http://dx.doi.org/10.4314/sajas.v54i3.05

 

The effect of dietary non-protein nitrogen content on the meat quality of finishing lambs

 

 

O.B. Einkamerer^I,; A.V. Ferreira^II; M.D. Fair^I; A. Hugo^I

^IDepartment of Animal Science, P.O. Box 339, University of the Free State, Bloemfontein, 9300, South Africa
^IIPresent address: Molatek, PO Box 47, Malelane, 1320, Republic of South Africa

 

 

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ABSTRACT

The effect of increasing the non-protein nitrogen content of low-fibre finishing diets on the meat quality of South African Mutton Merino wether lambs was investigated. Four similar dietary treatments were formulated with different non-protein nitrogen contents (16.6 g/kg, 28.3 g/kg, 40 g/kg, and 51.7 g/kg) on a dry matter basis. The study was conducted over 71 days. Muscle lipid content was higher on the 40 g/kg compared to 16.6 g/kg and 28.3 g/kg non-protein nitrogen diets. Myristic acid and total saturated fatty acid content of lamb muscle tissue was higher, whereas the total unsaturated fatty acid content of the same tissue was lower following a high dietary non-protein nitrogen content. A high non-protein nitrogen diet (51.7 g/kg) reduced conjugated linoleic acid content of adipose tissue, compared to 28.3 and 40 g/kg non-protein nitrogen treatments. Malonaldehyde content of fresh lamb meat was higher on the 28.3 g/kg compared to the 16.6 g/kg non-protein nitrogen diet. The malonaldehyde content of the treatment containing 40 g/kg non-protein nitrogen was higher than the 51.7 g/kg when stored for 90 days. Therefore, the non-protein nitrogen content of low-fibre lamb finishing diets does not affect mutton fatty acid composition and quality parameters. Protein quality and its effect on ruminant meat quality requires more attention.

Keywords: Fatty acid, mutton, shear force, soybean meal, urea

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Introduction

Elucidating protein metabolism in ruminants gives a clearer understanding of the complex system that separates nitrogen for microbes from that of post ruminal amino acid supply to the host (Owens et al., 2014). Crude protein, which is the simplest form, is provided to ruminants and can be divided into degradable and undegradable intake protein (Bohnert et al., 2002). Nutrients found in the blood of a ruminant depend on microbial fermentation, which plays a remarkable role in changing and producing substances to be absorbed and used by the animal. Degradable intake protein is broken down within the rumen by microorganisms, whereas undegradable intake protein escapes rumen fermentation and ends up in the small intestine for enzymatic digestion and absorption (Bohnert et al., 2002). Non-protein nitrogen (NPN) compounds are not proteins but can be converted into proteins by rumen microbes (Zurak et al., 2023) and include urea, uric acid, and ammonia (Tadele & Amha, 2015). NPN remains relevant in the field of ruminant nutrition (Zhu et al., 2022). Ammonia is not only the most important source of nitrogen for rumen bacterial growth (Bohnert et al., 2002) but is the preferred nitrogen source of cellulolytic bacteria (NRC, 2007). Hoover (1986) notes that urea as sole nitrogen source is not sufficient because microorganisms lack specific amino acids.

Ruminant products contain high amounts of saturated fatty acids (SFAs) as a result of ruminal biohydrogenation (BH) (Harfoot & Hazlewood, 1997). A high intake of SFAs is associated with increased risk of lifestyle-related diseases such as increased blood cholesterol levels and atherosclerotic growth (Junkuszew et al., 2020). Thus, to improve human nutrition, feeding strategies for ruminants aim to reduce SFAs and increase polyunsaturated fatty acids (PUFA). Fatty acid hydrogenation contributes to the accumulation of conjugated linoleic acid (CLA) isomers in ruminant products (Fievez et al., 2007) and contains anticarcinogenic properties (Mcguire & Mcguire, 1999) and improves immune response (Jenkins et al., 2008). The negative connotation to SFAs should be re-visited since only stearic acid (C18:0) has an atherogenic affect when consumed excessively (Chilliard et al., 2006).

Dietary nitrogen concentration affects the rates of lipolysis and hydrogenation (Gerson et al., 1983). Lipolysis is more extensive when nitrogen is increased in high starch diets (Dewhurst et al., 2006). With sufficient nitrogen, the relative rates are such that unsaturated fatty acids (UFA) accumulate in the rumen (Gerson et al., 1983). Additionally, some microorganisms require, or are stimulated by, different forms of nitrogen (Polan, 1992). Hydrogenating bacteria consist mainly of cellulolytic organisms. Cellulolytic bacteria such as Butyrivibrio fibrisolvens, Ruminococcus flavefaciens, and Ruminococcus albus are actively involved in the biohydrogenation (BH) of fatty acids (FA) (Harfoot & Hazlewood, 1997). Butyrivibrio fibrisolvens has proteolytic activity and is actively involved in the BH of FAs (Harfoot & Hazlewood, 1997). Therefore, any nutrient favouring the growth of bacteria responsible for ruminal BH, like ammonia (Steward et al., 1997) from NPN sources, can affect the free UFAs in the rumen. Hence, the research focusses on this concept.

Over a century of ruminant nutrition research has been devoted to understanding ruminant nitrogen metabolism and studying processes and practices that can increase nitrogen utilization efficiency (Hristov et al., 2019). However, the research on the nitrogen content of ruminant diets affecting FA composition only accounts for rumen contents (in vitro), blood plasma, liver, muscle, and perirenal fat in sheep (Gerson et al., 1982, 1983). No literature regarding the effect of finishing diet NPN concentrations on the FA composition of ruminant products was found. It is possible that free ammonia (from NPN sources) in the rumen can stimulate the growth of BH microbes and ultimately affect lamb meat FA composition and quality. The aim of this study was therefore to determine the effect of increasing dietary NPN content within a standard low-fibre finishing diet on meat quality of South African Mutton Merino (SAMM) lambs.

 

Materials and Methods

All procedures conducted during this study were approved by the Interfaculty Animal Ethics Committee for Animal Experimentation at the University of the Free State (Animal Experiment No. UFS-AED2016/0038).

A production study was conducted with 60 SAMM wether lambs over 71 days. All lambs with an initial live weight of 25.5 ± 2.6 kg (mean ± SD) were randomly allocated to four dietary treatments culminating in a randomised trial design with n = 15 lambs per treatment (n = 1 lamb per experimental unit). The animals received a standard health and vaccination programme prior to the study: they were injected with an antiparasitic remedy, dosed for tapeworm and inoculated against pulpy kidney, malignant oedema, blackquarter, tetanus, pasteurellosis, as well as pneumonic and septicaemic pasteurellosis. Animals were housed in pens (n = 1 lamb/pen; 1.404 m²) on elevated, wooden, slatted floors in a naturally-ventilated building.

Four finishing diets with a similar nutrient composition (155 g crude protein/kg dry matter (DM) and 180 g neutral detergent fibre (NDF)/kg DM) were formulated, with each containing increments in NPN content (Table 1). The NDF content was kept as low as possible because a low-fibre diet results in a low ruminal pH, which inhibits the growth of the main BH cellulolytic bacteria (Martin & Jenkins, 2002). The protein source for the incremental NPN content was feed grade urea. Soybean meal and prime gluten meal were used to ensure a similar degradable and undegradable intake protein content, respectively. Maize protein is relatively high in undegradable intake protein (Swanson et al., 2004). The bypass protein potential of soybean meal is low (Cheeke, 2005) and is an example of a protein source containing high degradable intake protein content (NRC, 2007) with a high percentage of nitrogen present as true protein (±90%) (Kellems & Church, 2010). Urea is 100% degradable within the rumen (Soto-Navarro et al., 2003).

Treatments were described according to NPN content in ascending order as control (CON: 16.6 g/kg), NPN1 (28.3 g/kg), NPN2 (40 g/kg), and NPN3 (51.7 g/kg). All other chemical parameters were formulated to be similar. Treatment diets were fed to the animals in a processed mash form.

The FA composition of the four experimental diets is presented in Table 2. Only the major FAs contained in the feed, as well as those deemed important to ruminant meat, were reported in this study. Because the prime gluten 60 inclusion increased with decreasing soybean meal inclusion (from CON to NPN3), maize germ oil was added by difference and calculated according to soybean oil inclusion. This ensured comparable FA composition between the diets and similar lipid content. Soybean oil was used in this study to increase the UFA content of all diets. Representative feed samples were taken at the start (day 0) of the production study and stored at -18 °C until the FA profile was determined.

No feed additives or rumen modifiers, which may have affected the rumen environment, were included in the diets. A synthetic antioxidant containing a combination of butylated hydroxy anisole (BHA), butylated hydroxytoluene (BHT), ethoxyquin and trisodium citrate was, however, included in all diets to prevent FA oxidation.

At the onset of the study (day 0), the lambs underwent a standard adaptation period. Lucerne hay was provided ad libitum and each respective treatment diet was fed to the lambs with incremental increases of 100 g/day/animal for 10 days. The animals were fed twice daily, at 08h00 and at 16h00. Feed intake was recorded on a weekly basis. Fresh, clean water was freely available to all animals.

At the end of the production study, all lambs (49.1 ± 4.4 kg; mean ± SD) were slaughtered at a commercial abattoir. Three loin chops (the left 9^th to the 11^th rib) from each carcass were evaluated for meat quality.

Total lipid from longissimus muscle and subcutaneous fat samples were quantitatively extracted according to the method of Folch et al. (1957). Chloroform and methanol were used in a ratio of 2:1. Total extractable intramuscular fat was determined gravimetrically from the extracted fat and expressed as percentage fat (w/w) per 100 g tissue. An antioxidant (butylated hydroxytoluene) was added at a concentration of 0.001% to the chloroform:methanol mixture. A rotary evaporator was used to dry the fat extracts under vacuum. The extracts were dried overnight in a vacuum oven at 50 °C using phosphorus pentoxide as a moisture adsorbent.

The extracted fat from the feed, muscle, and subcutaneous fat was stored in a polytop (glass vial, with push-in top) under a blanket of nitrogen and frozen at -20 °C, pending FA analyses. A lipid aliquot (20 mg) of feed, muscle, and subcutaneous lipid were converted to methyl esters by base-catalysed transesterification with sodium methoxide (0.5 M solution in anhydrous methanol) for 2 h at 30 °C to avoid CLA isomerisation, as proposed by Kramer et al. (2002) and Alfaia et al. (2007). Fatty acid methyl esters (FAME) from the feed, muscle, and subcutaneous lipid were quantified using a Varian 430 flame ionization gas chromatograph with a fused silica capillary column (Chrompack CPSIL 88; 100 m length; 0.25 mm ID; 0.2 μηι film thickness).

Analysis was performed using an initial isothermic period (40 °C for 2 min). Thereafter, temperature was increased at a rate of 4 °C/min to 230 °C. Finally, an isothermic period of 230 °C was held for 10 min. Fatty acid methyl esters in n-hexane (1 μΙ) were injected into the column using a Varian CP-8400 Autosampler. The injection port and detector were both maintained at 250 °C. Hydrogen, at 45 psi, functioned as the carrier gas, whereas nitrogen was used as the makeup gas. Galaxy Chromatography Data System Software recorded the chromatograms.

Fatty acid methyl ester samples were identified by comparing the retention times of FAME peaks from samples with standards obtained from Supelco (Supelco 37 Component Fame Mix 47885-U, Sigma-Aldrich Aston Manor, Pretoria, South Africa). Conjugated linoleic acid standards were obtained from Matreya Inc. (Pleasant Gap, Unites States of America). These standards included: C18:2c9,t11 and C18:2t10,c12 isomers. All other reagents and solvents were of analytical grade and obtained from Merck Chemicals (Pty Ltd, Halfway House, Johannesburg, South Africa).

Fatty acids were expressed as the proportion of each individual FA to the total of all FAs present in the sample. The following were also calculated: total SFAs, total monounsaturated fatty acids (MUFA), total PUFAs, total omega-3 (n-3), and total omega-6 (n-6) FAs. Total fatty acid data were used to calculate the following ratios: PUFA/SFA, n-6/n-3, and Δ⁹ desaturase index (C18:1c9/C18:0). Atherogenicity index was calculated as (Chilliard et al., 2003):

One loin chop from each lamb carcass was individually placed in a polystyrene tray containing an absorbent pad, wrapped with oxygen-permeable polyvinyl chloride (PVC) meat stretch wrap, and stored for 8 d (evaluated every second day) at 4 °C under fluorescent light for fresh meat stability studies. Another loin chop was vacuum sealed and stored for 90 d at -18 °C in the dark for frozen storage stability evaluation.

Muscle colour (L*, a* and b*-values) was subsequently determined in triplicate using the refrigerated (4 °C) loin chop over a period of 8 d using a Minolta chromometer. Chroma or saturation index, which is related to colour intensity of meat, and hue angle were calculated according to the formulae of Ripoll et al. (2011):

Thiobarbituric acid reactive substance (TBARS) was used to determine the malonaldehyde content/kg meat. A 5-g sample of lean meat was removed from the middle of each loin chop on day zero, day eight (refrigerated at 4 °C), and day 90 (frozen storage at -18 °C), and the aqueous acid extraction method of Raharjo et al. (1992) was applied.

Meat tenderness was determined using the íongissimus muscíe (left 11^th to 13^th rib sample), which was vacuum sealed and frozen at -20 °C. Frozen samples were thawed at 4 °C for 18 h before preparation. Thawed cuts were prepared according to an oven-broiling method using direct heat (AMSA, 1978). An electric oven was set on "broil" 10 min prior to preparation (260 °C). Steaks were placed on an oven pan on a rack to allow meat juices to drain during cooking and placed in the preheated oven, 9 cm below the heat source. The cuts were cooked to an internal temperature of 35 °C, then turned over and finished to 70 °C. Cuts were cooled at room temperature (20-25 °C) for at least 3 h before measuring shear force. Four cylindrical samples (12.5-mm core diameter) of each sample were cored parallel to the grain of the meat and sheared perpendicular to the fibre direction using a Warner Bratzler shear force device mounted on a Universal Instron apparatus (cross head speed = 200 mm/min; one shear in the centre of each core). The reported value in kg represents the average of the peak force measurements of each sample.

The data was analysed as a completely randomized design using the General Linear Model (GLM) procedures of the Statistical Analysis System (SAS) program (SAS, 1999). Means were compared using the LSMEANS/DIFF with treatment as fixed effects. For post hoc analysis, Tukey's honestly significant difference (HSD) test was used to identify significant differences between treatment means and significance was declared at the 5% probability level. The description of the model used for ANOVA was:

where Yij is the individual observations (dependent variable) of the i-th treatment (independent variable) and the j-th random error, μ is the general effect, ti is the effect of the i-th treatment, and εij is the random variation or experimental error.

The i-th treatment effect (dietary NPN content) during this study was defined and presented on a DM basis:

 

Results and Discussion

The daily dietary DM intake (g DM per animal) was not affected (P >0.05) by NPN addition for CON (1306 ± 139), NPN1 (1285 ± 114), NPN2 (1227 ± 130), and NPN3 (1234 ± 144) (Einkamerer et al., submitted for publication). Hence, the FA composition of treatment diets (total FA intake) was discounted as a possible cause for any substantial effects regarding meat FA composition. The effect of NPN content in low-fibre finishing diets on the lipid content and FA composition of wether lamb muscle tissue is presented in Table 3. A change in feed can influence total FA intake and consequently, the FA composition of ruminants and products (Dang Van et al., 2011). The amount (Beam et al., 2000; Scollan et al., 2003; Santos-Silva et al., 2004; Gómez-Cortés et al., 2009; Hur et al., 2017) and composition (Vatansever et al., 2000; Ivan et al., 2001; Chilliard & Ferlay, 2004; Cooper et al., 2004; Castro et al., 2009; Booyens et al., 2012; Lerch et al., 2012; Du Toit et al., 2013) of dietary lipid consumed influences the FA composition of rumen content, as well as ruminant products. If FAs are naturally protected from hydrogenation, like maize lipids due to the lower rumen degradability of maize protein and starch compared to other cereals (Bas & Morand-Fehr, 2000), it may aid the provision of intact FAs within the small intestine. An increased rumen outflow of oils (increased intake) may also lessen the effects of BH (Demeyer & Doreau, 1999) and therefore reduce exposure of lipids to lipases and BH in the rumen (Dewhurst et al., 2006).

The NPN content influenced the lipid content of lamb longissimus dorsi muscle tissue (Table 3). The lipid content was higher with an NPN content of 4.00% (treatment NPN2) than the CON (NPN 1.66%) and NPN1 (NPN 2.83%). There might have been a hormonal effect relating to dietary protein content and fat accretion/mobilisation in the lambs. However, Pittroff et al. (2006) found that protein: energy ratios could not indicate whether the diet given to sheep resulted in a change of internal energy reserves. The authors found that leptin, which indicated higher circulating content, of lambs fed straw and duodenal available protein (150 g/d fish meal) did not respond with an accelerated rate of fat mobilization or maintained protein mass due to available nitrogen, compared to lambs fed only straw. Thus, dietary protein provision has an apparent hormonal effect on lamb fat content. No literature could be found on dietary NPN content and lamb muscle lipid tissue content. More research is required in this regard.

The NPN content of low-fibre finishing diets had a limited effect on the FA composition of lamb muscle tissue. The myristic acid content of lamb muscle was, however, higher (P = 0.0365) on treatment NPN3 compared to treatments CON and NPN1. Total muscle SFA content of treatment NPN3 was also higher than treatment NPN1. The fatty acid profile of lamb becomes more saturated as the animal ages (Ye et al., 2020). The contents of MUFA and SFA both increase faster in the carcass with increasing fatness compared to the PUFA content (De Smet et al., 2004). These marked effects in muscle SFA content in the current study are therefore comparable to its lipid content. In contrast, increasing the NPN content of diets to 5.17% of DM (NPN3) decreased (P = 0.0214) the total UFA content of the same tissue compared to treatment NPN1 only. A negative association between meat PUFA and total lipid contents has been reported in ovine studies where PUFA decreases as animals age due to the relative increase of neutral lipids in tissue (Ye et al., 2020).

Dietary lipid amounts, blends thereof (Bessa et al., 2007), as well as full-fat whole seeds (Bauman et al., 1999; Chilliard & Ferlay, 2004; Lestingi et al., 2015) can influence the FA composition of animal products. Dietary plant protein feed ingredients, which increases protein content, may therefore influence the FA composition of adipose tissues and muscles of lambs, probably because of the high content of specific total FAs (Bas & Morand-Fehr, 2000). These authors found that the addition of cotton seed meal with a high FA content brought about a substantial rise in stearic and linoleic acid percentages in lamb fat deposits. Additionally, fish meal in lamb diets increased the oleic acid percentage in fat tissues (Bas & Morand-Fehr, 2000). Extruded linseed also had beneficial effects on FA composition of dairy bulls' meat (Dawson et al., 2010). The effect of varying dietary lipids was controlled in the current study by providing diets with similar FA compositions (Table 2). A possible hormonal effect from dietary protein content and fat accretion/mobilisation of lambs was reported (Pittroff et al., 2006), which was related to total protein consumption and not protein quality per se. No literature is available on diet protein quality and its effect on lamb meat FA composition and this requires more attention.

Proteolytic isolates are recognised as Ruminobacter amylophilus, Prevotella ruminicola, Butyrivibrio fibrisolvens, B. alactacidigens, Selenomonas ruminantium, and Streptococcus bovis (Dehority, 2003). Cellulolytic bacteria are actively involved in the BH of FAs (Harfoot & Hazlewood, 1997). Butyrivibrio fibrisolvens contains cellulolytic (French et al., 2000), proteolytic, and BH activities (Harfoot & Hazlewood, 1997). French et al. (2000) stated that the growth and activity of B. fibrisolvens was influenced by rumen conditions, which could subsequently determine the amount of CLA available for absorption from the gastrointestinal tract. Hence, it is plausible that the growth of B. fibrisolvens was stimulated by an increased NPN content, which could have affected the total SFA and total UFA content of lamb meat. Different B. fibrisolvens strains prefer to utilize either ammonia, or mixtures of amino acids (Dehority, 2003). Therefore, the correct bacterial strain needs to be identified. Further research is required in this regard as microorganism composition and rumen pH were not measured in the current study, which was a limitation of this study.

A significant effect on the atherogenicity index of lamb intramuscular lipid tissue was noted due to dietary treatment. This was primarily ascribed to the marked effect of a high NPN content (NPN3) on the same muscle's myristic acid content. Atherogenicity and thrombogenicity indices should both present smaller values than 1.0 and 0.5 to assure a protective potential for coronary artery health (Murariu et al., 2023). The atherogenicity index of muscle tissue can be reduced if the UFA content is increased (Carvalho et al., 2014). The contrary seems to occur with an increased SFA content. Manso et al. (2009) confirmed that a lack of influence on the intramuscular fat atherogenicity index was related to a lack of effect on the SFA and MUFA content. Palmitic acid concentration is important because it is harmful to human health by increasing low-density lipoprotein (LDL) levels in the blood (Carvalho et al., 2014). The marked effect on the atherogenicity index of lamb intramuscular lipid tissue in the current study is therefore justified due to the treatment effect on lamb muscle myristic acid, total SFA, and UFA content. Dietary treatment had no effect on the longer-chain FA (C20-plus) composition of lamb muscle tissue.

The effect of increasing NPN content in low-fibre finishing diets on the lipid content and FA composition of wether lamb subcutaneous lipid tissue is presented in Table 4. It is evident that dietary NPN content had less of an effect on the FA composition of lamb subcutaneous lipid tissue compared to that of the muscle tissue (Table 3). Even though differences in FA tissue response (adipose versus muscle tissue) are not uncommon (Oka et al., 2002), this result was not expected as the FA composition of muscle tissue is frequently less influenced by the diet than the adipose tissue (Scollan et al., 2006). This is because most of the muscle FAs are located in phospholipids and cellular membranes. Cell membrane FA composition often changes little despite large differences in dietary lipid composition (Jimenez et al., 2020). At least 90% of the lipids contained in adipose tissue are triacylglycerol or neutral lipids, whereas those within muscle tissue are predominantly phospholipids (Wood et al., 2008). This same deposit site effect was also acknowledged by Ladeira et al. (2014). Dietary NPN content did however affect the CLA (C18:c9,t11) content of lamb subcutaneous lipid tissue; treatment NPN3 was lower than treatments NPN1 and NPN2. It is important to note that dietary treatments within the current study contained no trace of any CLA isomers (Table 2).

Conjugated linoleic acids are a mixture of geometric and positional isomers of conjugated dienoic derivatives (Hur et al., 2017). An increased lipid CLA content could be connected to two possible causes: firstly, an incomplete BH affected by rumen pH with both a decreased (Qiu et al., 2004; Xu et al., 2014) and increased pH (Hur et al., 2017) and secondly, due to the activity of the Δ⁹ desaturase enzyme (CoA-desaturase) in body tissues (Ribeiro et al., 2020). The majority of CLA (c9,t11) is produced in animal tissues (Ishlak et al., 2015) and the activity of Δ⁹ desaturase is greatest in adipose tissue of growing ruminants (Kucuk et al., 2008). The second cause was ruled out as a possible tissue effect on the lipid CLA (c9,t11) content in the current study because the Δ⁹ desaturase index was unaffected by dietary treatment.

Similar to lamb muscle tissue, dietary treatment had no marked effect on the longer-chain FA composition of lamb adipose tissue. Wood et al. (2003) reported that the long chain (C20 to C22) n-3 PUFAs were not detectable in beef and lamb neutral lipids (triacylglycerol). This was similar to the current study with special reference to eicosopentaenoic, docosapentaenoic, and docosahexaenoic acids.

There is a paucity of research regarding proteins and their effect on ruminant meat FA composition. The available research concentrated on total nitrogen content (Gerson et al., 1982, 1983) and not quality per se. Gerson et al. (1982) studied the composition of rumen volatile and unesterified FAs and the FA composition of blood plasma, liver, muscle, and perirenal fat of Romney wethers on diets with varying proportions of nitrogen but similar digestible organic matter. In similar research, the rates of lipolysis and hydrogenation was determined in vitro using sheep rumen digesta after high-starch diets (30% to 50%) also containing increasing proportions of nitrogen (0.72%, 1.22%, 1.72%, 2.47%, and 3.72%) (Gerson et al., 1983). Rates of lipolysis and hydrogenation were lowered by low dietary nitrogen content (Gerson et al., 1983), and in diets containing approximately 1% nitrogen (DM basis), the relative rates were such that UFAs accumulated in the rumen.

There was a linear increase in the rate of lipolysis as nitrogen content increased in vitro (Gerson et al., 1983). The rate of in vitro BH increased after a 1.2% nitrogen concentration and tended to decrease above 2.5% nitrogen (Gerson et al., 1983). Gerson et al. (1983) concluded that microbial composition may have been a prime factor influencing the rates of lipolysis and hydrogenation. However, no conclusive evidence of a change in microbial species composition during incubation was presented. The authors confirmed that previous experience indicated that animals had to be kept for at least two weeks before microbial adjustment within the rumen was complete. This data refers to an in vitro study representing two highly-degradable intake protein sources with increased nitrogen content. It was, however, established that the addition of finely ground casein (true protein source) to the incubate was without affect (Gerson et al., 1983), probably due to the incubation period. Similar microbial populations and total bacterial count were recorded in sheep fed purified diets containing urea and casein (Oltjen, 1969). Calcium caseinate (900 g crude protein /kg DM) is referred to as a true protein source, which is 100% degradable in the rumen (Nolte & Ferreira, 2005).

Gerson et al. (1982) increased the amount of dietary nitrogen (0.54%, 1.10%, 1.42%, and 3.39%) in dietary DM fed to wethers for 50 d with similar degradable organic matter intake and recorded crude protein content of 3.38%, 6.88%, 8.88% and 21.19%, respectively. The percentage nitrogen is multiplied by 6.25 (McDonald et al., 2011) for the current discussion and comparisons. Gerson et al. (1982) explained that the proportion of nitrogen in wether diets rather than nitrogen intake, determined the amount and composition of plasma and tissue lipid, as well as the extent of BH in the rumen. Decreased BH in sheep fed 1.10% and 1.42% nitrogen (low nitrogen content) was noted in rumen contents. Increased concentrations of oleic and linoleic acids in the rumen were reflected in the plasma, muscle, and perirenal fat composition of the same sheep (Gerson et al., 1982). Similar results on BH were reported by Gerson et al. (1983). Tissue lipids were most unsaturated when nitrogen constituted approximately 1.40% (8.75% crude protein on a DM basis) of the diet (Gerson et al., 1982). The very low nitrogen treatment (0.54%), as well as highest (3.39%) in their research, resulted in higher lipolysis and BH, as judged by high saturation of rumen and plasma FAs. Gerson et al. (1982) found the effect of the low nitrogen treatment surprising because the opposite result was expected due to a depletion of the microbial population in the rumen. A higher dietary crude protein content fed to lambs again resulted in lower tissue palmitic and stearic acid contents, whereas the palmitoleic, oleic, and α-linolenic acid contents increased (Bas & Morand-Fehr, 2000). When the diet is deficient in protein or the protein resists degradation, the growth of rumen organisms will be slow (NRC, 2007). It appears that a more likely explanation for the results is a possible modification of the rumen bacterial population related to the 1.10% and 1.42% nitrogen treatments. The nitrogen content of these diets probably did not favour microorganisms involved in the completion of the hydrogenation process, where BH seemed to be affected by alternate rumen nitrogen contents (Gerson et al., 1982). The authors acknowledge that a number of possible causes for this change in rumen BH may be considered (Gerson et al., 1982).

Lastly, and in contrast, dietary crude protein content in differing roughage:concentrate diets had no influence on varying the concentration of microbial cell matter FA composition (Bas et al., 2003). Even though the crude protein content of treatment NPN3 was slightly higher than the other treatments (Table 1), the possible cause and its effect on the FA composition of ruminant products and rumen digesta is rejected in the current study due to the overall lack of effect on lamb meat FA composition.

There is a possibility that urea could affect rumen pH (Oltjen, 1969; Soto-Navarro et al., 2003). Its increased inclusion in the current treatment diets could have affected rumen pH. Hence, FA metabolism in a low pH results in decreased rumen BH and lipolysis (Jenkins, 1993). Lower CLA (c9,t11) is observed at low rumen pH conditions (Choi et al., 2005). High starch digestibility (AlZahal et al., 2008) and low dietary fibre content (Gerson et al., 1985) reduce the rate of lipolysis and BH and are connected to rumen pH. The statement regarding urea and its effect on rumen pH is referred to with caution as small fluctuations in rumen pH were noted (Kropp et al., 1977), whereas Soto-Navarro et al. (2003) referred to inconsistent results of urea on rumen pH. Some rumen pH values were even reported to be similar when urea and soybean protein isolate were fed to animals (Oltjen, 1969). The diets in the current study were also formulated on a low NDF content and rumen pH was not measured. Thus, information on rumen pH was not collected and more research is required in this regard.

Omega-3 and n-6 FAs are involved in human cardiovascular health. Dietary manipulation to alter lipid composition of small ruminants to favour human health have been investigated extensively (NRC, 2007; Ishlak et al., 2015). Fatty acid ratios are also considered important for human health. These include the PUFA:SFA ratio (0.45; Demirel et al., 2006) and n-6:n-3 ratio (4.00; Lestingi et al., 2015). The lower the n-6:n-3 ratio, the more beneficial it is for human health (Nong et al., 2020). Research has shown that the n-6:n-3 FA ratio is 15/1 to 16.7/1 in the typical Western diet, leading to increased incidences of lifestyle-related diseases. A lower n-6:n-3 FA ratio can reduce the risk of cardiovascular disease, cancer, and respiratory disease (Junkuszew et al., 2020). Dietary NPN content had no effect on any FA ratios within this study.

There is no literature available where protein quality (particularly NPN) was used as an independent variable to test for its effect on the FA composition of ruminant meat. Only literature regarding the quantity of nitrogen was found and reported in this study. It is recommended that more research should be conducted in this regard.

Because meat colour (Yagoubi et al., 2018), taste, and nutritional value are important quality attributes, any change in FA composition can influence quality aspects (Webb & O'Neill, 2008). The effects of increasing NPN content in low-fibre finishing diets on the colour stability and tenderness of wether lamb muscle tissue are presented in Table 5. Dietary NPN content of low-fibre finishing diets had no influence (P >0.05) on wether lamb muscle colour stability and tenderness (Table 5). This result was not expected as dietary treatment had a substantial effect on the total UFA composition of lamb muscle tissue (Table 3). The deterioration of red meat colour is triggered by a higher UFA content (Vatansever et al., 2000) but depends particularly on the content of PUFAs (Buckley et al., 1995). A meta-analysis showed that a high PUFA in pork decreased lightness (L*) because PUFA supplementation led to myoglobin oxidation and decreased the ratio of oxygen myoglobin to reduce lightness (Wang et al., 2021). Red meat colour is an important consumer sensory attribute (Abdalla Filho et al., 2017). The oxidation of lipids and pigment in meat are closely related, with the increase in one resulting in a similar increase in the other (Carvalho et al., 2014). Thus, the oxidation of myoglobin during storage leads to changes in meat colour (Hajji et al., 2016; Yagoubi et al., 2018).

Carvalho et al. (2014) found an increase in both L* (lightness) and b* (yellowness) indices in animal muscles as a result of higher lipid levels. Fat is lighter than muscle and its increased presence could contribute to an increase the luminosity value (Carvalho et al., 2014). Even though muscle lipid content in the current study was affected (P = 0.0021) by dietary NPN inclusion (Table 3), a different result than that mentioned by Carvalho et al. (2014) was recorded. In addition, the b* index has been correlated with the presence of carotenoids in diets (Carvalho et al., 2014). Carvalho et al. (2014) ascribed higher yellowness values in diets to the addition of maize gluten, an ingredient rich in beta-carotene. Even though prime gluten 60 was used in this study and included in treatments NPN1, NPN2, and NPN3 (Table 1), its addition was probably too low to effect any substantial differences.

The colour indices (L*, a*, and chroma) of longissimus dorsi muscle from animals consistently decrease during ground soybean meal consumption (Ladeira et al., 2014) and the consumption of concentrate diets. Concentrate diets produce muscle with a brighter red colour (a* value) (Cooke et al., 2004), whereas pasture-fed lambs have higher b* values (Hajji et al., 2016). The higher yellow colour of grass-fed animals is ascribed to the presence of carotenoids (Priolo et al., 2002). Hue angle, however, gives a more realistic perspective on meat browning than any other single parameter (Luciano et al., 2009). The closer the hue angle is to 90°, the more yellow the colour is. All measured values were also lower than this recommended value.

The effect of increasing NPN content in low-fibre finishing diets on the oxidative stability (malonaldehyde content) of wether lamb muscle tissue is presented in Table 6.

Dietary treatment had an effect on the malonaldehyde content of lamb muscle tissue (P <0.05). Malonaldehyde of NPN1 increased compared to CON on day 0 (fresh sample). In contrast, malonaldehyde content of NPN2 was higher than NPN3 on day 90 of refrigerated storage. Even though NPN content had an effect on the oxidative stability of lamb muscle tissue, the results were not consistent. The stability of meat is related to its FA composition (Scollan et al., 2006). Any alteration of the FA profile of meat to more UFA, increases oxidative breakdown during post-mortem storage (Vatansever et al., 2000; Ladeira et al., 2014). Therefore, there is a positive correlation with the degree of UFA and meat oxidative stability (Carvalho et al., 2014). The PUFA content is especially susceptible to lipid oxidation (Yagoubi et al., 2018). Due to the marked effect on muscle UFA composition (Table 3), a related response in lamb muscle oxidation was expected. This result was, however, not consistent with the UFA content of lamb muscle tissue.

A malonaldehyde content of 0.5 mg/kg and above is considered negative and indicates lipid oxidation, which causes the rancid odour and taste of meat (Wood et al., 2008). Higher malonaldehyde values than this were only evident for treatment CON, NPN1, and NPN2 (P >0.05) stored for 8 d. Fortunately, these values were much lower than the proposed threshold value of 1 mg/kg (Ripoll et al., 2011), and even the high 2 mg/kg value presented in other research (Vatansever et al., 2000; Wood et al., 2003).

Tissue lipids of ruminants are more saturated than non-ruminants (French et al., 2000; Jenkins et al., 2008). Sheep meat is high in SFAs (Chikunya et al., 2004) and lamb fat is particularly high in stearic acid content (Wood et al., 2003). Meat with a higher SFA content is less susceptible to lipid oxidation (Yagoubi et al., 2018).

Changes in the a* and the oxymyoglobin values of meat are driven by lipid oxidation and are strongly correlated with malonaldehyde content (Ladeira et al., 2014). Even though only the malonaldehyde content of fresh (day 0) lamb muscle tissue and that of frozen storage (90 d) were substantially affected by dietary treatment, the lack of effect (P >0.05) regarding the redness index of the same cuts on day 0 seemed not to support this hypothesis. A lack of literature regarding protein content and quality related to oxidative stability of meat as well as quality parameters is evident, and more research is required in this regard.

 

Conclusions

A higher diet NPN content of low-fibre finishing SAMM lamb diets increases the lipid and SFA content of muscle tissue but decreases UFA and CLA content of adipose tissue. Diet NPN content had a limited effect on the tenderness and stability of SAMM lamb muscle tissue. There appears to be inadequate literature regarding protein research and its effect on finishing lamb meat quality, which requires more attention. This study should also be repeated using the same treatments to determine the effect on lamb rumen pH and microbial composition.

 

Acknowledgements

Support staff at the Department of Animal Science (University of the Free State) and Ms Liesl van der Westhuizen (Science Writer, University of the Free State) are acknowledged.

Funding

This study was funded by the Directorate Research and Development of the University of the Free State, Bloemfontein, South Africa.

Authors' contributions

OBE, AVF, and AH designed the experiment and OBE carried out the research trial. MDF completed the statistical analyses. OBE and AH structured the scientific content and OBE drafted the manuscript. AVF and AH assisted with the experimental design and research trial, while all authors provided editorial suggestions and approved the final manuscript. AH conducted the meat quality analysis.

Conflict of interest

The authors declare that there is no conflict of interest.

 

References

Abdalla Filho, A.L., Corrêa, P.S., Lemos, L.N., Dineshkumar, D., Issakowicz, J., Ieda, E.H., Lima, P.M.T., Barreal, M., McManus, C., Mui, T.S., Abdalla, A.L. & Louvandini, H., 2017. Diets based on plants from Brazilian Caatinga altering ruminal parameters, microbial community, and meat fatty acids of Santa Inês lambs. Small Rumin. Res. 154, 70-77. https://doi.org/10.1016/j.smallrumres.2017.07.005        [ Links ]

Alfaia, C.M.M., Castro, M.L.F., Martins, S.I.V., Portugal, A.P.V., Alves, S.P.A., Fontes, C.M.G.A., Bessa, R.J.B. & Prates, J.A.M., 2007. Effect of slaughter season on fatty acid composition, conjugated linoleic acid isomers, and nutritional value of intramuscular fat in Barrosã-PDO veal. Meat Sci. 75, 44-52. https://doi.org/10.1016/j.meatsci.2006.06.013        [ Links ]

AlZahal, O., Odongo, N.E., Mutsvangwa, T., Or-Rashid, M.M., Duffield, T.F., Bagg, R., Dick, P., Vessie, G. & McBride, B.W., 2008. Effects of monensin and dietary soybean oil on milk fat percentage and milk fatty acid profile in lactating dairy cows. J. Dairy Sci. 91, 1166-1174. https://doi.org/10.3168/jds.2007-0232        [ Links ]

American Meat Science Association (AMSA), 1978. Guidelines for cooking and sensory evaluation of meat. American Meat Science Association, National Livestock and Meat Board, Chicago, IL.         [ Links ]

Bas, P., Archimède, H., Rouzeau, A. & Sauvant, D., 2003. Fatty acid composition of mixed-rumen bacteria: Effect of concentration and type of forage. J. Dairy Sci. 86, 2940-2948. https://doi.org/10.3168/jds.S0022-0302(03)73891-0        [ Links ]

Bas, P. & Morand-Fehr, P., 2000. Effect of nutritional factors on fatty acid composition of lamb fat deposits. Livest. Prod. Sci. 64, 61-79. https://doi.org/10.1016/S0301-6226(00)00176-7        [ Links ]

Bauman, D.E., Baumgard, L.H., Corl, B.A. & Griinari, J.M., 1999. Biosynthesis of conjugated linoleic acid in ruminants. Proc. Am. Soc. Anim. Sci. 77, 1-15. https://doi.org/10.1016/S1043-4526(05)50006-8        [ Links ]

Beam, T.M., Jenkins, T.C., Moate, P.J., Kohn, R.A. & Palmquist, D.L., 2000. Effects of amount and source of fat on the rates of lipolysis and biohydrogenation of fatty acids in ruminal contents. J. Dairy Sci. 83, 2564-2573. https://doi.org/10.3168/jds.S0022-0302(00)75149-6        [ Links ]

Bessa, R.J.B., Alves, S.P., Jerónimo, E., Alfaia, C.M., Prates, J.A.M. & Santos-Silva, J., 2007. Effect of lipid supplements on ruminal biohydrogenation intermediates and muscle fatty acids in lambs. Eur. J. Lipid Sci. Technol. 109, 868-878. https://doi.org/10.1002/ejlt.200600311        [ Links ]

Bohnert, D.W., Schauer, C.S. & DelCurto, T., 2002. Influence of rumen protein degradability and supplementation frequency on performance and nitrogen use in ruminants consuming low-quality forage: Cow performance and efficiency of nitrogen use in wethers. J. Anim. Sci. 80, 1629-1637. https://doi.org/10.2527/2002.8061629x        [ Links ]

Booyens, K.E., Einkamerer, O.B., Hugo, A., van der Merwe, H.J., Slippers, S.C. & Fair, M.D., 2012. Fatty acid composition and oxidative stability of lambs' meat as affected by a bioflavonoid antioxidant and fat sources. South Afr. J. Anim. Sci. 42, 483-487.         [ Links ]

Buckley, D.J., Morrissey, P.A. & Gray, J.I., 1995. Influence of dietary vitamin E on the oxidative stability and quality of pig meat. J. Anim. Sci. 73, 3122-3130.         [ Links ]

Carvalho, J.R.R., Chizzotti, M.L., Ramos, E.M., Machado Neto, O.R., Lanna, D.P.D., Lopes, L.S., Teixeira, P.D. & Ladeira, M.M., 2014. Qualitative characteristics of meat from young bulls fed different levels of crude glycerin. Meat Sci. 96, 977-983. https://doi.org/10.1016/j.meatsci.2013.10.020        [ Links ]

Castro, T., Manso, T., Jimeno, V., Del Alamo, M. & Mantecón, A.R., 2009. Effects of dietary sources of vegetable fats on performance of dairy ewes and conjugated linoleic acid (CLA) in milk. Small Rumin. Res. 84, 47-53. https://doi.org/10.1016/j.smallrumres.2009.05.005        [ Links ]

Cheeke, P.R., 2005. Applied Animal Nutrition: Feeds and Feeding. Pearson Prentice Hall.         [ Links ]

Chikunya, S., Demirel, G., Enser, M., Wood, J.D., Wilkinson, R.G. & Sinclair, L.A., 2004. Biohydrogenation of dietary n-3 PUFA and stability of ingested vitamin E in the rumen, and their effects on microbial activity in sheep. Br. J. Nutr. 91, 539-550. https://doi.org/10.1079/BJN20031078        [ Links ]

Chilliard, Y. & Ferlay, A., 2004. Dietary lipids and forages interactions on cow and goat milk fatty acid composition and sensory properties. Reprod. Nutr. Dev. 44, 467-92.         [ Links ]

Chilliard, Y., Ferlay, A., Rouel, J. & Lamberet, G., 2003. A review of nutritional and physiological factors affecting goat milk lipid synthesis and lipolysis. J. Dairy Sci. 86, 1751-1770. https://doi.org/10.3168/jds.S0022-0302(03)73761-8        [ Links ]

Chilliard, Y., Rouel, J. & Leroux, C., 2006. Goat's alpha-s1 casein genotype influences its milk fatty acid composition and delta-9 desaturation ratios. Anim. Feed Sci. Technol., Special Issue: Modifying Milk Composition 131, 474-487. https://doi.org/10.1016/j.anifeedsci.2006.05.025        [ Links ]

Choi, N.-J., Imm, J.Y., Oh, S., Kim, B.-C., Hwang, H.-J. & Kim, Y.J., 2005. Effect of pH and oxygen on conjugated linoleic acid (CLA) production by mixed rumen bacteria from cows fed high concentrate and high forage diets. Anim. Feed Sci. Technol. 123-124, 643-653. https://doi.org/10.1016/j.anifeedsci.2005.04.054        [ Links ]

Cooke, D.W.I., Monahan, F.J., Brophy, P.O. & Boland, M.P., 2004. Comparison of concentrates or concentrates plus forages in a total mixed ration or discrete ingredient format: Effects on beef production parameters and on beef composition, colour, texture and fatty acid profile. Ir. J. Agric. Food Res. 43, 201-216.         [ Links ]

Cooper, S.L., Sinclair, L.A., Wilkinson, R.G., Hallett, K.G., Enser, M. & Wood, J.D., 2004. Manipulation of the n-3 polyunsaturated fatty acid content of muscle and adipose tissue in lambs. J. Anim. Sci. 82, 1461-1470.         [ Links ]

Dang Van, Q.C., Focant, M., Mignolet, E., Turu, C., Froidmont, E. & Larondelle, Y., 2011. Influence of the diet structure on ruminal biohydrogenation and milk fatty acid composition of cows fed extruded linseed. Anim. Feed Sci. Technol. 169, 1-10. https://doi.org/10.1016/j.anifeedsci.2011.05.002        [ Links ]

Dawson, L.E.R., Fearon, A.M., Moss, B.W. & Woods, V.B., 2010. Effects of substitution of a proportion of the concentrate in grass silage/concentrate-based diets with extruded linseed on performance and meat quality of dairy bulls. Anim. Feed Sci. Technol. 156, 10-18. https://doi.org/10.1016/j.anifeedsci.2009.11.005        [ Links ]

De Smet, S., Raes, K. & Demeyer, D., 2004. Meat fatty acid composition as affected by fatness and genetic factors: A review. Anim. Res. 53, 81-98. https://doi.org/10.1051/animres:2004003        [ Links ]

Dehority, B.A., 2003. Rumen Microbiology. Nottingham University Press.         [ Links ]

Demeyer, D. & Doreau, M., 1999. Targets and procedures for altering ruminant meat and milk lipids. Proc. Nutr. Soc. 58, 593-607. https://doi.org/10.1017/S0029665199000786        [ Links ]

Demirel, G., Ozpinar, H., Nazli, B. & Keser, O., 2006. Fatty acids of lamb meat from two breeds fed different forage:concentrate ratio. Meat Sci. 72, 229-235. https://doi.org/10.1016/j.meatsci.2005.07.006        [ Links ]

Dewhurst, R.J., Shingfield, K.J., Lee, M.R.F. & Scollan, N.D., 2006. Increasing the concentrations of beneficial polyunsaturated fatty acids in milk produced by dairy cows in high-forage systems. Anim. Feed Sci. Technol. 131, 168-206. https://doi.org/10.1016/j.anifeedsci.2006.04.016        [ Links ]

Du Toit, A.N., Einkamerer, O.B., Hugo, A., van der Merwe, H.J. & Fair, M.D., 2013. The effect of dietary lipid saturation and monensin-Na on the CLA content of lambs' meat. South Afr. J. Anim. Sci. 43, 75-80.         [ Links ]

Fievez, V., Boeckaert, C., Vlaeminck, B., Mestdagh, J. & Demeyer, D., 2007. In vitro examination of DHA-edible micro-algae. 2. Effect on rumen methane production and apparent degradability of hay. Anim. Feed Sci. Technol. 136, 80-95. https://doi.org/10.1016/j.anifeedsci.2006.08.016        [ Links ]

Folch, J., Lees, M. & Sloane Stanley, G.H., 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509. https://doi.org/10.1016/S0021-9258(18)64849-5        [ Links ]

French, P., Stanton, C., Lawless, F., O'Riordan, E.G., Monahan, F.J., Caffrey, P.J. & Moloney, A.P., 2000. Fatty acid composition, including conjugated linoleic acid, of intramuscular fat from steers offered grazed grass, grass silage, or concentrate-based diets. J. Anim. Sci. 78, 2849-2855. https://doi.org//2000.78112849x        [ Links ]

Gerson, B.Y.T., John, A., Shelton, I.D. & Sinclair, B.R., 1982. Effects of dietary N on lipids of rumen digesta, plasma, liver, muscle and perirenal fat in sheep. J Agric Sci Camb 99, 71 -78. https://doi.org/10.1017/S0021859600055052        [ Links ]

Gerson, T., John, A. & King, A., 1985. The effects of dietary starch and fibre on the in vitro rates of lipolysis and hydrogenation by sheep rumen digesta. J Agric SciCamb 105, 27-30. https://doi.org/10.1017/S0021859600055659        [ Links ]

Gerson, T., John, A. & Sinclair, B.R., 1983. The effect of dietary N on in vitro lipolysis and fatty acid hydrogenation in rumen digesta from sheep fed diets high in starch. J. Agric. Sci. 101, 97-101. https://doi.org/10.1017/S0021859600036406        [ Links ]

Gómez-Cortés, P., Bach, A., Luna, P., Juárez, M. & de la Fuente, M.A., 2009. Effects of extruded linseed supplementation on n-3 fatty acids and conjugated linoleic acid in milk and cheese from ewes. J. Dairy Sci. 92, 4122-34. https://doi.org/10.3168/jds.2008-1909        [ Links ]

Hajji, H., Joy, M., Ripoll, G., Smeti, S., Mekki, I., Gahete, F.M., Mahouachi, M. & Atti, N., 2016. Meat physicochemical properties, fatty acid profile, lipid oxidation and sensory characteristics from three North African lamb breeds, as influenced by concentrate or pasture finishing diets. J. Food Compos. Anal. 48, 102-110. https://doi.org/10.1016/j.jfca.2016.02.011        [ Links ]

Harfoot, C.G. & Hazlewood, G.P., 1997. Lipid metabolism in the rumen, in: Hobson, P.N., Stewart, C.S. (Eds.), The Rumen Microbial Ecosystem. Springer, Dordrecht, pp. 382-426. https://doi.org/10.1007/978-94-009-1453-7_9        [ Links ]

Hoover, W.H., 1986. Chemical factors involved in ruminal fiber digestion. J. Dairy Sci. 69, 2755-2766. https://doi.org/10.3168/jds.S0022-0302(86)80724-X        [ Links ]

Hristov, A.N., Bannink, A., Crompton, L.A., Huhtanen, P., Kreuzer, M., McGee, M., Nozière, P., Reynolds, C.K., Bayat, A.R., Yáñez-Ruiz, D.R., Dijkstra, J., Kebreab, E., Schwarm, A., Shingfield, K.J. & Yu, Z., 2019. Invited review: Nitrogen in ruminant nutrition: A review of measurement techniques. J. Dairy Sci. 102, 5811-5852. https://doi.org/10.3168/jds.2018-15829        [ Links ]

Hur, S.J., Kim, H.S., Bahk, Y.Y. & Park, Y., 2017. Overview of conjugated linoleic acid formation and accumulation in animal products. Livest. Sci. 195, 105-111. https://doi.org/10.1016/j.livsci.2016.11.016        [ Links ]

Ishlak, A., Günal, M. & AbuGhazaleh, A.A., 2015. The effects of cinnamaldehyde, monensin and quebracho condensed tannin on rumen fermentation, biohydrogenation and bacteria in continuous culture system. Anim. Feed Sci. Technol. 207, 31-40. https://doi.org/10.1016/j.anifeedsci.2015.05.023        [ Links ]

Ivan, M., Mir, P.S., Koenig, K.M., Rode, L.M., Neill, L., Entz, T. & Mir, Z., 2001. Effects of dietary sunflower seed oil on rumen protozoa population and tissue concentration of conjugated linoleic acid in sheep. Small Rumin. Res. 41, 215-227. https://doi.org/10.1016/S0921-4488(01)00220-6        [ Links ]

Jenkins, T.C., 1993. Lipid metabolism in the rumen. J. Dairy Sci. 76, 3851-3863. https://doi.org/10.3168/jds.S0022-0302(93)77727-9        [ Links ]

Jenkins, T.C., Wallace, R.J., Moate, P.J. & Mosley, E.E., 2008. Board-Invited Review: Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J. Anim. Sci. 86, 397-412. https://doi.org/10.2527/jas.2007-0588        [ Links ]

Jimenez, A.G., Winward, J.D., Walsh, K.E. & Champagne, A.M., 2020. Effects of membrane fatty acid composition on cellular metabolism and oxidative stress in dermal fibroblasts from small and large breed dogs. J. Exp. Biol. jeb.221804. https://doi.org/10.1242/jeb.221804        [ Links ]

Junkuszew, A., Nazar, P., Milerski, M., Margetin, M., Brodzki, P. & Bazewicz, K., 2020. Chemical composition and fatty acid content in lamb and adult sheep meat. Arch. Anim. Breed. 63, 261-268. https://doi.org/10.5194/aab-63-261-2020        [ Links ]

Kellems, R.O. & Church, D.C., 2010. Livestock feeds and feeding, 6th ed. Pearson Prentice Hall.         [ Links ]

Kramer, J.K.G., Blackadar, C.B., Zhou, J., 2002. Evaluation of two GC columns (60-m SUPELCOWAX 10 and 100-m CP Sil 88) for analysis of milkfat with emphasis on CLA, 18:1, 18:2 and 18:3 isomers, and short- and long-chain FA. Lipids 37, 823-835.         [ Links ]

Kropp, J.R., Johnson, R.R., Males, J.R. & Owens, F.N., 1977. Microbial protein synthesis with low quality roughage rations: Isonitrogenous Substitution of urea for soybean meal. J. Anim. Sci. 45, 837-843. https://doi.org/10.2527/jas1977.454837x        [ Links ]

Kucuk, O., Hess, B.W. & Rule, D.C., 2008. Fatty acid compositions of mixed ruminal microbes isolated from sheep supplemented with soybean oil. Res. Vet. Sci. 84, 215-224. https://doi.org/10.1016/j.rvsc.2007.04.010        [ Links ]

Ladeira, M.M., Santarosa, L.C., Chizzotti, M.L., Ramos, E.M., Neto, O.R.M., Oliveira, D.M., Carvalho, J.R.R., Lopes, L.S. & Ribeiro, J.S., 2014. Fatty acid profile, color and lipid oxidation of meat from young bulls fed ground soybean or rumen protected fat with or without monensin. Meat Sci. 96, 597-605. https://doi.org/10.1016/j.meatsci.2013.04.062        [ Links ]

Lerch, S., Shingfield, K.J., Ferlay, A., Vanhatalo, A. & Chilliard, Y., 2012. Rapeseed or linseed in grass-based diets: Effects on conjugated linoleic and conjugated linolenic acid isomers in milk fat from Holstein cows over 2 consecutive lactations. J. Dairy Sci. 95, 7269-7287. https://doi.org/10.3168/jds.2012-5654        [ Links ]

Lestingi, A., Facciolongo, A.M., De Marzo, D., Nicastro, F. & Toteda, F., 2015. The use of faba bean and sweet lupin seeds in fattening lamb feed. 2. Effects on meat quality and fatty acid composition. Small Rumin. Res. 131, 2-5. https://doi.org/10.1016/j.smallrumres.2015.07.003        [ Links ]

Luciano, G., Monahan, F.J., Vasta, V., Pennisi, P., Bella, M. & Priolo, A., 2009. Lipid and colour stability of meat from lambs fed fresh herbage or concentrate. Meat Sci. 82, 193-199. https://doi.org/10.1016/j.meatsci.2009.01.010        [ Links ]

Manso, T., Bodas, R., Castro, T., Jimeno, V. & Mantecon, A.R., 2009. Animal performance and fatty acid composition of lambs fed with different vegetable oils. Meat Sci. 83, 511-516. https://doi.org/10.1016/j.meatsci.2009.06.035        [ Links ]

Martin, S.A. & Jenkins, T.C., 2002. Factors affecting conjugated linoleic acid and trans-C18:1 fatty acid production by mixed ruminal bacteria. J Anim Sci 80, 3347-3352.         [ Links ]

McDonald, P., Edwards, R.A., Greenhalgh, J.F.D., Morgan, C.A., Sinclair, L.A. & Wilkinson, R.G., 2011. Animal Nutrition, 7th ed. Pearson, Prentice Hall. https://doi.org/10.1016/S0271-5317(83)80066-9        [ Links ]

Mcguire, M.A. & Mcguire, M.K., 1999. Conjugated linoleic acid (CLA): A ruminant fatty acid with beneficial effects on human health. Proc. Am. Soc. Anim. Sci. 77, 1-8. https://doi.org/10.2527/jas2000.00218812007700ES0033x        [ Links ]

Murariu, O.C., Murariu, F., Frunza, G., Ciobanu, M.M. & Boisteanu, P.C., 2023. Fatty acid indices and the nutritional properties of karakul sheep meat. Nutrients 15, 1061. https://doi.org/10.3390/nu15041061        [ Links ]

National Research Council (NRC), 2007. Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids. The National Academies Press. Washington, DC, USA.         [ Links ]

National Research Council (NRC), 1996. Nutrient Requirements of Beef Cattle, 7th ed. National Academy Press, Washington D.C., USA.         [ Links ]

Nolte, J.V.E. & Ferreira, A.V., 2005. The effect of rumen degradable protein level and source on the duodenal essential amino acid profile of sheep. South Afr. J. Anim. Sci. 35, 162-171. https://doi.org/10.4314/sajas.v35i3.4055        [ Links ]

Nong, Q., Wang, L., Zhou, Y., Sun, Y., Chen, W., Xie, J., Zhu, X. & Shan, T., 2020. Low dietary n-6/n-3 PUFA ratio regulates meat quality, reduces triglyceride content, and improves fatty acid composition of meat in Heigai pigs. Anim. Open Access J. MDPI 10, 1543. https://doi.org/10.3390/ani10091543        [ Links ]

Oka, A., Iwaki, F., Dohgo, T., Ohtagaki, S., Noda, M., Shiozaki, T., Endoh, O. & Ozaki, M., 2002. Genetic effects on fatty acid composition of carcass fat of Japanese Black Wagyu steers. J Anim Sci 80, 1005-1011.         [ Links ]

Oltjen, R.R., 1969. Effects of feeding ruminants non-protein nitrogen as the only nitrogen source. Am. Soc. Anim. Sci. 60, 673-682.         [ Links ]

Owens, F.N., Qi, S. & Sapienza, D.A., 2014. INVITED REVIEW: Applied protein nutrition of ruminants-Current status and future directions. Prof. Anim. Sci. 30, 150-179. https://doi.org/10.15232/S1080-7446(15)30102-9        [ Links ]

Pittroff, W., Keisler, D.H. & Blackburn, H.D., 2006. Effects of a high-protein, low-energy diet in finishing lambs: Feed intake, estimated nutrient uptake, and levels of plasma metabolites and metabolic hormones. Livest. Sci. 101, 262-277. https://doi.org/10.1016/j.livprodsci.2005.11.018        [ Links ]

Polan, C.E., 1992. Protein and amino acids for lactating cows, in: Van Horn, H.H., Wilcox, C.J. (Eds.), Large Dairy Herd Management. American Dairy Science Association, pp. 236-247.         [ Links ]

Priolo, A., Micol, D., Agabriel, J., Prache, S. & Dransfield, E., 2002. Effect of grass or concentrate feeding systems on lamb carcass and meat quality. Meat Sci. 62, 179-185. https://doi.org/10.1016/S0309-1740(01)00244-3        [ Links ]

Qiu, X., Eastridge, M.L., Griswold, K.E. & Firkins, J.L., 2004. Effects of substrate, passage rate, and pH in continuous culture on flows of conjugated linoleic acid and trans C18:1. J. Dairy Sci. 87, 3473-3479. https://doi.org/10.3168/jds.S0022-0302(04)73482-7        [ Links ]

Raharjo, Sri., Sofos, J.N. & Schmidt, G.R., 1992. Improved speed, specificity, and limit of determination of an aqueous acid extraction thiobarbituric acid-C18 method for measuring lipid peroxidation in beef. J. Agric. Food Chem. 40, 2182-2185. https://doi.org/10.1021/jf00023a027        [ Links ]

Ribeiro, D.M., Planchon, S., Leclercq, C.C., Dentinho, M.T.P., Bessa, R.J.B., Santos-Silva, J., Paulos, K., Jerónimo, E., Renaut, J. & Almeida, A.M., 2020. The effects of improving low dietary protein utilization on the proteome of lamb tissues. J. Proteomics 223, 103798. https://doi.org/10.1016/j.jprot.2020.103798        [ Links ]

Ripoll, G., Joy, M. & Muñoz, F., 2011. Use of dietary vitamin E and selenium (Se) to increase the shelf life of modified atmosphere packaged light lamb meat. Meat Sci. 87, 88-93. https://doi.org/10.1016/j.meatsci.2010.09.008        [ Links ]

Santos-Silva, J., Mendes, I., Portugal, P.V. & Bessa, R.J.B., 2004. Effect of particle size and soybean oil supplementation on growth performance, carcass and meat quality and fatty acid composition of intramuscular lipids of lambs. Livest. Prod. Sci. 90, 79-88. https://doi.org/10.1016/j.livprodsci.2004.02.013        [ Links ]

Statistical Analysis Software (SAS), 1999. Statistical Analysis System User's Guide, 6th ed. SAS Institute Inc., Raleigh, North Carolina. USA.         [ Links ]

Scollan, N., Hocquette, J.F., Nuernberg, K., Dannenberger, D., Richardson, I. & Moloney, A., 2006. Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Sci. 74, 17-33. https://doi.org/10.1016/j.meatsci.2006.05.002        [ Links ]

Scollan, N.D., Enser, M., Gulati, S.K., Richardson, I. & Wood, J.D., 2003. Effects of including a ruminally protected lipid supplement in the diet on the fatty acid composition of beef muscle. Br. J. Nutr. 90, 709-716. https://doi.org/10.1079/BJN2003933        [ Links ]

Soto-Navarro, S.A., Goetsch, A.L., Sahlu, T., Puchala, R. & Dawson, L.J., 2003. Effects of ruminally degraded nitrogen source and level in a high concentrate diet on site of digestion in yearling Boer x Spanish wether goats. Small Rumin. Res. 50, 117-128. https://doi.org/10.1016/S0921-4488(03)00120-2        [ Links ]

Swanson, K.C., Freetly, H.C. & Ferrell, C.L., 2004. Nitrogen balance in lambs fed a high-concentrate diet and infused with differing proportions of casein in the rumen and abomasum. J. Anim. Sci. 82, 495-501. https://doi.org/10.2527/2004.822495x        [ Links ]

Tadele, Y. & Amha, N., 2015. Use of different non protein nitrogen sources in ruminant nutrition: A review. Adv. Life Sci. Technol. 29.         [ Links ]

Van Soest, P.J., Robertson, J.B. & Lewis, B., 1991. Polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583-3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2        [ Links ]

Vatansever, L., Kurt, E., Enser, M., Nute, G.R., Scollan, N.D., Wood, J.D. & Richardson, R.I., 2000. Shelf life and eating quality of beef from cattle of different breeds given diets differing in n-3 polyunsaturated fatty acid composition. Anim. Sci. 71, 471-482. https://doi.org/10.1017/S135772980005548X        [ Links ]

Wang, L., Huang, Y., Wang, Y. & Shan, T., 2021. Effects of polyunsaturated fatty acids supplementation on the meat quality of pigs: A meta-analysis. Front. Nutr. 8, 746765. https://doi.org/10.3389/fnut.2021.746765        [ Links ]

Webb, E.C. & O'Neill, H.A., 2008. The animal fat paradox and meat quality. Meat Sci. 80, 28-36. https://doi.org/10.1016/j.meatsci.2008.05.029        [ Links ]

Wood, J.D., Enser, M., Fisher, A.V., Nute, G.R., Sheard, P.R., Richardson, R.I., Hughes, S.I. & Whittington, F.M., 2008. Fat deposition, fatty acid composition and meat quality: A review. Meat Sci. 78, 343-358. https://doi.org/10.1016/j.meatsci.2007.07.019        [ Links ]

Wood, J.D., Richardson, R.I., Nute, G.R., Fisher, A.V., Campo, M.M., Kasapidou, E., Sheard, P.R. & Enser, M., 2003. Effects of fatty acids on meat quality: A review. Meat Sci. 66, 21-32. https://doi.org/10.1016/S0309-1740(03)00022-6        [ Links ]

Xu, L., He, M.L., Liang, R.F., McAllister, T.A. & Yang, W.Z., 2014. Effects of grain source and monensin level on growth performance, carcass traits, and fatty acid profile in feedlot beef steers. Anim. Feed Sci. Technol. 198, 141-150. https://doi.org/10.1016/j.anifeedsci.2014.10.015        [ Links ]

Yagoubi, Y., Joy, M., Ripoll, G., Mahouachi, M., Bertolín, J.R. & Atti, N., 2018. Rosemary distillation residues reduce lipid oxidation, increase alpha-tocopherol content, and improve fatty acid profile of lamb meat. Meat Sci. 136, 23-29. https://doi.org/10.1016/j.meatsci.2017.10.007        [ Links ]

Ye, Y., Eyres, G.T., Reis, M.G., Schreurs, N.M., Silcock, P., Agnew, M.P., Johnson, P.L., Maclean, P. & Realini, C.E., 2020. Fatty acid composition and volatile profile of m. longissimus thoracis from commercial lambs reared in different forage systems. Foods 9, 1885. https://doi.org/10.3390/foods9121885        [ Links ]

Zhu, J., Ren, A., Jiao, J., Shen, W., Yang, L., Zhou, C. & Tan, Z., 2022. Effects of non-protein nitrogen sources on in vitro rumen fermentation characteristics and microbial diversity. Front. Anim. Sci. 3. https://doi.org/10.3389/fanim.2022.891898        [ Links ]

Zurak, D., Kljak, K. & Aladrović, J., 2023. Metabolism and utilisation of non-protein nitrogen compounds in ruminants: A review. J. Cent. Eur. Agric. 24, 1-14. https://doi.org/10.5513/JCEA01/24.L3645        [ Links ]

 

 

Submitted 15 March 2024
Accepted 8 July 2024
Published 28 August 2024

 

 

# Corresponding author: einkamererob@ufs.ac.za