Diet supplemented with olive cake as a model of circular economy: Metabolic and endocrine responses of beef cattle

Introduction: Integrating by-products into livestock diet represents a great opportunity for implementing the concept of circular economy while reducing feed costs. Olive cake (OC) is considered an agro-industrial waste, but the high content of valuable metabolites makes it a promising feed integration. Therefore, this study investigated the effect of OC integration in beef cattle diet on different blood parameters.

Methods: Forty-eight young growing fattening Limousines-−24 bulls (body weight 350 ± 15 kg) and 24 heifers (280 ± 10 kg)—, aged 240 ± 20 days, were randomly allocated to 1 of 3 dietary treatments: concentrate at 0% (Control group: CTR), 10% (Low-olive cake group: L-OC), or 15% (High-olive cake group: H-OC) of OC inclusion. Blood samples and body weights were collected before administrating the supplemented diet (0 d), at the end of the stocker growing phase (56 d), and at the end of the fattening (147 d). After being slaughtered, animal carcasses were weighted. A linear regression model was fitted for each blood parameter with the 0 d as covariate and diet, time, sex, diet × time, and diet × sex as fixed effects.

Results: In males, body weight was highest in CTR, but carcass weight was similar in all the groups. All the blood parameters were within physiological ranges, independently from the animal diet. CTR group showed the highest alanine aminotransferase (ALT, P = 0.0027) and creatine kinase (P = 0.0119), whereas total bilirubin (P = 0.0023) was higher in H-OC than in CTR. Moreover, ALT was highest in CTR at 56 d, becoming similar in all the groups at 147 d (P = 0.0280). Instead, the increase observed in total cholesterol from 56 to 147 d was lower in H-OC compared with CTR and L-OC (P = 0.0451). A significant effect of diet × sex interaction was observed on triglycerides, urea, liver enzymes, and insulin. These data support the OC inclusion of up to 15% of the concentrate with no detrimental effect on beef cattle metabolic status.

Discussion: In conclusion, OC can be considered as a component in beef diet giving an opportunity to improve agriculture sustainability.

1. Introduction

In the Mediterranean area, the production of olive oil is significant; indeed, it contributes to 76% of the total production of olive oil, with Spain, Italy, and Greece being the main producers (Berbel and Posadillo, 2018). It is estimated that in European countries about 11.8 million tons of biomass are produced from the olive tree pruning process (Berbel and Posadillo, 2018) and since the production of olive oil is an important source of energy and water consumption, the increase in the olive oil industry has led to an inevitable rising of environmental impact. Besides the considerable emissions, it generates a relevant amount of waste that must be disposed (Salomone and Ioppolo, 2012). The main by-products generated from olive oil process are olive mill wastewater and olive cake (Foti et al., 2022). However, because of its properties, processing waste like olive cake (OC) could be used in different sectors, such as energy generation, food products, pharmaceutical industry, and animal feed (Espeso et al., 2021). In particular, the use of olive cake as animal feed is an interesting and sustainable alternative to its disposal, because it may decrease the costs associated with animal feeding, valorizing a waste biomass and at the same time improving the quality of the products (Keleş, 2015; Castellani et al., 2017; Vastolo et al., 2019). In fact, the spread of its use as integrator in animal feeding is mainly related to the presence of substances with antioxidant and radical scavenging activity, and to its richness in monounsaturated fatty acids (MUFAs) (Ghanbari et al., 2012). There are many studies on the incorporation of this by-product in livestock diet, for example in broilers (Al-Harthi, 2016), pigs (Joven et al., 2014; Liotta et al., 2019), goats (Alkhtib et al., 2021; El Otmani et al., 2021), sheep Chiofalo et al., 2004; Vargas-Bello-Pérez et al., 2013, dairy cattle (Zilio et al., 2015; Chiofalo B. et al., 2020; Neofytou et al., 2020), and beef cattle (Estaún et al., 2014; Branciari et al., 2015; Chiofalo V. et al., 2020).

According to Estaún et al. (2014), the addition of pitted and dehydrated olive cake at rate of 10 or 20% in the concentrate led to no differences in terms of either animal performance for the whole growth period or rumen fermentation parameters in Frisian steers from 100 to 450 kg of body weight. In addition, lack of differences found at rumen fermentation level (pH and volatile fatty acids) suggests that olive cake supplementation (10 or 20% in the concentrate) does not negatively affect the activity of microbial populations, at least in Frisian steers. From these outcomes it is reasonable to suppose that including pitted and dehydrated olive cake in the diet of beef cattle should not affect animal performance and at the same time might be suitable to implement a supply chain system at the economic and sustainable level.

However, to the best of our knowledge, a few studies have been carried out to investigate the effect of olive cake on the metabolic and endocrine traits of beef cattle. Hence, the aim of this study was to determine if the changes in plasma triglycerides (TG), total cholesterol (TCHOL), glucose (GLU), total bilirubin (TBIL), aspartate aminotransferase (AST), alanine aminotransferase (ALT), creatine kinase (CK), lactate dehydrogenase (LDH), and urea in heifers and bulls are substantial enough to indicate the need to establish specific reference intervals also for young growing fattening Limousine bulls and heifers. The direction and magnitude of the changes in these parameters could be used as diagnostic tools for the detection and monitoring of metabolic and endocrine traits that could arise during growth in this species fed concentrate with different percentages of olive cake inclusion.

2. Materials and methods

The experimental protocol was approved by the Ethical Committee of the Department of Veterinary Science, University of Messina, Italy (code 041/2020). The research complied with guidelines of Good Clinical Practices (The European Agency for the Evaluation of Medicinal Products, 2000) and the Italian and European regulations on animal welfare (Directive 2010/63/EU) (Council of the European Union, 2010).

2.1. Animal management and experimental design

The experiment was carried out using a total of 48 Limousine young growing fattening animals (24 bulls and 24 heifers), aged 250 ± 20 days at the time of the first sampling. The initial body weight (BW) was on average 350 ± 15 kg for bulls and 280 ± 10 kg for heifers. This breed was chosen because it is the most diffused in Sicily for breed production. All animals were housed in the same pen of a semi-open straw-bedded barn located in Santa Croce Camerina (Ragusa, Italy, 36°49′38″N 14°31′26″E). The farm is located within the Hyblean Mediterranean area with an unequally distributed rainfall throughout the year. Annual mean rainfall is about 700 mm. The annual average temperature is 19.58°C (with an average of maximum and minimum temperature of 21 and 17°C, respectively).

Animals were raised according to an approved UE disciplinary called “QS Sicilia,” which allows the inclusion of olive cake in feed for beef cattle not < 10% of the diet, as a strategy for the recovery of agro-industrial by-products.

After a 2-week adaptation period, animals were randomly allocated to one of three dietary treatments according to their BW: inclusion of olive cake at 0% (Control group: CTR), 10% (Low-olive cake group: L-OC), or 15% (High-olive cake group: H-OC) in the concentrate. The compositions of the concentrates and of the OC used for the study are reported in Table 1. All the animals were allowed ad libitum access to straw and water. After adaptation, animals received their concentrate (equal to 2% of their body weight, on average) twice daily (7.00 a.m. and 3.00 p.m.). During the whole experimental period (147 days), none of the animals had health problems. When animals reached the endpoint, they were transported to a licensed slaughterhouse located 20 min (19.2 km) away from the farm. Animals fasted for 12 h before slaughter, which was performed according to EU Regulations. The interval between the first and the last slaughter was 18 days.

TABLE 1

Table 1. Feed and nutrient composition of concentrate with 0% (Control group: CTR), 10% (Low-olive cake group: L-OC), or 15% (High-olive cake group: H-OC) of olive cake (OC) inclusion fed to growing fattening Limousine bulls and heifers.

2.2. Animal measurements in vita and post-mortem

Animals of each pen, before feed distribution, were individually weighed at the beginning of the trial, after 56 days, and at the end of the trial (147 days) using Brecknell PS-2000 Veterinary Floor Scale (capacity: 1,000 kg, readability: 0.5 kg). Individual average daily gain (ADG) was also calculated. At the end of the trial, animals were slaughtered, and after slaughter the hot carcass weight (CW) was recorded, and the dressing percentage was calculated. pH was determined 1 and 24 h after slaughter using a portable pH meter (Hanna Instruments, Woonsocket, RI, USA) and combined glass electrode, inserted ~5 cm into the longissimus thoracis muscle.

2.3. Blood samples collection and analysis

The blood samples were collected at the beginning (day 0, before administrating treated concentrates) and on days 56 and 147 of the trial, in the morning before dispensing the concentrate. Blood was collected from the tail vein by trained veterinarians through venipuncture into 10-mL tubes containing clot activator and separating gel (Terumo Corporation, Tokyo, Japan). Blood samples were centrifuged for 10 min at 2,000 × g; the supernatant serum was collected and stored at −20°C until analyses.

Biochemical lipids (TG, TCHO), liver (TBIL, AST, ALT, LDH), renal (Urea), and muscular (CK), parameters were analyzed by enzymatic colorimetric method, using an automated spectrophotometry (Biotechnical Instrument BP 3500) and reagents of the same commercial house.

Glucose concentration was measured by automated spectrophotometry (Biotecnica Instruments BT 3500) using the colorimetric enzymatic method GOD-POD.

Insulin concentration was analyzed using the Immulite^® two-site chemiluminescent immunometric assay (Maglium 800), with a sensitivity of 0.5 μIU/mL and intra- and inter-assay coefficients of variation equal to 1.56 and 4.07% at insulin concentrations of 16.54 and 45.804 μIU/mL.

2.4. Statistical analysis

Statistical analyses were performed with JMP^®, Version 16 (SAS Institute Inc., Cary, NC). Appropriate descriptive statistics was generated for all the variables. The correlation between all the parameters was expressed using Pearson's coefficient (r).

The blood parameters of interest (Y) were modelized as follows:

$\begin{array}{l}{Y}_{ijk}=m+D+T+S+DT+DS+T0+e\end{array}$

Where m is the mean, D is the diet (CTR, L-OC, or H-OC), T is the time of sampling (day 56 or day 147 of the trial), S is the sex of the animal (male or female), DT is the interaction between the diet and the time of sampling, DS is the interaction between the diet and the sex, T0 is the covariate representing the parameter level at the beginning of the trial (before administering the supplemented concentrated), and e is the random residual. With regard to the performance parameters, only the diet (D), the sex (S), and their interaction (DS) were included as factors. A logarithmic transformation was applied when necessary. When factors or interactions resulted significant, the Tukey-Kramer post-hoc test was used to identify the significantly different levels.

Differences were considered to be statistically significant when P < 0.05.

3. Results

Results of animal performance are reported in Table 2. As expected, differences between heifers and bulls were observed for all the variables with the exception of pH. Even though the diet was significant for dressing (P = 0.0308, with higher values for H-OC than CTR), when we considered heifers only, we observed similar values for all the performance-related variables. Instead, within bulls, we observed that the body weight was higher in the CTR group, but this was not supported by the average daily gain and the carcass weight, which were similar in all the diet groups. Consequently, the dressing resulted higher in H-OC than CTR bulls, with intermediate values for L-OC ones. One factor possibly affecting BW and CW is dry matter intake; several studies on ruminants showed no difference in feed intake between traditional and OC-integrated diets (Yáñez Ruiz et al., 2004; Awawdeh and Obeidat, 2013; Mele et al., 2014; de Evan et al., 2020) but we cannot exclude it, since it was not assessed in the present study, it being carried out in a commercial farm. It is possible that this result might also have been influenced by a difference in the feed intake among the groups; however, it was not possible to assess this data because the trial was performed in a commercial farm.

TABLE 2

Table 2. Means and results of the model for all the measured performance traits: body weight (BW), average daily gain (ADG), carcass weight (CW), dressing, and pH.

In this study, a wide range of blood plasma biomarkers associated with the metabolic variation was chosen. The descriptive statistics of the blood metabolic biomarker concentrations by sex, physiological stage, and diet, as well as the P-values and R² resulted from the model applied to each blood analyte are reported in Table 3. The parameters significantly affected by the diet, the diet × time interaction (indicating a different effect of the diet according to the time of sampling), and the diet × sex interaction (indicating a different effect of the diet on heifers than on bulls) are plotted in Figures 1–3, respectively.

TABLE 3

Table 3. Mean and standard deviation of all the blood analyte measurements, and P-values (in bold when significant) and R² of the applied model.

FIGURE 1

Figure 1. Significant effect of the diet on total bilirubin (A), ALT (B), and creatin kinase [CK, (C)]. The parameters' least square mean (LSM) and standard error are represented for all the groups with different olive cake inclusions, namely control (CTR, 0%), Low-olive cake (L-OC, 10%), and High-olive cake (H-OC, 15%) groups.

Data obtained showed that AST, TBIL, urea, TCHO, TG and insulin significantly increased from 56 to 147 d, whereas ALT and GLU decreased (P < 0.05).

CTR group showed the highest ALT (P = 0.0027) and CK (P = 0.0119), whereas TBIL (P = 0.0023) was higher in H-OC than in CTR group (Figure 1). Moreover, ALT was higher in CTR at 56 d (P = 0.0280), but it was similar in all the groups at 147 d (P = 0.028 for diet × time interaction, Figure 2B). Instead, the increase in the level of TCHO observed from 56 to 147 d was lower in H-OC compared with both CTR and L-OC groups (P = 0.0451 for diet x time interaction, Figure 2A). Compared with bulls, heifers showed higher TCHO (P = 0.0131), TG (P < 0.0001), and GLU (P = 0.0002) and lower insulin (P = 0.0075) concentrations.

FIGURE 2

Figure 2. Significant effect of the diet x time interaction on total cholesterol (A) and ALT (B). The parameters' least square mean (LSM) and standard error are represented for both the sampling times (56 and 147 days) and all the groups with different olive cake inclusions, namely control (CTR, 0%), Low-olive cake (L-OC, 10%), and High-olive cake (H-OC, 15%) groups.

The diet × sex interaction was significant for AST (P = 0.0005), ALT (P = 0.0015), LDH (P = 0.0102), and urea (P < 0.0001) (Figures 3B–E). Specifically, their concentrations were similar in heifers and bulls of CTR and H-OC groups, but higher in heifers than bulls of L-OC group. Considering bulls only, ALT was higher in CTR than L-OC group (Figure 3C), whereas LDH and TG (P = 0.0061) were higher in H-OC than L-OC group (Figures 3A, E); instead, no differences among the three diets were observed in heifers. On the other and, in heifers, urea was higher in L-OC than H-OC (Figure 3B), whereas bulls showed similar values independently from the diet. Insulin (P = 0.0007) was higher in bulls than in heifers of CTR and H-OC groups but did not differ between sex in L-OC group; in addition, within heifers, L-OC group showed the highest concentration of insulin, whereas within bulls we observed the highest values in H-OC (Figure 3F).

FIGURE 3

Figure 3. Significant effect of the diet x sex interaction on total triglycerides (A), urea (B), AST (C), ALT (D), LDH (E), and insulin (F). The parameters' least square mean (LSM) and standard error are represented for both the sexes and all the groups with different olive cake inclusions, namely control (CTR, 0%), Low-olive cake (L-OC, 10%), and High-olive cake (H-OC, 15%) groups.

Pairwise correlations between all the included parameters are reported in Table 4. Hepatic enzymes showed significant positive correlations among them and with CK, urea, and TCHO. CK was also positively correlated with TG. TBIL was positively correlated with TG as well, but negatively correlated to GLU, TCHO, and LDH. Lastly, we observed a negative correlation of insulin with glucose, but a positive correlation with AST, LDH, urea, and TCHO.

TABLE 4

Table 4. Pairwise correlations for all the included blood parameters.

4. Discussion

Olive by-products, including olive cake (OC), have raised the attention of the scientific community for their possible use as livestock diet integration, giving the opportunity to reduce feed costs while improving product quality and sustainability. Mediterranean countries are among the major producers of olive oil, and the processing of this product generates a large quantity of co-products with a high environmental impact (1–2). To answer to the current need to increase the sustainability of Mediterranean agricultural sectors by implementing solutions which result in a valuable output, and in this case, in terms of benefits for animal feeding from OC utilization.

Several ruminants (Yáñez-Ruiz and Molina-Alcaide, 2007; Awawdeh, 2011; Abbeddou et al., 2011a,b; Estaún et al., 2014; Castellani et al., 2017; Kotsampasi et al., 2017; Awawdeh et al., 2020; Chiofalo B. et al., 2020; Chiofalo V. et al., 2020; Neofytou et al., 2020; Alkhtib et al., 2021; Symeou et al., 2021; Tzamaloukas et al., 2021) and monogastric meat species (Rupić et al., 1999; Paiva-Martins et al., 2014; Parsaei et al., 2014; Ait-Kaki et al., 2018; Reda et al., 2020) have been investigated, but beef cattle appear to be under-represented. Moreover, most of the studies mainly focus on animal performance and/or the final product or the rumen function (Estaún et al., 2014). For this reason, there is little knowledge about the metabolic effect that OC integration might have on beef cattle metabolism, which represents the main subject of this work.

In all the enrolled Limousine beef cattle the serum concentrations of lipids (TG, TCHO), parameters of liver functions associated with energy and protein metabolism (GLU, TBIL, AST, ALT, LDH), renal function (urea), indicators of muscle protein turnover and energy utilization (CK), and lipogenic hormones (insulin) were in line with physiological ranges for bovine species (Kaneko et al., 2008), independently from the absence or the 10 or 15% integration of OC in their diet, becoming a relevant result of the current study. Specifically, values of urea and AST were in the range found by Doornenbal et al. (1988) and Gonano et al. (2014) in beef heifers. CK activity was higher than those observed in most studies but still within the range set by Latimer (2011) in cows and in beef heifers.

We also observed that diet or its interaction with sex and/or time of sampling proved to slightly, yet significantly, affect some of these parameters, which are described below.

It is to be considered that, according to our results, the inclusion of the OC did not negatively affect metabolism, as well as the growth of the enrolled animals, consistently with previous studies on beef cattle and lambs (Awawdeh, 2011; Estaún et al., 2014; Kotsampasi et al., 2017; Chiofalo V. et al., 2020; Tzamaloukas et al., 2021). Particularly, no differences were observed in body and carcass weights in heifers. Instead, body weight was higher in CTR bulls, but the carcasses had similar weights independently from the administered diet.

4.1. Lipids (TG, TCHO)

In the present study, growth of animals was characterized by an increase in triglyceridemia and total cholesterolemia. The increase in TCHO concentration can be explained by the marked growth of animals during the finishing phase and the consequent intensification of the anabolic activity of fat and liver metabolism (Van Soest, 1994). Moreover, several studies observed that a high level of TCHO during the early stages of growth is also related to the precocity of puberty attainment (Anderson et al., 2015; Rodríguez-Sánchez et al., 2015) and that TCHO concentrations increase with advancing age in beef cattle, according to the start of puberty and related sexual maturity. Concerning the effect of the diet, we also observed that the increase over time of TCHO was to a lesser extent in the H-OC group only. Accordingly, previous studies investigating olive by-products in sheep diets found no variation or a decrease in TG and TCHO concentrations (El-Tarabany et al., 2018; Awawdeh et al., 2020; Alkhtib et al., 2021). This may be due to the OC's high content in unsaturated fatty acids and phytosterols (Viveros et al., 2009; Cedó et al., 2019).

When considering the effect of sex, heifers showed significant higher TCHO and TG concentrations than bulls. Many aspects of sex differences in physiology arise due to the mechanisms of the sex hormones, including TG and TCHO biology. Estrogen has pleiotropic effects on many tissues and pathways that govern lipid and lipoprotein metabolism and also affects cholesterol efflux capacity (Matthews et al., 2000; Zhu et al., 2018). Heifers may potentially have the capacity to undergo different metabolic adjustments according to their sexual maturity, compared to bulls, as confirmed by the significant effect of age at first service on heifers' plasma concentrations of TG and TCHO observed in cattle and buffalos (Talavera et al., 1985; Wehrman et al., 1991; Ryan et al., 1992; Campanile et al., 2010; Hussein and Abdel-Raheem, 2013). This might explain why we could observe a slight difference in TG concentration due to the diet in bulls but not in heifers.

4.2. Total bilirubin

We observed that TBIL concentration increased from 56 to 147 d and was positively related to the OC inclusion. However, it is important to underline that all the measurements remained within the physiological range.

There are few studies reporting the effect of the diet on this parameter, and no study concerns the integration of olive by-products. It is known that, in cattle, a negative energy balance affects fat mobilization and liver function, leading to an increase in TBIL serum concentrations (Mayasari et al., 2019; Marcato et al., 2021; Hisadomi et al., 2022). It has been observed that unsaturated fatty acids, largely present in the OC, reduce bilirubin conjugation, thus increasing its serum concentration (Hargreaves, 1973; Oliveira et al., 2021). In fact, a similar effect was also observed in new-born calves fed with banana extracts (Keivani Rad et al., 2021).

4.3. Urea

The observed significant increase of urea concentrations from 56 to 147 d is consistent with data previously recorded in both beef and dairy cattle (Swali et al., 2008; Brickell et al., 2009; Gonano et al., 2014). A difference in urea concentration was observed in bulls fed with L-OC and H-OC diet, which showed the highest and lowest values, respectively. Instead, heifers showed similar concentrations regardless the OC inclusion. Urea is one of the few blood parameters that was often evaluated in studies regarding the integration of olive by-products in livestock diet, with most of them reporting a decrease in uremia, which supports our results (Yáñez-Ruiz and Molina-Alcaide, 2007; El-Tarabany et al., 2018; Awawdeh et al., 2020; Alkhtib et al., 2021). This effect was associated to a possible reduction in nitrogen intake or protein rumen degradability due to the bind between tannins and dietary proteins (Yáñez-Ruiz and Molina-Alcaide, 2007; Correddu et al., 2020).

4.4. Liver enzymes (AST, ALT, and LDH)

With regard to hepatic enzymes, we observed that ALT was higher in control animals, but the differences among the groups disappeared when we considered the last sampling period. Accordingly, animals of several species, both ruminant (El-Tarabany et al., 2018; Lipińska and Józwik, 2018; Awawdeh et al., 2020; Alkhtib et al., 2021) and monogastric (Paiva-Martins et al., 2014; Parsaei et al., 2014), showed similar or slightly lower ALT activity when fed with olive or chokeberry by-products. It can be hypothesized that this enzyme decreases due to the effect of antioxidants and polyphenols on the liver.

Interestingly, we also observed a similar effect of sex-diet interaction on all the hepatic enzymes. Particularly, lower activity of all of them were measured with the 10% integration (L-OC), in bulls only. Most of the studies on olive by-products administration showed no differences in these parameters (Paiva-Martins et al., 2014; El-Tarabany et al., 2018; Awawdeh et al., 2020; Alkhtib et al., 2021), but the extent of the integration might be important; in fact, in broilers, a small quantity of olive cake has been associated to a decreased AST, whereas a great quantity to increased AST activity (Parsaei et al., 2014). Moreover, a reduction of AST and LDH activities was also recorded in lambs fed with chokeberry by-products (Lipińska and Józwik, 2018). It might be speculated that these alterations depend on a lower diet nitrogen content, which can influence the hepatic metabolism decreasing AST and ALT activities (Puppel and Kuczyńska, 2016).

4.5. Creatin kinase

As well as AST, CK activity was higher in CTR animals than L-OC and H-OC. The CK is an indicator of muscle protein turnover and is also associated with energy utilization (Baird et al., 2012). Its activity can vary according to the time of the day, age, growth rate, and pregnancy (Gonano et al., 2014); nevertheless, in the present study it is possible to exclude the effect of these variables on the changes of CK activity, because animals were homogenous for age, growth rate, time, and physiological conditions.

In addition, elevated CK activity due to the muscle damage, which can be caused by the physical activity-related oxidative stress, can be prevented or reduced by antioxidant supplementation (Ostojic et al., 2008; Wang et al., 2008; Gupta et al., 2009; Marius-Daniel and Stelian Dragomir, 2010; Bentley et al., 2012). For example, red fruit oil, a natural source of antioxidant, showed to decrease significantly the CK activity during exercise when supplemented to mice (Sinaga and Purba, 2018). On this evidence, it is possible to presume that the antioxidants present in the OC contributed to decrease the activity of CK in both L-OC and H-OC. What is more, diets supplemented with olive or chokeberry by-products led to no variation or a decrease of creatin kinase activity, similarly to our study (Lipińska and Józwik, 2018; Awawdeh et al., 2020).

4.6. Glucose and insulin

Insulin is known to accelerate anabolic processes, such as the synthesis of muscular protein contributing to muscle development, and the synthesis and deposition of fat along developmental processes. Insulin is essential for the regulation of glucose and lipid metabolism and also affects growth through its promotion of the uptake of nutrients into body tissues as recorded by Martin et al. (Martin et al., 1984) and as shown by the existence of significant correlations between insulin and glucose, TCHO, TG, AST, and TBIL. On the other hand, glucose is the favored substrate for lipogenic adipocytes in muscle, whereas acetate is preferred in subcutaneous adipocytes and as precursor of de novo fatty acid synthesis (Smith and Crouse, 1984; Gilbert et al., 2003; Ladeira et al., 2016; Bionaz et al., 2020).

In the present study, insulin was higher in bulls and increased from 56 to 147 d, whereas the opposite was true for glucose, in accordance with the literature (Roy et al., 1983; Gray et al., 1986; Beeby et al., 1988; Plouzek and Trenkle, 1991; Shingu et al., 2001). Bulls, in fact, show higher concentrations of insulin-like growth factor 1, growth hormone, and insulin compared with cows, probably due to the effect of sex-dependent steroid, and this might partially explain their increased growth rate (Ronge and Blum, 1989; Plouzek and Trenkle, 1991; Sirotkin et al., 2002). Fat accumulation in different depots is also sexually dimorphic: in humans, men accumulate more visceral fat, whereas women accumulate more subcutaneous fat and have a higher overall percentage of body fat. There is also evidence indicating that insulin sensitivity differs between males and females (Sirotkin et al., 2002; Macotela et al., 2009). In mice, it was observed that the intra-abdominal depot is regulated by physiological levels of sex steroid and that female mice are more insulin-sensitive that males and their adipocyte show higher expression of glucose and lipid metabolism genes (Mittendorfer, 2005). However, how insulin action differs between males and females and how these differences account for a sex-specific regulation of adipose tissue development and function are not completely clear.

In the present study, we observed a similar insulin concentration in heifers and bulls of the L-OC group, even if diet or its interaction had no effect on glycemia. It should be noticed that, as far as we know, this is the first study analyzing the effect of an olive by-product inclusion on insulin in livestock, but on the other hand it has been demonstrated the phenols contained in olive leaves have a hypoglycemic effect in several species (Parsaei et al., 2014; Ait-Kaki et al., 2018; Lipińska and Józwik, 2018; Alkhtib et al., 2021). Moreover, it is known that a diet rich in carbohydrates tends to increase insulin (Mori et al., 2007) and that glucose kinetics is influenced by the intake of nitrogen and nutrients as well as the fasting length (Brickell et al., 2009; Zanton and Heinrichs, 2017); therefore, we cannot exclude that other mechanisms can be involved in the observed insulin alteration.

5. Conclusions

In the present study we demonstrated that olive cake inclusion in shows no detrimental effect on beef cattle performance and metabolism, according to several blood parameters analyzed at different time points. However, small changes in some analytes have been observed in groups fed with different amount of olive cake, sometimes with different effects in heifers and bulls or at different growing stages, opening the possibility of further research on this topic. Moreover, we provided data about the metabolic profile of beef cattle in the context of diet supplemented with olive cake, improving knowledge about the physiological characterization of these animals at different stages of development. According to the economic analysis, profitability level could be considered interesting, and it should be taken into account in Mediterranean regions. In this sense, in the last years there has been new research exploring the possibilities of further use of the olive residues, like the olive cake, to obtain a valuable outcome on the physiological responses of ruminants, also in terms of endocrine and metabolic adaptations.

Therefore, according to our results, we support an olive cake integration up to 15% of the concentrate in beef cattle diet, thus leading to several advantages also in terms of feed costs and environmental sustainability, as a model of circular economy.

Data availability statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Ethics statement

The animal study was reviewed and approved by Ethical Committee of the Department of Veterinary Science, University of Messina, Italy (code 041/2020). Written informed consent was obtained from the owners for the participation of their animals in this study.

Author contributions

EF and LL: conceptualization. VC: methodology. PC: software. AB and VL: validation. AB and MO: formal analysis. VL: investigation. AB, PC, AA, and VL: data curation. EF: writing—original draft preparation. EF, AB, and VL: writing—review and editing. AB and LL: visualization. LL: supervision, project administration, and funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by P.O. FESR SICILIA 2014/2020. Obiettivo Tematico 1—Ricerca, Sviluppo Tecnologico e Innovazione Obiettivo specifico 1.1—Incremento dell'attività di innovazione delle imprese Azione 1.1.5—Sostegno all'avanzamento tecnologico delle imprese attraverso il finanziamento di linee pilota e azioni di validazione precoce dei prodotti e di dimostrazione su larga scala. Project BIOTRAK. Grant No. 08SR1091000150–CUP G69J18001000007 (principal investigator: LL).

Acknowledgments

Authors wish to thank Feed Manufacturing Industry Dipasquale srl (Avola—SR, IT) for the production of feed, Oil mill Industry Consoli (Adrano—CT, IT) for the production of destoned olive cake, and Spadola Farm for guesting the in-field trials.

Conflict of interest

Author VC was employed by Consortium of Research for Meat Chain and Agrifood (CoRFilCarni).

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Abbreviations

OC, olive cake; FA, fatty acids; TG, triglycerides; TCHOL, total cholesterol; GLU, glucose; TBIL, total bilirubin; ASP, aspartate aminotransferase; ALT, alanine aminotransferase; CK, creatine kinase; BW, body weight; CTR, control group (0% inclusion); L-OC, low-olive cake group (10% inclusion); H-OC, high-olive cake group (15% inclusion); ADG, average daily gain; CW, carcass weight; LSM, least square mean.

References

Abbeddou, S., Rischkowsky, B., Hilali, M. E.-D., Hess, H. D., and Kreuzer, M. (2011a). 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. doi: 10.1017/S0022029911000665

PubMed Abstract | CrossRef Full Text | Google Scholar

Abbeddou, S., Rischkowsky, B., Richter, E. K., Hess, H. D., and Kreuzer, M. (2011b). Modification of milk fatty acid composition by feeding forages and agro-industrial byproducts from dry areas to awassi sheep. J. Dairy Sci. 94, 4657–4668. doi: 10.3168/jds.2011-4154

PubMed Abstract | CrossRef Full Text | Google Scholar

Ait-Kaki, A., Diaw, M., Geda, F., and Moula, N. (2018). Effects of artemisia herba-alba or olive leaf (Olea europaea) powder supplementation on growth performance, carcass yield, and blood biochemical parameters in broilers. Vet. World 11, 1624–1629. doi: 10.14202/vetworld.2018.1624-1629

PubMed Abstract | CrossRef Full Text | Google Scholar

Al-Harthi, M. A. (2016). The efficacy of using olive cake as a by-product in broiler feeding with or without yeast. Ital. J. Anim. Sci. 15, 512–520. doi: 10.1080/1828051X.2016.1194173

CrossRef Full Text | Google Scholar

Alkhtib, A., Muna, M., Burton, E., Wamatu, J., Darag, M., Alkhaled, E., et al. (2021). Effect of olive tree leaves and twigs on intake, digestibility, growth performance and blood variables of shami goats. Vet. Med. Sci. 7, 908–914. doi: 10.1002/vms3.419

PubMed Abstract | CrossRef Full Text | Google Scholar

Anderson, J. L., Kalscheur, K. F., Clapper, J. A., Perry, G. A., Keisler, D. H., Garcia, A. D., et al. (2015). Feeding fat from distillers dried grains with solubles to dairy heifers: II. Effects on metabolic profile. J. Dairy Sci. 98, 5709–5719. doi: 10.3168/jds.2014-9163

PubMed Abstract | CrossRef Full Text | Google Scholar

Awawdeh, M. S. (2011). Alternative feedstuffs and their effects on performance of awassi sheep: a review. Trop. Anim. Health Prod. 43, 1297–1309. doi: 10.1007/s11250-011-9851-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Awawdeh, M. S., Dager, H. K., and Obeidat, B. S. (2020). Dietary inclusion of alternative feedstuffs had no negative effects on hematological and biochemical parameters of growing awassi lambs. Trop. Anim. Health Prod. 52, 2157–2162. doi: 10.1007/s11250-020-02236-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Awawdeh, M. S., and Obeidat, B. S. (2013). Treated olive cake as a non-forage fiber source for growing awassi lambs: effects on nutrient intake, rumen and urine ph, performance, and carcass yield. Asian Austral. J. Anim. Sci. 26, 661–667. doi: 10.5713/ajas.2012.12513

PubMed Abstract | CrossRef Full Text | Google Scholar

Baird, M. F., Graham, S. M., Baker, J. S., and Bickerstaff, G. F. (2012). Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J. Nutr. Metab. 2012, 960363. doi: 10.1155/2012/960363

PubMed Abstract | CrossRef Full Text | Google Scholar

Beeby, J. M., Haresign, W., and Swan, H. (1988). Endogenous hormone and metabolite concentrations in different breeds of beef steer on two systems of production. Anim. Sci. 47, 231–244. doi: 10.1017/S0003356100003317

CrossRef Full Text | Google Scholar

Bentley, D. J., Dank, S., Coupland, R., Midgley, A., and Spence, I. (2012). Acute antioxidant supplementation improves endurance performance in trained athletes. Res. Sports Med. 20, 1–12. doi: 10.1080/15438627.2011.608050

PubMed Abstract | CrossRef Full Text | Google Scholar

Berbel, J., and Posadillo, A. (2018). Review and analysis of alternatives for the valorisation of agro-industrial olive oil by-products. Sustainability 10, 237. doi: 10.3390/su10010237

CrossRef Full Text | Google Scholar

Bionaz, M., Vargas-Bello-Pérez, E., and Busato, S. (2020). Advances in fatty acids nutrition in dairy cows: from gut to cells and effects on performance. J. Anim. Sci. Biotechnol. 11, 110. doi: 10.1186/s40104-020-00512-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Branciari, R., Ranucci, D., Miraglia, D., Urbani, S., Esposto, S., Servili, M., et al. (2015). Effect of dietary treatment with olive oil by-product (olive cake) on physico-chemical, sensory and microbial characteristics of beef during storage. Ital. J. Food Saf. 4, 5496. doi: 10.4081/ijfs.2015.5496

PubMed Abstract | CrossRef Full Text | Google Scholar

Brickell, J. S., Bourne, N., McGowan, M. M., and Wathes, D. C. (2009). Effect of growth and development during the rearing period on the subsequent fertility of nulliparous Holstein-Friesian heifers. Theriogenology. 72, 408–416. doi: 10.1016/j.theriogenology.2009.03.015

PubMed Abstract | CrossRef Full Text | Google Scholar

Campanile, G., Baruselli, P. S., Vecchio, D., Prandi, A., Neglia, G., Carvalho, N. A. T., et al. (2010). Growth, metabolic status and ovarian function in buffalo (Bubalus bubalis) heifers fed a low energy or high energy diet. Anim. Reprod. Sci. 122, 74–81. doi: 10.1016/j.anireprosci.2010.07.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Castellani, F., Vitali, A., Bernardi, N., Marone, E., Palazzo, F., Grotta, L., et al. (2017). Dietary supplementation with dried olive pomace in dairy cows modifies the composition of fatty acids and the aromatic profile in milk and related cheese. J. Dairy Sci. 100, 8658–8669. doi: 10.3168/jds.2017-12899

PubMed Abstract | CrossRef Full Text | Google Scholar

Cedó, L., Farràs, M., Lee-Rueckert, M., and Escolà-Gil, J. C. (2019). Molecular insights into the mechanisms underlying the cholesterol- lowering effects of phytosterols. Curr. Med. Chem. 26, 6704–6723. doi: 10.2174/0929867326666190822154701

PubMed Abstract | CrossRef Full Text | Google Scholar

Chiofalo, B., di Rosa, A. R., Lo Presti, V., Chiofalo, V., and Liotta, L. (2020). 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 therefrom. Animals 10, 977. doi: 10.3390/ani10060977

PubMed Abstract | CrossRef Full Text | Google Scholar

Chiofalo, B., Liotta, L., Zumbo, A., and Chiofalo, V. (2004). Administration of olive cake for ewe feeding: effect on milk yield and composition. Small Rumin. Res. 55, 169–176. doi: 10.1016/j.smallrumres.2003.12.011

CrossRef Full Text | Google Scholar

Chiofalo, V., Liotta, L., Lo Presti, V., Gresta, F., Di Rosa, A. R., and Chiofalo, B. (2020). Effect of dietary olive cake supplementation on performance, carcass characteristics, and meat quality of beef cattle. Animals 10, 1176. doi: 10.3390/ani10071176

PubMed Abstract | CrossRef Full Text | Google Scholar

Correddu, F., Lunesu, M. F., Buffa, G., Atzori, A. S., Nudda, A., Battacone, G., et al. (2020). Can agro-industrial by-products rich in polyphenols be advantageously used in the feeding and nutrition of dairy small ruminants? Animals 10, 131. doi: 10.3390/ani10010131

PubMed Abstract | CrossRef Full Text | Google Scholar

Council of the European Union (2010). Directive 2010/63/EU of the European Parliament and of the Council. Council of the European Union.

Google Scholar

de Evan, T., Cabezas, A., de la Fuente, J., and Carro, M. D. (2020). Feeding agroindustrial byproducts to light lambs: influence on growth performance, diet digestibility, nitrogen balance, ruminal fermentation, and plasma metabolites. Animals 10, 600. doi: 10.3390/ani10040600

PubMed Abstract | CrossRef Full Text | Google Scholar

Doornenbal, H., Tong, A. K., and Murray, N. L. (1988). Reference values of blood parameters in beef cattle of different ages and stages of lactation. Can. J. Vet. Res. 52, 99–105.

PubMed Abstract | Google Scholar

El Otmani, S., Chebli, Y., Taminiau, B., Chentouf, M., Hornick, J.-L., and Cabaraux, J.-F. (2021). Effect of olive cake and cactus cladodes incorporation in goat kids' diet on the rumen microbial community profile and meat fatty acid composition. Biology 10, 1237. doi: 10.3390/biology10121237

PubMed Abstract | CrossRef Full Text | Google Scholar

El-Tarabany, A., Mostafa, M., and Mohamed, A. (2018). Effect of dietary olive cake on reproductive and physiological traits of native pregnant ewes. Arab. J. Nucl. Sci. Applic. 51, 135–142. doi: 10.21608/ajnsa.2018.12788

CrossRef Full Text | Google Scholar

Espeso, J., Isaza, A., Lee, J. Y., Sörensen, P. M., Jurado, P., Avena-Bustillos, R. J., et al. (2021). Olive leaf waste management. Front. Sustain. Food Syst. 5, 660582. doi: 10.3389/fsufs.2021.660582

CrossRef Full Text | Google Scholar

Estaún, J., Dosil, J., Al Alami, A., Gimeno, A., and de Vega, A. (2014). Effects of including olive cake in the diet on performance and rumen function of beef cattle. Anim. Prod. Sci. 54, 1817. doi: 10.1071/AN14352

CrossRef Full Text | Google Scholar

Foti, P., Pino, A., Romeo, F. V., Vaccalluzzo, A., Caggia, C., Randazzo, C. L., et al. (2022). Olive pomace and pâté olive cake as suitable ingredients for food and feed. Microorganisms 10, 237. doi: 10.3390/microorganisms10020237

PubMed Abstract | CrossRef Full Text | Google Scholar

Ghanbari, R., Anwar, F., Alkharfy, K. M., Gilani, A.-H., and 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. doi: 10.3390/ijms13033291

PubMed Abstract | CrossRef Full Text | Google Scholar

Gilbert, C. D., Lunt, D. K., Miller, R. K., and Smith, S. B. (2003). Carcass, sensory, and adipose tissue traits of brangus steers fed casein-formaldehyde-protected starch and/or canola lipid1. J. Anim. Sci. 81, 2457–2468. doi: 10.2527/2003.81102457x

PubMed Abstract | CrossRef Full Text | Google Scholar

Gonano, C. V., Montanholi, Y. R., Schenkel, F. S., Smith, B. A., Cant, J. P., Miller, S. P., et al. (2014). The relationship between feed efficiency and the circadian profile of blood plasma analytes measured in beef heifers at different physiological stages. Animal 8, 1684–1698. doi: 10.1017/S1751731114001463

PubMed Abstract | CrossRef Full Text | Google Scholar

Gray, D. G., Unruh, J. A., Dikeman, M. E., and Stevenson, J. S. (1986). Implanting young bulls with zeranol from birth to four slaughter ages: III. Growth performance and endocrine aspects. J. Anim. Sci. 63, 747–756. doi: 10.2527/jas1986.633747x

PubMed Abstract | CrossRef Full Text | Google Scholar

Gupta, C., Gupta, P. H., and Singh, B. (2009). Effect of vitamin supplementation on exercise induced oxidative stress in trained elite indian cyclists. Am. J. Biomed. Sci. 1, 166–170. doi: 10.5099/aj090200166

CrossRef Full Text | Google Scholar

Hargreaves, T. (1973). Effect of fatty acids on bilirubin conjugation. Arch. Dis. Child. 48, 446–450. doi: 10.1136/adc.48.6.446

PubMed Abstract | CrossRef Full Text | Google Scholar

Hisadomi, S., Haruno, A., Fujieda, T., Sugino, T., and Oba, M. (2022). Effects of rumen-protected glutamate supplementation during the periparturient period on digestibility, inflammation, metabolic responses, and performance in dairy cows. J. Dairy Sci. 105, 3129–3141. doi: 10.3168/jds.2021-21357

PubMed Abstract | CrossRef Full Text | Google Scholar

Hussein, H. A., and Abdel-Raheem, S. M. (2013). Effect of feed intake restriction on reproductive performance and pregnancy rate in Egyptian buffalo heifers. Trop. Anim. Health Prod. 45, 1001–1006. doi: 10.1007/s11250-012-0324-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Joven, M., Pintos, E., Latorre, M. A., Suárez-Belloch, J., Guada, J. A., Fondevila, M., et al. (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. Technol. 197, 185–193. doi: 10.1016/j.anifeedsci.2014.08.007

CrossRef Full Text | Google Scholar

Kaneko, J. J., Harvey, J. W., and Bruss, M. L. (2008). Clinical Biochemistry of Domestic Animals, 6th Edn. San Diego, CA: Academic Press.

Google Scholar

Keivani Rad, N., Mohri, M., Seifi, H. A., and Haghparast, A. (2021). Supplementation of overripe pulp extract and green peel extract or powder of banana fruit peel (musa. cavendish) to diets of neonatal dairy calves: effects on haematological, immunological and performance characteristics. Vet. Med. Sci. 7, 876–887. doi: 10.1002/vms3.429

PubMed Abstract | CrossRef Full Text | Google Scholar

Keleş, G. (2015). The nutritive and feeding value of olive cake for ruminants. Turk. J. Agric. Food Sci. Technol. 3, 780. doi: 10.24925/turjaf.v3i10.780-789.435

CrossRef Full Text | Google Scholar

Kotsampasi, B., Bampidis, V. A., Tsiaousi, A., Christodoulou, C., Petrotos, K., Amvrosiadis, I., et al. (2017). Effects of dietary partly destoned exhausted olive cake supplementation on performance, carcass characteristics and meat quality of growing lambs. Small Rumin. Res. 156, 33–41. doi: 10.1016/j.smallrumres.2017.08.013

CrossRef Full Text | Google Scholar

Ladeira, M., Schoonmaker, J., Gionbelli, M., Dias, J., Gionbelli, T., Carvalho, J., et al. (2016). Nutrigenomics and beef quality: a review about lipogenesis. Int. J. Mol. Sci. 17, 918. doi: 10.3390/ijms17060918

PubMed Abstract | CrossRef Full Text | Google Scholar

Latimer, K. S. (2011). Duncan and Prasse's Veterinary Laboratory Medicine: Clinical Pathology, 5th Edn. West Sussex: Wiley-Blackwell.

Google Scholar

Liotta, L., Chiofalo, V., Lo Presti, V., and Chiofalo, B. (2019). In vivo performances, carcass traits, and meat quality of pigs fed olive cake processing waste. Animals 9, 1155. doi: 10.3390/ani9121155

PubMed Abstract | CrossRef Full Text | Google Scholar

Lipińska, P., and Józwik, A. (2018). Hepatoprotective, hypoglycemic, and hypolipidemic effect of chokeberry pomace on polish merino lambs. Anim. Biotechnol. 29, 136–141. doi: 10.1080/10495398.2017.1330209

PubMed Abstract | CrossRef Full Text | Google Scholar

Macotela, Y., Boucher, J., Tran, T. T., and Kahn, C. R. (2009). Sex and depot differences in adipocyte insulin sensitivity and glucose metabolism. Diabetes 58, 803–812. doi: 10.2337/db08-1054

PubMed Abstract | CrossRef Full Text | Google Scholar

Marcato, F., van den Brand, H., Jansen, C. A., Rutten, V. P. M. G., Kemp, B., Engel, B., et al. (2021). Effects of pre-transport diet, transport duration and transport condition on immune cell subsets, haptoglobin, cortisol and bilirubin in young veal calves. PLoS ONE 16, e0246959. doi: 10.1371/journal.pone.0246959

PubMed Abstract | CrossRef Full Text | Google Scholar

Marius-Daniel, R., and Stelian Dragomir, C. (2010). The effect of acute physical exercise on the antioxidant status of the skeletal and cardiac muscle in the Wistar rat. Rom. Biotechnol. Lett. 15, 56–61.

PubMed Abstract | Google Scholar

Martin, R. J., Ramsay, T. G., and Harris, R. B. S. (1984). Central role of insulin in growth and development. Domest. Anim. Endocrinol. 1, 89–104. doi: 10.1016/0739-7240(84)90024-9

CrossRef Full Text | Google Scholar

Matthews, J., Celius, T., Halgren, R., and Zacharewski, T. (2000). Differential estrogen receptor binding of estrogenic substances: a species comparison. J. Steroid Biochem. Mol. Biol. 74, 223–234. doi: 10.1016/S0960-0760(00)00126-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Mayasari, N., Trevisi, E., Ferrari, A., Kemp, B., Parmentier, H. K., van Knegsel, A. T. M., et al. (2019). Relationship between inflammatory biomarkers and oxidative stress with uterine health in dairy cows with different dry period lengths. Transl. Anim. Sci. 3, 607–619. doi: 10.1093/tas/txz040

PubMed Abstract | CrossRef Full Text | Google Scholar

Mele, M., Serra, A., Pauselli, M., Luciano, G., Lanza, M., Pennisi, P., et al. (2014). The use of stoned olive cake and rolled linseed in the diet of intensively reared lambs: effect on the intramuscular fatty-acid composition. Animal 8, 152–162. doi: 10.1017/S1751731113001924

PubMed Abstract | CrossRef Full Text | Google Scholar

Mittendorfer, B. (2005). Insulin resistance: sex matters. Curr. Opin. Clin. Nutr. Metab. Care. 8, 367–372. doi: 10.1097/01.mco.0000172574.64019.98

PubMed Abstract | CrossRef Full Text | Google Scholar

Mori, A., Urabe, S., Asada, M., Tanaka, Y., Tazaki, H., Yamamoto, I., et al. (2007). Comparison of plasma metabolite concentrations and enzyme activities in beef cattle raised by different feeding systems in Korea, Japan and New Zealand. J. Vet. Med. Ser. A 54, 342–345. doi: 10.1111/j.1439-0442.2007.00964.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Neofytou, M. C., Miltiadou, D., Sfakianaki, E., Constantinou, C., Symeou, S., Sparaggis, D., et al. (2020). The use of ensiled olive cake in the diets of Friesian cows increases beneficial fatty acids in milk and Halloumi cheese and alters the expression of SREBF1 in adipose tissue. J. Dairy Sci. 103, 8998–9011. doi: 10.3168/jds.2020-18235

PubMed Abstract | CrossRef Full Text | Google Scholar

Oliveira, M. X. S., Palma, A. S., Reis, B. R., Franco, C. S. R., Marconi, A. P. S., Shiozaki, F. A., et al. (2021). Inclusion of soybean and linseed oils in the diet of lactating dairy cows makes the milk fatty acid profile nutritionally healthier for the human diet. PLoS ONE 16, e0246357. doi: 10.1371/journal.pone.0246357

PubMed Abstract | CrossRef Full Text | Google Scholar

Ostojic, S. M., Stojanovic, M. D., Djordjevic, B., Jourkesh, M., and Vasiljevic, N. (2008). The effects of a 4-week coffeeberry supplementation on antioxidant status, endurance, and anaerobic performance in college athletes. Res. Sports Med. 16, 281–294. doi: 10.1080/15438620802523345

PubMed Abstract | CrossRef Full Text | Google Scholar

Paiva-Martins, F., Ribeirinha, T., Silva, A., Gonçalves, R., Pinheiro, V., Mourão, J. L., et al. (2014). Effects of the dietary incorporation of olive leaves on growth performance, digestibility, blood parameters and meat quality of growing pigs. J. Sci. Food Agric. 94, 3023–3029. doi: 10.1002/jsfa.6650

PubMed Abstract | CrossRef Full Text | Google Scholar

Parsaei, S., Amini, Z., and Houshmand, M. (2014). Effects of olive leaf on blood metabolites and humoral immunity response of broiler chickens. Int. J. Adv. Biol. Biomed. Res. 2, 741–751.

Google Scholar

Plouzek, C. A., and Trenkle, A. (1991). Insulin-like growth factor-I concentrations in plasma of intact and castrated male and female cattle at four ages. Domest. Anim. Endocrinol. 8, 73–79. doi: 10.1016/0739-7240(91)90041-H

PubMed Abstract | CrossRef Full Text | Google Scholar

Puppel, K., and Kuczyńska, B. (2016). Metabolic profiles of cow's blood; a review. J. Sci. Food Agric. 96, 4321–4328. doi: 10.1002/jsfa.7779

PubMed Abstract | CrossRef Full Text | Google Scholar

Reda, F. M., El-Kholy, M. S., Abd El-Hack, M. E., Taha, A. E., Othman, S. I., Allam, A. A., et al. (2020). Does the use of different oil sources in quail diets impact their productive and reproductive performance, egg quality, and blood constituents? Poult. Sci. 99, 3511–3518. doi: 10.1016/j.psj.2020.03.054

PubMed Abstract | CrossRef Full Text | Google Scholar

Rodríguez-Sánchez, J. A., Sanz, A., Tamanini, C., and Casasús, I. (2015). Metabolic, endocrine, and reproductive responses of beef heifers submitted to different growth strategies during the lactation and rearing periods. J. Anim. Sci. 93, 3871–3885. doi: 10.2527/jas.2015-8994

PubMed Abstract | CrossRef Full Text | Google Scholar

Ronge, H., and Blum, J. W. (1989). Insulin-like growth factor I binding proteins in dairy cows, calves and bulls. Acta Endocrinol. 121, 153–160. doi: 10.1530/acta.0.1210153

PubMed Abstract | CrossRef Full Text | Google Scholar

Roy, J. H. B., Hart, I. C., Gillies, C. M., Stobo, I. J. F., Ganderton, P., Perfitt, M. W., et al. (1983). A comparison of preruminant bull calves of the Hereford × Friesian, Aberdeen Angus × Friesian and Friesian breeds. Anim. Sci. 36, 237–251. doi: 10.1017/S1357729800001302

CrossRef Full Text | Google Scholar

Rupić, V., Bozikov, V., Bozac, R., Muzic, S., Vranesić, N., and Dikić, M. (1999). Effect of feeding olive by-products on certain blood parameters and serum enzyme activities of fattening rabbits. Acta Vet. Hung. 47, 65–75. doi: 10.1556/avet.47.1999.1.6

PubMed Abstract | CrossRef Full Text | Google Scholar

Ryan, D. P., Spoon, R. A., and Williams, G. L. (1992). Ovarian follicular characteristics, embryo recovery, and embryo viability in heifers fed high-fat diets and treated with follicle-stimulating hormone. J. Anim. Sci. 70, 3505–3513. doi: 10.2527/1992.70113505x

PubMed Abstract | CrossRef Full Text | Google Scholar

Salomone, R., and 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. doi: 10.1016/j.jclepro.2011.10.004

CrossRef Full Text | Google Scholar

Shingu, H., Hodate, K., Kushibiki, S., Ueda, Y., Watanabe, A., Shinoda, M., et al. (2001). Profiles of growth hormone and insulin secretion, and glucose response to insulin in growing Japanese Black heifers (beef type): comparison with Holstein heifers (dairy type). Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 130, 259–270. doi: 10.1016/S1532-0456(01)00249-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Sinaga, F. A., and Purba, P. H. (2018). The influence of red fruit oil on creatin kinase level at maximum physical activity. J. Phys. Conf. Ser. 970, 012007. doi: 10.1088/1742-6596/970/1/012007

CrossRef Full Text | Google Scholar

Sirotkin, A., Svetlanská, M., Sommer, A., Makarevich, A., Szakács, J., and Poláciková, M. (2002). Are IGF-I, thyroid hormone and metabolite concentrations in calf plasma associated with growth rate, sex and age? J. Anim. Feed Sci. 11, 265–275. doi: 10.22358/jafs/67811/2002

CrossRef Full Text | Google Scholar

Smith, S. B., and Crouse, J. D. (1984). Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J. Nutr. 114, 792–800. doi: 10.1093/jn/114.4.792

PubMed Abstract | CrossRef Full Text | Google Scholar

Swali, A., Cheng, Z., Bourne, N., and Wathes, D. C. (2008). Metabolic traits affecting growth rates of pre-pubertal calves and their relationship with subsequent survival. Domest. Anim. Endocrinol. 35, 300–313. doi: 10.1016/j.domaniend.2008.06.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Symeou, S., Miltiadou, D., Constantinou, C., Papademas, P., and Tzamaloukas, O. (2021). Feeding olive cake silage up to 20% of DM intake in sheep improves lipid quality and health-related indices of milk and ovine halloumi cheese. Trop. Anim. Health Prod. 53, 229. doi: 10.1007/s11250-021-02674-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Talavera, F., Park, C. S., and Williams, G. L. (1985). Relationships among dietary lipid intake, serum cholesterol and ovarian function in holstein heifers. J. Anim. Sci. 60, 1045–1051. doi: 10.2527/jas1985.6041045x

PubMed Abstract | CrossRef Full Text | Google Scholar

The European Agency for the Evaluation of Medicinal Products (2000). Guideline on Good Clinical Practices. London: The European Agency for the Evaluation of Medicinal Products.

Google Scholar

Tzamaloukas, O., Neofytou, M. C., and 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. doi: 10.3390/ani11020531

PubMed Abstract | CrossRef Full Text | Google Scholar

Van Soest, P. J. (1994). Nutritional Ecology of the Ruminant, 2nd edn. Itacha, NY: Cornell University Press. doi: 10.7591/9781501732355

CrossRef Full Text | Google Scholar

Vargas-Bello-Pérez, E., Vera, R. R., Aguilar, C., Lira, R., Peña, I., Fernández, J., et al. (2013). Feeding olive cake to ewes improves fatty acid profile of milk and cheese. Anim. Feed Sci. Technol. 184, 94–99. doi: 10.1016/j.anifeedsci.2013.05.016

PubMed Abstract | CrossRef Full Text | Google Scholar

Vastolo, A., Calabró, A., Liotta, L., Musco, N., Di Rosa, A. R., Cutrignelli, M. I., et al. (2019). In vitro fermentation and chemical characteristics of mediterranean by-products for swine nutrition. Animals 9, 556. doi: 10.3390/ani9080556

PubMed Abstract | CrossRef Full Text | Google Scholar

Viveros, A., Ortiz, L. T., Rodríguez, M. L., Rebolé, A., Alzueta, C., Arija, I., et al. (2009). Interaction of dietary high-oleic-acid sunflower hulls and different fat sources in broiler chickens. Poult. Sci. 88, 141–151. doi: 10.3382/ps.2008-00226

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, L., Zhang, H. L., Lu, R., Zhou, Y. J., Ma, R., Lv, J. Q., et al. (2008). The decapeptide CMS001 enhances swimming endurance in mice. Peptides 29, 1176–1182. doi: 10.1016/j.peptides.2008.03.004

PubMed Abstract | CrossRef Full Text | Google Scholar

Wehrman, M. E., Welsh, T. H., and Williams, G. L. (1991). Diet-induced hyperlipidemia in cattle modifies the intrafollicular cholesterol environment, modulates ovarian follicular dynamics, and hastens the onset of postpartum luteal activity. Biol. Reprod. 45, 514–522. doi: 10.1095/biolreprod45.3.514

PubMed Abstract | CrossRef Full Text | Google Scholar

Yáñez Ruiz, D. R., Moumen, A., Martín García, A. I., and Molina Alcaide, E. (2004). Ruminal fermentation and degradation patterns, protozoa population, and urinary purine derivatives excretion in goats and wethers fed diets based on two-stage olive cake: effect of PEG supply1. J. Anim. Sci. 82, 2023–2032. doi: 10.2527/2004.8272023x

PubMed Abstract | CrossRef Full Text | Google Scholar

Yáñez-Ruiz, D. R., and Molina-Alcaide, E. (2007). A comparative study of the effect of two-stage olive cake added to alfalfa on digestion and nitrogen losses in sheep and goats. Animal 1, 227–232. doi: 10.1017/S1751731107340032

PubMed Abstract | CrossRef Full Text | Google Scholar

Zanton, G. I., and Heinrichs, A. J. (2017). Short communication: glucose kinetics in dairy heifers limit-fed a low- or high-forage ration at 4 levels of nitrogen intake. J. Dairy Sci. 100, 3718–3724. doi: 10.3168/jds.2016-12037

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhu, L., Shi, J., Luu, T. N., Neuman, J. C., Trefts, E., Yu, S., et al. (2018). Hepatocyte estrogen receptor alpha mediates estrogen action to promote reverse cholesterol transport during western-type diet feeding. Mol. Metab. 8, 106–116. doi: 10.1016/j.molmet.2017.12.012

PubMed Abstract | CrossRef Full Text | Google Scholar

Zilio, D. M., Bartocci, S., di Giovanni, S., Servili, M., Chiariotti, A., Terramoccia, S., et al. (2015). Evaluation of dried stoned olive pomace as supplementation for lactating Holstein cattle: effect on milk production and quality. Anim. Prod. Sci. 55, 185. doi: 10.1071/AN14254

CrossRef Full Text | Google Scholar