or late-gestation on meat quality and fatty acid profile of progeny

Meat Science 152 (2019) 31–37

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Influence of maternal protein restriction in primiparous heifers during midand/or late-gestation on meat quality and fatty acid profile of progeny☆

T

M.J. Webba,1, J.J. Blocka,2, R.N. Funstonb, K.R. Underwooda, J.F. Legakoc, A.A. Hartya, ⁎ R.R. Salversona, K.C. Olsona, A.D. Blaira, a

Department of Animal Science, South Dakota State University, Brookings, SD 57007, United States West Central Research and Extension Center, University of Nebraska-Lincoln, North Platte, NE 69101, United States c Department of Animal and Food Sciences, Texas Tech University, Lubbock, TX 79409, United States b

ARTICLE INFO

ABSTRACT

Keywords: Beef Carcass composition Fetal programming Fatty acid Meat quality

The objective of this study was to evaluate the influence of metabolizable protein (MP) restriction in mid- and/or late-gestation on meat quality characteristics of progeny. Heifers were assigned to 2 levels of dietary protein (control [CON], 102% of MP requirements; or restricted [RES], 80% of MP requirements) at 2 stages of gestation (mid-gestation [MID] and late-gestation [LATE]) in a Balaam's Design crossover treatment structure resulting in 4 treatment combinations (CON-CON, CON-RES, RES-CON, RES-RES). A carryover effect of MID MP treatment on LATE CON indicated CON-CON steaks were more tender (P < .001) than RES CON. Mid-gestation restriction resulted in progeny with increased (P < .05) carcass water, soft tissue moisture, and decreased soft tissue fat percentage compared with progeny from dams receiving MID CON. Reduced maternal MP also differentially influenced the fatty acid profiles of progeny. Results suggest it is possible for progeny to overcome a moderate gestational MP restriction with minimal impacts on carcass composition or meat characteristics.

1. Introduction

lead to irreversible long-term effects on growth, performance, and carcass quality (Du et al., 2010). In addition, nutrient restriction in the dam can also increase fat deposition in the fetus due to changes in the metabolic and hormonal environment (Bispham et al., 2005). Any changes in the development and inherent properties of muscle and/or fat could result in a lasting impact on body composition and ultimately meat quality characteristics. Several studies have investigated the impact of global nutrient restriction on progeny skeletal muscle development, intrauterine growth, organ mass, health, reproduction, and angiogenesis (Du, Zhu, Means, Hess, & Ford, 2004; Funston & Summers, 2013; Long, Vonnahme, Hess, Nathanielsz, & Ford, 2009; Meyer et al., 2010; Vonnahme et al., 2007). However, little information is available regarding restriction of specific maternal nutrients such as protein, and subsequent effects on progeny carcass performance and meat quality. Protein is often the first limiting nutrient for gestating beef cows consuming low-quality forage-based diets, and protein restriction can influence energy status (Cochran et al., 1998). Our hypothesis was that MP restriction in mid- and late-

Nutrient status of cows can vary throughout gestation and is subject to changes in forage availability, quality, and access to supplemental feedstuffs (DelCurto, Hess, Huston, & Olson, 2000). Changes in maternal nutrient status can have long-term implications on progeny growth, feed efficiency, muscle development, and ultimately meat quality (Du et al., 2010; Funston, Larson, & Vonnahme, 2010; Wilson, 1999). Fetal skeletal muscle and fat cell development is primarily initiated in the second trimester (Du et al., 2010), at a time when fluctuations in forage quality and/or quantity can result in restricted nutrient intake in gestating cows (DelCurto et al., 2000). Research indicates maternal nutrient restriction may impair skeletal muscle development; predisposing progeny to increased fat deposition (Mohrhauser et al., 2015). Inadequate nutrition in the gestating beef female during the fetal stage has been shown to decrease the size and number of muscle fibers (Zhu, Ford, Nathanielsz, & Du, 2004). As there is no net increase in muscle fiber number after birth in cattle, this could

☆ This research was supported in part by the South Dakota Beef Industry Council, Pierre, SD, USA. Salaries and research support provided by state and federal funds appropriated to South Dakota State University, Brookings, SD, USA. ⁎ Corresponding author. E-mail address: [email protected] (A.D. Blair). 1 Present address: Department of Animal Science, University of Minnesota, St. Paul, MN 55180. 2 Present address: Hettinger Research Extension Center, North Dakota State University, Hettinger, ND 58639.

https://doi.org/10.1016/j.meatsci.2019.02.006 Received 24 May 2018; Received in revised form 12 February 2019; Accepted 12 February 2019 Available online 13 February 2019 0309-1740/ © 2019 Elsevier Ltd. All rights reserved.

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Table 1 Dietary components and nutrients consumed by heifers receiving a control (CON = slightly exceeding MP requirement) or restricted (RES = approximately 80% of MP requirement supplied) diet during mid- and/or late gestation based on NRC (2000) calculationsa. Item

Diet formulation 1b

Diet formulation 2b

CON

RES

CON % DM basis

Diet formulation 3b RES

CON

RES

53.65 15.27

51.22 14.52

51.28 14.54

10.02 11.43 7.46 – 1.43 0.67 0.031 0.019 0.013 0.004

10.79 11.84 7.74 1.54 1.73 0.54 0.034 0.010 0.013 0.005

11.03 12.51 8.20 – 1.62 0.75 0.034 0.010 0.015 0.005

Ca(OH)2 treated wheat strawc Crude glycerind Dry supplemente Ground corn Ground corn cobs Energy Booster 100®f Porcine bloodmeal Sodium phosphate (XP 40) Urea, 46% Magnesium oxide, 54% TM Greeng Selenium, 0.06% yellow Vitamin AD 10:1

59.81 15.66

59.62 17.97

54.14 13.27

– 16.77 3.42 1.62 1.57 1.08 0.032 0.015 0.009 0.004

– 16.56 3.06 – 1.56 1.18 0.034 0.014 0.012 0.004

10.27 11.33 7.38 1.65 1.39 0.51 0.032 0.020 0.011 0.004

Bacterial N balance, g/d MP, % Peptide balance, g/d NEm, Mcal/kg NEg, Mcal/kg

11 108.7 −23 1.24 0.67

Nutrient composition of diet predicted by NRC (2000) based on actual intake 11 −1 −1 2 88.4 101.4 78.3 93.2 −26 −20 −24 −24 1.17 1.37 1.40 1.44 0.61 0.79 0.82 0.85

2 77.2 −29 1.44 0.85

a

Diets formulated based on NRC (2000) Level 2 predictions for MP, NEm, and NEg requirements for heifers throughout gestation. Diet formulation 1 fed from 2Nov2013 – 14Dec2013, diet formulation 2 fed from 15Dec2013 – 18Jan2014, and diet formulation 3 fed from 19Jan2014 – calving. c Nutrient composition of wheat straw: 49.39% DM; 4.75% CP; 57.48% ADF; 66.78% NDF; 3.17% Ca; 0.07% P; 49.75% TDN; 0.95 Mcal/kg NEm; 0.40 Mcal/kg NEg. d Crude glycerin contained 82.3% glycerol, 9.5% water, 0.56% CP, 0.04% methanol, 8.07% ash, and 0.90% MONG (matter organic non-glycerol; defined as 100 – glycerol content (%) + water content (%) + ash content (%)). Crude glycerin sourced from Minnesota Soybean Processors, Brewster, MN. e Dry supplement formulated and mixed by Hubbard Feeds Inc., Mankato, MN. f Milk Specialties Global, Eden Prairie, MN. g TM Green mineral mix contained 6.6% Ca;15.2% S; 330 ppm Co; 33,000 ppm Cu; 1650 ppm I; 132,000 ppm Mn and 99,000 ppm Zn. b

combinations were randomly assigned to a pen within each block, resulting in 3 pen replicates per treatment combination. Diets consisted of calcium hydroxide treated wheat straw, crude glycerin, and concentrates (Table 1). Treatment diets were isocaloric within gestation period and met NRC net energy requirements (2000) for maintenance, growth and pregnancy. Wheat straw was treated with Ca(OH)2 using the SecondCrop™ process (ADM Animal Nutrition, Quincy, IL) to increase energy value. The target level for Ca(OH)2 was 6.6% DM basis and water was added to achieve approximately 50% moisture. Treated straw was packed into production-scale Ag-Bags (Ag-Bag, St. Nazianz, WI). Gestating heifers were delivered their assigned ration once per day beginning in early November 2013 until parturition in the spring of 2014. Average dietary intakes were 6.3 kg for diet formulation 1, 7.5 kg for diet formulation 2, and 8.6 kg for diet formulation 3 (DM basis; Table 1). Heifer body weight (BW) and body condition score (BCS; determined using a 9-point scale:1 = extremely emaciated, 9 = extremely obese, Wagner et al., 1988) data were collected at trial initiation, at treatment crossover, and approximately 3 weeks prior to calving. Mean heifer BW for CON and RES heifers was 431 and 418 kg ± 8.6 and mean BCS was 4.9 and 4.8 ± 0.05, respectively, during mid-gestation. In late gestation, mean heifer BW for CON and RES heifers was 451 and 445 kg ± 8.6 and mean BCS was 4.8 and 4.7 ± 0.05, respectively. Animal performance indicated that diets met targets based on nutrients supplied. After calving, cow-calf pairs were moved to pasture with a common level of nutrition for spring calving cows and managed as a common group through weaning. Bull calves were banded (Latex Castrating bands; Neogen, Lexington, KY) within 24 h after birth. All progeny were fed and managed under the same conditions from birth until harvest so the influence of gestational treatment could be determined. Steer and heifer progeny (n = 103) were backgrounded for 14 d after weaning at the SDSU Cottonwood Range and Livestock Research Station. Following the backgrounding period, progeny were transported 430 km to the University of Nebraska-Lincoln West Central Research and Extension Center, North Platte, NE, and adapted to a common finishing

gestation would result in reductions in postnatal growth and skeletal muscle and increased carcass adiposity. Therefore, the objective of this study was to evaluate the impacts of maternal protein restriction in mid-gestation, late-gestation, or throughout mid- and late-gestation on meat quality, carcass composition, and fatty acid profile of offspring. 2. Materials and methods 2.1. Animals All animal care and experimental protocols were approved by the South Dakota State University Animal Care and Use Committee (Approval number 13-076A). One hundred eight commercial crossbred Angus x Simmental primiparous heifers were allocated to 12 open feedlot pens with windbreaks at the SDSU Cottonwood Range and Livestock Research Station. Rectal ultrasonography was conducted in mid-September of 2013 for pregnancy detection and sex and age of the fetus. Heifers were assigned to blocks in a randomized complete block design according to body weight (BW) and method of conception (artificial insemination vs. natural service). After blocking, heifers were assigned to pens in order to equalize the number of male and female offspring in each pen. This blocking structure resulted in 3 blocks with 4 pens per block. A Balaam's Design crossover treatment structure was used to apply 2 levels of dietary metabolizable protein (MP): control (CON, receiving approximately 102% of MP requirements) and restricted (RES, receiving approximately 80% of MP requirements) during each of 2 periods; mid-gestation (MID, d 148 to d 216 of gestation based on estimated date of conception) and late-gestation (LATE, d 217 of gestation to parturition). The resulting 4 treatment combinations were mid-gestation MP control followed by late gestation MP control (CON-CON), mid-gestation MP control followed by late gestation MP restricted (CON-RES), mid-gestation MP restricted followed by late gestation MP control (RES-CON), and mid-gestation MP restricted followed by late gestation MP restricted (RES-RES). These 4 treatments 32

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diet (48% dry rolled corn, 7% grass hay, 40% corn gluten feed, and 5% finisher supplement containing vitamin and minerals, with nutrient composition of 11.5% crude protein, 1.9 Mcal/kg NEm, and 1.4 Mcal/kg NEg [dry matter basis]). Cattle were fed and managed to maintain health and achieve a common backfat thickness (~1.27 cm) prior to harvest. Cattle were transported 103 km to Tyson Fresh Meats, Lexington, NE for harvest. The AI-bred progeny were harvested 21 days earlier than the natural service bred progeny, which reflects the approximate difference in their birth dates. Actual mean backfat thickness was 1.37 cm and 1.34 cm for AI-bred and natural service groups, respectively. Cattle were tracked individually through slaughter to maintain identity.

orientation (AMSA, 2015). Immediately after coring each steak, a single peak shear force measurement was determined for each core using a Warner-Bratzler shear machine (G-R Electric Manufacturing Company, Manhattan, KS). Measurements of the peak shear force value were recorded and averaged to obtain a single shear force value per steak. 2.5. Fatty acid composition Steaks designated for FAME synthesis were thawed slightly and external fat, epimysial connective tissue, and additional muscles were trimmed from the LL. Slices (1-cm) of trimmed LL were minced, immersed in liquid nitrogen, and powdered using a commercial blender for 15 s at room temperature. Brief pulses were used to reduce fat smearing on the walls of the blender. Powdered samples were stored at −80 °C until ready for FAME synthesis. Duplicate 1 g samples were weighed and processed to generate FAME according to procedures outlined by O'Fallon, Busboom, Nelson, and Gaskins (2007). Measurement of FAME was done by gas chromatography (GC) using an HP-88 capillary column (30 m × 0.25 mm × 0.20 μm; Agilent Technologies, Palo Alto, CA, USA) and a flame ionization detector (FID). One microliter of sample was injected with a split ratio of 50:1. The oven method was as follows: 120 °C held for 1 min, increased to a temperature of 170 °C at the rate of 15 °C/min, held for 2 min, then increased to a temperature of 200 °C at the rate of 3 °C/min, held for 1 min, and finally increased to a temperature of 235 °C at a rate of 20 °C/min and held for 1 min. Hydrogen was used as the carrier gas. The FID was operated at 300 °C. Fatty acid methyl esters were identified and quantified by use of authentic standards (Supelco 37 Component FAME mix, Sigma-Aldrich, St. Louis, MO, USA). Concentrations of fatty acids were calculated on a raw wet-weight basis.

2.2. Objective color evaluation After chilling, carcasses were ribbed between the 12th and 13th rib and the exposed longissiumus thoracis (LT) was allowed to bloom for approximately 30 min. Objective color (L*, a*, and b*) was measured using a Minolta colorimeter (Model CR-310, Minolta Corp., Ramsey, NJ; 50 mm diameter measuring space; D65 illuminant). Measurements were recorded at 2 locations of the LT (medial and lateral) and averaged for each carcass. 2.3. Sampling procedures Following carcass chilling (approximately 24 h), the left striploin of all carcasses were collected and transported under refrigeration (2.2 °C) to the SDSU Meat Laboratory in Brookings, SD. Striploins were trimmed to 0.64 cm of external fat, faced to obtain a square anterior edge, and fabricated into 2.54-cm steaks. The anterior face of the longissimus lumborum (LL) was aged 3 d postmortem, frozen, and later used for determination of crude fat percentage using ether extract analysis. The first four most anterior steaks were assigned to a 3, 7, 14, or 21 d postmortem aging period and utilized to determine percent cook loss and Warner-Bratzler shear force (WBSF). Once vacuum-sealed, steaks were immediately stored in the absence of light at 2.2–3.8 °C for the specified aging period. After completion of the designated aging period, steaks were frozen (−20 °C) for subsequent evaluation of ether extractable fat, percent cook loss, and tenderness. Carcasses from a subsample of steer progeny (6 steers per treatment combination) selected from artificially inseminated heifers of moderate body condition score and BW were subjected to additional analysis. Because artificially inseminated heifers constituted 2 of the 3 blocks the experimental design for these data was a randomized complete block with two replicates per treatment. The fifth most anterior steak from the striploin of each subsampled carcass (n = 24) was aged 3 d postmortem, frozen, and used for direct fatty acid methyl ester (FAME) synthesis. The 9–10 − 11 rib section of this same subsample of carcasses (n = 23, 1 carcass was not available for rib dissection) were removed from the left side of each carcass using the anatomical reference points outlined by Hankins and Howe (1946) and utilized to determine carcass composition.

2.6. Carcass composition An initial total weight of the excised rib section was recorded. After dissection into soft tissue and bone, each portion was weighed separately for carcass composition determination as outlined by Mohrhauser et al. (2015). The soft tissue from each rib section was processed using a bowl chopper for later analysis of edible portions of protein, moisture, fat, and ash using equations described by Hankins and Howe (1946). 2.7. Statistical analysis All data were analyzed as a randomized complete block design with pen as the experimental unit. All analyses were conducted using the MIXED procedure of SAS (SAS Institute, Cary, NC) appropriate to a Balaam's Design. Fixed effects fitted were MP treatment, gestational period and the treatment × period interaction. Pen was specified as a random variable. Progeny sex was also included in the model as a fixed effect to absorb this source of variation. For WBSF and cook loss, meat aging period was included as a repeated measure and peak internal cook temperature was used as a covariate. Variance-covariance structures were evaluated for each variable using repeated measures analysis and were selected based on the best model structure fitting the data using the Schwarz's Bayesian Information Criteria (BIC). Denominator degrees of freedom were approximated using the Kenward-Roger option in the model statement (Kenward & Roger, 1997) for all analyses. When the treatment by period interaction was significant, contrast statements were used to evaluate carryover from MID to LATE by testing if LATE CON differed depending on whether it followed MID CON or MID RES, and likewise for LATE RES. All tests were considered significant at P < .05.

2.4. Percent crude fat, percent cook loss and tenderness evaluation The anterior face removed during fabrication was used to determine percent crude fat using the ether extract method outlined by Mohrhauser et al. (2015). Samples were extracted using petroleum ether in a side-arm Soxhlet extractor (Thermo Fischer Scientific, Rockville, MD). Steaks designated for WBSF determination were thawed for 24 h at 3.8 °C then cooked on an electric clamshell grill (George Forman 9 Serving Classic Plate Grill, Model GR2144P, Middleton, WI) to a target internal temperature of 71 °C. Prior to cooking, the raw weight of each steak was recorded. A hand-held thermometer (Model 35,140, CooperAtkins Corporation, Middlefield, CT) was used to record the peak internal cooked temperature, which was used as a covariate in the statistical model. After cooking, steaks were allowed to rest for 4 to 6 min then re-weighed to determine cook loss percentage. Cooked steaks were cooled at 2 °C until the internal temperature reached 4 °C before removing 6 to 8 cores (1.27 cm in diameter) parallel to the muscle fiber

3. Results and discussion Progeny from dams provided CON or RES MP during MID and/or LATE gestation were fed to a target fat thickness (~1.27 cm; as determined by visual appraisal), and harvested to determine the influence of maternal MP on meat quality and carcass composition. 33

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Table 2 Main effect least square means for meat characteristics from progeny of heifers fed a control (CON = slightly exceeding MP requirements) or restricted (RES = approximately 80% of MP requirements) diet during mid- and/or late-gestationa. Item

L⁎ a⁎ b⁎ Cook Loss, % Crude Fat, % WBSFb, N

Mid-gestation

Late-gestation

SEM

CON

RES

CON

RES

43.22 24.41 10.92 18.68 7.36 28.1

42.90 23.99 10.60 18.84 7.06 30.4

43.01 24.09 10.69 18.64 7.40 29.4

43.11 24.30 10.83 18.88 7.02 29.1

0.320 0.268 0.318 0.392 0.248 1.72

Mid

Late

Mid x Late

P-value

P-value

P-value

0.500 0.170 0.221 0.584 0.410 0.007

0.830 0.474 0.572 0.401 0.301 0.760

0.442 0.663 0.921 0.962 0.132 0.001

a Dietary MP levels based on NRC (2000) predicted requirements; mid-gestation treatment applied from mean d 148 through 216 of gestation, late gestation treatment applied from mean d 217 of gestation through parturition. b Warner Bratzler Shear Force.

Table 3 Least squares means for the interaction of mid-gestation MP treatment by late-gestation MP treatment for percentage of total lipid and concentration in raw tissue of lipid fatty acid categories (Saturated fatty acids, SFA; monounsaturated, MUFA; and polyunsaturated fatty acids, PUFA), Warner Bratzler Shear force (WBSF), and soft tissue protein percentage from steers of dams fed a control (CON = slightly exceeding MP requirement) or restricted (RES = approximately 80% of MP requirement supplied) diet during mid- and/or late-gestationa. CON-CON

C14:0 C16:0 C18:1n9 cis C20:4n6 SFA MUFA All lipid WBSF, N Soft tissue protein, %

CON-RES

RES-CON

RES-RES

3.25

Fatty acid percentages (%, g/100 g total fatty acids) 3.23 2.87

49.7 76.6 0.790 90.8 92.5 200.0

20.6 35.0 0.690 31.9 40.2 73.2

Fatty acid concentrations (mg/g raw wet tissue) 39.5 37.9 59.2 55.2 0.473 0.613 73.2 78.2 72.3 88.1 155.3 169.5

26.9 14.651

29.3 13.981

3.11

Meat characteristics 31.9 28.9 13.901 14.877

SEM

Contrast 1b

Contrast 2c

P-value

P-value

0.117

0.286

0.026

2.09 2.23 < 0.001 2.21 2.23 2.24

0.026 0.005 < 0.001 0.005 0.003 < 0.001

0.004 0.003 < 0.001 < 0.001 < 0.001 < 0.001

< 0.001 < 0.001

0.710 < 0.001

1.81 0.0197

Significant main effect or interaction p-vales were bolded. a Dietary MP levels based on NRC (2000) predicted requirements; mid-gestation treatment applied from mean d 148 through 216 of gestation, late-gestation treatment applied from mean d 217 of gestation through parturition. b Contrast to test if the effect of CON in late gestation differs depending on whether it follows CON or RES in mid-gestation. c Contrast to test if the effect of RES in late gestation differs depending on whether it follows CON or RES in mid-gestation.

Meat color (L*, a*, b*), percent ether extractable fat and percent cook loss were not influenced by gestational treatment (P > .05, Table 2). A MID x LATE MP treatment interaction (P < .001) was detected for WBSF (Table 2). Interactions in Balaam's Design indicate that the first period (MID) caused carryover effects on the second period (LATE). In this case, the contrasts indicated that MID MP treatments had carryover effects on LATE CON (P < .001), but not LATE RES (P > .05). The MID MP carryover on LATE CON contrast resulted because progeny of dams exposed to MID RES produced less tender steaks than MID CON, indicating restriction in mid-gestation (MID RES) followed by increased availability of MP (LATE CON) may alter the mechanisms involved in meat tenderness. Nonetheless, the WBSF values in the current study ranged from 26.9 to 31.9 N, which implies all treatment combinations produced progeny with steaks that could be certified tender (≤ 43.2 N; ASTM International, 2011). Miller, Carr, Ramsey, Crockett, and Hoover (2001) determined untrained consumers' perceived steaks to be tough at 45.1 N and tender at 42.2 N. While all samples in this study would likely be considered tender by consumers, the average detected difference in WBSF value was 3.5 N between dams on the RES CON treatment (31.9 N) and all other treatments (28.4 N). Considering the sensitivity of panelists evaluated by Miller et al. (2001), it is possible that increased WBSF of steaks from progeny of dams restricted in MID compared with all other treatments could be detectable by consumer panelists. Alvarenga et al. (2016) evaluated meat quality traits of 20-monthold bull progeny from Santa Gertrudis heifers receiving either high

(14%) or low (7%) CP diets 60 d pre breeding until 24 d post conception. Half of each high and low group were changed to the alternative group 24 d post conception. Alvarenga et al. (2016) determined protein availability during early gestation influenced meat tenderness. Dams receiving low crude protein diets pre-breeding and post-conception produced progeny with tougher semitendinousus muscle than progeny from dams receiving high crude protein pre-breeding and post-conception. Although the timing of gestational protein restriction differed between Alvarenga et al. (2016) and the current study, results indicate maternal nutrition can influence meat quality of progeny. Underwood et al. (2010) evaluated dams grazing either improved pasture (6.0–11.1% crude protein) or native range (5.4–6.5% crude protein) from mid-gestation (d 120–150) through the beginning of the third trimester (d 180–210). Similar to results from the current study, maternal protein availability influenced progeny steak tenderness. Although the number of experimental units was small, with limited details regarding total nutrient availability in the diet, cows grazing improved pasture with increased protein content produced progeny with more tender steaks than cows grazing native range. Different responses among these studies could be related to variations in study design such as timing of maternal protein restriction, drylot versus range environments, number of observations, and use of cows versus heifers. In the Western diet, there has been a focus on decreasing saturated fatty acid (SFA) intake (Cordain et al., 2005) and substituting these fats 34

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Table 4 Percentage of total lipidnd concentration in raw tissue of lipid fatty acid categories (Saturated fatty acids, SFA; monounsaturated, MUFA; and polyunsaturated fatty acids, PUFA) from steers of dams fed a control (CON = slightly exceeding MP requirement) or restricted (RES = approximately 80% of MP requirement supplied) diet during mid- and/or late-gestationa. Fatty acids

Mid-gestation CON

RES

C14:0 C15:0 C16:0 C17:0 C18:0 C20:0 C21:0 C23:0 C14:1n5 C16:1n7 C17:1n8 C18:1n9 cis C18:1 trans C20:1n9 C18:2n6 C18:3n3 C18:3n6 C20:2 C20:3n6 C20:4n6 C20:5n3 SFA MUFA PUFA

3.18 0.52 26.91 1.28 14.6 0.097 0.078 0.030 0.69 2.95 1.10 41.92 2.45 0.487 2.55 0.128 0.022 0.059 0.160 0.50 0.037 46.67 49.76 3.45

3.05 0.53 26.26 1.22 14.3 0.103 0.078 0.042 0.67 3.02 1.10 42.02 2.74 0.487 3.04 0.146 0.031 0.053 0.196 0.68 0.075 46.47 50.11 4.21

C14:0 C15:0 C16:0 C17:0 C18:0 C20:0 C21:0 C23:0 C14:1n5 C16:1n7 C17:1n8 C18:1n9 cis C18:1 trans C20:1n9 C18:2n6 C18:3n3 C18:3n6 C20:2 C20:3n6 C20:4n6 C20:5n3 SFA MUFA PUFA All Lipid

5.0 0.69 35.2 1.57 18.2 0.140 0.108 0.058 1.9 5.09 1.44 55.8 3.6 0.71 3.65 0.251 0.031 0.112 0.237 0.740 0.083 61.3 66.3 5.2 136.6

5.3 0.51 38.7 1.15 19.3 0.120 0.090 0.062 1.7 4.43 1.09 57.2 3.1 0.59 3.33 0.196 0.030 0.091 0.223 0.543 0.099 75.7 80.2 5.1 162.4

Late-gestation CON

SEM

RES

Fatty acid percentages (%, g/100 g total fatty acids) 3.17 3.06 0.108 0.51 0.54 0.139 26.64 26.53 0.298 1.23 1.27 0.231 14.2 14.7 1.14 0.098 0.103 0.00698 0.070 0.086 0.0180 0.038 0.034 0.0145 0.71 0.65 0.116 3.07 2.90 0.425 1.10 1.10 0.128 42.19 41.75 0.452 2.46 2.73 0.770 0.491 0.484 0.0646 2.78 2.81 0.375 0.137 0.136 0.0126 0.027 0.026 0.0267 0.051 0.061 0.0251 0.179 0.177 0.0561 0.60 0.58 0.376 0.058 0.055 0.0492 46.65 46.48 0.855 50.14 49.73 0.518 3.82 3.83 0.212 Fatty acid concentrations (mg/g raw wet tissue) 6.1 4.2 1.13 0.59 0.61 0.281 44.6 29.2 1.48 1.43 1.29 0.872 22.0 15.5 1.58 0.123 0.136 0.0406 0.088 0.110 0.0344 0.061 0.059 0.0108 1.9 1.7 1.11 5.19 4.33 0.866 1.31 1.23 0.468 67.9 45.1 1.58 3.2 3.4 1.51 0.65 0.65 0.255 3.58 3.39 0.672 0.221 0.225 0.0796 0.030 0.030 0.00451 0.093 0.110 0.0122 0.229 0.231 0.0212 0.631 0.652 < 0.001 0.089 0.093 0.0200 82.0 55.1 1.56 82.4 64.1 1.58 5.1 5.1 1.21 177.6 121.4 1.58

Mid

Late

Mid x Late

P-value

P-value

P-value

0.140 0.947 0.032 0.584 0.638 0.205 0.994 0.673 0.785 0.793 0.995 0.733 0.792 0.996 0.059 0.088 0.371 0.892 0.733 0.729 0.149 0.881 0.262 0.103

0.179 0.917 0.560 0.685 0.444 0.221 0.635 0.897 0.432 0.534 0.976 0.196 0.808 0.950 0.858 0.914 0.982 0.827 0.981 0.968 0.885 0.899 0.212 0.966

0.031 0.900 0.431 0.997 0.681 0.996 0.796 0.911 0.874 0.610 0.896 0.587 0.823 0.679 0.650 0.102 0.676 0.899 0.934 0.981 0.836 0.826 0.324 0.807

0.852 0.741 0.170 0.734 0.660 0.324 0.225 0.571 0.871 0.634 0.689 0.560 0.431 0.273 0.796 0.714 0.899 0.048 0.259 < 0.001 0.676 0.003 0.003 0.935 < 0.001

0.289 0.973 0.002 0.909 0.043 0.500 0.168 0.791 0.909 0.544 0.926 0.001 0.724 0.993 0.876 0.977 0.953 0.087 0.870 < 0.001 0.911 < 0.001 0.001 0.993 < 0.001

0.355 0.966 0.003 0.887 0.113 0.416 0.358 0.551 0.800 0.569 0.861 0.001 0.512 0.291 0.729 0.928 0.687 0.620 0.076 < 0.001 0.897 < 0.001 < 0.001 0.645 < 0.001

Significant main effect or interaction p-vales were bolded. a Dietary MP levels based on NRC (2000) predicted requirements; mid-gestation treatment applied from mean d 148 through 216 of gestation, late-gestation treatment applied from mean d 217 of gestation through parturition.

with polyunsaturated fatty acids (PUFA) to support cardiovascular benefits (Siri-Tarino, Sun, Hu, & Krauss, 2010). Moreover, the 2015–2020 Dietary Guidelines for Americans suggest consuming < 10% of calories from SFA per day (USDHHS-USDA, 2015). Fatty acid composition results are presented in Table 4. Myristic acid (C14:0) displayed a treatment by period interaction (P < .05; Table 4). Contrasts revealed that the percentage of C14:0 in progeny samples from dams restricted LATE was reduced (P < .05; Table 3) when dams were provided RES diet during MID (2.87%) compared with dams receiving CON during MID (3.25%). This indicates a carryover effect in which MID RES followed by LATE RES depressed deposition of C14:0 in progeny steaks. When samples were evaluated on a mg/g of raw wet tissue

basis, the concentrations of palmitic acid (C16:0), oleic acid (C18:1n9 cis), total saturated fatty acid (SFA), total monounsaturated fatty acid (MUFA) and total lipid displayed carryover effects from MID MP treatments on both LATE CON and LATE RES. The carryover effect for LATE CON indicated steaks from progeny from dams that received MID CON (CON CON) had elevated levels of each of these FA relative to MID RES (RES CON). The carryover effect for LATE RES indicated the opposite wherein steaks from progeny from dams receiving MID CON (CON RES) had depressed levels of each of these relative to MID RES (RES RES). The concentration of arachidonic acid (C20:4n6) was increased (P < .05) in progeny from LATE CON dams when provided MID CON, however it also increased (P < .05) when the LATE RES 35

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M.J. Webb, et al.

Table 5 Main effect least square means for carcass composition (derived from 9 to 10-11 rib sections) from steers of dams fed a control (CON = slightly exceeding MP requirements) or restricted (RES = approximately 80% of MP requirements) diet during mid- and/or late-gestationa. Trait

Carcass bone, % Carcass protein, % Carcass water, % Carcass fat, % Soft tissue protein, % Soft tissue moisture, % Soft tissue fat, % Soft tissue ash, %

Mid-gestation

Late-gestation

SEM

CON

RES

CON

RES

13.18 12.45 43.55 30.1 14.316 49.95 35.15 0.641

13.10 12.82 45.16 29.0 14.389 51.75 32.76 0.676

13.38 12.59 43.94 30.6 14.276 50.51 34.35 0.656

12.91 12.68 44.77 28.5 14.429 51.19 33.55 0.662

0.496 0.475 0.363 1.06 0.0139 0.432 0.587 0.0360

Mid

Late

Mid x Late

P-value

P-value

P-value

0.727 0.117 0.035 0.502 0.021 0.042 0.045 0.619

0.108 0.615 0.182 0.233 0.002 0.328 0.388 0.924

0.931 0.437 0.194 0.541 < 0.001 0.212 0.221 0.746

Significant main effect or interaction p-vales were bolded. a Dietary MP levels based on NRC (2000) predicted requirements; mid-gestation treatment applied from mean d 148 through 216 of gestation, late-gestation treatment applied from mean d 217 of gestation through parturition.

gestation altered FA profile of progeny steaks, with mid-gestation MP restriction often increasing FA content and late-gestation MP restriction often decreasing FA content in progeny steaks. Mid-gestation and/or lategestation periods of maternal MP restriction did not negatively influence beef color, percent cook loss, or ether extractable fat. Mid-gestation MP restriction shifted soft tissue composition toward increased protein and decreased fat content, but the differences were minor and may not be biologically relevant. Progeny from dams in this study were not subjected to any additional nutrient restrictions beyond gestational treatments; therefore, it is possible progeny were able to overcome a moderate MP restriction during development with adequate postnatal nutrient intake. Alternatively, dams may have mobilized protein reserves to buffer against the MP restriction imposed. Continued research to evaluate specific impacts of maternal nutrient restriction during various stages of gestation on progeny meat quality is important to develop improved feeding and management strategies for gestating beef females.

treatment followed MID CON. Despite these carryover effects for some individual FA and categories, MID RES often decreased FA concentrations (mg/g) compared to MID CON, while LATE RES often increased FA concentrations relative to LATE CON as indicated by main effect responses (Table 4). To date, evaluation of the effects of maternal diet on the fatty acid composition of progeny have not been studied (Greenwood, Clayton, & Bell, 2017). However, in sheep Hou, Hellgren, Kongsted, Vaag, and Nielsen (2013) supplied twin-bearing ewes a normal (100% of protein and energy requirements) or restricted (50% of protein and energy requirements) diet during the final 6 weeks of gestation. Pre-natal nutrition 6 weeks prior to lambing did not influence FA composition in lipid analyses of the hepatic triglyceride or free FA concentration (Hou et al., 2013). Results from the current study indicate maternal MP restriction in both MID and LATE can influence FA composition of steaks from progeny and warrants further investigation. Carcass composition of progeny may be altered by nutrient availability during gestation as mesenchymal stem cells are developing into muscle, fat, and connective tissue (Du et al., 2010). The composite 9–10 − 11 rib sum for carcass composition and edible portions in this study ranged from 99.3% to 100.5% (Table 5). Percent carcass water was increased (P < .05) in progeny carcasses from dams receiving MID RES compared with MID CON. Evaluation of soft tissue responses indicated that dams receiving MID RES resulted in increased (P < .05) progeny soft tissue moisture percentage and reduced (P < .05) fat percentage in the tissue. Soft tissue protein displayed a MID by LATE treatment interaction (P < .05; Table 5). Percent protein in progeny samples from dams receiving LATE CON was decreased (P < .001; Table 3) when dams received MID RES compared to MID CON, whereas protein percentage of progeny from dams receiving LATE RES was increased (P < .001) when dams received MID RES compared to MID CON. The thrifty phenotype hypothesis suggests that maternal dietary insults during fetal development can result in developmental changes that ‘program’ the offspring to adapt to the environment it is born into. Perhaps progeny that experienced a gestational protein restriction were programmed to conserve protein tissue. Although differences in soft tissue composition were detected, these differences were small and may not have biological significance. Evaluation of maternal nutrition effects on beef carcass composition is limited, however, Underwood et al. (2010) also reported increased percent moisture and decreased percent crude fat in the LM from progeny of dams grazing native range (limited protein) compared with progeny of dams grazing improved pasture.

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