https://orcid.org/0000-0003-0533-3763
Abstract
Advances in foodomics have demonstrated the feasibility of detecting specific molecules, known as ‘foodomes’, that can serve as biomarkers in fresh meat and dairy products to identify the origin of feeding foods. Identifying these biomarkers is crucial to establish traceability, as consumers demand products of guaranteed quality. In this work, after conducting an exhaustive review of the most relevant scientific documents from the last twenty years, we present a collection of as many as 76 and 66 lipidomes, 42 and 14 metabolomes, 53 and 61 volatile compounds and 8 and 4 isotope ratios (from fresh meat and dairy products, respectively) as potential biomarkers to determine feeding regime in farm ruminants (e.g. fresh herbage, conserved forage or concentrate). CLA9cis-11trans, stearoyl-CoA desaturase, toluene, skatole, and δ13C and δ15N have been widely cited in scientific research to determine the feeding system in ruminants. A combination of these biomarkers with mathematical techniques (discriminant analysis and machine learning) could be used to determine origin and quality in meat and dairy products from ruminants.
1. Introduction
Currently, a significant number of consumers prefer to purchase meat and dairy products from animals raised on pasture or grass (Basdagianni et al., Citation2019), rather than from more intensive production systems where the animal feed is based mainly on the use of concentrate. This is partially due to the fact that consumers perceive meat products and dairy production systems, obtained using grass/pasture, as having favourable ethical and environmental implications, sensory and nutritional quality and associated health benefits (Parlasca & Qaim, Citation2022). The beneficial health effect of consuming meat from grass fed animals has been widely shown, mainly due to the evident reduction of total saturated fatty acids content and n-6/n-3 ratio and the increase of total polyunsaturated fatty acids when compared to other types of feeding (Battacone et al., Citation2024). Moreover, the use of labels indicating the designation of local origin such as the protected designation of origin (PDO) or protected geographical indication (PGI), or quality trademarks, has gained considerable importance in both meat (Bernabéu et al., Citation2018) and dairy (Zhu et al., Citation2021) markets in recent years. For this reason, mechanisms to identify the provenance of meat and dairy products are in high demand from both industries and consumers.
Recent advances in foodomics have shown the possibility of identifying certain molecules, which can be used as biomarkers to identify the distinctive signatures of food products depending on their origin. In fact, the detection and quantification of specific biomarkers using different laboratory analytical methods can be used to classify, identify, diagnose or determine the origin of animal foods from specific regions that have undergone specific production processes (Munekata et al., Citation2021). Such analytical techniques, including lipidomics, metabolomics, proteomics, volatilomics and stable isotope analysis, have evolved rapidly in recent years (Chen et al., Citation2019) due to their potential to provide comprehensive and accurate results with non-invasive methods. These emerging techniques have been successfully applied in the investigation of medical processes, in the field of food sciences and, specifically, in the area of quality assessment in meat and dairy products (Levy et al., Citation2019).
As mentioned, several of the analytical techniques used for biomarkers identification have become crucial for the assessment of food quality and authenticity. For instance, gas chromatography (GC) and liquid chromatography–tandem mass spectrometry (LC–MS/MS) technologies are used to characterise fatty acid profiles (the field of lipidomics) (Ashokan et al., Citation2021). O’Callaghan et al. (Citation2018), proposed proton nuclear magnetic resonance (NMR) techniques to identify metabolites (metabolomics). These technologies can also be used to identify proteins and peptides (proteomics) (Ribeiro et al., Citation2020b) in combination with colorimetric and electrophoretic techniques (Rysova et al., Citation2021). Volatile biomarkers (volatilomic analysis) are preferably profiled by GC coupled to mass spectrometry (MS) combined with NMR spectroscopy (Shang et al., Citation2022). Moreover, isotope ratios determined by inductively-coupled plasma followed by mass spectrometry (ICP-MS) are also commonly used for origin authentication in animal foods (Camin et al., Citation2016). All of these analytical techniques have been applied to detect fraud related to the origin of animal food production. In fact, important efforts to obtain novel analytical technologies are being made by governments to prevent fraud and achieve a more transparent market in essential foods such as cereals, meat or dairy products (Sentandreu & Sentandreu, Citation2011), or to guarantee and trace the production of animal foods. In this context, the profile of biomarkers found in meat or dairy products can be used as a tool to trace production systems in farm ruminant based on fresh grass, preserved grass or concentrated feed.
The aim of this review was therefore to compile a comprehensive overview of the available literature about the most recent advances in food-omics (lipidomics, metabolomics, proteomics, volatilomics and stable isotope analysis), in order to identify and propose potential biomarkers in fresh meat and dairy products that can be used to determine the origin and feeding system in farm ruminants (i.e. bovine, ovine and caprine).
2. Meat and dairy biomarkers and feeding systems in ruminants
2.1. Lipidic biomarkers
Among all omics studies, lipidomics aims to identify and quantify the lipids in biological organisms, and has been considered an essential tool for many applications in the field of food control, such as investigating the geographical origin of dairy and meat products (Li et al., Citation2017), identifying on-farm animal feeding regimes, or assessing the authenticity of food products (Shang et al., Citation2022).
For instance, Wang et al. (Citation2021), proposed an untargeted lipidomic method, based on ultra-performance liquid chromatography quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF/MS) combined with chemometric analysis, to investigate the lipid differences between meat from sheep and goats reared intensively on pasture or concentrate. Discriminant analysis was then conducted to identify specific potential biomarkers and a total of 20 lipids were selected to differentiate between meat from pasture-fed or concentrate-fed systems (more details in ).
Table 1. An overview of lipidomes suggested in the literature as biomarkers in fresh meat and dairy products to authenticate feeding system origins in ruminants.
Fatty acid (FA) profiles in animal food products are closely associated with the animals’ dietary composition. FA profiles in meat and dairy products have therefore been used as a practical means of providing information on animal feeding regimes and to track the origin of food products from different production systems (Qie et al., Citation2021). Researchers have already reported the use of a single FA, or a set of FAs, extracted from meat from young bulls (Dias et al., Citation2008), lambs (Juarez et al., Citation2010) or goats (Mellado-González et al., Citation2009), to identify different feeding regimes. Martínez et al. (Citation2013) distinguished beef samples from different types of finishing diet based on ten FAs from intramuscular fat in bulls. Based on the literature consulted, shows several lipid biomarkers in meat and dairy products used to identify feeding patterns (fresh herbage, conserved forage or concentrate) in the categories of bovine, ovine and goats.
2.1.1. Saturated fatty acids
Compared to monogastric animals, ruminant meat is characterized by having a high content of saturated fatty acids (SFA), which make up around 30–40% of the total FA. This is because in the rumen, microbes largely hydrogenate the unsaturated fatty acids (UFA) in the feed into SFA (Vahmani et al., Citation2020).
In general, a decreased percentage of SFA in meat and dairy products can be expected when grass is included in animal’s diet. Recently, Cabiddu et al. (Citation2022), analysed several metadata from Scopus databases from cows and sheep and specifically showed a reduction of around 5% in SFA as a percentage of the total fatty acids detected in fresh meat and dairy products when fresh forage was used in the diets. In fact, after extensively collecting metadata, a general reduction of 0.1% SFA was recorded in dairy bovine and ovine products for each unit increase in fresh herbage in their diet. Regarding SFA C16:0, Cabiddu et al. (Citation2022), described a reduction of 5–10% in meat and milk in diets including fresh herbage compared to conserved forage feeding systems. These results are in line with Daley et al. (Citation2010), who reported slightly higher values of 16:0 and 14:0 FA in beef from concentrate-fed animals. However, this observation is not evident in C18:0. In fact, Elgersma (Citation2015) reported an increase in C18:0 content in meat from animals fed with conserved forage (hay or silage) or fresh herbage compared to concentrate, probably due to the high specific activity of ruminal microorganisms in converting C18:1 to C18:0.
2.1.2. Monounsaturated fatty acids
Moreover, monounsaturated fatty acids (MUFA), specifically the isomers of C18:1 (C18:1trans11 and C18:1cis9), can also be used as lipid biomarkers to identify the origin of meat or dairy products based on the feeding regime. In fact, Cabiddu et al. (Citation2022), reported an increase of around 9% in the MUFA content of dairy products when fresh herbage was included in the cattle’s diet, while no significant effect was observed in fresh meat. C18:1trans11 is one of the most commonly used lipid biomarkers in dairy cow products, and controlled trials have reported consistent increases of C18:1trans11 content, ranging from +150% to +478%, when fresh herbage is included in the ruminants’ diet (Daley et al., Citation2010). On-farm feeding practices have also shown an increase of 72% and 59% in C18:1trans11 in dairy cow products and lamb meat, respectively, when fresh herbage is included in the animals’ diet (Cabiddu et al., Citation2022). These results are consistent with those reported by D’Urso et al. (Citation2008) in goats raised with free access to pasture, which showed a significant increase in C18:1trans11 and C18:1cis9 content in milk compared to goats raised indoors with concentrate and alfalfa hay during lactation.
A higher C18:1cis9 content has also been reported in dairy animal products from fresh herbage intake in cattle (Lopez et al., Citation2022). Using a large on-farm metadata set, Cabiddu et al. (Citation2022), reported a 7% increase in C18:1cis-9 content in dairy cattle products, with an estimated linear increase of 0.2% in C18:1cis9 in dairy products for each unit increase in the proportion of fresh pasture herbage in the diet. However, the influence of fresh pasture herbage on C18:1 content in fresh meat remains unclear. While Cabiddu et al. (Citation2022) reported no significant differences in C18:1cis9 content from cattle between fresh meat based on using fresh herbage or conserved forage (hay and silage), Margetín et al. (Citation2018) found that the proportion of C18:1cis9 in meat from grazing lambs was higher than meat from lambs fed on diets including concentrates.
Regarding dairy goat products, Mancilla-Leytón et al. (Citation2013) observed few significant differences and trends in MUFA percentage between concentrate and fresh pasture herbage feeding models in Payoya dairy goats. In fact, from the ten total MUFAs detected in milk, only C20:1n-9 was higher in Payoya dairy goats raised using concentrate compared to grazing.
2.1.3. Polyunsaturated fatty acids
A significant proportion of the lipid profile in ruminant fresh meat and dairy products consists of polyunsaturated fatty acids (PUFA) (Santos-Silva et al., Citation2023). Several studies have reported an increase in PUFAs, particularly n-3 PUFA, in fresh meat (Wood et al., Citation2003) and dairy products (Ponte et al., Citation2022) from animals raised on grass herbage diets. Consistent with the findings of Keller et al. (Citation2022) in beef, the influence of diet on the content of C18:2trans11, cis15; C18:2n-6; C18:3n-3; C20:4n-3; C20:5n-3; C22:4n-6; C22:5n-3; and C22:6n-3 can be observed with increasing dietary amounts of grass silage. Furthermore, according to Zárate et al. (Citation2017), the proportions of the nutritionally valuable long-chain C20:5n-3 and C22:6n-3 increase when the amount of dietary grass and/or grass silage is increased in the diet. References in ovine fresh meat have reported higher proportions of PUFAs, including C20:4, C20:5n-3, C22:5n-3, and C22:6n-3 FAs, in meat from lambs raised on pasture compared to concentrate-fed sheep (Margetín et al., Citation2018).
Cabiddu et al. (Citation2022) reported a significant increase in the content of C18:3n-3 (around 41% and 73% in dairy products and fresh meat cow, respectively) based on on-farm feeding practices using fresh herbage or conserved forage diets. In fact, the content of C18:3n-3 was seen to increase by 1.1% per unit increase in the proportion of fresh herbage in the animals’ diet (Elgersma, Citation2015), since C18:3n-3 is the major FA in fresh herbage, and can be efficiently transferred to animal products as it is allocated to cell membrane lipids (Buccioni et al., Citation2012). However, as regards C18:2n-6, Cabiddu et al. (Citation2022) found that the content of C18:2n-6 decreased linearly by 0.2% per unit increase in the proportion of fresh herbage in the animals’ diet. Controlled trials conducted by Mancilla-Leytón et al. (Citation2013) in goats reported similar results.
In goat milk, Mancilla-Leytón et al. (Citation2013), observed significantly higher percentages of nutritionally desirable FA (such as C20:5n-3 and total n-3 PUFA) from goats raised in a free-range grazing group compared to those raised using a mixture of alfalfa hay, pea straw, and supplementary concentrate. Additionally, the C18:2n-6 cis and total n-6 PUFA was significantly lower in the free-range grazing group compared to the conserved forage group.
Conjugated linoleic acids (CLA) are a PUFA group found in meat and dairy products from ruminant animals and have been reported to have health benefits for humans. Patino et al. (Citation2015), reported a 50% and 94% increase in CLAcis9 trans11 content in meat and dairy cow products, respectively, with the inclusion of fresh herbage in animal diets. Similarly, Coppa et al. (Citation2015a), reported consistent increases in dairy products from cattle raised with an increase in fresh herbage intake, with a linear range increase of 0.7% for C18:2 cis9 trans11, leading to an increase in CLA content of 177% to 380% under on-farm conditions. The proportions of CLA were also found to be three times higher in pasture-raised French ovine meat (Margetín et al., Citation2018) and milk (Scano et al., Citation2020). According to Bohui et al. (Citation2018), the CLA contents in pasture-grazed meat were significantly higher than conserved forage-fed meat, due to the abundance of Fibrobacter, Ruminococcus, and Alistipes bacteria found in pasture-grazed ruminants. Moreover, studies have reported that animal diets could induce variations in mammary stearoyl-CoA desaturase activity in the synthesis of CLA 9cis-11trans (Toral et al., Citation2021).
2.1.4. Glycerides, terpenoids, carotenoids and fat-soluble vitamins
Glycerides are esters formed from glycerol molecules, which can be esterified with one, two, or three FAs to form mono- (MG), di- (DGs), and triglycerides (TGs), respectively. Such molecules are used as an energy reservoir stored in the adipocytes. The use of TG profiles to verify the origin of butter from cows fed with fresh grass or concentrate in a conventional production system was proposed by Pustjens et al. (Citation2017). The results showed that seven TGs (CN24; CN28; CN40; CN44; CN46; CN48, and CN54) detected in butters made with organic milk from pasture-raised animals differed significantly from their conventional counterparts made using milk from conventional animals raised on concentrate.
Terpenoids, carotenoids and fat-soluble vitamins are a complex variety of lipids present in herbage. Terpenoids (monoterpenes and sesquiterpenes, with 10 and 15 carbon atoms, respectively) are the main components of plant essential oils and are derived almost exclusively from the secondary metabolism of the plant (Tornambé et al., Citation2006). Carotenoids are fat-soluble pigments of plant origin that animals cannot synthesize, although they can partially modify them. These compounds are of considerable importance for their biological function as pro-vitamin A (Granado-Lorencio et al., Citation2017). Grass and grains contain different proportions and concentrations of four fat-soluble vitamins (A, D, E and K). Among these, vitamin E, also called α-tocopherol, is shown to be the main antioxidant agent against the oxidative deterioration of myoglobin in meat (Tansawat et al., Citation2013). Overall, β-carotene and α-tocopherol, together, are natural antioxidants that play a role in maintaining redness in meat (Salim et al., Citation2022).
Plant biomarkers found in dairy products, such as terpenes and phenolic compounds, seem to be a promising approach for the authentication of pasture-derived milk and cheeses, especially those produced on highly bio-diversified upland pastures (Valdivielso et al., Citation2017). Terpenoids are volatile lipid compounds produced as secondary plant metabolites, which can be transferred directly from herbage to milk and meat (Tornambé et al., Citation2006). In controlled trials, some of these compounds were lost early during forage harvesting and storage, resulting in a lower terpene content in meat and dairy products derived from animals fed with preserved forage (Cabiddu et al., Citation2019). In fact, in controlled diet trials including preserved forage, the monoterpene and total terpene content was reduced in dairy products by around 9%, when compared to cattle fed on fresh herbage.
Probably, the use of carotenoids as biomarkers to identify feeding diets is much more relevant for dairy products than for fresh meat. Several reports (Chudy et al., Citation2022; Șanta et al., Citation2022) refer to the suitability of using β-carotene in the milk from goats, sheep and cows to differentiate feeding regimen based on the use of fresh grass from those using different types of diets (e.g. preserved foods, by-products or concentrates). However, for fresh meat, the references are scarcer (Mateo et al., Citation2023). Frequently, carotenoids and fat-soluble vitamins are evaluated together as possible origin biomarkers of animal products, because both compounds are closely related, as some carotenoids function as precursors of vitamin A in mammals (e.g. retinol and retinyl esters) (Stephenson et al., Citation2021). The switch in diet from grass silage to hay induced a rapid decrease in the concentration of β-l-carotene and vitamin E in milk. Therefore, the efficient extraction and accurate quantification of β-carotene and its metabolites is crucial for the authenticity and traceability of milk products. High Performance Liquid Chromatography/Mass Spectrometry (HPLC/MS) has been used to show that β-carotene could be used as a distinctive biomarker for the origin of cows’ milk, while retinol, retinaldehyde, retinoic acid and abscisic acid are better for authenticating goat milk (Zhang & Jia, Citation2022).
In sheep-derived dairy and meat products, sheep raised on fresh herbage diet had increased levels of all carotenoids (α-tocopherol, retinol, β-carotene, lutein and zeaxanthin) compared to conserved grasses (Cabiddu et al., Citation2022). According to Nozière et al. (Citation2006), this is due to the fact that carotenoids are preserved in fresh herbage, while a photo-degradation effect can be observed during forage harvesting and drying. For instance, an increase of 30% for α-tocopherol, 41% for β-carotene, 45% for zeaxanthin, and 63% for lutein was observed in dairy cow products when fresh herbage was included in the animals’ daily feeding regime. As reported by Cabiddu et al. (Citation2022), the α-tocopherol and β-carotene content increased in cows’ milk by 0.9% and 1.8%, respectively, per unit increment in the proportion of fresh herbage in the animals’ diet. In Mediterranean dairy goats, a much larger increase in α-tocopherol content in milk (approximately 480%) was reported and a similar increment was noted for retinol content. Also, the inclusion of fresh herbage in the animals’ diet led to a 73% increase in α -tocopherol content in sheep’s meat.
Vitamin E is a lipid family of eight natural compounds (α, β, γ, and δ-tocopherols, and α, β, γ, and δ-tocotrienols) with a well-known antioxidant capacity in foods (Descalzo & Sancho, Citation2008). The most active forms are α-tocopherol and γ-tocopherol isoforms, which are widely distributed in grass and are often used in vitamin supplements. The effect on vitamin E content in meat of gradual increments of grass silage in the diet of Limousin × dairy breed crossbred bulls was studied in animals slaughtered at a body weight of 520 kg (Keller et al., Citation2022). Even though the vitamin E content in the grass was higher than in the concentrate, the total vitamin E content in the fresh meat remained unaffected by the diet. However, in 21-day-old meat, higher contents of vitamin E were found from animals raised with high grass silage diet than from animals raised mainly on concentrate diet. This observation is in line with the previous report by Warren et al. (Citation2008), who observed an increase in vitamin E content in the plasma and muscle of Aberdeen Angus crossed with Holstein-Friesian, when increased proportions of grass silage were included in the animals’ diet. Similar results were reported by Gatellier et al. (Citation2004), who showed that the concentration of vitamin E in muscle was significantly higher in grass-fed Charolais cattle than in concentrate-fed animals.
According to Keller et al. (Citation2022), the animals’ diet also affected the γ-tocopherol content in fresh and aged beef. In contrast to the way vitamin E acts in fresh meat, after the meat had been aged for 21 days, γ-tocopherol content were higher in meat from animals raised on concentrate than meat from cattle raised on a diet high in grass silage.
The α-tocopherol and retinol that appear in ruminants’ milk mainly originate from the animals’ diet. Roncero et al. (Citation2021) proposed these compounds as potential traceability biomarkers in goat milk from the Payoya breed, to give consumers a guarantee of the system in which these animals were raised and fed. The results of the analysis using retinol concentrations in plasma and milk and α-tocopherol in plasma as variables showed that differences between management regimes (pasture grazing versus total mixed diet) and sampling times could be observed in the contents of retinol and α-tocopherol.
Recently, a high-resolution technique using the Rapid Evaporative Ionisation Mass Spectrometry (REIMS) has been proposed successfully to identify lipid compounds in lambs’ meat specifically related to different diets. In fact, Zhang et al. (Citation2022), using REIMS reported that glycerolipids and glycerophospholipids were the two key lipid groups driving the differences between permanent pasture and mixed pasture diets with concentrate. In weaning lambs, phospholipids (including sphingolipids and glycerophospholipids) were the main lipid molecules found to be more abundant in mixed diets compared to grass diets (Zhang et al., Citation2022).
2.1.5. Lipid biomarkers general overview
Traditionally, chromatography techniques have been used to identify lipid molecules in fresh meat and dairy products. Now, these techniques are becoming more robust and more accurate, with lower limits of detection.
Advances in chromatography techniques are making it possible to successfully identify new specific molecules in animal derived products that can be used to identify the feeding diet of animals. Additionally, advances in our knowledge of the digestive processes of ruminants has enabled us to identify specific molecules that are generated by the complex bio-hydrogenation systems in animals’ digestive tract when grass is included in their diet. Therefore, unlike the case of non-ruminant animals, these molecules are key in identifying the origin and composition of bovine, ovine or goats’ diets. Among them, the isomers of conjugated linolenic acid (e.g. CLA9cis-11trans) and other monounsaturated fatty acids (e.g. C18:1cis9; C18:1trans11) are of special relevance, since these have been frequently proposed as potential origin biomarkers; meanwhile, saturated fatty acids are less obvious biomarkers. In particular, recent advances in the identification of complex lipid molecules through the combination of different analytical techniques (GC/HPLC/MS-MS) have allowed the identification of new molecules present in the grass (e.g. α-tocopherol or β-carotenes) that provide information about the origin of ruminant nutrition. These novel techniques are being successfully incorporated into the food production industry and could be used as a tool to guarantee control and traceability plans in the production of meat and dairy products from ruminants.
2.2. Metabolomic and proteomic biomarkers
2.2.1. Metabolomics
Metabolomics is an omics tool that focuses on small hydrophilic molecules/metabolites (also known as metabolomes) that are found in foods and produced through the cellular metabolism. In recent years, small molecule metabolites have been identified and quantified in cells, tissues and biological fluids and metabolomics is widely used in nutritional and livestock research (Scuderi et al., Citation2020). In fact, its application in livestock has mainly been directed towards detecting disease, as well as the assessment of meat and dairy production. summarizes, considering the differences among feeding regimes, the list of metabolomic biomarkers collected in fresh meat and dairy products to authenticate feeding diets in ruminants.
Table 2. An overview of metabolomes and proteomes suggested in the literature as biomarkers in fresh meat and dairy products to authenticate feeding system origins in ruminants.
The metabolomic approach has mainly been used in dairy production to identify candidate biomarkers to assess the differential properties of dairy products and to detect fraud based on species, sensory properties or rearing and production systems. Meanwhile, the metabolomic approach is usually used in meat products to assess product quality by detecting irregularities, or to obtain a better knowledge of the underlying processes and changes in the molecular compounds that could be related to differences in tenderness, marbling, sensory properties, differences between species, or aging conditions. However, despite the fact that different animal feeding regimes have been explored, until now, few metabolomic studies have explored the biomarkers and metabolic processes in ruminant meat in relation to different feeding or rearing systems.
In a mini-review reported by Munekata et al. (Citation2021), several metabolites such as polyphenols, sugars, organic acids, amino acids, vitamins, and minerals were reported in animal products. They concluded that these compounds, which originate from the endogenous metabolism or from the ingestion of exogenous foods, can directly reflect the present and past metabolic processes occurring in a food product. Those compounds then could be used as biomolecular markers in fresh meat or dairy products. For example, Lana et al. (Citation2015), proposed that glutamate, serine and arginine could serve as good predictors of key meat quality attributes (e.g. tenderness or water holding capacity) during meat aging from Piedmontese culled cows. On the other hand, Subbaraj et al. (Citation2016) reported that primary metabolites (i.e. amino acids, sugars, nucleotides, nucleosides, organic acids and their breakdown products) could be identified as biomarkers to estimate aging time in lamb meat.
O’Callaghan et al. (Citation2018), using the modern technology of 1H-NMR combined with multivariate analyses, observed that milk from pasture-based feeding regimes was shown to have significantly higher concentrations of potential biomarkers such as p-cresol (a product of microbiome metabolism) and formate (a substrate compound for methanogenesis) than milk from a concentrate diet. Moreover, when a total mix ration (silage and concentrate) was used in cow feed, a significantly higher content in choline and succinate (a product of carbohydrate metabolism) production was observed than with milk from pasture diet. On the other hand, a higher content of urea milk and hippuric acid was observed in the pasture-derived milk.
A previous study by Saleem et al. (Citation2012), highlighted the correlation between the inclusion of cereal grains in the ruminants’ diet and high levels of metabolomes such as methylamines and putrescine in the rumen. This increase in methylamines and putrescine has been associated with unfavourable effects on rumen health. Conversely, a diet primarily composed of pasture has been shown to enhance rumen health and promote milk production. More recently, the application of advanced technology, specifically an untargeted metabolomic approach using UPLC-QTOF in conjunction with chemometric analysis, has brought attention to the potential of various MS/MS fragments. These fragments are derived from five amino acids (L-proline, L-glutamine, methionine, L-phenylalanine, tryptophan), three amino acid derivatives (pyroglutamate, methylhistidine, acetylcarnitine), creatine, two small peptides (carnosine, anserine), two nucleic acids (IMP, hypoxanthine), nicotinamide, and carnitine. All the above have been identified as potential biomarkers that can differentiate between ovine and goat meats produced from pasture and concentrate feeding regimes (all the fragments can be consulted in Wang et al., Citation2021).
2.2.2. Proteomics
The term proteome (proteomic biomarker) refers to the complete set of proteins expressed by a genome, cell, tissue, or organism at a specific time. The application of proteomics in the identification of biomarkers in meat or milk is not limited to the expression of proteins from a single cell type or tissue, but it also involves examining the protein composition of milk or meat-based products and sub-fractions thereof (Baldassini et al., Citation2022). Taking this into account, provides a comparative summary of the proteomes that have been chosen to authenticate feeding regimes in ruminants for fresh meat and dairy products.
Among other purposes, there are also common references on the use of proteomics in meat to focus on meat sensory qualities, such as tenderness (Picard & Gagaoua, Citation2020), colour and related proteolytic patterns (Della Malva et al., Citation2022). Since the technology of proteomics is advancing apace, there is a growing number of references to documents reporting on the evaluation of the origin of meat or dairy products using proteomic biomarkers. In fact, fresh meat proteomic techniques have been reported which are based on the use of spectrophotometry to quantify how the activity of glycolytic enzymes affects the proteolytic pattern of meat after ageing with different dietary supplementation systems (Mezgebo et al., Citation2017), while proteomics is being applied mainly to detect unknown adulterants in dairy products using HPLC or electrophoresis technology, among other techniques (Qin et al., Citation2022). In this context, sarcoplasmic protein profiles are commonly used in meat products (Della Malva et al., Citation2022), while a quantitative proteomic technique based on data-independent acquisition is often used in milk products to analyse differentially expressed caseins (O’Callaghan et al., Citation2018).
In a study conducted by Scuderi et al. in 2020, the researchers examined the influence of short-term pasture grazing, specifically focusing on the milk proteome in cows, including the impact of annual forage crops. Their findings revealed that the composition of both the milk fraction and the fraction associated with the milk fat globule membrane were influenced by the specific type of grazing, whether it involved the presence or absence of annual forage crops. Using liquid chromatography–tandem MS analysis (LC–MS/MS), the researchers identified 443 proteins in the milk, including αS1-casein and 8 low-abundance proteins such as β-2-Microglobulin, Polymeric immunoglobulin receptor, Acetyl-CoA carboxylase 1, Aminopeptidase, Mucin-16 isoform X4, Volume-regulated anion channel subunit LRRC8C, Elongation factor 2, and an Oncostatin-M-specific receptor subunit β precursor. Milk from cows grazing on grass–legume herbage and conserved forage crops had a higher concentration or abundance of these proteins compared to milk from cows grazing only on grass–legume herbage. These findings suggest that several proteomes in milk could be used as biomarkers of the origin of feed in cows (see ).
In 2017, Gagaoua et al. (Citation2017), conducted a proteomic analysis of beef from French PDO Maine-Anjou cows that were fed on either grass herbage or conserved forage in North-Western France. The study revealed that Superoxide dismutase (SOD1) and αB-crystallin, quantified by Dot-Blot, were the only proteins to be more abundant in grass herbage compared to conserved forage feed systems. Conversely, Mysoin heavy chain IIx (MyHC-IIx) was found to be higher in the conserved forage group than in the grass-fed group. These findings provide further evidence that the impact of animal feeding regimes on meat quality are influenced by sophisticated biological processes that are finely orchestrated during the animal’s life.
Supplementing the diets of farm ruminants with various additives is a common practice aimed at reducing production costs and improving the quality of meat. Some of these practices may have implications for the proteomics of meat. For instance, lambs fed on a basic diet supplemented with sea buckthorn pomace exhibited an increase in Akt/mTOR signaling activity, and a downregulation of myostatin expression, which led to a decrease in shear force in the resulting meat (Qin et al., Citation2020). Additionally, lambs fed on a diet that included Cistus ladanifer L. had higher levels of glycolysis pathway proteins and Fe-carrying proteins in their muscle tissue compared to those raised on concentrate. The inclusion of Cistus ladanifer L. in the lambs’ diets also resulted in a higher abundance of hepatic flavin reductase and FA synthase in adipose tissue than in concentrate-fed lambs (Ribeiro et al., Citation2020a).
The proteome basis for biological variations in the tenderness of meat from crossbred steers (Angus × Nellore) was reported to be affected by different feeding regimes (feedlot and pasture-finished), with sixteen proteins showing altered abundance levels (Antonelo et al., Citation2022). Specifically, triosephosphate isomerase (TPI), phosphoglucomutase-1 (PGM1), and phosphoglycerate kinase 1 (PGK1) were overabundant in beef raised in high-growth-rate indoor conditions, while troponin T (TNNT3), α-actin (ACTA1), myosin regulatory light chain 2 (MYLPF), PGM1, fosfoglicerato mutasa 2 (PGAM2), and anexina 2 (ANXA2) were overabundant in beef from cattle finished on pasture (see ). These results suggest that ANXA2, MYLPF, PGK1, PGM1, PGAM2, and TNNT3 could be proposed as potential biomarkers for beef tenderness in relationship origin feeding diet of animals.
2.2.3. Proteomic and metabolomic overview
To date, in terms of food production for human consumption, efforts to identify metabolomic and proteomic biomarkers have been focused primarily on detecting fraud in the origin of food and finding correlations between the targeted molecules and the organoleptic and sensory properties of food. Indeed, research has identified biomarkers arising from metabolic pathways associated with carbohydrates, lipids, or proteins during the conversion of muscle into meat (such as glycogen, triglycerides, amino acids, nucleotides, or nucleosides), as well as in the production of dairy products (e.g. β-hydroxybutyrate, isocitrate, glucose, or p-cresol, among others), and these biomarkers have been used to characterize the technological processes involved in the manufacture of fresh meat and dairy products. However, the presence or absence of these molecules, to a greater or lesser extent in fresh meat or dairy products seems to be closely related to the content of the precursor compounds (sugars, lipids or proteins) that the animals have ingested. Hence, it appears plausible that these molecular biomarkers can be potentially employed in determining the dietary composition fed to the animals. Additionally, as previously shown in the context of lipid compounds, the rapid evolution of analytical technologies such as 1H-NMR or LC–MS/MS, which facilitate the profiling of metabolomes, specific proteomes, or peptidomes, have demonstrated their effectiveness and have potential for ensuring the traceability protocols in the beef, lamb, and goat meats and dairy production sectors. Here, novel perspectives focused on the use of metabolomes and proteomes as biomarkers have been introduced to guarantee the provenance of ruminant-derived food products.
2.3. Volatile compound biomarkers
In the realm of omics, the study of volatile compounds in food plays a crucial role in determining authentication. To analyse volatile compound profiles in foods, efficient modern techniques like solid phase microextraction (SPME) coupled with gas chromatography-mass spectrometry (GC–MS) are utilized. These techniques provide a comprehensive description of the volatile compounds present in food samples. The volatile compound profiles are typically intricate, but by employing multivariate data analysis, it becomes possible to identify specific biomarkers. For instance, these biomarkers can be used to characterize the quality of meat or dairy products (Pavlidis et al., Citation2019) and even to authenticate the animals’ diet (Lytou et al., Citation2019).
One particular method employed for the identification and differentiation of distinct volatile fingerprints in foods is headspace solid-phase microextraction, in combination with gas chromatography-mass spectrometry (HS-SPME/GC–MS). This method allows for the analysis and discrimination of various volatile compounds.
By applying multivariate statistical techniques to the results obtained, it becomes feasible to visualize, group, and classify the sample populations (Pavlidis et al., Citation2019). In , a comparative summary of the variations among feeding regimes is provided, along with a selection of volatilomic biomarkers specifically chosen to authenticate feeding diet in farm ruminant in fresh meat and dairy products. In general, several families of volatile compounds identified in fresh meat and milk products can be classified as follows: aldehydes, ketones, aromatic hydrocarbons, alcohols, furans, sulphur compounds, pyrazines, pyrroles and carboxylic acids (Vasta et al., Citation2007). Among these, branched-chain FA, lactones, aldehydes, indoles, 2,3- octanedione, terpenes and sulphur compounds showed a higher discrimination capacity for differentiating between feeding diets in ruminants (Abilleira et al., Citation2011). Some of these compounds (e.g. terpenes) are volatile components taken up directly into animal tissue, while others (e.g. skatole and indole) are produced during animal metabolism. Finally, other aromatic volatile compounds (e.g. sulphur compounds, and products of Maillard reactions or lipid oxidation) are formed when meat or milk are subjected to thermic treatment (cooking, pasteurization, etc.). Depending on the phenological stage of the grass and the proportion of fresh herbage or concentrate in livestock diets, the content of several volatile compounds could be affected in meat and milk. For example, Monahan et al. (Citation2018) identified four volatile compounds (skatole, 3-undecanone, cuminic alcohol, and 2-methyl-1-butanol) as biomarkers in beef that enabled discrimination between beef cattle fed on pasture and concentrate.
Table 3. An overview of volatilome compounds suggested in the literature as biomarkers in fresh meat and dairy products to authenticate feeding system origins in ruminants.
Meanwhile, in a study conducted by Vasta et al. (Citation2011), the researchers investigated the presence of specific volatile compounds in meat from Charolais × Limousin crossbred heifers as biomarkers for distinguishing their dietary sources. Their findings revealed that meat from heifers raised on a diet of concentrate exhibited significantly higher levels of decane, 2,2-diethyl, and furan, 2-pethyl compounds. Conversely, meat from animals fed on pasture demonstrated significantly elevated concentrations of 2-heptanol (alcohol family), toluene (hydrocarbons), furan, 2-ethyl (furans family), 3-undecanone (ketones), and skatole (etherocyclic compound) compared to meat from animals on a diet of concentrate. Extensive research conducted over the years, such as the work by Mottram (Citation1998), has also focused on identifying and characterizing the large number (>1,000) of volatile compounds responsible for the flavour of meat in various animal species. Recent advances in highly-sensitive equipment have enabled the discovery of new volatile compounds in meat and dairy products. According to a study by Priolo et al. (Citation2001), the complex diet of livestock has an impact on the volatile compounds found in both ovine and bovine meat. However, the specific components involved in these effects vary across different species. In ovine meat, the grass flavour is primarily influenced by branched-chain fatty acids (FAs), certain volatile compounds resulting from the oxidation of linolenic acid, and skatole. In contrast, in bovine meat, the role of skatole appears to be less significant compared to sheep meat, as beef contains lower levels of branched-chain FAs compared to lamb meat. Many studies, including those cited in , have highlighted the similar impact of livestock feeding diets on the volatile compound content of both lamb and beef. Vasta et al. (Citation2007) employed dynamic headspace GC-MS to analyse lamb meat and identified 204 volatile compounds, from which 33 were identified as potential biomarkers to distinguish between concentrate-fed and pasture-fed lambs. A leave-one-out cross-validation procedure demonstrated that the type of animal feeding regime had an impact on these 33 compounds. 22 of these compounds were tentatively identified, including two aldehydes (2-propenal and 2-methyl-propanal), five alcohols (ethanol, 1-butanol, pentan-1-ol, 1-hexanol, and 1-octen-3-ol), three alkenes (trans-2-octene, cis-2-octene, and 2-methyl-prop-1-ene), five alkanes (tridecane, tetradecane, pentadecane, dodecane, and heptadecane), two ketones (2-butanone and 2-propanone), three terpenes (menthol, lilial, and jasmal), one aromatic hydrocarbon (1,2-dimethyl-benzene), and one nitrogen compound (1-methyl-pyrrole), with 11 other compounds remaining unidentified. All of these discriminative compounds were found in higher concentrations in the meat of concentrate-fed lambs compared to pasture-fed lambs.
However, despite the ability of volatile compounds to differentiate between lambs reared on pasture and those finished on different diets involving concentrates, these differences did not significantly impact sensory quality. The variations were primarily attributed to higher levels of indole and skatole in concentrate-fed lambs when compared to lambs fed on conserved grass (Gkarane et al., Citation2019). The use of volatile biomarkers has also been demonstrated in ruminant fat tissues to distinguish between exclusive pasture and concentrate diets. Sivadier et al. (Citation2010) demonstrated the use of volatile compounds as biomarkers derived from sheep perirenal and subcutaneous fat to track the origin of pasture or concentrate. In total, 41 and 36 compounds were selected as volatile biomarkers, including terpenes, 2, 3-octanedione, and toluene, which can distinguish between grass and concentrate diets in lambs. Their results showed that 2, 3-octanedione and terpene compounds exhibited a ‘short’ persistence in these fat depots, while some, such as nonane, 1-pentene, hexadecane, 1-penten-3-ol, (Z)-4-heptenal, benzene, toluene, styrene, and ß-caryophyllene, displayed a ‘medium’ persistence, while a ‘long’ persistence was observed for 2, 3-and acetophenone. Performing discriminant analysis on ratios of biomarkers from the perirenal and subcutaneous fat seems to permit the correct differentiation of pasture and concentrate diets. However, Del Bianco et al. (Citation2021), found the effect of diet on the volatile profile in lamb perirenal fat to be generally limited. In fact, among 45 compounds detected in this tissue from Mediterranean lambs (Sarda × Comisana cross), only six volatile compounds were significantly affected by treatments using tannin extracts in feeding lambs. These were from lipid oxidation products (2-heptadecanone, tetradecanal, 1-octanol, octadecane, and γ-dodecalactone) and from tyrosine metabolism in the rumen (4-methylphenol).
Few references were found on volatile compounds in suckling kid goat meat. Unlike the bovine and ovine species, goat meat has lower content of volatile compounds, since goat meat is leaner and the vast majority of the volatile compounds originate from lipids and fat after a thermal treatment. Nevertheless, in the traditional practice of substituting natural milk for milk replacers to feed suckling Mediterranean goats, the main aldehyde, hexanal, was related to the use of natural milk, while hydrocarbons, such as hexane, were related to the use of milk replacers (Ripoll et al., Citation2019).
Indeed, the presence of volatile compounds in fresh meat and dairy products can be affected by animal feeding. These compounds can arise from a direct transfer from the feed or when endogenously metabolized by the animal through ruminal microorganisms (Coppa et al., Citation2011). Cheese quality, among other factors, depends on the characteristics of the milk, which is affected by several factors such as diet in goats (Lucas et al., Citation2008) or cows (Coppa et al., Citation2015b). The different floral compositions of grass can affect cheese quality by transferring volatile organic compounds from the grass to the milk and finally to the cheese (Giaccone et al., Citation2016). Some research has focused on how supplements in cows’ diets may modify the quantity and quality of herbage intake and the metabolic pathways that lead to the formation of volatile compounds in milk starting from the rumen, ultimately affecting cheese quality (Jenkins & McGuire, Citation2006). In 2016, Aprea et al. reported that alcohols (butan-1-ol, pentan-2-ol, 4-methyl-pentan-2-ol, hexan-1-ol, heptan-2-ol), aldehydes (hexanal, nonanal, benzaldehyde), ketones (diacetyl, heptan-2-one, undecan-2-one), lactone (δ-octalactone), carboxylic acids (acetic acid, butanoic acid, hexanoic acid, octanoic acid, nonanoic acid, decanoic acid), phenolic compounds (3-methylphenol, 4-methylphenol), monoterpenes (α-pinene, β-pinene, β-citronellene dimethyl, camphene, limonene), sesquiterpene (β-caryophyllene), and sulphur compounds (e.g. dimethyl sulphide) were less abundant in the headspace of cheeses from nutrient-poor pastures compared to nutrient-rich pastures, while the total content of esters (including ethyl acetate, ethyl butanoate, ethyl hexanoate, and ethyl octanoate) and one hydrocarbon (m-Xylene) was higher in cheeses from nutrient-rich pastures. An interesting finding emerged from the report by Aprea et al. (Citation2016) comparing low and high concentrate diets in sheep cheese production: cheeses from the diet low in concentrate showed a significantly higher content of volatile compounds compared to those from the diet with a higher proportion of concentrate. These volatile compounds included butan-1-ol, pentan-1-ol, 4-methyl-pentan-2-ol, hexan-1-ol, heptan-2-ol, benzaldehyde, butyrolactone, δ-octalactone, toluene, acetic acid, butanoic acid, octanoic acid, nonanoic acid, decanoic acid, phenol, 3-methylphenol, 4-methylphenol, 4-allyl phenol, β-caryophyllene, dimethyl sulphide, and dimethyl sulfone.
In a study conducted by Cabiddu et al. in 2019, it was observed that goat milk cheese derived from pasture-raised goats contained a higher concentration of volatile compounds compared to cheese from sheep that were fed in stalls. This difference can be attributed to the transfer of various volatile compounds present in the herbage to the milk, making them valuable biomarkers for distinguishing between milk sourced from grazed herbage and from sheep fed in stalls. In their research, Cabiddu et al. (Citation2019) identified terpinolene, triciclene, 3,7-dimethyl-1,6-octadiene, α-pinene, and camphene as biomarkers which were specifically indicative of milk derived from pasture diets, in contrast to sheep fed on conserved forage and in stalls.
Similar findings were reported in a study by Decandia et al. (Citation2007) concerning goat milk. The study revealed that ketones and aldehydes served as biomarkers for goat milk obtained from goats grazing on Mediterranean lentisk-based shrubland, as opposed to those raised under confined conditions with concentrate and hay feed. Additionally, Pizzoferrato et al. (Citation2007) identified phenols as biomarkers in goat milk sourced from goats which grazed on the same type of shrubland. These collective findings suggest that the composition of livestock diets can significantly influence the presence of volatile compounds in their milk, and these compounds can be employed effectively to distinguish between milk from different sources. In the case of lambs, several volatile compounds were proposed by Sivadier et al. (Citation2010) to identify lamb meat from pasture or concentrate feed (see ). Among these, compounds 1-octen-3-ol and 2,3-octanedionone were found to have the highest values in meat from pasture-fed animals compared to those fed on concentrate.
2.3.1. Volatile compound biomarkers overview
A huge variety of volatile compounds are generated during the cooking of meat products, depending on the cooking method itself and combinations of temperature and cooking time, since cooking temperature can affect the generation of the volatile compounds (e.g. Maillard reactions or lipid oxidation). Additionally, the analytical method employed can have an impact on the amount and type of volatile compounds detected and quantified. Therefore, in cooked meat, it is not clear whether we can apply volatolomics to assign its origin or the feeding regime. However, the identification of volatilomes aimed at authenticating the origin of dairy products or raw meat is less dependent on the method and preparation of the sample to obtain a more consistent profile, since cooking is not required. Due to the large number of volatile compounds that meat and dairy products contain and the interaction that occurs among them, the combined use of several volatilomes could be proposed to help identify the composition of ruminants’ diets. Meanwhile, on the other hand, the use of only a few volatilomes may not be enough to allow us to assign the origin of the feeding regime in ruminants.
2.4. Isotope ratios biomarkers
In 2016, a review by Camin et al. (Citation2016) stated the importance of isotope ratio mass spectrometry (IRMS) in assessing the authentication of foodstuffs of animal origin. More recently, studies have also been conducted using IRMS to assess the authentication of such food (Zhao et al., Citation2022), and techniques involving radioisotopes, combined with linear discriminant analysis and artificial neural networks, have been proposed to assess geographical origin and animal diet (Cristea et al., Citation2022). In the last 30 years, important advances in techniques based on the use of isotope ratio mass spectrometry (IRMS) have been developed to, among others, guarantee the traceability plans of production systems for foods of animal origin (Camin et al., Citation2007). This technology includes identification of stable isotopes of light elements (such as hydrogen, carbon, nitrogen, oxygen and sulphur) occurring in foods. Recently, Perini et al. (Citation2021) showed the promising effectiveness of using isotope ratios of five bioelements (2H,18O,13C, 15N, and 34S) to trace the regional origin of beef and zebu feeding regimes in Cameroon, while Zhao et al. (Citation2020) used stable isotope variations (2H, 18O, 13C, 15N) and the concentrations of seven elements (K, Na, Mg, Ca, Fe, Cu and Se) as an instrument to verify the organic provenance of pork purchased in four regions of China. Along these lines, Erasmus et al. (Citation2018) used the stable isotopic signature (13C, 15N) to determine the origin of South African lamb. This reference, together with others collected in , serve as a comparative summary of a full list of stable isotope biomarkers used for the authentication of feeding regimes in ruminant animals in meat and dairy products.
Table 4. An overview of isotope ratios suggested in the literature as biomarkers in fresh meat and dairy products to authenticate feeding system origins in ruminants.
Diets with concentrated feed are used in ruminant feeding, and stable carbon isotopes (13C/12C) can help identify corn-based feeding in farm animals compared with other animals raised on wheat, barley, oats, or rye (Monahan et al., Citation2018). It is widely known, for instance, that corn, being a C4 plant, has a different isotopic carbon signature than C3 plants like wheat, barley, oats, and rye (Camin et al., Citation2016). The δ13C values of photosynthetic C4 plants range between −14 and −12‰, while those of photosynthetic C3 cycle plants range from −30 to −23‰. If maize has been added to animal feed, an increase in the carbon isotopic composition of δ13C in muscle can be estimated at 1.9‰ (Harrison et al., Citation2011), and δ13C values above −23‰ are found in a full corn-feeding regime (Boner & Förstel, Citation2004).
In cows’ milk, the use of multi-elemental and isotopic fingerprints to differentiate the origin of milk samples from different forage feeding diets has also been studied (Griboff et al., Citation2019). Their use of canonical Correlation Analysis of the ratios of elements, such as K/Rb and Ca/Sr between milk and forage, showed significant correlations between the origin of the milk and forage intake in Argentinian cows.
To study the origin of an animal’s diet, a significant number of studies have focused on using δ13C and/or δ15N, depending on the specific diet that needs to be traced back (such as C3/C4 plants, legumes, pasture/stall breeding). Osorio et al. (Citation2011), Longobardi et al. (Citation2012) and Erasmus et al. (Citation2018) in bovine, goat and ovine, respectively, have proposed satisfactory results from investigations into the proportion of C4 plant material in beef cattle using the δ13C values in fresh meat and other animal tissues. Additionally, Osorio et al. (Citation2013) added that combining δ13C and δ15N with other isotope ratios such as δ2H and δ34S, measured in meat, can be effective in reflecting the diet (silage, C3, C4 concentrates, or pasture) administered to the cattle. Despite the fact that numerous works report the use of δ13C and δ15N as identifiers of meat origin (Monahan et al., Citation2018), the combined use of these biomarkers with others could achieve a better identification of the origin in animal products. For example, Longobardi et al. (Citation2012), in goat meat, recommended the combined use of δ13C and δ15N, along with other biomarkers such as proximal composition (moisture, ashes, fat, and protein content), together with major metals (Ca, Mg, Na, and K) and trace metals (Zn, Mn, Cu, Fe, and Cr) in meat, to distinguish the highly valuable Garganica kid goat meat. With regard to dairy milk products, McLeod et al. (Citation2015) also proposed that the chemical fingerprint obtained using δ13C, δ15N, combined with the analyses of concentrations of some trace elements (Na, Mg, K, Mn, and Rb, and higher concentrations of Ba and Cu) in goat milk could enable us to verify the product’s origin.
In the case of lambs, Devincenzi et al. (Citation2014), using only δ15N, and Prache et al. (Citation2009), using a combination of δ15N from muscle and δ-cadinene from perirenal fat, were able to clearly distinguish lambs raised indoors on high levels of alfalfa from lambs fed on pasture. In 2007, evidence was shown of the use of biomarker δ13C to identify milk system production in goats. In fact, Camin et al. (Citation2007) reported that the content of δ13C was relatively higher in milk-fed lambs (e.g. lambs from Tuscany) compared to lambs raised on pasture.
While molecular biomarkers (e.g. lipidomes, volatilomes, or proteomes) have been successfully used in identifying the origin of ruminants’ diets, the use of stable isotope ratios of several bio-elements, combined with concentrations of several inorganic elements, is mainly being used to trace the regional origin of meat and dairy products. In fact, in the literature, the stable isotopes δ13C and δ15N, combined with other inorganic biomarkers such as K, Na, Mg, Ca, Fe, Cu and Se, are the most widely used to determine the geographical origin of meat and dairy products in ruminants. The use of the isotope ratios of several bio-elements combined with concentrations of inorganic elements in meat and dairy product could probably contribute to improving the identification of feeding type in ruminants.
3. Conclusions and future perspective
The present review highlights the feasibility of applying a foodomics chemical fingerprint approach when using biomarkers to verify feeding regimes and origin in farm ruminant. Extensive studies suggest that both organic and inorganic compounds can serve as biomarkers, ensuring the traceability of ruminant meat and dairy production in terms of feeding regime. Among the compounds studied in the scientific literature, lipids such as saturated and polyunsaturated fatty acids, terpenes, and carotenoids, have been reported frequently. In addition, metabolomes such as polyphenols, organic acids, amino acids, vitamins, and minerals, proteomes derived from myosin and casein proteins, and volatilomes such as aldehydes, lactones, alcohols, and skatol, among others, have been studied as biomarkers of feeding diet in farm ruminants. Several proteomes have been proposed as biomarkers for the origin of dairy products in farm ruminants, while in meat products, further studies are needed to identify protein biomarkers in meat related to the identification of ruminant diet.
By combining multiple foodomics compounds (lipidomes, metabolomes, proteomes, volatile compounds) with mathematical tools such as discriminant analysis or new machine learning techniques, it is possible to potentially ensure the origin and quality of meat and dairy products derived from farm ruminant, thereby meeting the customers’ demands.
The collection of biomarkers identified to date in fresh meat and dairy products is extensive, because efforts have been ongoing for a long time to identify the authentication of meat and dairy products from animals that are reared on grass. However, the development of new analytical technologies (GC, LC–MS/MS, NMR, MS, ICP-MS, UPLC-Q-TOF/MS, electrophoresis, and IRMS, among others), together with advances in our knowledge of the digestive physiology of ruminants, will allow to identify with greater precision specific and genuine molecules generated in the rumen of animals that have grass and/or concentrated feed in their diet. For this reason, through foodomics, future research work should aim to further expand the set of biomarkers in fresh meat and dairy products, with the objective of guaranteeing the authenticity of feeding regimes of farm animals demanded by consumers. To achieve this, the combined use of a collection of biomarkers (lipidomes, metabolomes, proteomes, volatile compounds, isotope ratios) seems promising, and will allow companies and the food sector to improve the fingerprinting of fresh meat and dairy products in order to authenticate the origin of animal foodstuffs.
Author contributions
Alberto Horcada conceived the document, obtained and analysed the literature resources, wrote and supervised the manuscript. Carlos Álvarez conceived the document, wrote and supervised the manuscript. Manuel García-Infante wrote and supervised the original draft. Jingjing Liu supervised and wrote the original draft. All authors read, reviewed, and agreed to the final version of the manuscript.
Disclosure statement
The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.
Data availability statement
Because this work is a review, the data supporting the findings of this study are available online on several websites. All references (doi) are reported in references section.
Additional information
Funding
Notes on contributors
Alberto Horcada
Alberto Horcada phD is a Lecturer at the Higher Technical School of Agricultural Engineering of the University of Seville, Spain. His research career focusses mainly on meat quality of autochthonous ruminant breeds.
Manuel García-Infante
Manuel García-Infante is an Agricultural Engineer and phD student in Animal Production.
Jingjing Liu
Jingjing Liu is a Research Officer at Teagasc Ashtown Food Research Center. Her scientific work is focused on livestock production, farming system, beef/lamb carcass grading operation, and meat quality control and assessment.
Carlos Álvarez
Carlos Álvarez phD is a Senior Research Officier. His scientific work is focused in recovering compounds of interest from food co-products, looking for innovative applications, in order to reduce the environmental impact of these industrial activities.
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