Shedrach Benjamin Pewan1,2
John Roger Otto1
Robert Tumwesigye Kinobe1
Oyelola Abdulwasiu Adegboye3
Aduli Enoch Othniel Malau-Aduli1*- 1Animal Genetics and Nutrition, Veterinary Sciences Discipline, College of Public Health, Medical and Veterinary Sciences, Division of Tropical Health and Medicine, James Cook University, Townsville, QLD, Australia
- 2National Veterinary Research Institute, Vom, Plateau State, Nigeria
- 3Public Health and Tropical Medicine Discipline, College of Public Health, Medical and Veterinary Sciences, Division of Tropical Health and Medicine, James Cook University, Townsville, QLD, Australia
Meat eating quality indices such as intramuscular fat content (IMF) and fat melting point (FMP) of the Longissimus thoracis et lumborum muscle and the feedlot performance, carcass traits, and commercial wholesale cuts of lot-fed Tattykeel Australian White (TAW) MARGRA lambs as a result of dietary fortification of the diet with omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA) were evaluated. A total of 75 TAW MARGRA lambs at 6 months of age with an average liveweight of 30 ± 1.2 kg were used. The lambs were randomly allocated to the following three dietary treatments of 25 lambs each in a 47-day feeding trial using a completely randomized experimental design: (1) control diet of hay plus pellets without omega-3 oil, (2) hay plus commercial whole grain pellets (MSM) without omega-3 oil, and (3) hay plus pellets fortified with omega-3 oil. It was hypothesized that dietary supplementation with omega-3 fortified pellets will improve feedlot performance, meat-eating quality indices of IMF, FMP, and carcass characteristics. Lot-fed lambs on the MSM whole grain had the highest feed intake of 1.69 kg/day, followed by the control at 1.57 kg/day and the lowest in the omega-3 diet at 1.01 kg/day (p = 0.0001). However, the omega-3 diet had the highest average daily gain of 230 g/head/day (p = 0.0001), indicating the greatest feed efficiency since it had the best growth response with minimal feed intake. Post-slaughter evaluation of the Longissimus thoracis et lumborum muscle revealed significant treatment variations in IMF (p = 0.0001), FMP (p = 0.0001), pH (p = 0.0380), and wholesale French rack primal cut (p = 0.0001). Strong correlations (p < 0.05) between liveweight, temperature, pH, FMP, and IMF were observed. Similarly, significant correlations between carcass characteristics of total saleable meat yield, lean trim, fat trims, bones, and leg shank were evident (p < 0.05). However, there were no treatment differences in the final liveweight, GR fat depth, hot standard carcass weight, or dressing percentage. The findings indicate that feedlot performance, meat-eating quality traits such as IMF and FMP, and commercial wholesale French rack cuts can be further improved during feedlot finishing of TAW MARGRA lambs through dietary supplementation with omega-3 oils, and hence the tested hypothesis of improved meat quality attributes is partially confirmed.
Introduction
As the world's fourth most consumed meat after pork, poultry, and beef (1), lamb meat contributes significantly to global human nutrition since it contains nutrients of high biological value (2). In 2021, Australia was ranked second in global sheep production after China, and the latter still imports sheep meat as local production cannot meet its domestic needs (3). As the world's largest sheep exporter in 2021, Australia's overall sheep meat exports increased by 5.3% to $3.96 billion, representing a 0.5% increase in contribution to the overall worth of exports to the national economy (3).
Lamb consumers demand fresh, tasty, safe, and microbe-free meat with high eating quality and nutrient content, thus necessitating advanced nutrition and breeding strategies that integrate appropriate meat quality characteristics by sheep producers (4) to improve feedlot performance, dressing percentage, lean yield, and marbling score (5, 6). To achieve accelerated lamb growth and early attainment of appropriate slaughter weights that meet market specifications, feedlotting remains a critical lamb finishing strategy for improving profitability (7, 8). It also facilitates the production of more uniform lamb carcasses (9) from a low mortality system that ensures more efficient use of human and technical resources to attain improved meat yield and quality (10). However, increased feed cost is a major limiting factor in the feedlot system (11), accounting for 65%−70% of the total cost of small ruminant production (12). As such, nutritional strategies for increasing animal growth performance using cheap feeds without compromising carcass nutrient value and eating quality are essential elements for a profitable livestock production enterprise to consider (13). Hence, there is a need for concerted research efforts in exploring diverse dietary fortification options.
The red meat industry is experiencing modernization in its production system to meet current consumer demands associated with health, quality of life, and sustainability (14). The profile and quality of fatty acids in lamb can be improved by incorporating lipid sources into the diet of lot-fed lambs to boost the levels of omega-3 long-chain polyunsaturated fatty acids (n-3 LC PUFA) known to be beneficial for human health (14, 15). Meat industry producers and processors aim at producing heavy carcasses of young animals with good musculature, supplying desired meat cut yields and an attainable fat layer to protect carcasses while in cold storage (16). Intramuscular fat (IMF), fat melting point (FMP), and pH are essential quality indicators of red meat (17). The high marbling score represents the improved amount of IMF, water holding capacity, tenderness, flavor, juiciness, lamb palatability (18, 19), content, and distribution of protein in the muscle fibers (20).
To the best of our current knowledge of the published literature, this is the first study to fortify the diets of TAW MARGRA lambs with n-3 LC-PUFA to enhance feedlot performance, carcass characteristics, commercial wholesale cut yields, and meat eating quality traits.
Materials and methods
Animals, study location, dietary treatments, experimental design, and feed intake
The animals, study location, dietary treatments, and experimental design have already been described in detail by Pewan et al. (21). Briefly, TAW MARGRA lamb breed was developed from the rigorous selection, culling, and linebreeding of Texel, Van Rooy, Dorper, and Poll Dorset with an extensive utilization of natural mating, artificial insemination, and embryo transfer (21). TAW MARGRA lamb is a special breed of lamb with a low FMP (28–39oC) compared to the ranges of 40.6–48.0°C and 41.5–44.0°C reported in the study by Flakemore et al. (22) and Holman et al. (23) for purebred and crossbred Merino, Dorset, Black, and White Suffolk sheep. Similarly, TAW lambs contained EPA+DHA content of 32.4 ± 8.5 mg per 100 g of muscle, surpassing the 30 mg limit set by Food Standards of Australia and New Zealand (FSANZ) for the “source” claim (24).
The feedlot finishing feeding trial was performed at Crown Agriculture's lamb feedlot facility at Borenore, New South Wales, Australia, from April to June 2019. The study utilized 75 TAW MARGRA lambs at 6 months of age with an average liveweight of 30 ±1.2 kg. The lambs were dewormed and allowed a 14-day adjustment period with ad libitum access to water and the gradual introduction of three experimental diets to minimize any gastrointestinal disorders. The lambs were randomly allocated to the following three dietary treatments of 25 lambs each in a 47-day feeding trial using a completely randomized experimental design: (1) control diet of hay plus pellets without omega-3 oil, (2) hay plus commercial whole grain pellets (MSM) without omega-3 oil, and (3) hay plus pellets fortified with omega-3 oil. All lambs were fed in groups (control, MSM, and omega-3). All these three diets were formulated to be isonitrogenous (CP = 14%) and isocaloric (ME = 10.258 Mj/kg DM). Details of the nutrient compositions have been published by Pewan et al. (21). The feeding troughs had electronic sensors, where each animal's identification, liveweight, feed intake, average daily gains, and other vital parameters were automatically recorded, cloud-stored, and downloaded at the required time. At the end of the feeding trial, the lambs were transported to the Gundagai Meat Processing plant, held in lairage overnight, and humanely sacrificed as a single mob in line with Meat Standards Australia specifications. The carcasses were subjected to medium-voltage electrical stimulation before being trimmed and dressed (25). Carcasses were kept in the chiller room for 24 h during which in situ pH and temperature were recorded.
Carcass measurements
Hot standard carcass weight was recorded prior to chilling, and cold carcass weight was measured after removing from the chiller at 4°C after 24 h. The dressing percentage was determined as the hot standard carcass weight (HSCW) divided by the liveweight (LWT) × 100%. In the boning room, the carcasses were cut between the 12th and 13th ribs to measure longissimus dorsi eye muscle area (LMA), back-fat thickness (BF), body wall thickness (BWT), loin marbling score, body and leg conformation scores, and the percentage of boneless, closely trimmed retail cuts (% BCTRC) as described previously by Jaborek et al. (26). Wholesale primal cuts, fat trims, lean, and bone weights were recorded.
Determination of IMF
The technique of Flakemore et al. (27) was used to determine the IMF content of muscle samples. This was carried out by homogenizing and extracting in CHCl3:MeOH (2:1) fat-soluble solvent, phase partition in 5 ml of 10% KCl, and evaporation of the organic layer in weighed porcelain crucibles to get the fat content. The % IMF was computed as follows: [Crucible including fat weight (g) – empty crucible weight (g)]/sample weight (g) × 100.
Determination of FMP
The FMP was determined as described by Mwangi et al. (28) and Pewan et al. (29). Briefly, the muscle samples were placed in an oven at 100°C for 1–2 min to obtain fat that was used for FMP determination. Through air suction, the melted fat was sucked into thin capillary tubes and kept in a refrigerator for 10 min at 4°C to permit the fat to freeze. The fat level was marked with an indelible pen, and the capillary tube was affixed to a thermometer held in a glass beaker with ~80 ml of deionised H2O positioned on a heating block. The heating block was slowly heated until the fat “slipped” off the mark. The temperature at which the “slip” occurred was recorded as the FMP.
pH and temperature measurements
pH and temperature were recorded at the 12th to 13th rib from longissimus lumborum muscle from the left side of each carcass as documented by Holman et al. (25) and Hussain et al. (30). Briefly, the initial pH measurement was performed immediately upon entry into the chiller (~30 min post-slaughter). At ~24 h post-mortem, four intermediate measurements were taken before the last pH measurement. A pH meter (WP-80, TPS Pty Ltd., Queensland) fitted with a polypropylene spear-type gel electrode (IJ-44, Ionode™, TPS Pty Ltd., Queensland) and calibrated using pH 4.00 and pH 7.00 standards was used for all measurements. The pH meter was initially recalibrated at each interval using standard buffers at a temperature that matched the estimated muscle temperature. This was to compensate for the influence of temperature on pH readings, as per the technical bulletin (WP-80, TPS Pty Ltd., Queensland). Muscle temperature was concurrently documented with the aid of the same pH meter, tailored with a spear-type temperature sensor (no. 121247, TPS Pty Ltd., Queensland).
Statistical analysis
The data were analyzed utilizing nonparametric analytical methods in R. Each animal was regarded as an experimental unit. Meat quality, carcass characteristics, and wholesale cut yields were presented as medians and interquartile range (IQR) and visualized in boxplots after adjustment for treatment effect. Spearman's correlation procedure was used to quantify the relationship between variables. To analyse the effect of treatment on FMP, IMF, and carcass traits, the treatment was defined as the fixed effect. The Kruskal–Wallis test was also used to decide whether or not a statistically significant difference existed between the different feed treatments as previously described (31). Tukey's adjusted multiple comparisons were also used for the pairwise comparison test at p < 0.05.
Results
Liveweight, average daily feed intake, average daily gain, and feed cost
Figure 1 shows the liveweights, average daily feed intake (ADFI), average daily gain (ADG), and feed cost per unit gain as influenced by treatment. In all treatment groups, the liveweights at commencement and the 3-week adaptation period were similar and not significantly different from each other. Similarly, at the end of the 47-day feeding trial, the final liveweights did not differ significantly between treatments. However, lambs fed the omega-3 diet had a significantly (p < 0.0140) lower ADFI (1.01 kg/day) compared to those fed the control (1.57 kg/day) and MSM whole grain (1.69 kg/day) diets. Lambs fed omega-3 diet gained the most weight with an ADG of 230 g/head/day, followed by MSM whole grain (224 g/head/day) and control (194 g/head/day) (p < 0.0390). The result also revealed that n-3 LC PUFA-fortified dietary treatment had the lowest cost in terms of ADFI, followed by control, while MSM whole grain was the most expensive feed. The cost of producing a ton of the control diet was Au$381.55, Au$426.44 for MSM whole grain, and Au$528.30 for the omega-3 diets.
Figure 1. (A–D) Liveweights, average daily feed intake, daily gain, and feed cost per unit gain in lot-fed Tattykeel Australian White MARGRA lambs in different treatment groups. Hays without omega-3 (control); whole grain pellets (MSM); hay plus pellets fortified with omega-3 (Omega). abcSuperscript letters indicate a significant difference among the means in each variable (Tukey's adjusted).
Carcass characteristics, IMF, and FMP
Table 1 shows that IMF and FMP differed significantly among treatments (p < 0.0001). The IMF from lambs fed omega-3 pellets was markedly higher than those fed control and MSM whole grains. The FMP of meat from lambs fed omega-3 diet was the lowest at 30.15°C (29.62–31.85°C) than the control at 34.75°C (34.3–35.3°C) and MSM whole grain at 36.8°C (36.8–37.22°C). The diet fortified with omega-3 led to a marked decrease in FMP (p ≤ 0.0001). Overall, the median (IQR) pH level of TAW MARGRA lambs was 6.13 (6.06–6.19) and significantly differed between treatments (p = 0.0380; Table 1). On the contrary, there was no significant difference in temperature. Using the Kruskal–Wallis test, fortification with omega-3 had no influence on final LWT, GR fat depth, HSCW, and dressing percentage. Regarding cut yields of lot-fed Tattykeel Australian White MARGRA lambs, only wholesale French rack (p = 0.0300) and bones (p = 0.0190) showed significant differences. Tukey's adjusted tests for pairwise comparisons between treatment groups indicate a significant difference in pH between control and MSM whole grain (−0.33, 95% CI: −0.60 to −0.06, p = 0.0198). The omega-3 diet had the lowest FMP and highest IMF.
Table 1. Median (inter-quartile range) of meat quality and carcass characteristics in lot-fed Tattykeel Australian White MARGRA lambs in different treatment groups.
Correlations
There was a significantly strong negative correlation between temperature and pH (r = −0.67, p < 0.05) and between FMP and IMF (r = −0.76, p < 0.05; Figure 2A). As shown in Figure 2B, there was a very strong positive and significant relationship between LWT and HSCW (r = 0.93), while a moderate and positive relationship (r = 0.46) was observed between LWT and fat score and between fat score and HSCW (r = 0.46). Moderately positive and significant correlations (p < 0.001) were observed between fat trim and total yield, bones, and eye of loin (p < 0.001), lean trim and tenderloin (p < 0.001) in Figure 2C. There was a weak and negative correlation between saleable meat and fat trim (p < 0.001).
Figure 2. Correlations between (A) meat quality indices, (B) carcass parameters, and (C) cut yields of lot-fed Tattykeel Australian White MARGRA lambs. Hays without omega-3 (control); whole grain pellets (MSM); hay plus pellets fortified with omega-3 (omega); GR fat depth; hot standard carcass weight (HSCW); liveweight (LWT). ***p = 0.001, **p ≤ 0.01, *p ≤ 0.05.
Discussion
The n-3 LC-PUFA, especially DHA (docosahexaenoic acid; C22:6n-3) and EPA (eicosapentaenoic acid; C20:5n-3), are mainly found in large quantities in oily cold-water fish and seafood, but in insufficient amounts in ruminant meat and milk (32). The n-3 LC-PUFA are known to perform vital physiological roles in maintaining and growing fetuses, neonates, and infant brains (33). The low concentration of n-3 LC PUFA in ruminant muscle tissue is mainly due to extensive lipolysis and biohydrogenation of unsaturated fatty acids (UFA) by ruminal microbes (34, 35). The content of a lamb's diet influences the composition and value of its tissues (36). Furthermore, several trials have indicated that numerous feeding approaches can facilitate the deposition of n-3 LC PUFA in muscle tissues in lambs, resulting in healthier meat (16, 24, 37–42). The use of vegetable seed oils in ruminant diets was found to increase energy and the level of UFA deposited in meat (43). Thus, the resultant meat product had reduced levels of FA that were termed undesirable and enhanced levels that were characterized as beneficial to human health (44). Meat quality indices can be improved by the inclusion of lipid supplements in diets fed to animals raised under feedlot conditions to increase the levels of oleic, linoleic, and linolenic acids and other n-3 LC-PUFA (45, 46). To the best of our knowledge, this is the first study that evaluated the supplementation of diets in TAW MARGRA with promising results.
Liveweight, average daily feed intake, average daily gain, and feed cost
The inclusion of omega-3 oils decreased dry matter intake but led to significantly higher ADG, an indication of better feed conversion efficiency. The higher average daily gain with less feed consumption implies a better utilization of absorbed nutrients from the abomasum either due to a modification of the rumen environment and ecology that favors less biohydrogenation and more by-pass proteins from the rumen or a higher turnover rate of volatile fatty acid absorption. In economic terms, the relatively higher feed cost of the omega-3 fortified diet was offset by the highest feed efficiency of consuming less but growing the fastest in terms of average daily gains, thus leading to improved profitability (47). Therefore, fortification of diets with omega-3 resulted in better feed conversion efficiency, and this may assist lot-fed lambs to attain finishing weight early, thus saving costs and improving profitability for sheep farmers.
Intramuscular fat
Fats are essential nutrients associated with vital physiological functions and are widely distributed within animal tissues and organs such as subcutaneous, intermuscular, and intramuscular fat. Malgwi et al. (48) defined IMF as the quantity of fat resident in meat also referred to as marbling fat. In lambs, Pannier et al. (49) reported IMF values of 1.5–9.5%. In this current study, lambs fed omega-3 diet had IMF values between 1.5 and 9.5% (49) recommended for consumers. Australian lamb consumers prefer a 4–5% IMF threshold for palatability and tenderness (50). Lambs fed control diet had IMF values between 3 and 4%, while lambs fed MSM whole grain diets had IMF values between 2 and 3%. IMF has a significant influence on tenderness, flavor, and juiciness, overall liking (51), meat processing (52), and water holding capacity (53). Tenderness, according to Zhao et al. (54), is an essential factor for the valuation of meat quality, and it affects consumer purchasing and market acceptability decisions. IMF is influenced by both genetic and environmental factors, depending on species, breed, genotype, muscle type, age, gender, and nutritional status (55, 56). Consequently, increasing the level of IMF is fundamental to improving meat quality (56, 57).
The n-3 LC-PUFA profile of muscle tissue and organs of TAW MARGRA lambs in this experiment had been published by Pewan et al. (21). Herein, lambs fed the omega-3 fortified diet had better growth performance indicators than the lambs fed the control and MSM whole grain diets.
Generally, consumers prefer lean lamb with low SFA and high n-3 LC-PUFA. The association between total fat content and relative proportions of fatty acids has long been established owing to the minor impact of membrane phospholipids (58, 59). Furthermore, Scollan et al. (57) reported that the potential for IMF accumulation rests on the equilibrium between uptake, synthesis, and degradation of triacylglycerols. This enhances the accessibility of net energy for fat production during finishing and results in higher IMF content.
Fat melting points
The proportions of single and double bonds influence FMP constituents of fatty acids. For instance, the SFA stearic acid (18:0) and UFA α-linolenic acid (18:3) have melting temperatures of 69.7 and −11°C, respectively (60). The UFA are softer with little heat or energy required to melt them compared to SFA, which are harder requiring more energy to melt. Therefore, the omega-3 fortified diet increased the level of UFA in the muscle tissue, thus accounting for the low FMP recorded in this study.
Muscle pH
The mean pH values (>6.00) obtained were slightly outside the range of 5.3–5.8 after 24 h of slaughter reported by Yagoubi et al. (61), but there were no incidences of dark, firm, and dry (DFD) muscles. This study's results were in accordance with the report of Inserra et al. (62), who fed lambs on diets containing 0% citrus, 24% citrus, and 35% citrus, but in contrast to those of Chiofalo et al. (35) and Ozdogan et al. (63) in cattle and lambs supplemented with olive oil cake. A series of physiological processes, especially glycolysis, occurs before muscles are converted to meat. Under anaerobic conditions after slaughter, the glycogen stored in muscle tissues is converted to lactic acid, leading to a drop in pH (64) and the onset of rigor mortis. Stenberg et al. (64) reported that lambs fed high-energy diets tend to have higher pH values than their counterparts fed low-energy diets. These lambs could have lost a lot of glycogen during transport from the feedlot facility to the abattoir. Generally, muscle pH is a significant indicator of post-mortem animal muscle glycolysis, which is related to water-holding capacity and meat color (65, 66). Lower pH values make the muscle more acidic, bacteriostatic, and fungistatic, thereby hindering bacterial and fungal growth. Lambs fed energy-dense diets have a better capacity to store and replenish glycogen in the muscle tissue and are more capable of coping with pre-slaughter processing, including transport (45). According to Holman et al. (25), the degree of pH decline is significant as meat tenderness is dependent on it. When muscle temperatures decline rapidly, the meat assumes a more rigid state and cold shortening ensues.
Muscle temperature
Dietary treatment did not influence (p > 0.05) temperature, probably due to identical protein, carbohydrate contents, and dry matter intake (45, 67). It is highly unlikely that other physiological factors could have affected the observations in muscle pH since all the animals were wethers of the same breed and age. Stress and excessive exercise before slaughter and electrical inputs during dressing should be minimized as much as possible to reduce muscle temperature.
Wholesale commercial meat cut yields
Lamb cuts have been designed and marketed based on their nutritional quality, offering processors and retailers the ability to use heavy lambs more efficiently (68). The percentage of bone has been reported to be higher and edible tissues lower in younger than older animals (69). This implies that other tissues develop with advancing age, where the proportion of edible tissues rises as the animal ages. This, unfortunately, has its drawbacks, as the meat becomes less tender, but has a more intense odor and flavor (70). Carcasses of lambs on the omega-3 fortified diet were of better conformation, hence the superior French rack yield, more saleable meat, and lean-to-bone ratio than their counterparts fed both MSM and control diets. Body measurements are vital in estimating liveweights for farm animals (71), and this valuable information contributes to decisions in terms of selection and husbandry system aimed at raising the edible lean meat yield and reduction in fat content in carcasses (5). In sheep and goats, cut yields are predictors of overall carcass tissue composition (72). In this study, the measures of the primal cut weights were identical in the three groups, except for bones and French racks. The proportions of bone, muscle, and fat shift during the growth of an animal concurrently with its carcass water, protein, fat, and mineral contents. These are influenced by the animal's age, weight, breed, sex, nutritional status (73, 74), and production system. The weight and yield of carcasses are significant determinants of commercial value with better returns (75). The mean tissue content of the leg showed that the muscles had the greatest contribution (66.70%), followed by bone (18.89%) and fat (10.09%) (76). Bautista-Díaz et al. (77) reported that bones made up 1.46 ± 0.27 kg of suckling lambs. On account of the weights of primal cuts recorded in this study, the carcasses provided reasonable cut yields when the leg, loin, and shoulder were considered (78). Da Trindade Silva et al. (76) reported that these are responsible for an estimated 60% of the entire yield of cuts. Results generated from this study with other carcass traits could therefore be useful when making decisions regarding the selection and the most appropriate husbandry system to employ.
Conclusion
The results of this study showed that dietary fortification with n-3 LC-PUFA enhanced feedlot performance in TAW MARGRA lambs with significant improvement in health-beneficial intramuscular fat content, low-fat melting point, and French rack primal cut yield. The results align with the tested hypothesis that the inclusion of n-3 LC-PUFA in feedlot diets will improve productive performance, carcass characteristics, wholesale commercial French rack primal cut yields, and meat quality traits in TAW MARGRA lambs. The inclusion of omega-3 oils in feedlot diets decreased dry matter intake, increased feed efficiency resulting in faster growth, and healthier meat from supplemented lambs.
Data availability statement
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.
Ethics statement
The animal study was reviewed and approved by James Cook University Animal Ethics Committee (Permit No. A0015657).
Author contributions
Conceptualization, software, project administration, and funding acquisition: AEOM-A. Methodology: AEOM-A, JRO, SBP, OAA, and RTK. Validation: AEOM-A, SBP, and JRO. Formal analysis: SBP and OAA. Investigation: AEOM-A, JRO, SBP, OAA, and RTK. Resources: AEOM-A, RTK, and OAA. Data curation and writing-original draft preparation: SBP. All authors have read and agreed to the published version of the manuscript.
Funding
This study was funded by the Australian Commonwealth Innovations Connections Research Grant, the Science and Industry Endowment Fund (SIEF) Ross Metcalf STEM Business Industrial Research Fellowship jointly funded by Tattykeel Australian White Pty Ltd (awarded to JRO), and a PhD Research Scholarship from the James Cook University, Townsville, Queensland, Australia (awarded to SBP).
Acknowledgments
The authors gratefully acknowledge the James Cook University Postgraduate Research Scholarship Program and College of Public Health, Medical and Veterinary Sciences (for the PhD scholarship awarded to SBP), the Australian Commonwealth Department of Industryd VInnovations Connections, CSIRO SIEF Ross Metcalf STEM Business Industrial Research Fellowship co-funded by Tattykeel Australian White Pty Ltd (awarded to JRO). We are grateful to Tattykeel Australian White Pty Ltd. for access to flock and farm resources, and to the National Veterinary Research Institute Vom, Nigeria (study leave approval for SBP). We are also grateful to Michelle Lauren Elizabeth Henry, Staff and Management of the Gundagai Meat Processing plant for their assistance with abattoir meat sampling, and technical support from Benjamin William Behrens Holman and Felista Waithira Mwangi during sampling and data collection at the Gundagai Meat Processing plant.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
1. Carl BM. Organization for Economic Cooperation and Development (OECD): Members. Trade and the Developing World in the 21st Century. Leiden: Brill Nijhoff (2001), p. 527. doi: 10.1163/9789004480629
2. Flakemore AR, Malau-Aduli BS, Nichols PD, Malau-Aduli AEO. Omega-3 fatty acids, nutrient retention values, and sensory meat eating quality in cooked and raw Australian lamb. Meat Sci. (2017) 123:79–87. doi: 10.1016/j.meatsci.2016.09.006
3. Khadre AABA, Karabacak A. Comparison of fattening performance and carcass traits measurements of Akkaraman and Awassi male lambs. Selcuk J Agr Food Sci. (2018) 32:542–8. doi: 10.15316/SJAFS.2018.135
4. de Nadai Bonin M, Pedrosa VB, e Silva SdL, Bünger L, Ross D, da Costa Gomes R, et al. Genetic parameters associated with meat quality of Nellore cattle at different anatomical points of longissimus: Brazilian standards. Meat Sci. (2021) 171:108281. doi: 10.1016/j.meatsci.2020.108281
5. Sood V, Rodas-González A, Lam S, López-Campos Ó, Segura J, Schwinghamer T, et al. Influence of production factors on beef primal tissue composition. Foods. (2022) 11:518. doi: 10.3390/foods11040518
6. Ross EG, Ball JJ, Werth SJ, Mejia-Turcios SE, Zhao Y, Pan Y, et al. Effect of ractopamine hydrochloride on environmental gas emissions, growth performance, and carcass characteristics in feedlot steers. J Anim Sci. (2021) 99:skab143. doi: 10.1093/jas/skab143
7. Saldanha RB, Cirne LGA, Brant LMS, Rodrigues CS, dos Santos Pina D, de Carvalho Matos S, et al. Productive characteristics of feedlot Santa Inês and Dorper lambs: intake, digestibility, feeding behavior, performance, carcass traits, and meat quality. Trop Anim Health Prod. (2022) 54:1–9. doi: 10.1007/s11250-021-03011-8
8. Arruda MCG, Almeida MTC, Bertoco JPA, Pereira-Junior SA, Castro-Filho ES, Feliciano AL, et al. Soybean molasses to replace corn for feedlot lambs on growth performance, carcass characteristics, and meat quality. Transl Anim Sci. (2021) 5:txaa230. doi: 10.1093/tas/txaa230
9. Brand T, Van Der Merwe D, Swart E, Hoffman L. Comparing the effect of age and dietary energy content on feedlot performance of Boer goats. Small Rumin Res. (2017) 157:40–6. doi: 10.1016/j.smallrumres.2017.10.009
10. van Cleef F, van Cleef E, Longhini V, Nascimento T, Ezequiel J, Ruggieri A. Feedlot performance, carcass characteristics, and meat characteristics of lambs grown under silvopastoral systems. Can J Anim Sci. (2019) 100:385–8. doi: 10.1139/cjas-2019-0057
11. Castro W, Zanine A, Ferreira D, Souza A, Pinho R, Parente M, et al. Delinted cottonseed in diets for finishing sheep. Trop Anim Health Prod. (2020) 52:2461–8. doi: 10.1007/s11250-019-02134-3
12. Zhang X, Li G, Li F, Zhang D, Yuan L, Zhao Y, et al. Effect of feed efficiency on growth performance, body composition, and fat deposition in growing Hu lambs. Anim Biotechnol. (2021) 1–16. doi: 10.1080/10495398.2021.1951747 [Epub ahead of print].
13. Vahedi V, Hedayat-Evrigh N, Holman BW, Ponnampalam EN. Supplementation of macro algae (Azolla pinnata) in a finishing ration alters feed efficiency, blood parameters, carcass traits and meat sensory properties in lambs. Small Rumin Res. (2021) 203:106498. doi: 10.1016/j.smallrumres.2021.106498
14. Fernández-López J, Viuda-Martos M, Pérez-Alvarez JA. Quinoa and chia products as ingredients for healthier processed meat products: technological strategies for their application and effects on the final product. Curr Opin Food Sci. (2021) 40:26–32. doi: 10.1016/j.cofs.2020.05.004
15. Nudda A, Bee G, Correddu F, Lunesu MF, Cesarani A, Rassu SPG, et al. Linseed supplementation during uterine and early post-natal life markedly affects fatty acid profiles of brain, liver and muscle of lambs. Ital J Anim Sci. (2022) 21:361–77. doi: 10.1080/1828051X.2022.2038039
16. da Silva PCG, Brandão Ferreira Ítavo CC, Vinhas Ítavo LC, de Nadai Bonin Gomes M, Dias Feijó GL, Monteiro Ferelli KLS, et al. Carcass traits and meat quality of Texel lambs raised in Brachiaria pasture and feedlot systems. Anim Sci J. (2020) 91:e13394. doi: 10.1111/asj.13394
17. Dixit Y, Al-Sarayreh M, Craigie C, Reis M. A global calibration model for prediction of intramuscular fat and pH in red meat using hyperspectral imaging. Meat Sci. (2021) 181:108405. doi: 10.1016/j.meatsci.2020.108405
18. Realini C, Pavan E, Purchas R, Agnew M, Johnson P, Bermingham E, et al. Relationships between intramuscular fat percentage and fatty acid composition in M. longissimus lumborum of pasture-finished lambs in New Zealand. Meat Sci. (2021) 181:108618. doi: 10.1016/j.meatsci.2021.108618
19. Hitchman S, Loeffen M, Reis M, Craigie C. Robustness of hyperspectral imaging and PLSR model predictions of intramuscular fat in lamb M. longissimus lumborum across several flocks and years. Meat Sci. (2021) 179:108492. doi: 10.1016/j.meatsci.2021.108492
20. Chen F, Wei JT, Yang XH, Zhao N, Zhang W, Huang SW, et al. Effect of pelleted total mixed rations with different levels of intact rapeseed on performance, carcass traits, serum biochemical indices and meat quality of Boer goats. Anim Prod Sci. (2019) 59:82–8. doi: 10.1071/AN17172
21. Pewan SB, Otto JR, Kinobe RT, Adegboye OA, Malau-Aduli AEO. Nutritional enhancement of health beneficial omega-3 long-chain polyunsaturated fatty acids in the muscle, liver, kidney, and heart of Tattykeel Australian White MARGRA lambs fed pellets fortified with omega-3 oil in a feedlot system. Biology. (2021) 10:912. doi: 10.3390/biology10090912
22. Flakemore AR, McEvoy PD, Balogun RO, Malau-Aduli BS, Nichols P, Malau-Aduli AEO. Degummed crude canola oil supplementation affects fat depot melting points in purebred and first-cross Merino sheep. Anim Vet Sci. (2014) 2:75–80. doi: 10.11648/j.avs.20140203.14
23. Holman B, Flakemore A, Kashani A, Malau-Aduli A. Spirulina supplementation, sire breed, sex and basal diet effects on lamb intramuscular fat percentage and fat melting points. Int J Vet Med. (2014) 2014:1–9. doi: 10.5171/2014.263951
24. Van Le H, Nguyen DV, Vu Nguyen Q, Malau-Aduli BS, Nichols PD, Malau-Aduli AEO. Fatty acid profiles of muscle, liver, heart and kidney of Australian prime lambs fed different polyunsaturated fatty acids enriched pellets in a feedlot system. Sci Rep. (2019) 9:1–11. doi: 10.1038/s41598-018-37956-y
25. Holman BW, Kerr MJ, Refshauge G, Diffey SM, Hayes RC, Newell MT, et al. Post-mortem pH decline in lamb semitendinosus muscle and its relationship to the pH decline parameters of the longissimus lumborum muscle: a pilot study. Meat Sci. (2021) 176:108473. doi: 10.1016/j.meatsci.2021.108473
26. Jaborek J, Zerby H, Moeller S, Fluharty F. Effect of energy source and level, and sex on growth, performance, and carcass characteristics of lambs. Small Rumin Res. (2017) 151:117–23. doi: 10.1016/j.smallrumres.2017.04.009
27. Flakemore AR, Balogun RO, McEvoy PD, Malau-Aduli BS, Nichols P, Malau-Aduli AEO. Genetic variation in intramuscular fat of prime lambs supplemented with varying concentrations of degummed crude canola oil. Int J Nutr Food Sci. (2014) 3:203–9. doi: 10.11648/j.ijnfs.20140303.22
28. Mwangi FW, Blignaut DJ, Charmley E, Gardiner CP, Malau-Aduli BS, Kinobe RT, et al. Lipid metabolism, carcass characteristics and Longissimus dorsi muscle fatty acid composition of tropical crossbred beef cattle in response to Desmanthus spp. forage backgrounding. Metabolites. (2021) 11:804. doi: 10.3390/metabo11120804
29. Pewan SB, Otto JR, Kinobe RT, Adegboye OA, Malau-Aduli AEO. MARGRA lamb eating quality and human health-promoting omega-3 long-chain polyunsaturated fatty acid profiles of Tattykeel Australian White Sheep: linebreeding and gender effects. Antioxidants. (2020) 9:1118. doi: 10.3390/antiox9111118
30. Hussain M, Nauman K, Asghar B, Iqbal S, Rashid MA. Effect of low voltage electrical stimulation and chilling on microbial safety and quality attributes of Beetal Bucks and Lohi Rams carcass. Small Rumin Res. (2021) 196:106315. doi: 10.1016/j.smallrumres.2020.106315
31. R Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing (2013).
32. Widmann P, Nuernberg K, Kuehn C, Weikard R. Association of an ACSL1 gene variant with polyunsaturated fatty acids in bovine skeletal muscle. BMC Genet. (2011) 12:1–13. doi: 10.1186/1471-2156-12-96
33. Abdel-Tawwab M, Khalil HS, Maulu S, Nawanzi K. Fish nutritional value as an approach to children's nutrition. Front Nutr. (2021) 8:780844. doi: 10.3389/fnut.2021.780844
34. Amills M, Clop A, Óvilo C. Nutrigenomics of lipid supplementation in ruminants and pigs. In: Galanakis GM editor. Lipids and Edible Oils. Amsterdam: Elsevier (2020). p. 93-131. doi: 10.1016/B978-0-12-817105-9.00003-3
35. Chiofalo V, Liotta L, Lo Presti V, Gresta F, Di Rosa AR, Chiofalo B. Effect of dietary olive cake supplementation on performance, carcass characteristics, and meat quality of beef cattle. Animals. (2020) 10:1176. doi: 10.3390/ani10071176
36. Holman BW, Hayes RC, Newell MT, Refshauge G, McGrath SR, Fowler SM, et al. The quality and mineral composition of the longissimus lumborum and semimembranosus muscles from lambs fed perennial or annual wheat forage with or without lucerne. Meat Sci. (2021) 180:108564. doi: 10.1016/j.meatsci.2021.108564
37. Forwood DL, Holman BW, Hopkins DL, Smyth HE, Hoffman LC, Chaves AV, et al. Feeding unsaleable carrots to lambs increased performance and carcass characteristics while maintaining meat quality. Meat Sci. (2021) 173:108402. doi: 10.1016/j.meatsci.2020.108402
38. Gravador RS, Brunton NP, Fahey AG, Gkarane V, Claffey NA, Moloney AP, et al. Effects of dietary fat sources on the intramuscular and subcutaneous adipose tissue fatty acid composition, and consumer acceptability of lamb. J Sci Food Agric. (2020) 100:2176–84. doi: 10.1002/jsfa.10242
39. Guerreiro O, Alves SP, Soldado D, Cachucho L, Almeida JM, Francisco A, et al. Inclusion of the aerial part and condensed tannin extract from Cistus ladanifer L. in lamb diets–Effects on growth performance, carcass and meat quality and fatty acid composition of intramuscular and subcutaneous fat. Meat Sci. (2020) 160:107945. doi: 10.1016/j.meatsci.2019.107945
40. Le HV, Nguyen QV, Nguyen DV, Otto JR, Malau-Aduli BS, Nichols PD, et al. Enhanced omega-3 polyunsaturated fatty acid contents in muscle and edible organs of Australian prime lambs grazing lucerne and cocksfoot pastures. Nutrients. (2018) 10:1985. doi: 10.3390/nu10121985
41. Nguyen DV, Malau-Aduli BS, Nichols PD, Malau-Aduli AE. Growth performance and carcass characteristics of Australian prime lambs supplemented with pellets containing canola oil or flaxseed oil. Anim Prod Sci. (2018) 58:2100–8. doi: 10.1071/AN16812
42. Flakemore AR, Malau-Aduli BS, Nichols PD, Malau-Aduli AEO. Degummed crude canola oil, sire breed and gender effects on intramuscular long-chain omega-3 fatty acid properties of raw and cooked lamb meat. J Anim Sci Technol. (2017) 59:1–13. doi: 10.1186/s40781-017-0143-7
43. Diogénes L, Bezerra L, Pereira Filho J, Silva Junior J, Oliveira J, Moura J, et al. Effects of the dietary inclusion of buriti oil on lamb performance, carcass traits, digestibility, nitrogen balance, ingestive behavior and blood metabolites. Animals. (2020) 10:1973. doi: 10.3390/ani10111973
44. Shan LC, De Brún A, Henchion M, Li C, Murrin C, Wall PG, et al. Consumer evaluations of processed meat products reformulated to be healthier–a conjoint analysis study. Meat Sci. (2017) 131:82–9. doi: 10.1016/j.meatsci.2017.04.239
45. Fusaro I, Cavallini D, Giammarco M, Manetta AC, Martuscelli M, Mammi LME, et al. Oxidative status of marchigiana beef enriched in n-3 fatty acids and vitamin E, treated with a blend of oregano and rosemary essential oils. Front Vet Sci. (2021) 8:513. doi: 10.3389/fvets.2021.662079
46. Torres R, Ghedini C, Paschoaloto J, da Silva D, Coelho L, Junior GA, et al. Effects of tannins supplementation to sheep diets on their performance, carcass parameters and meat fatty acid profile: a meta-analysis study. Small Rumin Res. (2022) 206:106585. doi: 10.1016/j.smallrumres.2021.106585
47. Nascimento CO, Pina DS, Cirne LG, Santos SA, Araújo ML, Rodrigues TC, et al. Effects of whole corn germ, a source of linoleic acid, on carcass characteristics and meat quality of feedlot lambs. Animals. (2021) 11:267. doi: 10.3390/ani11020267
48. Malgwi IH, Halas V, Grünvald P, Schiavon S, Jócsák I. Genes related to fat metabolism in pigs and intramuscular fat content of pork: a focus on nutrigenetics and nutrigenomics. Animals. (2022) 12:150. doi: 10.3390/ani12020150
49. Pannier L, Pethick D, Geesink G, Ball A, Jacob R, Gardner G. Intramuscular fat in the longissimus muscle is reduced in lambs from sires selected for leanness. Meat Sci. (2014) 96:1068–75. doi: 10.1016/j.meatsci.2013.06.014
50. Hopkins D, Hegarty R, Walker P, Pethick DW. Relationship between animal age, intramuscular fat, cooking loss, pH, shear force and eating quality of aged meat from sheep. Aust J Exp Agric. (2006) 46:879–84. doi: 10.1071/EA05311
51. Holman BW, Hopkins DL. The use of conventional laboratory-based methods to predict consumer acceptance of beef and sheep meat: a review. Meat Sci. (2021) 181:108586. doi: 10.1016/j.meatsci.2021.108586
52. Alvarenga TI, Hopkins DL, Morris S, McGilchrist P, Fowler SM. Intramuscular fat prediction of the semimembranosus muscle in hot lamb carcases using NIR. Meat Sci. (2021) 181:108404. doi: 10.1016/j.meatsci.2020.108404
53. Tao Y, Ma L, Li D, Tian Y, Liu J, Liu D. Proteomics analysis to investigate the effect of oxidized protein on meat color and water holding capacity in Tan mutton under low temperature storage. LWT. (2021) 146:111429. doi: 10.1016/j.lwt.2021.111429
54. Zhao X-H, Yang Z-Q, Bao L-B, Wang C-Y., Zhou S, Gong J-M, et al. Daidzein enhances intramuscular fat deposition and improves meat quality in finishing steers. Exp Biol Med. (2015) 240:1152–7. doi: 10.1177/1535370214564755
55. Bao G, Liu X, Wang J, Hu J, Shi B, Li S, et al. Effects of slaughter age on myosin heavy chain isoforms, muscle fibers, fatty acids, and meat quality in longissimus thoracis muscle of Tibetan sheep. Front Vet Sci. (2021) 8:689589. doi: 10.3389/fvets.2021.689589
56. Xiao C, Wei T, Liu LX, Liu JQ, Wang CX, Yuan ZY, et al. Whole-Transcriptome analysis of preadipocyte and adipocyte and construction of regulatory networks to investigate lipid metabolism in sheep. Front Genet. (2021) 12:662143. doi: 10.3389/fgene.2021.662143
57. Scollan ND, Price EM, Morgan SA, Huws SA, Shingfield KJ. Can we improve the nutritional quality of meat? Proc Nutr Soc. (2017) 76:603–18. doi: 10.1017/S0029665117001112
58. Bessa RJ, Alves SP, Santos-Silva J. Constraints and potentials for the nutritional modulation of the fatty acid composition of ruminant meat. Eur J Lipid Sci Technol. (2015) 117:1325–44. doi: 10.1002/ejlt.201400468
59. Manni K, Rinne M, Huuskonen A, Huhtanen P. Effects of contrasting concentrate feeding strategies on meat quality of growing and finishing dairy bulls offered grass silage and barley based diets. Meat Sci. (2018) 143:184–9. doi: 10.1016/j.meatsci.2018.04.033
60. Toral PG, Hervás G, Frutos P. Use of high doses of 18: 0 to try to mitigate the syndrome of milk fat depression in dairy ewes fed marine lipids. Anim Feed Sci Technol. (2018) 236:68–75. doi: 10.1016/j.anifeedsci.2017.12.001
61. Yagoubi Y, Joy M, Ripoll G, Mahouachi M, Bertolín J, Atti N. Rosemary distillation residues reduce lipid oxidation, increase alpha-tocopherol content and improve fatty acid profile of lamb meat. Meat Sci. (2018) 136:23–9. doi: 10.1016/j.meatsci.2017.10.007
62. Inserra L, Priolo A, Biondi L, Lanza M, Bognanno M, Gravador R, et al. Dietary citrus pulp reduces lipid oxidation in lamb meat. Meat Sci. (2014) 96:1489–93. doi: 10.1016/j.meatsci.2013.12.014
63. Ozdogan M, Ustundag A, Yarali E. Effect of mixed feeds containing different levels of olive cake on fattening performance, carcass, meat quality and fatty acids of lambs. Trop Anim Health Prod. (2017) 49:1631–6. doi: 10.1007/s11250-017-1369-6
64. Stenberg E, Karlsson A, Öghren C, Segerkvist KA. Carcass characteristics and meat quality attributes in lambs reared indoors, on cultivated pasture, or on semi-natural pasture. Agric Food Sci. (2020) 29:432–41−41. doi: 10.23986/afsci.91706
65. Hughes JM, Clarke FM, Purslow PP, Warner RD. Meat color is determined not only by chromatic heme pigments but also by the physical structure and achromatic light scattering properties of the muscle. Compr Rev Food Sci Food Saf. (2020) 19:44–63. doi: 10.1111/1541-4337.12509
66. Abhijith A, Warner RD, Ha M, Dunshea FR, Leury BJ, Zhang M, et al. Effect of slaughter age and post-mortem days on meat quality of longissimus and semimembranosus muscles of Boer goats. Meat Sci. (2021) 175:108466. doi: 10.1016/j.meatsci.2021.108466
67. Vodolazska D, Lauridsen C. Effects of dietary hemp seed oil to sows on fatty acid profiles, nutritional and immune status of piglets. J Anim Sci Biotechnol. (2020) 11:1–18. doi: 10.1186/s40104-020-0429-3
68. Fowler SM, Morris S, Hopkins DL. Nutritional composition of lamb retail cuts from the carcases of extensively finished lambs. Meat Sci. (2019) 154:126–32. doi: 10.1016/j.meatsci.2019.04.016
69. Castro LG, Olleta JL, Martin N, et al. Nutrient composition of Spanish small ruminants. J Food Composit Anal. (2021) 102:104019. doi: 10.1016/j.jfca.2021.104019
70. Schönfeldt H, Naude R, Bok W, Van Heerden S, Smit R, Boshoff E. Flavour-and tenderness-related quality characteristics of goat and sheep meat. Meat Sci. (1993) 34:363–79. doi: 10.1016/0309-1740(93)90084-U
71. Canul-Solis J, Angeles-Hernandez JC, García-Herrera RA, del Razo-Rodríguez OE, Lee Rangel HA, Piñeiro-Vazquez AT, et al. Estimation of body weight in hair ewes using an indirect measurement method. Trop Anim Health Prod. (2020) 52:2341–7. doi: 10.1007/s11250-020-02232-7
72. Barcelos S, Vargas J, Mezzomo R, Gionbelli M, Gomes D, Oliveira L, et al. Predicting the chemical composition of the body and the carcass of hair sheep using body parts and carcass measurements. Animal. (2021) 15:100139. doi: 10.1016/j.animal.2020.100139
73. de Albuquerque Borges CR, de Carvalho FFR, Neves MLMW, Neto JDP, Vieira GHP, Pessoa RAS. Carcass and meat traits of bubaline finished on sugarcane-based diets supplemented with spineless cactus as a replacement for wheat bran. Anim Biosci. (2022) 35:47. doi: 10.5713/ab.20.0825
74. Owens FN, Dubeski P, Hanson C. Factors that alter the growth and development of ruminants. J Anim Sci. (1993) 71:3138–50. doi: 10.2527/1993.71113138x
75. Fernandes SR, Monteiro ALG, da Silva MGB, da Silva CJA, Zanotelli JM, Junior PR, et al. Weaning and concentrate supplementation on the characteristics of carcass cuts and longissimus muscle of Suffolk lambs finished on pasture. Acta Sci Anim Sci. (2022) 44:e53445-e. doi: 10.4025/actascianimsci.v44i1.53445
76. da Trindade Silva MG, Geraldo Costa M, Campelo Medeiros M, dos Santos Difante G, Sérgio de Azevedo P, Gurgel ALC, et al. Use of spineless cactus associated with legume hay in the feedlot-finishing of lambs in semi-arid regions. PloS ONE. (2021) 16:e0261554. doi: 10.1371/journal.pone.0261554
77. Bautista-Díaz E, Mezo-Solis JA, Herrera-Camacho J, Cruz-Hernández A, Gomez-Vazquez A, Tedeschi LO, et al. Prediction of carcass traits of hair sheep lambs using body measurements. Animals. (2020) 10:1276. doi: 10.3390/ani10081276
Keywords: omega-3 fatty acids, meat eating quality, wholesale primal cuts, intramuscular fat, fat melting point, MARGRA lamb
Citation: Pewan SB, Otto JR, Kinobe RT, Adegboye OA and Malau-Aduli AEO (2022) Fortification of diets with omega-3 long-chain polyunsaturated fatty acids enhances feedlot performance, intramuscular fat content, fat melting point, and carcass characteristics of Tattykeel Australian White MARGRA lambs. Front. Vet. Sci. 9:933038. doi: 10.3389/fvets.2022.933038
Received: 30 April 2022; Accepted: 22 August 2022;
Published: 12 September 2022.
Edited by:
Xuezhao Sun, Jilin Agricultural Science and Technology University, ChinaReviewed by:
Panagiotis Simitzis, Agricultural University of Athens, GreeceMaghsoud Besharati, University of Tabriz, Iran
Copyright © 2022 Pewan, Otto, Kinobe, Adegboye and Malau-Aduli. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Aduli Enoch Othniel Malau-Aduli, aduli.malauaduli@jcu.edu.au