https://orcid.org/0000-0003-4296-7589
Abstract
Including grape pomace in goat diets presents a potentially valuable strategy for enhancing the sustainability of goat farming and mitigating environmental risks. This work aimed to investigate the impact of dietary dried grape pomace (DGP) on milk yield, milk composition and milk fatty acid (FA) profile in goats. Gas chromatography was utilised to obtain an extensive profile of FA in milk fat. Dry matter intake, as well as milk yield and composition were not altered by dietary DGP. Despite the predominance of linoleic acid (LA, 18:2 cis-9,cis-12) in the lipids of DGP and the presence of phenolic compounds, its inclusion in the diet did not negatively affect the quantitatively main groups of FA. Furthermore, there was no significant impact on butyric, caproic, caprylic, and capric acids, the major 18:1 trans isomers, including vaccenic acid (18:1 trans-11), LA, α-linolenic acid (18:3 n-3), and the long chain polyunsaturated n-6 and n-3 FA. However, rumenic acid in milk fat was significantly reduced from 0.36 to 0.30 g/100 g of total fatty acid methyl esters. This study supports that up to 6%, DGP can be safely included in conventional dairy goat diets without compromising the production results or altering to great extent the milk FA profile.
HIGHLIGHTS
Milk changes due to dried grape pomace (DGP) consumption were assessed in goats.
Milk yield increased without changes in milk composition following DGP consumption.
Some minor FA contents were modified by DGP.
DGP had no impact on most FA related to milk fat’s nutritional properties.
Introduction
Grape pomace is the main residue, comprised of skins, stems, residual pulp, and seeds, that remains after the grapes are crushed and pressed during winemaking (Bordiga et al. Citation2019). The inadequate disposal of this waste generates several environmental issues such as land and water contamination, malodors, and the proliferation of pests (Bustamante et al. Citation2008). On the other hand, grape pomace contains substantial amounts of a wide range of biologically active substances of the group of phenolic compounds (Onache et al. Citation2022), which can modulate the rumen microbiota (Vasta et al. Citation2019).
World caprine milk production has steadily increased over the last two decades, being both economically and nutritionally relevant not only in less favoured areas worldwide but also in developed countries (Miller and Lu Citation2019). Moreover, dairy goat farming is a relevant sector of agri-food industries in Europe and the Mediterranean basin (Dubeuf et al. Citation2018; Pulina et al. Citation2018). As other livestock sectors, the dairy goat sector faces economic challenges and needs to embrace sustainability principles and practices to enhance its resilience and competitiveness (Paraskevopoulou et al. Citation2020). Including agro-industrial by-products in intensively farmed dairy goat diets has the potential to control feed costs and contribute to a circular economy (Pardo et al. Citation2016). However, promoting the inclusion of any agro-industrial by-product in the diet of dairy goats would be only advisable if no negative effects on production performance or nutritional quality of milk are demonstrated (Romero-Huelva et al. Citation2017).
The available literature suggests that incorporating grape pomace into the diets of dairy ruminants typically results in a decrease of total saturated FA (SFA) and an increase of total monounsaturated FA (MUFA), total polyunsaturated fatty acids (PUFA), vaccenic acid (VA) and rumenic acid (RA) (Correddu et al. Citation2023). However, literature describing the potential impact of dietary grape pomace on caprine milk is scarce (Tsiplakou and Zervas Citation2008). To address this gap, the present work investigated the effects of incorporating dried grape pomace (DGP) into the diet of dairy goats. We specifically evaluated its impact on milk production and composition, focusing especially on changes in the milk FA profile.
Materials and methods
Experimental design and animal management
The experimental design was developed in compliance with the European Directive/63/EU on the protection of animals used for scientific purposes (EU Citation2010), and Council Directive 98/58/EC setting minimum standards for the protection of farmed animals (EU Citation1998). Twenty-two Camosciata delle Alpi goats from a commercial flock, all with similar parity (3.8 ± 1.54), stage of lactation (86 ± 4.8 days in milk), milk yield (2.0 ± 0.65 kg/d), and milk composition (fat, 40.5 ± 7.08 g/L; protein, 33.01 ± 3.28 g/L), were randomly assigned to one of two different dietary treatments. The animals in the control treatment (CON) were fed mixed hay ad libitum plus 800 g/d of a commercial concentrate (Table ). The animals in the experimental treatment (DGP) were fed the same mixed hay ad libitum plus 650 g/d of the commercial concentrate and 150 g/d of DGP. The amount of DGP to be fed was established following the review of the relevant literature on the use of DGP in small ruminants (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Resconi et al. Citation2018; Nudda et al. Citation2019) and in order to minimise the differences between the CON and DGP diets in the supply of protein and energy to the animals. The concentrate was administered in equal amounts during the morning (7:00 a.m.) and evening (6:00 pm) milkings. The DGP was derived from Barbera grape, a red variety cultivated in North Italy. After the vinification process, hot air drying of wet grape pomace was carried out in a conventional dryer using natural convection at a fixed temperature of 60 °C. The trial lasted 45 d. For the initial 15 d, the animals in the DGP treatment had DGP gradually introduced into their diet at a rate of 50 g on every five days, replacing equal amounts of the commercial concentrate. The remaining 30 d served as the experimental period. The goats were housed indoors in individual straw-bedded pens (1.5 m2), with clean and fresh water freely available during the trial.
Table 1. Proximate composition and fatty acid profile (g/kg dry matter, unless otherwise stated) of the feedstuffs included in the experimental diets.
Measurements and chemical analysis
Daily amount of feed offered and refusals were weighed and recorded for each goat to calculate individual daily intake on an average basis. Representative samples of mixed hay, commercial concentrate and DGP were collected at the beginning of the trial. Dry matter (DM), crude protein, acid detergent fibre (ADF), and acid detergent lignin (ADL) were analysed according to AOAC (Citation2000). Ether extract was determined according to AOAC (Citation2003). Neutral detergent fibre (NDF) was analysed following Mertens (Citation2002). Total extractable phenols (TEP), non-tannin phenols (NTP) and condensed tannins (CT) in DGP were determined as described by Iussig et al. (Citation2015).
The FA composition of hay, commercial concentrate and DGP was determined as detailed by Renna et al. (Citation2014). Briefly, fatty acid methyl esters (FAME) were prepared using a combined direct transesterification and solid-phase extraction method. The FAME were identified and quantified using a high-resolution gas chromatograph (Shimadzu GC 2010 Plus; Shimadzu, Kyoto, Japan) equipped with a flame-ionisation detector, and a CP-Sil 88 capillary column (100 m × 0.25 mm ID, 0.20 µm film thickness; Varian Inc., Palo Alto, CA, USA). Peaks were identified by comparing retention times to pure standards and by comparison with published chromatograms (Alves et al. Citation2008).
Milk yield was recorded and milk samples were collected from each goat in the last day of the trial. Milk samples were collected by proportionally mixing the milk from the morning and afternoon milkings. Two sub-samples were obtained from each milk sample. The first sub-sample was immediately stored at 4 °C in a portable refrigerator and transported to the laboratory of A.R.A. Piemonte (Madonna dell’Olmo, CN; Italy), where it was analysed in duplicate for fat, protein and lactose, using a MilkoScan FT 6000 (Foss Electric, Hillerød, Denmark). The second sub-sample was immediately stored at 4 °C in a portable refrigerator and transported to the laboratories of the Department of Agricultural, Forest and Food Sciences of the University of Turin, where it was frozen at −80 °C until FA composition was analysed. Milk fat was extracted by centrifugation at 7300 rpm for 30 min at −4 °C. The resulting molten butter was filtered through a paper filter (Whatman International Ltd, Maidstone, England), the pure milk fat was dissolved in heptane and FAME were prepared by base-catalyzed methanolysis of glycerides with KOH in methanol (Renna et al. Citation2012). The same analytical instruments described for FAME analysis in feed samples were used. Chromatographic conditions as well as peak identification and quantification were detailed by Kramer et al. (Citation2008). Elongation, desaturation and shortening indexes for FA were calculated as [product/(substrate + product)]. All the analyses were performed in duplicate.
Statistical analysis
Statistical analyses were carried out with the GLM procedure of SAS OnDemand for Academics (SAS Institute Inc., Cary, USA). The dietary treatment was the fixed effect, and the goat was the experimental unit. A P value of <0.05 was considered statistically significant, and P values of 0.05 ≤ p < 0.10 were discussed as trends. The results were presented as mean and pooled standard error of mean (SEM).
Results and discussion
Composition of dried grape pomace
The DGP exhibited an appreciable concentration of lipids, primarily consisting of FA, and a high content of lignified fibre in accordance with the published literature (Molina-Alcaide et al. Citation2008; Tsiplakou and Zervas Citation2008; Resconi et al. Citation2018) (Table ). The concentration of TEP was 27.0 mg gallic acid equivalents/g DM, with TT constituting more than 95% of TEP, in line with the values previously reported in several grape pomaces from white and red cultivars (Onache et al. Citation2022). The CT concentration was 10.3 mg leucocyanidin equivalents/g DM.
The PUFA were predominant in DGP lipids, mostly due to their high content of linoleic acid (LA, 18:2 cis-9,cis-12), in accordance with previous studies (Ribeiro et al. Citation2015; Mohamed Ahmed et al. Citation2020). Low amounts of trans-octadecadienoic acids, including both non-conjugated (18:2 trans-9,trans-12, cis-9,trans-12 and trans-9,cis-12) and conjugated (18:2 cis-9,trans-11 and trans-9,trans-11) isomers were detected. The 18:2 cis-9,trans-12, trans-9,cis-12 and trans-9,trans-11 isomers were also found by Yi et al. (Citation2009) in the pomaces from two red grape varieties. Moreover, the total content of trans-octadecadienoic acids in the DGP of the present work (74 g/100 g of total fatty acid methyl esters) was in between the values reported in the pomaces from two red grape varieties (Ribeiro et al. Citation2015). The presence of such FA in the pomace could be explained by the microbial metabolism of LA during the fermentation before the pomace is generated in the red wine processing (Virdis et al. Citation2020).
Milk yield and milk composition
The goats totally consumed the concentrate and DGP in the treatments (Table ). However, hay dry matter intake was 7% higher in the DGP treatment (p < 0.05). Milk yield was numerically higher in the DGP treatment, but the difference did not reach statistical significance (p = 0.19). It is worth mentioning that the calculated metabolisable energy content of the DGP was at least 45% inferior to that of the commercial concentrate (7.0 vs 12.9 MJ/kg DM), thus despite the higher hay intake slightly lower metabolisable energy (0.41 MJ/d) was consumed by the goats in the DGP treatment. Moate et al. (Citation2020) observed a 10% lower milk yield in dairy cows fed up to 5 kg DM/d of DGP linked to a reduction of metabolisable energy intake of 11 MJ/d in that group. However, Nudda et al. (Citation2019) found that ewes fed 93 g DM/d of DGP produced more milk than the control ewes despite the lower consumption of metabolisable energy (0.81 MJ/d). Furthermore, Tsiplakou and Zervas (Citation2008) observed no differences in milk yield either in ewes or goats that consumed about 480 g DM/d of DGP, as compared with their respective controls.
Table 2. Daily hay intake (dry matter basis) and milk yield and composition in dairy goats fed a conventional diet (CON) or the same diet with 150 g of concentrate replaced by an equal amount of dried grape pomace (DGP).
The DGP diet did not alter milk composition (p > 0.05) (Table ), a result that may be considered beneficial from the perspective of cheesemaking efficiency (Vacca et al. Citation2018). Some authors have reported a decrease in the content of protein and/or fat in milk following the dietary inclusion of DGP (Moate et al. Citation2014; Nudda et al. Citation2019). However, most studies have found no significant changes (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Chedea et al. Citation2017; Ianni et al. Citation2019; Bennato et al. Citation2022).
Milk fatty acid profile
A total of 77 FA was identified in the milk fat samples. To the best of our knowledge, this is the first report of such an extensive milk FA profile in goats fed with DGP. For this reason, the discussion will primarily reference previously published findings on ewes and cows.
The SFA were the most important group from a quantitative point of view in milk fat and did not differ between treatments (p > 0.05) (Table ), in agreement with previous studies in ewes and goats (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Buffa et al. Citation2020). The levels of the short chain FA, butyric (4:0), caproic (6:0), caprylic (8:0) and capric (10:0), did not decrease in response to dietary DGP (p > 0.05), which is a favourable outcome. In the human diet, milk fat supplies nearly all the butyric acid, which has been found to confer numerous health benefits (Gómez-Cortés et al. Citation2018). Meanwhile, caproic, caprylic an capric acids are positively associated with the distinct 'goaty’ flavour characteristic of caprine milk, contributing to the organoleptic properties of the derived dairy products (Park Citation2017). Furthermore, short-chain FA contribute to the enhanced digestibility of caprine milk fat compared to that of bovine milk fat (Zervas and Tsiplakou Citation2013; Bernard et al. Citation2018). Again, the absence of changes in the contents of FA almost exclusively synthesised de novo in the mammary gland (6 to 14 atoms of carbon) would support that dietary DGP did not negatively affect rumen fermentation of carbohydrates (Moate et al. Citation2008). The absence of differences in the contents of palmitic acid (16:0) would suggest that the amount of DGP consumed by the goats did not elicit changes in methane yield (Moate et al. Citation2020; Requena et al. Citation2020).
Table 3. Saturated fatty acid contents (g/100 g of total fatty acid methyl esters) in milk fat from dairy goats fed a conventional diet (CON) or the same diet with 150 g of concentrate replaced by an equal amount of dried grape pomace (DGP).
The DGP treatment exhibited a reduced content of iso 17:0 (p < 0.05). This contradicts the findings of Manso et al. (Citation2016), who reported no change in the milk fat content of iso 17:0 in their low DGP treatment. However, those authors did observe a decrease of iso 17:0 when the proportion of DGP in the diet was doubled. It is worth noting that nearly half of the iso 17:0 in caprine milk fat could potentially derive from the extraruminal elongation of iso 15:0 in non-mammary tissues, while the other half likely originates from ruminal bacteria (Gómez-Cortés et al. Citation2019). In this regard, the elongation index of iso 17:0 did not differ between the treatments (0.53 ± 0.031; p > 0.05). Thus, a reduced availability of ruminal iso 17:0 iso to the mammary gland in the DGP treatment was more plausible in the present work than a reduced activity of the fatty acid elongase 6 (ELOVL6) in body tissues.
No differences were found in the milk fat content of MUFA between the treatments (p > 0.05) (Table ), as observed in previous studies (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Ianni et al. Citation2019). The most prominent MUFA group was 18:1 cis, which was predominantly (over 95%) comprised of 18:1 cis-9 (oleic acid). The content of this FA tended to be lower in the DGP treatment (p = 0.06), in agreement with other authors (Manso et al. Citation2016; Resconi et al. Citation2018). Vaccenic acid, 18:1 trans-10, and 18:1 trans-9 were not affected by dietary DGP (p > 0.05) and accounted for about 40%, 11% and 9% of total 18:1 trans FA, respectively. In previous research involving ewes and goats, no changes in VA and 18:1 trans-10 contents were observed following DGP inclusion in the diet (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Buffa et al. Citation2020; Bennato et al. Citation2022). However, 18:1 trans-9 has been reported to increase in these species (Manso et al. Citation2016; Buffa et al. Citation2020), and the levels of all three isomers rose in cows fed DGP (Moate et al. Citation2014; Ianni et al. Citation2019; Moate et al. Citation2020). Studies conducted in vitro and utilising animal models suggest that an increase in VA, along with no change or a decrease in the concentrations of 18:1 trans-9 and 18:1 trans-10 in milk fat, could be desirable from the point of view of human health (Wang et al. Citation2016; Vahmani et al. Citation2017; Song et al. Citation2019).
Table 4. Monounsaturated fatty acid contents (g/100 g of total fatty acid methyl esters) in the milk fat from dairy goats fed a conventional diet (CON) or the same diet with 150 g of concentrate replaced by an equal amount of dried grape pomace (DGP).
The minor isomers 18:1 cis-12, 18:1 trans-12 and 18:1 trans-13/trans-14, which are very related to the biohydrogenation (BH) pathways of α-linolenic acid (ALA, 18:3 n-3) in the rumen (Martínez Marín et al. Citation2015; Ferlay et al. Citation2017), exhibited divergent responses in milk fat (Table ). Specifically, there was a decrease of 18:1 cis-12 and an increase of 18:1 trans-12 and 18:1 trans-13/trans-14 (p < 0.05). Notably, Manso et al. (Citation2016) found no alterations in the levels of 18:1 cis-12 and 18:1 trans-12 in their low DGP treatment and an increase in these levels in their high DGP treatment, whereas the level of 18:1 trans-13/trans-14 showed the opposite pattern.
The content of palmitoleic acid (16:1 cis-9), the desaturation product of palmitic acid (16:0), was lower in the milk fat of the DGP treatment (p < 0.05) (Table ), which aligns with the findings of some authors (Moate et al. Citation2014; Resconi et al. Citation2018), but contrasts with the observations made by others (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Buffa et al. Citation2020). The desaturation index of palmitic acid tended to be lower in the DGP treatment (0.016 vs. 0.019 in the CON treatment; p = 0.08), which suggests a potential inhibitory effect on Δ-9 desaturase activity in the mammary gland with this treatment. A similar trend was observed by Manso et al. (Citation2016), but not by Tsiplakou and Zervas (Citation2008).
The content of 16:1 cis-7, the second most abundant 16:1 isomer after palmitoleic acid (Table ), was reduced in the DGP treatment (p < 0.05), consistent with the results of Manso et al. (Citation2016). Luna et al. (Citation2009) hypothesised that a significant proportion of 16:1 cis-7 in milk fat could result from the chain shortening of oleic acid via peroxisomal β-oxidation. The significant reduction in the shortening index of oleic acid found in the DGP treatment (0.014 vs. 0.016 in the CON treatment; p < 0.05), coupled with the trend towards a lower content of oleic acid in the same treatment, likely contributed to the observed decrease of 16:1 cis-7 content.
Total PUFA contents in milk fat were not affected by dietary DGP (p > 0.05) (Table ) in concordance with earlier research in ewes (Manso et al. Citation2016; Resconi et al. Citation2018). However, other authors have reported increases of milk fat PUFA in ewes, cows and goats fed DGP (Tsiplakou and Zervas Citation2008; Buffa et al. Citation2020; Ianni et al. Citation2019). Linoleic acid was the predominant PUFA (over 61% of total PUFA), followed by far by RA, the major conjugated linoleic acid (CLA) isomer, and ALA in almost equal amounts (11% and 10% of total PUFA). The milk fat content of LA, despite LA was the most abundant individual FA in DGP lipids (Table ), as well as that of ALA were not affected by dietary DGP (p > 0.05), which is in line with previous observations of Tsiplakou and Zervas (Citation2008) in goats.
Table 5. Polyunsaturated fatty acid contents (g/100 g of total fatty acid methyl esters) in the milk fat from dairy goats fed a conventional diet (CON) or the same diet with 150 g of concentrate replaced by an equal amount of dried grape pomace (DGP).
Dietary DGP reduced the content of RA in milk fat by 16.5% (p < 0.05) (Table ). This result was unexpected because a common finding in previous studies with ewes and goats is the absence of changes in RA contents (Tsiplakou and Zervas Citation2008; Manso et al. Citation2016; Buffa et al. Citation2020; Bennato et al. Citation2022), while an increase has been reported in dairy cows (Moate et al. Citation2014; Ianni et al. Citation2019; Moate et al. Citation2020). The VA desaturation index was not different between treatments in the present work (0.30 ± 0.029; p = 0.11), thus it was likely that RA from direct ruminal origin was diminished in the DGP treatment. Since RA in the rumen originates from the incomplete BH of available LA (Martínez Marín et al. Citation2015; Ferlay et al. Citation2017), it might be hypothesised that LA in the DGP fed in the present work was not fully accessible to rumen bacteria due to its encapsulation in uncrushed seeds (Guerra-Rivas et al. Citation2017), that the amount of consumed tannins was too low to affect BH (Carreño et al. Citation2015), or both. The RA in human nutrition has raised great interest over the last decades due to its potential benefits for human health (Bauman et al. Citation2020). Chromatographic column and conditions allowed the identification of other minor CLA isomers (de la Fuente et al. Citation2006; Kramer er al. Citation2008), but their contents were not affected by dietary DGP (Table ).
The minor isomers, 18:2 trans-9,trans-12 and 18:2 trans-11,cis-15, that are related to the ruminal BH of ALA (Martínez Marín et al. Citation2015; Ferlay et al. Citation2017), exhibited a common positive response to dietary DGP (p < 0.05), while none of the long chain PUFA was affected (p > 0.05) (Table ). These results agreed with the observations of Resconi et al. (Citation2018) and Manso et al. (Citation2016), except for 18:2 trans-9,trans-12. Conversely, Buffa et al. (Citation2020) observed a reduction of 22:5 n-3 and 22:6 n-3 contents in their DGP treatment. The long-chain PUFA, eicosapentaenoic (20:5 n-3), docosapentaenoic (22:5 n-3) and docosahexaenoic (22:6 n-3) acids, play an important role in human health by reducing the risk or severity of several chronic diseases (Calder Citation2018).
Conclusions
Feeding dairy goats a diet that included up to 6% DGP did not exhibit any negative effect on milk yield, milk composition, or the contents of most of the nutritionally relevant milk FA, in comparison with a conventional diet. The utilisation of grape pomace in goat feeding would provide an environmentally friendly way for its disposal that could potentially enhance the sustainability of goat farming without compromising the quality or cheese-making properties of the milk produced. The observed negative effect on RA content deserves further research.
Ethical approval
Ethical approval was not needed according to EU regulations because the experimental procedures were not likely to cause pain, suffering, distress or lasting harm equivalent to, or higher than, that caused by the introduction of a needle in accordance with good veterinary practice.
Acknowledgements
This paper is the result of a research stay of Andrés L. Martínez Marín at the Department of Veterinary Sciences of the University of Turin (Italy). The authors gratefully thank the farmer, Dr. Aurelio Ceresa, for technical assistance and care of animals, Mrs. Vanda Maria Malfatto (DISAFA, Turin, Italy) for the chemical analysis of feedstuffs, and Dr. Miguel Angel de la Fuente (CIAL, Madrid, Spain) for the comments and critical lecture of the manuscript.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
The data that support the findings of this study are available from the corresponding author, [A. L. M. M.], upon reasonable request.
Additional information
Funding
References
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