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Research Article

Artificial Raising on Milk Replacer and Finishing Diet Did Not Affect Color and Oxidative Stability of Longissimus Lumborum Muscles From Polypay Ram Lambs

Authors
  • Koushik Mondal (University of Kentucky)
  • Surendranath P. Suman orcid logo (University of Kentucky)
  • Katherine G. Purvis (University of Kentucky)
  • Gregg Rentfrow (University of Kentucky)
  • Donald G. Ely (University of Kentucky)
  • Brittany E. Davis (USDA, Agricultural Research Service)
  • Jennifer Weinert-Nelson (USDA, Agricultural Research Service)
  • Yifei Wang orcid logo (The Ohio State University)
  • Ana Paula A. A. Salim (University of Kentucky)

Abstract

Lamb production traits are affected by pre-weaning management (such as artificial raising on milk replacer) and finishing (forage vs. concentrate) strategies. The objective of the current study was to examine the effects of pre-weaning management and finishing systems on the color and oxidative stability of longissimus lumborum (LL) muscles from ram lambs. Polypay ram lambs were raised conventionally with ewes (CR; n = 10) or artificially on milk replacer (AR; n = 10). After weaning at 60 d, ram lambs in AR and CR were equally divided and randomly allocated to finishing on a high-forage (50:50 forage:concentrate; HF) or a high-concentrate (85:15 concentrate:forage; HC) diet until reaching the live weight of 59 kg. The lambs were harvested, and the LL muscles from both sides of the carcasses (24 h postmortem) were fabricated into 2.5-cm-thick chops. Carcass characteristics were evaluated while harvesting and fabricating. The chops were placed on polystyrene trays, overwrapped with oxygen-permeable polyvinyl chloride film, and randomly assigned to refrigerated storage (2°C) in the darkness for either 0, 3, or 6 d. Instrumental color, R630/580, pH, lipid oxidation, and metmyoglobin reducing ability (MRA) were evaluated at the end of each storage period. Pre-weaning management and finishing system (HF and HC) had no influence (P > 0.05) on the carcass characteristics, surface L* (lightness), a* (redness), b* (yellowness), R630/580, pH, and MRA of LL chops. The R630/580 and MRA decreased (P < 0.05) during storage in both CR and AR chops, whereas lipid oxidation and yellowness (b* value) increased (P < 0.05) in both CR and AR during storage. These findings suggested that milk replacer could be employed as a practical strategy in lamb production without compromising fresh lamb color.

Keywords: artificial raising, color stability, lamb color, milk replacer

How to Cite:

Mondal, K., Suman, S. P., Purvis, K. G., Rentfrow, G., Ely, D. G., Davis, B. E., Weinert-Nelson, J., Wang, Y. & Salim, A. A., (2025) “Artificial Raising on Milk Replacer and Finishing Diet Did Not Affect Color and Oxidative Stability of Longissimus Lumborum Muscles From Polypay Ram Lambs”, Meat and Muscle Biology 9(1): 18343, 1-13. doi: https://doi.org/10.22175/mmb.18343

Rights:

© 2025 Mondal, et al. This is an open access article distributed under the CC BY license.

Funding

Name
Agricultural Research Service
FundRef ID
https://doi.org/10.13039/100007917
Funding ID
5042-32630-004-00D

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56 Downloads

Published on
2025-01-27

Peer Reviewed

Introduction

The global demand for meat from small ruminants (i.e., sheep and goats) is increasing (Ke et al., 2023). The sheep industry strives to improve the quality attributes of fresh lamb such as color, tenderness, and flavor (Prache et al., 2022). Fresh meat color is the most important attribute considered by consumers at the point of sale as an indicator of wholesomeness (Mancini and Hunt, 2005). Therefore, maintaining the color stability of fresh red meats is necessary to avoid consumer rejection and concomitant economic loss to meat industry (Ramanathan et al., 2022).

Color of fresh meat is dependent on pre-harvest (e.g., feeding systems, live animal management, muscle source) and post-harvest (e.g., packaging, aging, and storage conditions; pH; mitochondrial activity) factors (Faustman and Cassens, 1990; Mancini and Hunt, 2005; Suman et al., 2014; Ramanathan et al., 2020). Among these factors, diet is an important one (Karaca et al., 2016; Cabiddu et al., 2022) influencing the quality of fresh lamb (Zervas and Tsiplakou, 2011; Watkins et al., 2013). The energy content in diet influences lamb color stability, and lambs finished on a low-energy diet exhibited greater color stability (R630/580) than those raised on a high-energy diet (Chauhan et al., 2019). Meat from pasture-raised lambs was darker and redder compared to the meat from animals fed a concentrate-based diet (Karaca et al., 2016), which could be due to a high ultimate pH and myoglobin content in muscles (Vestergaard et al., 2000). In addition, fresh lamb color is a muscle-specific trait (Tschirhart-Hoelscher et al., 2006). Lamb muscles with a high proportion of oxidative fibers (e.g., psoas major and semimembranosus) are considered color-labile and exhibit greater oxygen consumption rate, redness, and myoglobin content (Gao et al., 2013; Ithurralde et al., 2015). In contrast, glycolytic muscles (e.g., longissimus lumborum [LL] and longissimus thoracis) are color-stable and exhibit low ultimate pH and lower oxygen consumption rate, increased lightness (Tschirhart-Hoelscher et al., 2006), and increased metmyoglobin reducing activity (MRA) (Gao et al., 2013; Ithurralde et al., 2015).

To enhance lamb production efficiency and live weight gains, milk replacer has been utilized as an artificial raising strategy (Napolitano et al., 2002a, 2002b; Osorio et al., 2007; Campbell, 2019) to raise triplets, surplus, or orphan lambs to improve their growth and survival rates (Notter et al., 2018). Despite these advantages, the use of milk replacer may affect the harvested lamb color, and investigations in this aspect have demonstrated conflicting results. Chai et al. (2018) reported a brighter meat color in lambs raised on milk replacer compared to those exclusively fed on ewe’s milk. Ward et al. (2017) reported similar redness and muscle pH in meat from both naturally (control) and artificially raised lambs.

During the fattening period, the lambs can be subject to different finishing systems, such as pasture and concentrate feeding. Pasture-based finishing systems are low-cost and are associated with improved animal welfare, whereas this practice may result in less efficient production performance, carcass grade and conformation compared to concentrated-finished lambs in confinement (Aguayo-Ulloa et al., 2013). Moreover, the meat from pasture-fed lambs is associated with a high ultimate pH and dark color (Calnan et al., 2016).

Previous investigations evaluated the influence of artificial raising on milk replacer on the lamb color. However, the influence of artificial raising combined with finishing systems on color and oxidative stability of fresh lamb is yet to be investigated. Therefore, the present study aimed to investigate the influence of artificial raising on milk replacer and finishing systems on color stability and lipid oxidation of lamb LL muscles during refrigerated storage.

Materials and Methods

Lamb production

All protocols were approved by the Institutional Animal Care and Use Committee of the University of Kentucky (Protocol #2021-3772). Twenty Polypay ram lambs from twin-baring ewes were used for this experiment. Polypay is an American dual-purpose sheep breed developed for a superior reproductive capacity and has a composition of ¼ Dorset, ¼ Finnsheep, ¼ Targhee, and ¼ Rambouillet (Zhang et al., 2013). Due to its high prolificacy and strong maternal qualities, Polypay breed was chosen for the present study. The rams were selected as they are more commonly used for meat production, whereas ewes are often retained for breeding purposes. The lambs were born at the University of Kentucky C. Oran Little Research Center Sheep Unit (Versailles, KY; geographic coordinates: 38°4′36″N, 84°44′22″W). Ewes were selected based on the following criteria: Polypay breed, twin-bearing, multiparous, and no apparent lambing difficulties. The ewe flock was managed together and were provided gestation diets that met the nutrient requirements for sheep with an expected 180–225% lambing rate (Benson and Morrical, 2015). Immediately after lambing, ewes and their lambs were moved to individual indoor pens to facilitate bonding and adequate colostrum intake. After 24 h, twin lambs (birth weight: 4948.7 ± 257.9 g) were blocked by weight and sex and assigned to either be conventionally raised (CR; with ewes as a single lamb) or raised with artificial milk replacer ad libitum using an automatic, warmed, milk feeding system (AR; LAC-TEK II Milk Feeding System, Biotic Industries LLC; Sav-A-Lam Products Lamb Milk Replacer, 30% Fat min., Milk Products LLC). Lambs selected for AR were removed from their dams and placed in indoor group pens. Lambs selected for CR remained with their dams in the individual pens for up to 72 h and then were managed in indoor, group mixing pens. After lambing, ewes were provided a diet that met the nutrient requirements for lactation (alfalfa hay and concentrate mix; Benson and Morrical, 2015). During the pre-weaning period, lambs assigned to both treatments were provided ad libitum access to alfalfa hay and a concentrate mix in creep feeding pens. After weaning at 60 d of age, the ram lambs from AR (n = 10; initial body weight [BW]: 32.9 ± 0.6 kg) and CR (n = 10; initial BW: 38.9 ± 1.6 kg) treatments were blocked by BW and then randomly allocated to either finishing on a high-forage (HF; 50:50 forage:concentrate) or a high-concentrate (HC; 85:15 concentrate:forage) diet. This approach provided 5 replicates (n = 5) for each of the 4 treatments (CR-HF; CR-HC; AR-HF; and AR-HC). The lambs were individually fed during the finishing stages. The ingredients and chemical compositions of the finishing diets are presented in Tables 1 and 2, respectively. All finishing diets were made to be isonitrogenous. The lambs in all dietary treatments were fed ad libitum until they reached the target live weight of 59 kg (84.0 ± 0.8 finishing days).

Table 1.

Ingredient composition of high-concentrate (HC) and high-forage (HF) diets.


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Ingredient, % Diet1
HC HF
Cracked Corn 63.3 38.0
Protein Pellet2 18.7 12.02
Orchardgrass Pellet 15.0 50.0
Total 100.0 100.0
  • HC = 85:15 concentrate:forage; HF = 50:50 concentrate:forage.

  • Composition: 63.33% soybean meal (48% crude protein), 21.25% distillers dried grains with solubles, 4.38% ground limestone, 3.13% salt, 2.50% ammonium chloride, 1.50% sheep premix, 0.50% vitamin E (20,000 IU/lb), 0.25% vitamin A (10,000 IU/lb), 0.25% vitamin D3 (15,000 IU/lb).

Table 2.

Chemical composition of high-concentrate (HC) and high-forage diets (HF).


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Component, %1 Diet2
HC HF
Dry Matter 89.6 91.5
Crude Protein 16.1 15.6
Acid Detergent Fiber 8.0 23.0
Neutral Detergent Fiber 16.6 33.4
Starch 44.2 19.0
TDNb3 84 79
  • All components, excluding dry matter (DM), on a 100% DM basis.

  • HC = 85:15 concentrate:forage; HF = 50:50 concentrate:forage.

  • TDNb = total digestible nutrients.

Lamb harvest, fabrication, and carcass characteristics

The lambs were humanely harvested at the USDA-inspected Meat Laboratory of the University of Kentucky (Lexington, KY, USA). The average live weights of lambs were 59.06 kg for CR-HC; 58.97 kg for CR-HF; 58.79 kg for AR-HC; and 58.33 kg for AR-HF. Hot carcass weights were recorded, and the carcasses were chilled for 24 h at 2°C. Following the chilling, cold carcass weight, carcass conformation, quality grade (flank fat streaking), overall grade, dressing percentage, rib eye area, fat thickness, and body wall thickness were measured. All carcass grading and measurements were performed according to the methods described in Meat Evaluation Handbook of the American Meat Science Association (AMSA, 2001). The neck, foreshank (IMPS #210), shoulder (IMPS #207), rack (IMPS #204), loin (IMPS #232), and leg (IMPS #233A) were removed and weighed individually (NAMP, 2010). Primal cuts were recorded in absolute weight (weight in kg of the primal).

The LL muscles from both sides of the carcasses were excised. The muscles were fabricated into 2.5-cm-thick chops, placed into Styrofoam trays, overwrapped with oxygen-permeable polyvinyl chloride film (15,500–16,275 cm3/m2/24 h oxygen transmission rate at 23°C) and randomly assigned to refrigerated storage (2°C) in darkness. Instrumental color, R630/580, pH, lipid oxidation, and MRA were evaluated on days 0, 3, and 6, whereas myoglobin concentration was determined on day 0.

Myoglobin concentration

Duplicate 5 g muscle samples were homogenized with 45 mL ice-cold sodium phosphate buffer (40 mM, pH 6.8) for 45 s and centrifuged at 15,000 × g for 30 min at 4°C (Faustman and Phillips, 2001). The supernatant was filtered through Whatman No. 1 paper, and the absorbance of the filtrate was measured at 525 nm utilizing a UV-241PC spectrophotometer (Shimadzu Inc., Columbia, MD) with 40 mM sodium phosphate buffer as a blank. The myoglobin concentration was calculated using the following equation:

Myoglobin(mg/g)=[A525/(7.6mM1cm1×1cm)]×(17,000/1000)×10

where 7.6 mM−1 cm−1 = mM absorptivity coefficient of myoglobin at 525 nm; 1 cm = length of the light path in the cuvette; 17,000 Da = average molecular weight of myoglobin; and 10 = dilution factor.

Meat pH

The pH value of chops was determined according to the method of Strange et al. (1977). Five grams of samples were homogenized with 30 mL of distilled deionized water (at 25°C), and the pH was measured utilizing an Accumet AR25 pH meter (Fisher Scientific, Pittsburg, PA).

Instrumental color

The surface color of chops was measured using a HunterLab LabScan XE colorimeter (Hunter Associates Laboratory, Reston, VA) with a 1.27-cm-diameter aperture, illuminant A, and 10° standard observer. The colorimeter was calibrated with standard black and white plates. On day 0 of storage, the oxygen-permeable film was removed from the packages, and the chops were allowed to bloom for 2 h at 2°C before the evaluation of the instrumental color. CIE (1976) L* (lightness), a* (redness), and b* (yellowness) values were measured at 3 random locations on the oxygen-exposed surface of each chop (King et al., 2023). Additionally, the reflectance was measured from 700 to 400 nm, and the ratio of reflectance at 630 nm and 580 nm (R630/580) was determined as an indirect estimate of surface color stability (King et al., 2023).

Metmyoglobin reducing activity

The MRA was evaluated according to Sammel et al. (2002). The lamb chops were submerged in 0.3% sodium nitrite solution for 30 min at room temperature to facilitate metmyoglobin formation. After 30 min, the samples were removed from the solution, blotted dry, and vacuum packaged in Prime Source vacuum pouches (3 mil, Bunzl Koch Supplies Inc., Kansas City, MO). The reflectance spectra were measured from 700 to 400 nm on the light-exposed surface using a HunterLab LabScan XE colorimeter immediately after vacuum packaging to calculate pre-incubation surface metmyoglobin values (King et al., 2023). The samples were then incubated at 30°C for 2 h allowing for metmyoglobin reduction, and subsequently the surface reflectance was rescanned to calculate post-incubation metmyoglobin values (King et al., 2023). MRA was calculated using the following equation:

MRA = 100 × [(% pre-incubation surface metmyoglobin − % post-incubation surface metmyoglobin)/% pre-incubation surface metmyoglobin]

Lipid oxidation

Lipid oxidation was measured using the thiobarbituric acid assay (Yin et al., 1993). Duplicate 5-g of sample was homogenized with 22.5 mL of 11% trichloroacetic acid (TCA) solution and filtered through Whatman No. 1 filter paper (GE healthcare, Little Chalfont, UK). From the resulting filtrate, an aliquot of 1.5 mL was added in a glass tube and mixed with 1.5 mL of 20 mM thiobarbituric acid (TBA) solution and then incubated at 25°C for 20 h. A blank of 20 mM TBA and 11% TCA was simultaneously incubated with the other samples. The absorbance value at 532 nm was measured utilizing a UV-2401PC spectrophotometer (Shimadzu Inc., Columbia, MD), and the results were presented as thiobarbituric acid reactive substances (TBARS).

Statistical analysis

The experimental design was a split-plot with a 2 × 2 factorial and pre-weaning and finishing system as the main plot, and days of storage as a sub-plot factor applied within each main plot. The LL muscles from a lamb carcass served as the experimental unit, whereas the sub-plot experimental units consisted of chops fabricated from each lamb carcass and assigned for 0, 3, or 6 d of refrigerated storage. The analysis of variance was determined utilizing the PROC GLIMMIX procedure of SAS version 9.4 (SAS Institute Inc., Cary, NC). The least-squares means were separated using the PDIFF option with a Tukey-Kramer adjustment, and the differences among means were considered statistically different at a 0.05 level.

Results and Discussion

Carcass characteristics

The results of live weight, hot carcass weight, cold carcass weight, carcass conformation, quality grade (flank fat streaking), overall grade, dressing percentage, ribeye area, fat thickness, body wall thickness, neck, foreshank, left and right shoulder, rack, loin, and left and right leg are presented in Table 3. There was an effect of pre-weaning on rack (P = 0.0056) and loin (P = 0.0421) cuts, but no effect of finishing system was observed (Table 3). The rack from AR lambs exhibited greater (P < 0.05) weights compared to those from the CR lambs. On the other hand, the loins from AR lambs exhibited lighter (P < 0.05) weight than their counterparts from CR lambs. A pre-weaning × finishing system interaction (P = 0.0284) was observed for right shoulder cuts (Table 3).

Table 3.

Carcass characteristics of Polypay ram lambs raised conventionally (CR) or artificially with milk replacer (AR) and finished with high-forage (HF; 50:50 forage:concentrate) or high-concentrate (HC; 85:15 concentrate:forage) diets1.


View Larger Table
Carcass Characteristics Raising System P Values
Conventional Raising Artificial Raising Pre-weaning Finishing System Pre-weaning × Finishing System
HF HC HF HC
Live Weight (kg) 58.97 ± 1.04 59.06 ± 0.52 58.33 ± 0.42 58.79 ± 1.17 0.6213 0.7385 0.8267
Hot Carcass Weight (kg) 27.44 ± 0.73 28.17 ± 0.64 27.31 ± 0.36 26.72 ± 0.55 0.1958 0.933 0.2831
Cold Carcass Weight (kg) 27.31 ± 0.68 28.08 ± 0.60 27.13 ± 0.36 26.81 ± 0.59 0.2082 0.7183 0.3679
Carcass Conformation2 580.00 ± 37.42 560.00 ± 40.00 620.00 ± 37.42 620.00 ± 37.42 0.2077 0.7962 0.7962
Quality Grade (FFS)3 332.00 ± 63.51 354.00 ± 58.10 396.00 ± 56.36 376.00 ± 43.08 0.4519 0.9859 0.7115
Overall Grade2 600.00 ± 31.62 580.00 ± 20.00 660.00 ± 50.99 640.00 ± 60.00 0.1876 0.6525 1.0000
Dressing Percentage (%) 46.53 ± 0.81 47.69 ± 0.85 46.82 ± 0.68 45.46 ± 0.56 0.2058 0.8900 0.105
Ribeye Area (cm2) 15.87 ± 0.99 15.39 ± 0.69 15.23 ± 0.49 16.23 ± 1.57 0.9277 0.8006 0.4757
Fat Thickness (cm) 0.38 ± 0.06 0.52 ± 0.08 0.41 ± 0.06 0.41 ± 0.04 0.4916 0.289 0.2495
Body Wall Thickness (cm) 2.12 ± 0.17 2.17 ± 0.15 2.59 ± 0.13 2.45 ± 0.28 0.0702 0.8224 0.6253
Neck (kg) 0.92 ± 0.07 0.89 ± 0.07 0.95 ± 0.02 0.93 ± 0.04 0.4884 0.6084 1.0000
Foreshank; IMPS #210 (kg) 1.44 ± 0.03 1.48 ± 0.10 1.30 ± 0.03 1.41 ± 0.06 0.0968 0.2126 0.6016
Left Shoulder; IMPS #207 (kg) 2.72 ± 0.11 2.79 ± 0.06 2.74 ± 0.13 2.65 ± 0.04 0.5382 0.8981 0.4219
Right Shoulder; IMPS #207 (kg) 2.72 ± 0.09c 2.99 ± 0.10a 2.87 ± 0.05b 2.70 ± 0.12c 0.4972 0.5803 0.0284
Rack; IMPS #204 (kg) 2.64 ± 0.12b 2.70 ± 0.09b 3.11 ± 0.05a 2.93 ± 0.15a 0.00564 0.5769 0.2866
Loin; IMPS #232 (kg) 2.47 ± 0.12a 2.43 ± 0.16a 2.15 ± 0.12b 2.14 ± 0.15b 0.04214 0.8750 0.9202
Left Leg; IMPS #233A (kg) 4.27 ± 0.14 4.42 ± 0.13 4.19 ± 0.06 4.11 ± 0.10 0.0904 0.7609 0.3231
Right Leg; IMPS #233A (kg) 4.33 ± 0.11 4.43 ± 0.05 4.17 ± 0.10 4.26 ± 0.13 0.1236 0.3653 1.0000
  • CR = conventionally raised with ewes; AR = artificially raised on milk replacer; HF = finished on high-forage; HC = finished on high-concentrate.

  • Means without common superscripts in a row are different (P < 0.05).

  • Results are expressed as mean ± standard error of the mean (SEM).

  • 400 = low choice (C−); 500 = average choice (C0); 600 = high choice (C+); 700 = low prime (P−); 800 = average prime (P0); 900 = high prime (P+).

  • FFS = flank fat streaking. 100 = traces (Tr); 200 = slight (Sl); 300 = small (Sm); 400 = modest (Mt); 500 = moderate (Md); 600 = slightly abundant (Sa); 700 = moderately abundant (Ma); 800 = abundant (Ab).

  • The statistically different results.

The observed lack of difference in carcass traits could be due to the similar target finishing weights (live weights at slaughter; Table 3) for the lambs in all treatments. Milk replacers, when used in conjunction with formulated forage and concentrate-based diets, can achieve similar nutritional goals and comparable rates of muscle growth and fat deposition. As a result, these similarities could lead to similarities in the carcass characteristics of lambs (Gonzalez-Martínez et al., 2023).

Chai et al. (2018) examined the carcass traits of artificially and naturally raised Hu lambs and reported similarities in hot dressing percentage and back fat thickness in both groups. Lanza et al. (2006) found no differences in slaughter weight and carcass yield percentages between the naturally and artificially raised lambs. Rodriguez et al. (2008) examined the effect of artificial and natural raising systems on the carcass characteristics of lambs and reported no differences in the cold carcass weight and dressing percentage of lambs raised conventionally and artificially.

Napolitano et al. (2002a) evaluated the effect of artificial raising on meat production and behavioral response of lambs and reported no differences in the percentages of carcass yield and secondary cuts between the groups; the authors documented a greater slaughter weight and percentages of rack as well as loin in ewe-raised lambs than in artificially raised lambs. The observations (Napolitano et al., 2002a) on rack agreed with the findings of the present study. Further studies (Napolitano et al., 2002b) evaluated the effect of conventional and artificial raising on the lamb carcass characteristics and reported no differences in slaughter weight, hot carcass weight, first-grade wholesale cuts (rack, loin, and leg) percentage, leg lean percentage, and leg bone percentage; however, the authors reported that the milk replacer fed lambs produced greater carcass yield, greater second grade wholesale cuts (shoulder, neck, breast) percentage, and lower leg fat percentage than their naturally fed counterparts.

In contrast to the findings of the present study, previous investigations reported variations in carcass characteristics of lambs raised under different finishing systems. Karaca et al. (2016) evaluated the effect of the finishing system (pasture vs. concentrate) on slaughter-carcass characteristics and meat quality of Norduz lambs and reported that lambs fed with concentrate exhibited a greater hot carcass weight and dressing percentage, whereas the foreleg was heavier in the pasture-raised group. The observed differences in carcass characteristics between the present study and previous ones could be attributed to variations in the live weight, breed, and age at harvest.

Myoglobin concentration

There was no pre-weaning × finishing system interaction (P = 0.6900) for myoglobin concentration in lamb chops. Additionally, there was no effect of pre-weaning (P = 0.7880) and finishing (P = 0.6064) systems for myoglobin concentration (Table 4). This similarity may be partially attributed to the observed similar live weight and age of the lambs in the four treatments. Myoglobin concentration and redox form play an important role in the perception of fresh lamb color (Faustman et al., 2023). Several factors can affect myoglobin concentration in lamb such as slaughter age (Gardner et al., 2007) and slaughter weight (Miguel et al., 2021). Myoglobin concentration increases as age and slaughter age increase (Gardner et al., 2007), influencing oxidative capacity and the color of meat (Warner et al., 2007). From this perspective, the similarities in animals’ slaughter age and slaughter weight may have contributed to the similarity in myoglobin concentration.

Table 4.

Myoglobin concentration, pH, L*, a*, b*, R630/580, metmyoglobin reducing activity (MRA), and lipid oxidation (TBARS) of longissimus lumborum chops from Polypay ram lambs conventionally raised (CR) or artificially raised with milk replacer (AR) and finished with high-forage (HF; 50:50 forage:concentrate) or a high-concentrate (HC; 85:15 concentrate:forage) diet during 6 d of refrigerated storage.


View Larger Table
Days of Storage P Values
Parameter Pre-weaning and Finishing System 0 3 6 Pre-weaning Finishing System Pre-weaning × Finishing System Days of Storage Pre-weaning × Days of Storage Finishing System × Days of Storage Pre-weaning × Finishing system × Days of Storage
Myoglobin Concentration (mg/g) CR-HF 7.9 ± 0.35 0.7880 0.6064 0.6900
AR-HF 8.5 ± 0.49
CR-HC 7.8 ± 0.83
AR-HC 7.7 ± 0.74
Meat pH CR-HF 5.63 ± 0.07 5.53 ± 0.05 5.60 ± 0.05 0.5923 0.0807 0.7761 0.0936 0.1255 0.5305 0.8744
AR-HF 5.62 ± 0.04 5.58 ± 0.04 5.59 ± 0.07
CR-HC 5.69 ± 0.04 5.61 ± 0.03 5.66 ± 0.03
AR-HC 5.68 ± 0.04 5.71 ± 0.06 5.68 ± 0.02
L* Value CR-HF 39.89 ± 1.09 42.37 ± 0.81 40.93 ± 1.14 0.1657 0.5379 0.6133 0.1028 0.3651 0.4142 0.666
AR-HF 38.28 ± 0.61 39.66 ± 0.53 40.65 ± 0.91
CR-HC 38.95 ± 0.49 49.13 ± 0.70 40.76 ± 1.29
AR-HC 38.24 ± 1.12 40.84 ± 1.67 40.07 ± 0.86
a* Value CR-HF 12.43 ± 0.47 13.30 ± 0.61 12.94 ± 0.55 0.5775 0.8734 0.1659 0.6784 0.5587 0.1332 0.6617
AR-HF 14.07 ± 0.80 14.25 ± 0.68 13.49 ± 0.74
CR-HC 13.39 ± 0.85 13.26 ± 0.70 12.52 ± 0.76
AR-HC 13.91 ± 0.62 13.31 ± 0.81 12.61 ± 0.45
b* Value CR-HF 11.92 ± 0.54b 14.40 ± 0.42a 14.40 ± 0.39a 0.0636 0.3617 0.7703 <0.00011 0.2902 0.012 0.6405
AR-HF 12.80 ± 0.20b 14.36 ± 0.26a 15.04 ± 0.27a
CR-HC 12.79 ± 0.26b 14.47 ± 0.36a 14.02 ± 0.29a
AR-HC 13.60 ± 0.61b 15.01 ± 0.18a 14.69 ± 0.23a
R630/580 CR-HF 3.29 ± 0.25a 2.54 ± 0.26b 2.35 ± 0.24c 0.2021 0.865 0.6634 <0.00011 0.2449 0.3734 0.9704
AR-HF 3.64 ± 0.34a 2.70 ± 0.17b 2.46 ± 0.25c
CR-HC 3.47 ± 0.37a 2.59 ± 0.30b 2.33 ± 0.33c
AR-HC 3.72 ± 0.46a 2.61 ± 0.46b 2.37 ± 0.24c
MRA CR-HF 33.57 ± 9.07a 15.95 ± 2.76b 19.58 ± 5.36b 0.5784 0.082 0.6968 <0.00011 0.4047 0.7603 0.6289
AR-HF 28.36 ± 8.18a 15.46 ± 2.96b 18.56 ± 11.82b
CR-HC 37.32 ± 8.13a 19.78 ± 6.72b 22.17 ± 5.71b
AR-HC 35.14 ± 5.80a 17.12 ± 6.80b 25.84 ± 6.23b
TBARS CR-HF 0.01 ± 0.00b 0.02 ± 0.01b 0.05 ± 0.02a 0.7703 0.3349 0.3055 <0.00011 0.3214 0.5198 0.2911
AR-HF 0.02 ± 0.01b 0.03 ± 0.01b 0.06 ± 0.03a
CR-HC 0.01 ± 0.00b 0.02 ± 0.01b 0.05 ± 0.04a
AR-HC 0.02 ± 0.01b 0.02 ± 0.01b 0.03 ± 0.01a
  • Results are expressed as mean ± standard error of the mean (SEM). CR = conventionally raised with ewes; AR = artificially raised on milk replacer; HF = finished on high-forage; HC = finished on high-concentrate.

  • Means without common superscripts in a row are different (P < 0.05).

  • The statistically different results.

Supporting our results, Osorio et al. (2008) evaluated the effect of artificial raising on the color and lipid oxidation in the longissimus dorsi from suckling lambs and observed similar myoglobin content in conventionally and artificially raised animals. In contrast, Rivera-Bautista et al. (2023) evaluated the effect of a diet with alfalfa hay or 100% concentrate on meat quality parameters of Rambouillet ewes and reported greater myoglobin concentration in lambs fed with alfalfa hay than in their counterparts fed with concentrate.

Meat pH

There was no pre-weaning × finishing system × storage interaction (P = 0.8744) for pH (Table 4). Additionally, there was no effect of pre-weaning (P = 0.5923), finishing system (P = 0.0807), and storage (P = 0.0936) on the pH. The pH values measured 24 h after slaughter (day 0) ranged from 5.63 to 5.69 in the lamb chops (Table 4), which agreed with previous reports (Diaz et al., 2002; Martinez-Cerezo et al., 2005) and suggested that the animals experienced minimal stress during slaughter (Devine et al., 1993). The observed similarity in pH could be attributed to the similar slaughter weight. Previous investigations documented significant effects of slaughter weight on pH, with higher pH in heavy lambs (Diaz et al., 2002; Miguel et al., 2021).

In agreement with our results, Osorio et al. (2008) examined the effect of conventional and artificial raising on lamb quality and documented similar pH in the longissimus dorsi muscles in both naturally and artificially raised animals. Additionally, Rodriguez et al. (2008) reported no differences in pH in longissimus thoracis and longissimus dorsi muscles from lambs raised with mother’s milk, milk replacer ad libitum twice a day, and milk replacer at 70% of ad libitum. Lanza et al. (2006) evaluated the meat quality of lambs fed with milk replacer or naturally raised and reported similarities in pH in longissimus dorsi muscle in both raising systems. Napolitano et al. (2006) examined the meat quality of lambs raised artificially and conventionally and reported no differences in pH in longissimus dorsi, semimembranosus, and semitendinosus muscles from both treatments. In contrast, Zullo et al. (2006) reported greater pH values in longissimus dorsi, semimembranosus, rectus femoris, and gluteobiceps muscles from naturally raised lambs than in their counterparts from artificially raised lambs.

Sadrarhami et al. (2022) investigated the effects of production systems (50:50 roughage: concentrate, and 30:50 roughage: concentrate) on carcass characteristics and meat quality of longissimus dorsi from lambs. The authors reported similar ultimate pH in lamb from both diets. In addition, no differences in the pH were observed in previous studies on day 0 of storage in rectus abdominis of Churra Tensina lambs (Carrasco et al., 2009), and longissimus thoracis of Rambouillet ewes fed with forage (grazed perennial pasture) or concentrate (Rivera-Bautista et al., 2023). In contrast, Karaca et al. (2016) evaluated the effect of the finishing system (pasture or concentrate) on the meat quality of longissimus thoracis from Norduz lambs and reported greater ultimate pH in muscles of pasture-fed animals than their counterparts from lambs fed with concentrate.

Lightness (L* value)

There was no pre-weaning × finishing system × storage interaction (P = 0.666) for L* value (lightness; Table 4). Also, there was no effect of pre-weaning (P = 0.1657), finishing system (P = 0.5379), and storage (P = 0.1028) for L* value. The observed similarity in L* values could be attributed to the similar meat pH (Abril et al., 2001), which could have contributed to a similar light reflectance as well as similar lightness on the samples (Ramanathan et al., 2020).

Results from multiple previous studies agreed with the present study’s findings. Santos-Silva et al. (2002) evaluated the meat quality of lambs raised on three different feeding systems—pasture with dams, pasture with dams plus concentrate ad libitum, weaning and concentrate ad libitum—and reported similar L* value in longissimus thoracis muscle. Napolitano et al. (2006) evaluated the effects of artificial raising on meat quality of lambs and reported similar lightness in semitendinosus muscles from conventionally and artificially raised lambs. Rodriguez et al. (2008) examined the impact of natural and artificial raising systems on carcass and meat characteristics of milk-fed Assaf lambs and reported no differences in L* value in the LL muscles between naturally raised, artificially raised as well as restricted artificially raised animals.

In contrast, Lanza et al. (2006) evaluated the influence of natural or artificial milk feeding regimes and reported that the meat from naturally raised lambs exhibited higher L* value when compared to their artificially raised counterparts. Chai et al. (2018) evaluated the effect of raising system on meat quality of Hu lambs and reported greater L* value in the longissimus thoracis muscle from artificially raised lambs. Osorio et al. (2008) evaluated the quality of meat from artificially and naturally raised suckling lambs and reported greater L* values in longissimus dorsi muscles of suckling lambs naturally raised than those from artificially fed lambs.

No variations in L* value was observed in longissimus thoracis from Churra Tensina lambs (Carrasco et al., 2009) reared under grazing or concentrate diets. On the contrary, variations in L* value have been reported in lamb from concentrate- and pasture-fed animals. A greater L* value was documented in longissimus thoracis muscles from Norduz lambs fed concentrate diet compared to those from pasture-fed lambs (Karaca et al., 2016), whereas a lower L* value was reported in longissimus thoracis muscles from Rasa Aragonesa lambs fed on concentrate (Ripoll et al., 2012).

Redness (a* value)

There was no pre-weaning × finishing system × storage interaction (P = 0.6617) for a* value (redness; Table 4). Additionally, there was no effect of pre-weaning (P = 0.5775), finishing system (P = 0.8734), and storage (P = 0.6784) for a* value. Myoglobin is the water-soluble protein responsible for the red color of fresh lamb. The similarity in myoglobin concentrations (Table 4) may have contributed to the similarities in a* values observed in the present study. Supporting our results, previous studies observed no differences in a* value of semitendinosus (Napolitano et al., 2006), longissimus dorsi (Lanza et al., 2006), LL (Rodriguez et al., 2008), and longissimus thoracis (Chai et al., 2018) muscles from artificially and naturally raised lambs.

In contrast, Osorio et al. (2008) evaluated the influence of raising system (raising with maternal milk or with milk replacer) on quality traits of suckling lamb and documented increased a* value in longissimus dorsi muscle from artificially raised lambs compared to their naturally raised counterparts. Zullo et al. (2006) evaluated the effect of raising system on the lamb quality and documented greater a* value in longissimus dorsi, semimembranosus, rectus femoris, and gluteobiceps muscles from naturally raised animals than their artificially raised counterparts.

The results of previous investigations on the impact of the finishing systems on a* value of fresh lamb have been inconsistent. Silva et al. (2002) evaluated the meat quality of lambs raised on three different feeding systems—pasture with dams, pasture with dams plus concentrate ad libitum, and weaning and concentrate ad libitum—and documented lower a* value in longissimus dorsi muscle of animals from pasture-fed systems. Carrasco et al. (2009) documented greater a* value in rectus abdominis and longissimus thoracis muscles from Churra Tensina lambs reared in pasture than those raised with a concentrate diet. Similarly, Ripoll et al. (2012) documented greater a* value in rectus abdominis and LL from Rasa Aragonesa lambs raised through grazing than concentrate-fed ones. Sante-Lhoutellier et al. (2008) reported greater a* value in longissimus dorsi from lambs fed concentrate than those from pasture-fed for 7 d. However, Sadrarhami et al. (2022) reported no differences in surface a* value in longissimus dorsi from Turki-Ghashghaei lambs raised in both medium (50:50 roughage: concentrate) and high (30:70 roughage: concentrate) concentrate diets. Karaca et al. (2016) documented similar a* value in longissimus thoracis from Norduz lambs raised on pasture and concentrate systems. Furthermore, Hajji et al. (2016) reported no difference in a* value of longissimus dorsi from Barbarine, Queue Fine de l’Ouest, and Noire de Thibar lambs from pasture- and concentrate-feeding systems.

Yellowness (b* value)

There was no pre-weaning × finishing system × storage interaction (P = 0.6405) for b* value (yellowness; Table 4). Additionally, there was no effect of pre-weaning (P = 0.0636) and finishing system (P = 0.3617) on b* value. However, an effect of storage (P < 0.0001) was found on b* value (Table 4), with the chops exhibiting an increase (P < 0.05) in b* value from day 0 to 6 of storage. In support to these findings, earlier investigations documented similarities in the b* value of longissimus (Lanza et al., 2006; Rodriguez et al., 2008) and semitendinosus (Napolitano et al., 2006) muscles from ewe-raised and artificially raised lambs. Moreover, an increase of b* value in LL muscles from conventionally and artificially raised lambs during 21 d of storage was observed, which agreed with the findings of the present study (Osorio et al., 2008).

In contrast, multiple studies reported differences in the b* value of meat from lambs raised artificially and conventionally. Osorio et al. (2008) reported a greater b* value in the LL muscle from lambs fed with naturally raised compared to their milk replacer-fed counterparts, whereas Chai et al. (2018) documented greater b* value in longissimus thoracis muscle from artificially raised lambs. Zullo et al. (2006) documented greater b* value in longissimus dorsi, semimembranosus, rectus femoris, and gluteobiceps muscles from lambs naturally raised in comparison with the artificially raised ones (reconstituted milk).

Several previous studies on finishing lambs (on roughage or concentrate) agreed with the findings on b* value in the present study. Sadrarhami et al. (2022) documented no difference in yellowness of longissimus dorsi from Turki-Ghashghaei lambs raised in medium (50:50 roughage: concentrate) and high-concentrate (30:70 roughage: concentrate) diets. Moreover, Ripoll et al. (2012) reported that the feeding system (alfalfa grazing and concentrate-based) did not influence the b* value of rectus abdominis and longissimus thoracis from Rasa Aragonesa lambs. Carrasco et al. (2009) also reported similar b* value in muscles rectus abdominis and longissimus thoracis from Churra Tensina lambs reared under grazing or in confinement. Sante-Lhoutellier et al. (2008) documented similar b* values in longissimus dorsi from concentrate- and pasture-fed lambs. Contrary to the present results, Karaca et al. (2016) reported greater b* value in longissimus thoracis from Norduz lambs raised under concentrate feeding than their counterparts from pasture-fed animals.

Color stability (R630/580)

No pre-weaning × finishing system × storage interaction was found (P = 0.9704) for R630/580 (Table 4). Additionally, there was no effect of pre-weaning (P = 0.2021) and finishing system (P = 0.865), but an effect of storage (P < 0.0001) was observed in R630/580. All samples exhibited a decrease (P < 0.05) in R630/580 from day 0 to day 6 of storage. The observed decrease in R630/580 could be attributed to myoglobin oxidation and metmyoglobin accumulation (Faustman et al., 2010). The R630/580 (redness indicator) estimates surface discoloration; greater ratios indicate lower surface metmyoglobin accumulation and, consequently, increased oxymyoglobin and color stability (King et al., 2023). In agreement with our results, previous studies also reported a decrease in R630/580 of lamb longissimus thoracis (Alvarenga et al., 2019), LL (Ponnampalam et al., 2017), and semimembranosus (Ponnampalam et al., 2017) muscles during refrigerated storage.

In agreement with the observations in the present study, Ponnampalam et al. (2010) reported similar R630/580 in LL from crossbred lambs (Poll Dorset × Border Leicester × Merino) finished on pasture and grain on day 0 of storage. Luciano et al. (2009) documented lower metmyoglobin percentages in semimembranosus muscles from Comisana lambs fed forage than in their counterparts from concentrate-fed animals on day 0. On the other hand, Ponnampalam et al. (2017) evaluated the effect of diet (ryegrass with sub-clover pasture or feedlot pellets) on the color stability of crossbred lamb and reported greater R630/580 in LL of feedlot-fed lambs than the pasture-fed counterparts during 4 d of storage.

Metmyoglobin reducing activity

There was no pre-weaning × finishing system × storage interaction (P = 0.6289) for MRA (Table 4). Additionally, there was no effect of pre-weaning (P = 0.5784) and finishing system (P = 0.082). However, an effect of storage (P < 0.0001) was observed with a decrease (P < 0.05) in MRA from day 0 to day 6 of storage (Table 4). The observed decrease in MRA could be attributed to the decrease of nicotinamide adenine dinucleotide (NADH) content in fresh meat during storage (Kim et al., 2009). Metmyoglobin reducing activity is the ability of meat to delay discoloration through an electron addition to metmyoglobin through enzymatic or nonenzymatic processes (Ramanathan et al., 2014). NADH plays an important role in MRA since it acts as a coenzyme and electron carrier in the reduction of metmyoglobin (Renerre, 1990) and can be regenerated by lactate dehydrogenase activity (Ramanathan et al., 2014). During storage, there is a decline in lactate dehydrogenase activity as well as in NADH content, which could decrease the MRA of fresh meat (Kim et al., 2009).

In agreement with the observations of the present study, a decrease in MRA has been documented in lamb during refrigerated storage. Li et al. (2017) reported a decrease in MRA of lamb LL muscles during 10 d of storage under refrigeration. Gao et al. (2013) reported a decrease in MRA of lamb longissimus dorsi, semitendinosus, and psoas major muscles over 6 d of refrigerated storage. Further work (Gao et al., 2014) examined the impacts of different production strategies on color stability of lamb semitendinosus muscle and reported a decrease in MRA during 9 d of refrigerated storage.

Lipid oxidation

There was no pre-weaning × finishing system × storage interaction (P = 0.2911) for TBARS. Additionally, there was no effect of pre-weaning (P = 0.7703) and finishing system (P = 0.3349) for TBARS values. However, there was an effect of storage (P < 0.0001) for lipid oxidation, with the chops exhibiting an increase in lipid oxidation from day 0 to 6 of storage (Table 4). The increase in lipid oxidation during storage could be associated with the generation of free radicals responsible for triggering lipid oxidation (Min and Ahn, 2005). The oxidation of myoglobin and lipids in meats is inter-influential (Suman and Joseph, 2013). The heme iron in myoglobin can be oxidized generating reactive intermediates (e.g., hydrogen peroxide), which can further increase myoglobin and lipid oxidation (Faustman et al., 2010). The decline in color stability (Table 4) agreed with the observed increase in TBARS (Table 4) during storage. An increase in lipid oxidation of lamb during a refrigerated storage period has been reported previously in longissimus dorsi (Berruga et al., 2005), LL (Ponnampalam et al., 2017; Gonzales-Barron et al., 2021), and semimembranosus (Ponnampalam et al., 2017) muscles. On the contrary, similar TBARS were reported in longissimus dorsi muscles from pasture-fed lambs during refrigerated storage (Luciano et al., 2012, 2013).

Luciano et al. (2013) investigated the effect of forage or concentrate-based diet on the oxidative stability of lamb LL and documented similar TBARS in lamb from both feeding systems on day 0. In addition, an increase in lipid oxidation was observed for the concentrate-fed group, while lipid oxidation in the forage counterparts remained stable during storage. Luciano et al. (2009) also reported an effect of diet and storage in TBARS of semimembranosus muscle from Comisana lambs fed with forage or concentrate diets; while there was an increase of TBARS during 14 d of storage, lamb fed with forage exhibited lower TBARS than concentrate-fed counterparts. Hajji et al. (2016) investigated the influence of concentrate or pasture finishing diet on lipid oxidation of North African lambs and reported greater TBARS in longissimus dorsi from lambs fed with concentrate than those from pasture-fed lambs. Similar results were reported by Sante-Lhoutellier et al. (2008) in lamb longissimus dorsi; lipid oxidation was greater in the concentrate-fed lambs than the pasture-fed animals.

Conclusions

The findings of the present study indicate that artificially raising ram lambs with milk replacer and subsequently finishing them either in a high-forage or high-concentrate diet did not influence the color and oxidative stability of meat. The lambs raised conventionally and artificially (with milk replacer) and subsequently finished on high-forage or high-concentrate exhibited similar carcass characteristics, color attributes, and oxidative stability. These findings suggest that milk replacer can be successfully utilized as a practical artificial raising strategy in lamb production without negatively impacting fresh meat color.

Declaration of Competing Interest

The authors declare no conflicts of interest.

Acknowledgments

This work was supported by the U.S. Department of Agriculture–Agricultural Research Service, National Program 101, Food Animal Production (ARS Project 5042-32630-004-00D).

Author Contribution

Koushik Mondal: data curation, formal analysis, and writing – original draft. Surendranath P. Suman: conceptualization, funding acquisition, investigation, methodology, project administration, resources, supervision, validation, and writing – review & editing. Katherine G. Purvis: data curation. Jennifer Weinert-Nelson: data curation. Gregg Rentfrow: conceptualization, funding acquisition, investigation, methodology, resources, and supervision. Donald G. Ely: methodology and resources. Brittany E. Davis: conceptualization, investigation, methodology, resources, and supervision. Yifei Wang: data curation, formal analysis, and software. Ana Paula A. A. Salim: formal analysis, validation, visualization, writing – original draft, and writing – review & editing.

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