patterson, J.A., 2008. Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella enteritidis colonization in broilers. Poult. Sci. 87: 1734-1741.         [ Links ]

Cappelli, K., Ferlisi, F., Mecocci, S., et al., 2021. Dietary supplementation of olive mill waste water polyphenols in rabbits: Evaluation of the potential effects on hepatic apoptosis, inflammation, and metabolism through RT-qPCR approach. Animals. 11(10): 2932.         [ Links ]

Carabaño, R., Badiola, I., Licois, D., Gidenne, T., 2006. The digestive ecosystem and its control through nutritional or feeding strategies. In: Maertens L., Coudert P. (Eds.), Recent Advances in Rabbit Sciences. ILVO, Merebleke, Belgium. pp. 221-227.         [ Links ]

Cavalheiro, C.V., Picoloto, R.S., Cichoski, A.J., Wagner, R., deMenezes, C.R., Zepka, L.Q., Da Croce D.M., Barin, J.S., 2015. Olive leaves offer more than phenolic compounds: Fatty acids and mineral composition of varieties from southern Brazil. Industrial Crops and Products. 71: 122-127.         [ Links ]

Chiofalo, V., Liotta, L., Lo Presti, V., Gresta, F., Di Rosa, A.R., Chiofalo, B., 2020a. Effect of dietary olive cake supplementation on performance, carcass characteristics, and meat quality of beef cattle. Animals. 10(7): 1176.         [ Links ]

Chiofalo, B., Di Rosa, A.R., Lo Presti, V., Chiofalo, V., Liotta, L., 2020b. Effect of supplementation of herd diet with olive cake on the composition profile of milk and on the composition, quality, and sensory profile of cheeses made there from. Animals. 10: 977.         [ Links ]

Colica, C., Di Renzo, L., Trombetta, D., Smeriglio, A., Bernardini, S., Cioccoloni, G., Costa de Miranda, R., Gualtieri, P., Sinibaldi Salimei, P., De Lorenzo, A., 2017. Antioxidant effects of a hydroxytyrosol-based pharmaceutical formulation on body composition, metabolic state, and gene expression: A randomized double-blinded, placebo-controlled crossover trial. Oxid. Med. Cell. Longev. 2017: 2473495.         [ Links ]

Contreras-Calderón, J., Calderón-Jaimes, L., Guerra-Hernández, E., García-Villanova, B., 2011. Antioxidant capacity, phenolic content and vitamin C in pulp, peel, and seed from 24 exotic fruits from Colombia. Food Res. Int. 44: 2047-2053.         [ Links ]

Corona, G., Spencer, J., Dessl, M., 2009. Extra virgin olive oil phenolics: Absorption, metabolism, and biological activities in the GI tract. Toxicol. Ind. Health. 25: 285-293.         [ Links ]

Correddu, F., Lunesu, M.F., Buffa, G., Atzori, A.S., Nudda, A., Battacone, G., Pulina, G., 2020. Can agro-industrial by-products rich in polyphenols be advantageously used in the feeding and nutrition of dairy small ruminants? Animals. 10: 131.         [ Links ]

Cullere, M., Dalle Zotte, A., 2018. Rabbit meat production and consumption: State of knowledge and future perspectives. Meat Science. 143: 137-146.         [ Links ]

D'Antuono, I., Kontogianni, V.G., Kotsiou, K., Linsalata, V., Logrieco, A.F., Tasioula-Margari, M., Cardinali, A., 2014. Polyphenolic characterization of olive mill wastewaters, coming from Italian and Greek olive cultivars, after membrane technology. Food Res. Int. 65: 301 -310.         [ Links ]

Da Rosa, G.S., Vanga, S.K., Gariepy, Y., Raghavan, V., 2019. Development of biodegradable films with improved antioxidant properties based on the addition of carrageenan containing olive leaf extract for food packaging applications. J. Polymers Env. 28: 123-130.         [ Links ]

Dal Bosco, A., Mourvaki, E., Cardinali, R., Servili, M., Sebastiani, B., Ruggeri, S., Castellini, C., 2012. Effect of dietary supplementation with olive pomaces on the performance and meat quality of growing rabbits. Meat Sci. 92: 783-788.         [ Links ]

Dal Bosco, A., Mattioli, S., Matics, Z., Szendrö, Z., Gerencsér, Z., Mancinelli, A.C., Kovacs, M., Cullere, M., Castellini, C., Dalle Zotte, A., 2019. The antioxidant effectiveness of liquorice (Glycyrrhiza glabra L.) extract administered as dietary supplementation and/or as a burger additive in rabbit meat. Meat Sci. 158: 107921.         [ Links ]

Dalle Zotte, A., Celia, C., Szendrö, Z., 2016. Herbs and spices inclusion as feedstuff or additive in growing rabbit diets and as additive in rabbit meat: A review. Livest. Sci. 189: 82-90.         [ Links ]

Dalle Zotte, A., 2014. Rabbit farming for meat purposes. Animal Frontiers. 4: 62-67.         [ Links ]

Dalle Zotte, A., 2002. Perception of rabbit meat quality and major factors influencing the rabbit carcass and meat quality. Livest. Prod. Sci. 75: 11-32.         [ Links ]

Dalle Zotte, A., Szendrö, Z., 2011. The role of rabbit meat as functional food. Meat Sci. 88: 319-323.         [ Links ]

Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A., Colombo, R., 2003. Protein carbonyl groups as biomarkers of oxidative stress. Clinic. Chim. Acta. 329: 23-38.         [ Links ]

Danneskiold-Sams0e, N. B., Dias de Freitas Queiroz Barros, H., Santos, R., Bicas, J. L., Cazarin, C. B. B., Madsen, L., 2019. Interplay between food and gut microbiota in health and disease. Food Res. Int. 115: 23-31. doi: 10.1016/j.foodres.2018.07.043        [ Links ]

De Blas, J.C., Chamorro, S., García-Alonso, J., García-Rebollar, P., García-Ruiz, A.I., Gómez-Conde, M.S., Menoyo, D., Nicodemus, N., Romero, C., Carabaño, R., 2012. Nutritional digestive disturbances in weaner rabbits. Anim. Feed Sci. Tech. 173: 102-110.         [ Links ]

De Bruno, A., Romeo, R., Fedele, F.L., Sicari, A., Piscopo, A., Poiana, M., 2018. Antioxidant activity shown by olive pomace extracts. J. Environ. Sci. Health Part B. 53: 526-533.         [ Links ]

De Cara A., Saladana B., Vazquez P., Ray, A., 2023. Dietary protected sodium butyrate and/or olive leaf and grape-based by-product supplementation modifies productive performance, antioxidant status and meat quality in broilers. Antioxidants. 12(1): 201.         [ Links ]

Dedousi, A., Kritsa, M.Z., Dukic Stojcic, M., Sfetsas, T., Sentas, A., Sossidou, E., 2022. Production performance, egg quality characteristics, fatty acid profile and health lipid indices of produced eggs, blood biochemical parameters and welfare indicators of laying hens fed dried olive pulp. Sustainability. 14(6): 3157.         [ Links ]

Deiana, M., Serra, G., Corona, G., 2018. Modulation of intestinal epithelium homeostasis by extra virgin olive oil phenolic compounds. Food Funct. 9: 4085-4099.         [ Links ]

Delzenne, N. M., Neyrinck, A. M., Cani, P. D., 2011. Modulation of the gut microbiota by nutrients with prebiotic properties: Consequences for host health in the context of obesity and metabolic syndrome. Microb. Cell Fact. 10(1): S10. doi: 10.1186/1475-2859-10-S1-S10        [ Links ]

De Marco, E., Savarese, M., Paduano, A., Sacchi, R., 2007. Characterization and fractionation of phenolic compounds extracted from olive oil mill wastewaters. Food Chem. 104(2): 858-867.         [ Links ]

Di Nunzio, M., Picone, G., Pasini, F., Chiarello, E., Caboni, M.F., Capozzi, F., Gianotti, A., Bordoni, A., 2019. Olive oil by-product as functional ingredient in bakery products. Influence of processing and evaluation of biological effects. Food Res. Int. 19: 131, 108940.         [ Links ]

Donohue, M., Cunningham, D., 2009. Effects of grain and oilseed prices on the costs of US poultry production. J Appl Poult Res. 18: 325-337. doi: 10.3382/japr.2008-00134        [ Links ]

Dub, A.M., Dugani, A.M., 2013. Antithrombotic effect of repeated doses of the ethanolic extract of local olive (Olea europaea L.) leaves in rabbits. Libyan J. Med. 8: 1-6.         [ Links ]

EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA) 2011. "Scientific opinion on the substantiation of health claims related to polyphenols in olive and protection of LDL particles from oxidative damage (ID 1333, 1638, 1639, 1696, 2865), maintenance of normal blood HDL cholesterol concentrations (ID 1639), maintenance of normal blood pressure (ID 3781), "anti-inflammatory properties" (ID 1882), "contributes to the upper respiratory tract health" (ID 3468), "can help to maintain a normal function of gastrointestinal tract" (3779), and "contributes to body defences against external agents" (ID 3467) pursuant to article 13(1) of regulation (EC) no 1924/2006," EFSA Journal 9: 2033-2058.         [ Links ]

Elazab, M.A., Khalifah, A.M., Elokil, A.A., Elkomy, A.E., Rabie, M.M., Mansour, A.T., Morshedy, S.A., 2022. Effect of dietary rosemary and ginger essential oils on the growth performance, feed utilization, meat nutritive value, blood biochemicals, and redox status of growing NZW rabbits. Animals. 12: 375.         [ Links ]

European Food Safety Authority, 2008. Scientific Opinion of the Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) on functional groups of additives as described in Annex 1 of Regulation (EC) No 1831/2003. EFSA J. 920, 1-19.         [ Links ]

European Union Commission, 2020. EC Farm to Fork Strategy: For a Fair, Healthy and Environmentally-friendly Food System. Communication from the EU Commission, COM, 2020.         [ Links ]

European Union, 2012. Commission Regulation (EU) No 432/2012 of 16 May 2012 establishing a list of permitted health claims made on foods, other than those referring to the reduction of disease risk and to children's development and health. Off. J. Eur. Union, L136: 1-40.         [ Links ]

Evans, M.D., Griffiths, H.R., Lunec, J., 1997. Reactive oxygen species and their cytotoxic mechanisms. Adv. Mol. Cell Biol. 20: 25-73.         [ Links ]

Falcão-e-Cunha, L., Castro-Solla, L., Maertens, L., Marounek, M., Pinheiro, V., Freire, J., Mourão, J.L., 2007. Alternatives to antibiotic growth promoters in rabbit feeding: A review. World Rabbit. Sci. 15: 127-140.         [ Links ]

Farràs M., Martinez-Gili L., Portune K., Arranz S., Frost G., Tondo M., Blanco-Vaca, F., 2020. Modulation of the gut microbiota by olive oil phenolic compounds: Implications for lipid metabolism, immune system, and obesity. Nutrients. 12(8): 2200.         [ Links ]

Fasolato, L., Cardazzo, B., Balzan, S., Carraro, L., Taticchi, A., Montemurro, F., Novelli, E., 2015. Minimum bactericidal concentration of phenols extracted from oil vegetation water on spoilers, starters, and food-borne bacteria. Ital. J. Food Saf. 4: 75-77.         [ Links ]

Faustman, C., Sun, Q., Mancini, R., Suman, S.P., 2010. Myoglobin and lipid oxidation interactions: Mechanistic bases and control. Meat Sci. 86: 86-94.         [ Links ]

FDA News Release, 2004. FDA allows qualified health claim to decrease risk of coronary heart disease. Available at: http://www.fda.gov/newsevents/newsroom/pressannouncements/2004/ucm108368.html.         [ Links ]

Ferrer, P., 2021. Valorization of Mediterranean Agro-Industrial By-Products in Pig Production as Feed and Anaerobic Co-Digestion of Slurry. Ph.D. thesis. València: Technical University of Valencia.         [ Links ]

Ferrer, P., Calvet, S., García-Rebollar, P., de Blas, C., Jiménez-Belenguer, A.I., Hernández, P., Piquer, O., Cerisuelo, A., 2020. Partially defatted olive cake in finishing pig diets: Implications on performance, faecal microbiota, carcass quality, slurry composition and gas emission. Animal. 14(2): 426-434.         [ Links ]

Finicelli M., Di Salle A., Galderisi U., Peluso, G., 2022. The Mediterranean diet: An update of the clinical trials. Nutrients. 14(14): 2956.         [ Links ]

Finzi A., Morera, P., Kuzminsky, G., 2010. Sperm abnormalities as possible indicators of rabbit chronic heat stress. World Rabbit Sci. 4:157-161.         [ Links ]

Forman, H.J., Zhang, H., 2021. Targeting oxidative stress in disease: Promise and limitations of antioxidant therapy. Nat. Rev. Drug Discov. 20: 689-709.         [ Links ]

Foti, P., Pino, A., Romeo, F.V., Vaccalluzzo A., Caggia C., Randazzo C.L., 2022. Olive pomace and pâté olive cake as suitable ingredients for food and feed. Microorganisms. 10: 237.         [ Links ]

Foti, P., Romeo, F.V., Russo, N., Pino, A., Vaccalluzzo, A., Caggia, C., Randazzo, C.L., 2021. Olive mill wastewater as renewable raw materials to generate high added-value ingredients for agro-food industries. Appl. Sci. 11: 7511.         [ Links ]

Frankel, E., Bakhouche, A., Lozano-Sánchez, J., Segura-Carretero, A., Fernández-Gutiérrez, A., 2013. Literature review on production process to obtain extra virgin olive oil enriched in bioactive compounds. Potential use of byproducts as alternative sources of polyphenols. J Agric Food Chem. 61: 5179-5188.         [ Links ]

Furneri, P.M., Marino, A., Saija, A., Uccella, N., Bisignano, G., 2002. In vitro antimycoplasmal activity of oleuropein. Int. J. Antimicrob. Agents. 20: 293-296.         [ Links ]

Furneri, P.M., Piperno, A., Sajia, A., Bisignano, G., 2004. Antimycoplasmal activity of hydroxytyrosol. Antimicrob. Agents Chemother. 48: 4892-4894.         [ Links ]

Gaforio, J.J., Visioli, F., Alarcon-de-la-Lastra, C., Castaner, O., Delgado-Rodriguez, M., Fito, M., et al., 2019. Virgin olive oil and health: summary of the III international conference on virgin olive oil and health consensus report, JAEN (Spain) 2018. Nutrients. 11(9): 2039.         [ Links ]

Galanakis, C.M., 2018. Phenols recovered from olive mill wastewater as additives in meat products. Trends Food Sci. Technol. 79: 98-105.         [ Links ]

Gerasopoulos, K., Stagos D., Kokkas, S., Petrotos, K., Kantas, D., Goulas, P., Kouretas, D., 2015a. Feed supplemented with byproducts from olive oil mill wastewater processing increases antioxidant capacity in broiler chickens. Food Chem. Toxicol. 82: 42-49.         [ Links ]

Gerasopoulos, K., Stagos, D., Petrotos, K., Kokkas, S., Kantas, D., Goulas, P., Kouretas, D., 2015b. Feed supplemented with polyphenolic by-product from olive mill wastewater processing improves the redox status in blood and tissues of piglets. Food Chem. Toxicol. 86: 319-327.         [ Links ]

Ghanbari, R., Anwar, F., Alkharfy, K.M., Gilani, A-H., Saari, N., 2012. Valuable nutrients and functional bioactives in different parts of olive (Olea europaea L.): A review. Int J Mol Sci. 13: 3291-3340.         [ Links ]

Gidenne, T., Jehl, N., Perez, J. M., Arveux, P., Bourdillon, A., Mousset, J. L., Duperray, J., Stephan, S., Lamboley, B., 2005. Effect of cereal sources and processing in diets for the growing rabbits. II effects on performances and mortality by enteropathy. Anim. Res. 54: 65-72.         [ Links ]

Gray, J. I., Gomaa, E. A., Buckley, D. J., 1996. Oxidative quality and shelf life of meats. Meat Sci. 43: S111-S123.         [ Links ]

Grigoras C. G., Destandau, E., Laz_ar, G., Elfakir, C., 2012. Bioactive compounds extraction from pomace of four apple varieties. J. Eng. Stud. Res. 18(1): 96e103.         [ Links ]

Gurr, M. I., Borlak, N., Ganatra, S., 1989. Dietary fat and plasma lipids. Nutr. Res. Rev. 2: 63-86.         [ Links ]

Hayes, J.E., Stepanyan, V., Allen, P., O'Grady, M.N., O'Brien, N.M., Kerry, J.P., 2009. The effect of lutein, sesamol, ellagic acid, and olive leaf extract on lipid oxidation and oxymyoglobin oxidation in bovine and porcine muscle model systems. Meat Sci. 83: 201-208.         [ Links ]

Hukerdi, Y.J., Nasri, M.H.F., Rashidi, L., Ganjkhanlou, M., Emami, A., 2019. Effects of dietary olive leaves on performance, carcass traits, meat stability and antioxidant status of fattening Mahabadi male kids. Meat Sci. 153: 2-8.         [ Links ]

Ibrahim, D., Moustafa, A., Shahin, S., Sherief, W., Farag, M., Nassan, M., 2021. Impact of fermented or enzymatically-fermented dried olive pomace on growth, expression of digestive enzymes and glucose transporters genes, oxidative stability of frozen meat and economic efficiency of broiler chickens. Front. Vet. Sci. 8: 442.         [ Links ]

International Olive Council, 2017. Accessed Mar., 2022.         [ Links ]

Joven, M., Pintos, E., Latorre, M.A., Suárez-Belloch, J., Guada, J.A., Fondevila, M., 2014. Effect of replacing barley by increasing levels of olive cake in the diet of finishing pigs: Growth performances, digestibility, carcass, meat, and fat quality. Anim. Feed Sci. Tech. 197: 185-193.         [ Links ]

Kadi, S. A., Belaidi-Gater, N., Chebat, F., 2004. Inclusion of crude olive cake in growing rabbit diets: Effect on growth and slaughter yield. Proc. 8th World Rabbit Congress, September 7-10, 2004, Puebla, Mexico.         [ Links ]

Kalogeropoulos, N., Tsimidou, M.Z., 2014. Antioxidants in Greek virgin olive oils. Antioxidants. 3: 387-413.         [ Links ]

Kapellakis, I.E., Paranychianakis, N.V., Tsagarakis, K.P., Angelakis, A.N., 2012. Treatment of olive mill wastewater with constructed wetlands. Water 4: 260-271        [ Links ]

Kasapidou, E., Sossidou, E., Paraskevi, M., 2015. Fruit and vegetable co-products as functional feed ingredients in farm animal nutrition for improved product quality. Agriculture. 5(4): 1020-1034.         [ Links ]

Kermauner, A., Laurenčič, A., 2008. Supplementation of rabbit diet with chestnut wood extract: Effect on in vitro gas production from two sources of protein. In: Proceedings of the 9th World Rabbit Congress, Verona, June 10-13. pp 689-693.         [ Links ]

Khalil, S., Awad, A., Elewa, Y., 2013. Antidotal impact of extra virgin olive oil against genotoxicity, cytotoxicity and immunotoxicity induced by hexavalent chromium in rat. Int. J. Vet. Sci. Med. (IJVSM). 1: 65-73.         [ Links ]

Khwaldia, K., Attour, N., Matthes, J., Beck, L., Schmid, M., 2022. Olive byproducts and their bioactive compounds as a valuable source for food packaging applications. Compr. Rev. Food Sci. Food Saf. 21: 1218-1253.         [ Links ]

King, A.J., Griffin, J.K., Roslan, F., 2014. In vivo and in vitro addition of dried olive extract in poultry. J. Agric. Food Chem. 62: 7915-7919.         [ Links ]

Koné, A.P., Desjardins, Y., Gosselin, A., Cinq-Mars, D., Guay, F., Saucier, L., 2019. Plant extracts and essential oil product as feed additives to control rabbit meat microbial quality. Meat Sci. 150: 111-121.         [ Links ]

Kowalska, H., Czajkowska, K., Cichowska, J, Lenart, A., 2017. What's new in biopotential of fruit and vegetable by-products applied in the food processing industry. Trends Food Sci Tech. 67: 150-159.         [ Links ]

Lipinski, K., Mazur, M., Antoszkiewicz, Z., Purwin, C., 2017. Polyphenols in monogastric nutrition. A review. Ann. Anim. Sci. 17: 41-58.         [ Links ]

Luciano, G., Pauselli, M., Servili, M., Mourvaki, E., Serra, A., Monahan, F.J., Lanza, M., Priolo, A., Zinnai, A., Mele M., 2013. Dietary olive cake reduces the oxidation of lipids, including cholesterol, in lamb meat enriched in polyunsaturated fatty acids. Meat Sci. 93: 703-714.         [ Links ]

Luciano, A., Tretola, M., Ottoboni, M., Baldi, A., Cattaneo, D., Pinotti, L., 2020. Potentials and challenges of former food products (food leftovers) as alternative feed ingredients. Animals. 10: 125.         [ Links ]

Luisi, M.L.E., Lucarini, L., Biffi, B., Rafanelli, E., Pietramellara, G., Durante, M., Vidali, S., Provensi, G., Madiai, S., Gheri, C.F., Masini, E., Ceccherini, M.T., 2019. Effect of Mediterranean Diet enriched in high quality extra virgin olive oil on oxidative stress, inflammation and gut microbiota in obese and normal weight adult subjects. Front. Pharmacol. 10: 1366.         [ Links ]

Lykkesfeldt, J., Svendsen, O., 2007. Oxidants and antioxidants in disease: Oxidative stress in farm animals. Vet. J. 173(3): 502-511.         [ Links ]

Macari M. Fisiologia aviária aplicada a frangos de corte. Jaboticabal: Funep/Unesp, 2008.         [ Links ]

Madhupriya, V., Shamsudeen, P., Manohar, G.R., Senthilkumar, S., Soundarapandiyan, V., Moorthy, M., 2018. Phyto feed additives in poultry nutrition: A review. Int. J. Sci. Environ. Technol. 7: 815-822.         [ Links ]

Mancini, S., Secci, G., Preziuso, G., Parisi, G., Paci, G., 2018. Ginger (Zingiber officinale Roscoe) powder as dietary supplementation in rabbits: Life performances, carcass characteristics, and meat quality. Ital. J. Anim. Sci. 17: 867-872.         [ Links ]

Marai, I., Habeeb, A., Gad, A., 2002. Rabbits' productive, reproductive and physiological performance traits as affected by heat stress: A review. Livest Prod Sci. 78: 71-90.         [ Links ]

Markin, D., Duek, L., Berdicevsky, I., 2003. In vitro antimicrobial activity of olive leaves. Mycoses. 46: 132-133.         [ Links ]

Marlier, D., Dewrée, R., Lassence, C., Licois, D., Mainil, J., Coudert, P., Meulemans, L., Ducatelle, R., Vindevogel, H., 2006. Infectious agents associated with epizootic rabbit enteropathy: Isolation and attempt store produce the syndrome. Vet. J. 172: 493-500.         [ Links ]

Martin-Garcia, A.I., Yanez-Ruiz, D.R., Moumen, A., Molina-Alcaide, E., 2003. Chemical composition and nitrogen availability for goats and sheep of some olive by-products. Small Rumin. Res. 49: 61-74.         [ Links ]

Martín-Peláez, S., Mosele, J. I., Pizarro, N., Farràs, M., de la Torre, R., Subirana, I., 2017. Effect of virgin olive oil and thyme phenolic compounds on blood lipid profile: implications of human gut microbiota. Eur. J. Nutr. 56: 119-131. doi: 10.1007/s00394-015-1063-2        [ Links ]

Mattioli, S., Machado Duarte, J. M., Castellini, C., D'Amato, R., Regni, L., Proietti, P., Businelli, D., Cotozzolo, E., Rodrigues, M., Dal Bosco, A., 2018. Use of olive leaves (whether or not fortified with sodium selenate) in rabbit feeding: Effect on performance, carcass and meat characteristics, and estimated indexes of fatty acid metabolism. Meat Sci. 143: 230-236.         [ Links ]

Memon, M.A., 2010. Integrated solid waste management based on the 3R approach. J. Mater. Cycles Waste Manag. 12: 30-40.         [ Links ]

Meziane, S., 2011. Drying kinetics of olive pomace in a fluidized bed dryer. Energy Conv. Mgmt. 52(3): 1644-1649.         [ Links ]

Micol, V., Caturla, N., Perez-Fons, L., Mas, V., Perez, L., Estepa, A., 2005. The olive leaf extract exhibits antiviral activity against viral haemorrhagic septicaemia rhabdovirus (VHSV). Antiviral Res. 66: 129-136.         [ Links ]

Mirabella, N., Castellani, V., Sala, S., 2014. Current options for the valorization of food manufacturing waste: A review. J. Clean. Prod. 65: 28-41.         [ Links ]

Molina-Alcaide, E., Yáñez-Ruiz, D.R., 2008. Potential use of olive by-products in ruminant feeding: A review. Anim Feed Sci Technol. 147: 247-264. doi: 10.1016/j.anifeedsci.2007.09.021        [ Links ]

Morshedy, S.A., Abdelmodather, A.M., Basyony, M.A., Zahran, S.A., Hassa, M.A., 2021. Effects of rocket seed oil, wheat germ oil, and their mixture on growth performance, feed utilization, digestibility, redox status, and meat fatty acid profile of growing rabbits. Agriculture. 11: 662.         [ Links ]

Nazzaro, F., Fratianni, F., Cozzolino, R., Martignetti, A., Malorni, L., De Feo, V., Cruz, A.G., d'Acierno, A., 2019. Antibacterial activity of three extra virgin olive oils of the Campania region, Southern Italy, related to their polyphenol content and composition. Microorganisms. 7: 321.         [ Links ]

Nunes, M.A., Pimentel, F.B., Costa, A.S., Alves, R.C., Oliveira, M.B.P., 2016. Olive byproducts for functional and food applications: Challenging opportunities to face environmental constraints. Innov Food Sci Emerg Technol. 35: 139-148.         [ Links ]

Nychas, G.J.E., Tassou, C., Board, R.G., 1990. Phenolic extract from olives: Inhibition of Staphylococcus aureus s-6'. Lett. Appl. Microbiol. 10: 217-220.         [ Links ]

Obied, H.K., Prenzler, P., Konczak, I., Rehman, A.-U., Robards, K., 2008a. Chemistry and bioactivity of olive biophenols in some antioxidant and antiproliferative in vitro bioassays. Chem. Res. Toxicol. 22: 227-234.         [ Links ]

Obied, H.K., Prenzler, P., Robards, K., 2008b. Potent antioxidant biophenols from olive mill waste. Food Chem. 111: 171 -178.         [ Links ]

Oluwafemi, R.A., Olawale, A.I., Alagbe, J.O., 2020. Recent trends in the utilization of medicinal plants as growth promoters in poultry nutrition: A review. Agric. Vet. Sci. 4: 5-11.         [ Links ]

Paixao, S.M., Anselmo, A.M., 2002. Effect of olive mill wastewaters on the oxygen consumption by activated sludge microorganisms: An acute toxicity test method. J. Appl. Toxicol. 22: 173-176.         [ Links ]

Papadomichelakis, G., Pappas, A.C., Tsiplakou, E., Symeon, G.K., Sotirakoglou, K., Mpekelis, V., Fegeros, K., Zervas, G., 2019. Effects of dietary dried olive pulp inclusion on growth performance and meat quality of broiler chickens. Livest. Sci. 221: 115-122.         [ Links ]

Pappas, A.C., Tsiplakou, E., Papadomichelakis, G., Mitsiopoulou, C., Sotirakoglou, K., Mpekelis, V., Fegeros Haroutounian, K., Zervas, G., 2019. Effects of olive pulp addition to broiler diets on performance, selected biochemical parameters and antioxidant enzymes. J. Hell. Vet. Med. Soc. 70: 1687-1696.         [ Links ]

Paraskeva, P., Diamadopoulos, E., 2006. Technologies for olive mill wastewater (OMW) treatment: a review. J. Chem. Technol. Biotechnol. 81: 475e1485.         [ Links ]

Pfaltzgraff, L.A., Cooper, E.C., Budarin, V., Clark, J.H., 2013. Food waste biomass: A resource for high-value chemicals. Green Chem. 15: 307-314.         [ Links ]

Pinotti, L., Manoni, M., Fumagalli, F., Rovere, N., Luciano, A., Ottoboni, M., Ferrari, L., Cheli, F., Djuragic, O., 2020. Reduce, reuse, recycle for food waste: A second life for fresh-cut leafy salad crops in animal diets. Animals. 10: 1082.         [ Links ]

Poorghasemi, M., Seidavi, A., Qotbi, A.A.A., Chambers, J.R., Laudadio, V., Tufarelli, V., 2015. Effect of dietary fat source on humoral immunity response of broiler chickens. Eur Poult Sci. 79: 1-8.         [ Links ]

Poorghasemi, M., Seidavi, A., Qotbi, A.A.A., Laudadio, V., Tufarelli, V., 2013. Influence of dietary fat source on growth performance responses and carcass traits of broiler chicks. Asian-Australasian J Anim Sci. 26: 705-710.         [ Links ]

Puvaca, N., Cabarkapa, I., Bursic, V., Petrovic, A., Acimovic, M., 2018. Antimicrobial, antioxidant and acaricidal properties of tea tree (Melaleuca alternifolia). J. Agron. Technol. Eng. Manag. 1: 29-38.         [ Links ]

Rey, A.I., de-Cara, A., Segura, J.F., Martí, P., Hechavarría, T., Calvo, L., 2020. Dietary oleuropein extract supplementation and their combination with α-tocopheryl acetate and selenium modifies free fatty acid profile and improves stability of pork. J. Sci. Food Agric. 101: 2337-2344.         [ Links ]

Rodis, P.S., Karathanos, V.T., Mantzavinou, A., 2002. Partitioning of olive oil antioxidants between oil and water phases. J. Agric. Food Chem. 50: 596-601.         [ Links ]

Rodríguez, G., Lama, A., Rodríguez, R., Jiménez, A., Guillén, R., Fernández-Bolaños, J., 2008. Olive stone an attractive source of bioactive and valuable compounds. Bioresour. Technol. 99: 5261-5269.         [ Links ]

Roila, R., Valiani, A., Ranucci, D., Ortenzi, R., Servili, M., Veneziani, G., Branciari, R., 2019. Antimicrobial efficacy of a polyphenolic extract from olive oil by-product against "Fior di latte" cheese spoilage bacteria. Int. J. Food Microbiol. 295: 49-53.         [ Links ]

Romeo, F.V., Granuzzo, G., Foti, P., Ballistreri, G., Caggia, C., Rapisarda, P., 2021. Microbial application to improve olive mill wastewater phenolic extracts. Molecules. 26: 1944.         [ Links ]

Roselló-Soto, E., Koubaa, M., Moubarik, A., Lopes, R.P., Saraiva, J. A., Boussetta, N., Grimi N., Barba, F.J., 2015. Emerging opportunities for the effective valorization of wastes and byproducts generated during olive oil production process: Non-conventional methods for the recovery of high-added value compounds. Trends Food Sci Tech. 45(2): 296-310.         [ Links ]

Rubió, L., Macià, A., Castell-Auví, A., Pinent, M., Blay, M.T., Ardévol, A., Romero, M.P., Motilva, M.J., 2014. Effect of the co-occurring olive oil and thyme extracts on the phenolic bioaccessibility and bioavailability assessed by in vitro digestion and cell models. Food Chem. 149: 277-284.         [ Links ]

Sagar, N.A., Pareek, S., Sharma, S., Yahia, E.M., Lobo, M.G., 2018. Fruit and vegetable waste: Bioactive compounds, their extraction, and possible utilization. Compr. Rev. Food Sci. Food Saf. 17: 512-531.         [ Links ]

Sakai, S.-I., Yoshida, H., Hirai, Y., Asari, M., Takigami, H., Takahashi, S., Tomoda, K., Peeler, M.V., Wejchert, J., Schmid-Unterseh, T., et al., 2011. International comparative study of 3R and waste management policy developments. J. Mater. Cycles Waste Manag. 13: 86-102.         [ Links ]

Salomone, R., Ioppolo, G., 2012. Environmental Impacts of olive oil production: A life cycle assessment case study in the province of Messina (Sicily). J. Clean. Prod. 28: 88-100.         [ Links ]

Sánchez de Medina, V., Priego-Capote, F., Luque de Castro, M.D., 2012. Characterization of refined edible oils enriched with phenolic extracts from olive leaves and pomace. J. Agric. Food Chem. 60: 5866-5873.         [ Links ]

Santana-Méridas, O., González-Coloma, A., Sánchez-Vioque, R., 2012. Agricultural residues as a source of bioactive natural products. Phytochem. Rev. 11: 447-466.         [ Links ]

Sanz, M., Lopez-Bote, C.J., Menoyo, D., Bautista, J.M., 2000. Abdominal fat deposition and fatty acid synthesis are lower and ß-oxidation is higher in broiler chickens fed diets containing unsaturated rather than saturated fat. J. Nutr. 130: 3034-3037.         [ Links ]

Sarapis, K., George, E.S., Marx, W., Mayr, H.L., Willcox, J., Esmaili, T., Powell, K.L., Folasire, O.S., Lohning, A.E., Garg, M., Thomas C.J., Itsiopoulos C., Moschonis G., 2022. Extra virgin olive oil high in polyphenols improves antioxidant status in adults: A double-blind, randomized, controlled, cross-over study (OLIVAUS). Eur. J. Nutr. 61: 1073-1086.         [ Links ]

Savournin, C., Baghdikian, B., Elias, R., Dargouth-Kesraoui, F., Boukef, K., Balansard, G., 2001. Rapid high-performance liquid chromatography analysis for the quantitative determination of oleuropein in Olea europaea leaves. J. Agric. Food Chem. 49: 618-621.         [ Links ]

Sayehban, P., Seidavi, A., Dadashbeiki, M., Ghorbani, A., Araújo, W.A.G., Albino, L.F.T., 2015. Effects of different dietary levels of two types of olive pulp and exogenous enzyme supplementation on the gastrointestinal tract size, immunology and hematology of broilers. Braz J Poultry Sci. 17: 73-85.         [ Links ]

Selim, S., Albqmi, M., Al-Sanea, M.M., Alnusaire, T.S., Almuhayawi, M.S., AbdElgawad, H., Al Jaouni, S.K., Elkelish, A., Hussein, S., Warrad, M., El-Saadony M.T., 2022. Valorizing the usage of olive leaves, bioactive compounds, biological activities, and food applications: A comprehensive review. Front. Nutr. 9: 1008349.         [ Links ]

Simitzis, P.E., Deligeorgis, S.G., 2018. Agroindustrial by-products and animal products: A great alternative for improving food-quality characteristics and preserving human health. In: Food Quality: Balancing Health and Disease. Handbook of Food Bioengineering, 1st ed., Holban, A.M., Grumezescu, A.M., Eds., Academic Press Elsevier: London, UK, Volume 13, pp. 253-290.         [ Links ]

Soultos, N., Tzikas, Z., Christaki, E., Papageorgiou, K., Steris, V., 2009. The effect of dietary oregano essential oil on microbial growth of rabbit carcasses during refrigerated storage. Meat Sci. 81: 474-478.         [ Links ]

Sreelatha, S., Padma, P.R., 2009. Antioxidant activity and total phenolic content of Moringa oleifera leaves in two stages of maturity. Plant Foods Hum. Nutr. 64: 303-311.         [ Links ]

Stempfle, S., Carlucci, D., de Gennaro, B.C., Roselli, L., Giannoccaro, G., 2021. Available pathways for operationalizing circular economy into the olive oil supply chain: Mapping evidence from a scoping literature review. Sustainability. 13: 9789.         [ Links ]

Sudjana, A.N., D'Orazio, C., Ryan, V., Rasool, N., Ng, J., Islam, N., Riley, T.V., and Hammer, K.A., 2009. Antimicrobial activity of commercial Olea europaea (olive) leaf extract. Int J Antimicrob. Agents. 33: 461-463.         [ Links ]

Tan, H.W., Tuck, K.L., Stupans, I., Hayball, P.J., 2003. Simultaneous determination of oleuropein and hydroxytyrosol in rat plasma using liquid chromatography with fluorescence detection. J Chromatog. B. 785: 187-191.         [ Links ]

Terramoccia, S., Bartocci, S., Taticchi, V., Di Giovanni, S., Pauselli, M., Mourvaki, E., Urbani, S., Servili, M., 2013. Use of dried stoned olive pomace in the feeding of lactating buffaloes: Effect on the quantity and quality of the milk produced. Asian-Australas. J. Anim. Sci. 26: 971 -980.         [ Links ]

Trebusak, T., Levant, A., Salobir, J., Pirman, T., 2014. Effect of Ganoderma lucidum (Reishi mushroom) or Olea europaea (olive) leaves on oxidative stability of rabbit meat fortified with n-3 fatty acids. Meat Sci. 96: 1275-1280.         [ Links ]

Tsala, A., Mpekelis, V., Karvelis, G., Tsikakis, P., Goliomytis, M., Simitzis, P., 2019. Effects of dried olive pulp dietary supplementation on quality characteristics and antioxidant capacity of pig meat. Foods. 9(1): 81.         [ Links ]

Tufarelli, V., Colonna, M. A., Losacco, C., Puvaca, N., 2023. Biological health markers associated with oxidative stress in dairy cows during lactation period. Metabolites. 13: 405.         [ Links ]

Tufarelli V., Passantino L., Zupa R., Crupi P., Laudadio, V., 2022a. Suitability of dried olive pulp in slow-growing broilers: Performance, meat quality, oxidation products, and intestinal mucosa features. Poult. Sci. 101(12).         [ Links ]

Tufarelli, V., Tateo, A., Schiavitto, M., Mazzei, D., Calzaretti, G., Laudadio, V., 2022b Evaluating productive performance, meat quality, and oxidation products of Italian white breed rabbits under free-range and cage rearing system. Anim. Biosci. 35: 884-891.         [ Links ]

Tufarelli, V., Laudadio, V., Casalino, E., 2016. An extra-virgin olive oil rich in polyphenolic compounds has antioxidant effects in meat-type broiler chickens. Environ. Sci. Pollut. Res. 23: 6197-6204.         [ Links ]

Tzamaloukas, O., Neofytou, M.C., Simitzis, P.E., 2021. Application of olive by-products in livestock with emphasis on small ruminants: Implications on rumen function, growth performance, milk, and meat quality. Animals. 11: 531.         [ Links ]

Vargas-Bello-Pérez, E., Vera, R.R., Aguilar, C., Lira, R., Peña, I., Fernández, J., 2013. Feeding olive cake to ewes improves fatty acid profile of milk and cheese. Anim. Feed Sci. Technol. 184: 94-99.         [ Links ]

Vastolo, A., Calabro, S., Cutrignelli, M.I., 2022. A review on the use of agro-industrial CO-products in animal diets. Ital. J. Anim. Sci. 21: 577-594.         [ Links ]

Visioli, F., Poli, A., Gall, C., 2002. Antioxidant and other biological activities of phenols from olives and olive oil. Med Res Rev. 22: 65-75.         [ Links ]

Vissers, M.N., Zock, P.L., Roodenburg, A.J.C., Leenen, R., Katan, M.B., 2002. Olive oil phenols are absorbed in humans. J Nutr. 132: 409-417.         [ Links ]

Wahle, K.W., Caruso, D., Ochoa, J.J., Quiles, J.L., 2004. Olive oil and modulation of cell signaling in disease prevention. Lipids. 39: 1223-1231.         [ Links ]

Wenk, C., 2002. Herbs, botanicals, and other related substances. WPSA-Bremen. Germany.         [ Links ]

Wenk, C., 2000. Recent advances in animal feed additives such as metabolic modifiers, antimicrobial agents, probiotics, enzymes, and highly available minerals. Review. Asian-Australas. J. Anim. Sci. 13: 86-95.         [ Links ]

Wickramasuriya, S.S., Park, I., Lee, K., Lee, Y., Kim, W.H., Nam, H., Lillehoj, H.S., 2022. Role of physiology, immunity, microbiota, and infectious diseases in the gut health of poultry. Vaccines. 10: 172.         [ Links ]

Xie, P., Deng, Y., Huang, L., Zhang, C., 2022. Effect of olive leaf (Olea europaea L.) extract addition to broiler diets on the growth performance, breast meat quality, antioxidant capacity, and caecal bacterial populations. Ital. J. Anim. Sci. 21: 1246-1258.         [ Links ]

Younan, G.E., Mohamed, M.S., Morsy, W.A., 2018. Effect of dietary supplementation of olive leaf extract on productive performance, blood parameters, and carcass traits of growing rabbits. Egypt. J. Nutr. Feeds. 22(1): 173-182.         [ Links ]

Zhang, W., Xiao, S., Ahn, D.U., 2013b. Protein oxidation: Basic principles and implications for meat quality. Crit. Rev. Food Sci. Nutr. 53(11): 1191-1201.         [ Links ]

Zhang, Z.F., Zhou, T.X., Kim, I.H., 2013a. Effects of dietary olive oil on growth performance, carcass parameters, serum characteristics, and fatty acid composition of breast and drumstick meat in broilers. Asian-Australas. J. Anim. Sci. 26: 416-422.         [ Links ]

Zsédely, E., Tóth, T., Eiben, C. S., Virág, G. Y., Fábián, J., & Schmidt, J., 2008. Effect of dietary vegetable oil (sunflower, linseed) and vitamin E supplementation on the fatty acid composition, oxidative stability, and quality of rabbit meat. 9th World Rabbit Congress. Verona, Italy. pp. 1473-1478.         [ Links ]

 

 

Submitted 18 May September 2023
Accepted 22 August 2023
Published 16 November 2023

 

 

# Corresponding author: vincenzo.tufarelli@uniba.it