Antioxidant diet supplementation and lamb quality throughout preservation time E. Muela, V. Alonso, M.M. Campo, C. Sa˜nudo, J.A. Beltr´an PII: DOI: Reference:

S0309-1740(14)00166-1 doi: 10.1016/j.meatsci.2014.05.035 MESC 6442

To appear in:

Meat Science

Received date: Revised date: Accepted date:

4 September 2013 27 March 2014 30 May 2014

Please cite this article as: Muela, E., Alonso, V., Campo, M.M., Sa˜ nudo, C. & Beltr´an, J.A., Antioxidant diet supplementation and lamb quality throughout preservation time, Meat Science (2014), doi: 10.1016/j.meatsci.2014.05.035

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ACCEPTED MANUSCRIPT Antioxidant diet supplementation and lamb quality throughout preservation time

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Muela, E., Alonso, V., Campo, M.M., Sañudo, C., and Beltrán, J.A*

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Departamento de Producción Animal y Ciencia de los Alimentos,

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Universidad de Zaragoza, Miguel Servet, 177, 50013, Zaragoza, Spain.

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Abstract

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Diet supplementation (DS) (100, 200, 300 ppm vitamin E -VE; 150 ppm product rich in flavonoids -PRF; 100 + 100 ppm VE-PRF; no supplementation) effect was evaluated on lamb quality throughout 10 days after sampling (preservation time: PT). pH, colour,

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myoglobin forms and lipid oxidation were analyzed on Longissimus thoracis et lumborum. Trained panellists evaluated colour intensity of loin chops packaged in

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modified atmosphere under display up to 12 days. Preservation time had a larger effect on quality than DS. Diet supplementation showed a clear antioxidant effect on lipids,

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especially at long PT and at high doses of VE. Results of the visual test indicated statistical differences among DS from day 4 of display where 200 and 300 ppm VE improved visual colour score. In general, supplementation with antioxidants showed better meat quality and diets higher than 100 ppm VE showed higher antioxidant capacity than the rest. The PRF diet was similar for a short PT but lower at a long PT. More research on flavonoids is necessary.

Keywords: flavonoids, vitamin E, lamb meat, lipid oxidation, visual test.

* Corresponding author. Tel.: +34 976762738; E-mail address: [email protected] (J.A. Beltrán).

ACCEPTED MANUSCRIPT 1. Introduction

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Meat appearance plays an important role in consumer acceptance and purchase since the

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visual aspect is their only tool available to make a purchase decision (Faustman, &

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Cassens, 1990). Colour is considered as one of the most influential factors (Faustman, & Cassens, 1990) where ‘red’ and ‘bright red’ are associated with freshness of the raw product and any brownish colour as an indicator of being stale or spoiled (Forbes,

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Vaisey, Diamant, & Cliplef, 1974). Thus, brown meat often cannot be sold at the full

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retail price resulting in an economic loss (Khliji, van de Ven, Lamb, Lanza, & Hopkins, 2010; Ripoll, González-Calvo, Molino, Calvo, & Joy, 2013).

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Oxidative processes lead to the degradation of meat lipids and proteins which, in turn, contribute to the deterioration in flavour, texture and colour of displayed meat products

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(Ripoll et al., 2013). As time passes, the change of meat colour from red to brown occurs due to metmyoglobin formation (Renerre, 1990). This is related to lipid

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oxidation and microbial growth which are the main factors that determine food quality loss and shelf-life reduction (Fernández-López, Zhi, Aleson-Carbonell, Pérez-Alvarez, & Kuri, 2005).

The use of antioxidants is a widespread practice for preserving meat colour and maintaining lipid stability. These are added either into the feed of the animal or directly as additives in the meat. Synthetic antioxidants are commonly used as alimentary additives (Verhagen, Deerenberg, Marx, ten Hoor, Henderson, & Kleinjans, 1990) however they have been associated with potential human health risks and consumer rejection (Camo, Beltrán, & Roncalés, 2008). Consequently, there is a practical need to

ACCEPTED MANUSCRIPT search and select natural antioxidants as effective alternatives for meat preservation (Kikuzaki, & Nakatani, 1993) and, even, for preventing food diseases (Fernández-López

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et al., 2005). Furthermore, natural antioxidants are less strictly regulated internationally

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(Weiss, Gibis, Schuh, & Salminen, 2010).

Dietary supplementation of natural antioxidant substances into animal feeds has proven to be a simple and convenient strategy to uniformly introduce them into the inner and

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outer sides of phospholipid membranes (Descalzo & Sancho, 2008; Nieto, Díaz, Bañón,

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& Garrido, 2010). These cell-integrated antioxidants are more effective than those added directly to the meat to prevent oxidative damage (Kerry, Buckley, Morrissey, O’Sullivan, & Lynch, 1998). Natural antioxidants are mainly fat soluble substances and

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enzymes (in the skeletal muscle the most important are: superoxide dismutase, catalase and glutathione peroxidase; Descalzo, & Sancho, 2008). Together, non- and enzymatic

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systems operate to counteract the action of pro-oxidants in muscle tissues (Decker, Livisay, & Zhou, 2000). It has been shown that these enzymes exhibit residual activity

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in muscles post-mortem (De Vore, & Greene, 1982; Renerre, Dumont, & Gatellier, 1996) maintained only to the remnant at the onset of cell death (Descalzo, & Sancho, 2008). Hence, since this activity is limited after slaughter, antioxidant substances offer the only pathway to maintain antioxidant activity as time passes.

Among potential antioxidants vitamin E is the most commonly used because of its known effect on retarding lipid oxidation, improving colour stability (Jacob, & Thomson, 2012; Yang, Lanari, Brewster, & Tume, 2002), flavour, texture, and nutritional value (Salvatori, Pantaleo, Di Cesare, Maiorano, Filetti, & Oriani, 2004). All of that is reflected for extending shelf-life (Gobert, Gruffat, Habeanu, Parafita,

ACCEPTED MANUSCRIPT Bauchart, & Durand, 2010; Wulf, Morgan, Sanders, Tatum, Smith, & Williams, 1995) from 1.6 to 5 days of retail-display life without compromising microbiological quality

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(Descalzo, & Sancho, 2008). However, there is little information on the use of vitamin

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E as a feed additive for light lambs fed concentrates in indoor conditions and its

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subsequent effect on meat production (Guidera, Kerry, Buckley, Lynch, & Morrissey, 1997; Ripoll, Joy, & Muñoz, 2011) or quality (Ripoll et al., 2013). The knowledge gap is more noticeable when comparing or combining it with other antioxidant substances.

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In fact, dietary requirements of vitamin E for sheep are not clear (Salvatori et al., 2004)

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and so far only the NRC has published recommendations. López-Bote, Daza, Soares, & Berges (2001) have suggested e.g. 550 to 625 mg /kg diet as recommendable levels of

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vitamin E to delay meat deterioration.

Vitamin E is not the only compound with antioxidant advantages. In fact, the effects of

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other dietary compounds such as carotenoids and flavonoids are being increasingly investigated (Petron, Raes, Claeys, Lourenço, Fremaut, & de Smet, 2007). Among

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natural antioxidants, flavonoids have gained large interest since they are widely distributed in plants (Bodas, Prieto, López-Campos, Giráldez, & Andrés, 2011). The term ‘flavonoid’ is a generic name that identifies a group of secondary metabolites derived in vegetables which are synthesized from phenylalanine and malonyl-CoA. All flavonoids are water soluble and produce polyphenolic compounds as a final by-product (for more information see Rice-Evans, Miller, & Paganga, 1996). The antioxidant activity of phenolic compounds is due to their ability to scavenge free radicals, donate hydrogen atoms or electrons or chelate metal cations as a result of their chemical structure (Rice-Evans et al., 1996). Qualities include the preservation of colour (Yang et al., 2002), limiting lipid peroxidation in meat as well as preserving animal health and

ACCEPTED MANUSCRIPT product quality (Wood, & Enser, 1997). Additional benefits include positive effects on anti-inflammatory, anti-viral and cardiovascular diseases, cancer and other pathologies

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(Rice-Evans, et al. 1996). As a consequence of these numerous benefits, there is a

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growing number of investigations in bioflavonoids (e.g. Andrés, Tejido, Bodas, Morán,

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Prieto, Blanco, & Giráldez, 2013; Bodas, et al., 2011; Simitzis, Ilias-Dimopoulus, Charismiadou, Biniari, & Deligeorgis, 2013). However, there is little knowledge about the effect of each flavonoid, their combinations, doses or association with other

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antioxidant substances, especially in light lambs.

There is also a growing interest in implementing strategies to extend the shelf-life of meat cuts under retail display conditions (Bañón, Méndez, & Almela, 2012). The use of

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modified atmospheres that are rich in oxygen improves the stability of meat colour (Nieto et al., 2010) especially for red meats, and prevents microbial growth of anaerobic

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pathogens (Bañón et al., 2012). A disadvantage is that lipid oxidation is increased (Gobert et al., 2010; Ripoll et al., 2011) and this is one of the primary causes of quality

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loss during such storage (Renerre, & Labadie, 1993). To retard or minimize oxidative deterioration antioxidants may be added, since the short shelf-life of packed lamb is one of the principal concerns for its commercialization (Camo et al., 2008). Thus the combination of both technologies could provide a successful strategy to improve the shelf-life of lamb products.

The aim of this study was to evaluate whether a citric dietary flavonoid, vitamin E supplementation or their combination would have a benefit on lamb quality throughout preservation time.

ACCEPTED MANUSCRIPT 2. Materials and methods

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2.1. Animals

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The study used 60 Rasa Aragonesa lambs (for more details see Sañudo, 2011). After weaning at 50 days of age, animals were randomly selected based on live weight from a feedlot to obtain a homogenous population. Animals were divided into six groups.

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Three groups were 100, 200 or 300 ppm Vitamin E treatments (VE) supplemented with

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commercial vitamin E (Microvit E Promix 50®; DL-α-tocopheryl acetate: 54%, precipitated silica: 46%). A fourth group was 150 ppm Product Rich in Flavonoids (PRF) supplemented with Evencit® (powder composed of extracts of citrus fruits -

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Citrus paradisi, Citrus aurantium bergamia, Citrus sinensis, and Citrus reticulata - over an inert support of vegetal glycerin, with a minimum of 5% of ascorbic acid, 3.5% of

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polyphenols and 0.8% of bioflavonoids - naringin: 653,66 ± 26,46 mg/100 g; quercetin: 60,46 ± 2,53 mg/100 g and rutin: 644,93 ± 58,46 mg/100 g -). The fifth was a

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combination of VE plus PRF (100 + 100 ppm, respectively) and finally a control group without supplementation. Animals were reared intensively and fed commercial concentrate (Ovirum AE®, Table 1) with the correspondent diet supplementation (DS) and cereal straw ad libitum up to 80-90 days of age.

2.2. Slaughtering and cooling

Animals were slaughtered in a local EU-licensed abattoir (Mercazaragoza S.A.). Within 15 minutes of dressing, carcasses were transported under refrigerated conditions (0-4 ºC, 85-90% relative humidity) to the facilities of Pastores Cooperative Group and kept

ACCEPTED MANUSCRIPT in refrigeration (0-2 ºC, 90-95% relative humidity). At 18 hours post-slaughter (cold carcass weight = 11.08 - 12.86 kg) carcasses were butchered into commercial cuts. Both

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sides of each carcass, without the neck, shoulder and leg, were obtained and refrigerated

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at 0-2 ºC for a further 30 hours, with a total of 48 hours of ageing before sampling at the

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Meat Quality Laboratory of the Veterinary Faculty of Zaragoza.

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2.3. Sampling protocol. Instrumental and sensory analyses

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The Longissimus thoracis et lumborum muscle (LTL) was dissected and sliced/chopped following method sample requirements.

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To quantify meat colour a Minolta CM 2002 reflectance spectrophotometer was used with an illuminant D65 and a 10° standard observer following the CIE L*a*b* system

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(CIE, 1976). Lightness (L*), redness (a*) and yellowness (b*) were recorded. The hue angle (H*) and chroma (C*) indexes were calculated as: H*= tan-1 (b*/a*), expressed in

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degrees, and C*= √ a*2+b*2. The relative contents of Myoglobin, Oxymyoglobin and Metmyoglobin were calculated from the reflectance curve according to Krzywicki (1979) using 690 nm (the highest wavelength of the instrument). Since the reflectance spectrophotometer only measures the reflectance between 400 nm and 710 nm at 10 nm intervals, the wavelengths 473, 525 and 572 nm were calculated using linear interpolation. Samples were three-cm-wide slices of the left Longissimus thoracis (LT), with four slices per animal so that there was one slice per preservation time (PT) (0, 4, 7 or 10 days). Slices were placed in polystyrene trays overwrapped with an oxygen permeable film (650 cc/m2/h, 23h oxygen permeability; Irma, Zaragoza, Spain) and kept in refrigeration (2-4 ºC) and darkness simulating household conditions. Readings were

ACCEPTED MANUSCRIPT performed at different locations on the surface area of the same slice at each PT with 15 minutes of blooming before the measurement at 0d (considered after 48h of ageing).

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Results were expressed as the average of three measurements.

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To assess lipid oxidation, slices of about 30 grams were obtained from the left LTL, vacuum-packed and kept in the same PT conditions as the colour samples. After the correspondent PT, these samples were frozen and stored at -20 ºC until analysis which

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was performed in less than 1 month from freezing. Prior to analysis, samples were

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thawed in tepid water for 2 hours when a CRISSON 503 pH-meter equipped with a penetrating electrode was used to measure the pH. Lipid oxidation was measured with

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Frigg, & Steinhart (1995).

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the TBARS (Thiobarbituric Acid-Reactive Substances) method described by Pfalzgraf,

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The right cut side of the carcass was sliced into 15-mm-wide chops for the visual test. Samples were stored in a modified atmosphere packaging -MAP- (70%O2:30%CO2)

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performed with an Ulma Smart 500 machine and having three chops per tray per animal. These trays were placed in a Zafrío expositor (Zafrío S.L., Zaragoza, Spain) at 2-4 ºC with 16 hours of light exposure (1200 lx). Both MAP and retail display simulates commercial conditions. The trays were evaluated daily up to 8d of display and again on days 11 and 12 for colour intensity by seven panelists using a structured 8-point scale from 1 (low intensity) to 8 (high intensity). Each tray was identified with a 2-digit code which was randomly changed every day to avoid sample recognition.

2.4. Statistical analyses

ACCEPTED MANUSCRIPT Data were analyzed using the Mixed procedure of SAS statistical package (8.02) and mean separation was carried out using Duncan’s Multiple Range Test with the level for

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statistical significance set at P≤0.05. The statistical model included dietary

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supplementation (DS) and preservation time (PT) as fixed effects and animal within

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treatment as random.

Among the parameters analyzed in the meat, only colour was not affected significantly

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by the interactions between DS and PT. Thus, a second model was performed where DS

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was analyzed within PT effect and vice versa. This model allowed the authors to determine the quality differences among DS within one PT as well as changes of one

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DS over various PTs.

The mean and the standard error of the difference (SED) were calculated for each

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variable. To describe the relationship between meat quality traits, Pearson’s Correlations were performed using all data as a block. Principal Component Analysis

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(PCA) was also performed using the average of DS within PT in order to obtain a clear view of which variables are of importance at each PT.

3. Results and discussion

3.1. pH

pH values (Table 2) ranged from 5.64 to 5.76 along the PT which can be considered normal since a value lower than 5.8 has been previously described as normal pH in lamb (Devine, Graafhuis, Muir, & Chrystall, 1993). DS had a significant effect on pH at

ACCEPTED MANUSCRIPT 4 and 10d PT. At 4d PT the control, 100 ppm VE and 100 + 100 ppm VE/PRF diets showed the lowest values with significant differences found between the control and

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100 ppm VE groups compared to other DS groups. At 10d PT, the 100 ppm VE had the

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lowest value and the control group had the highest pH. There is no apparent explanation

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for this result, although several authors have reported higher values in grazing lambs (Coulon, & Priolo, 2002) with a known high VE content. Nevertheless, these differences would not have practical implications. In the study of Ripoll et al. (2013) no

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significant differences among 3 feeding durations with 500 mg VE/kg (10, 20 or 30d)

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were found and the observed pHs were lower than in the current study which may be related to their use of fresh meat, but were similar to those reported in thawed meat

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throughout preservation by Muela, Sañudo, Medel, & Beltrán (2012).

PT had a significant effect on pH values for all the DS except 300 ppm VE (Table 2).

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The pH was rather stable throughout PT although a general increase was shown from 7 to 10d PT. The increase was probably due to protein degradation caused by

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microorganisms and enzymes (Devine, Graham, Lovatt, & Chrystall, 1995).

3.2. Colour

Lightness (L*) was not affected by DS (Table 3) with the control treatment having the lowest values. In the study of Andrés et al. (2013), comparing lambs supplemented with flaxseed, quercetin or a combination of both, there were no significant L* differences over a 14d-display among diets. However, in the study of Ripoll et al. (2011), where different vitamin E and selenium doses or the combination of both were tested, VE

ACCEPTED MANUSCRIPT samples showed lower L* values due to less superficial moisture linked to a higher

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water holding capacity related to VE.

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Hue (H*) and Chroma (C*) were affected by DS and PT but in different patterns. There

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were observed significant differences among DS on H* where 100 ppm VE and 100 ppm + 100 ppm VE/PRF showed the highest values at 7 and 10d PT, respectively (Table 3). Thus, 100 ppm could be considered less favourable for colour preservation

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than all other VE treatments and 150 ppm PRF. In regards to C*, DS was only

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significant at 4d PT (Table 3) where 200 ppm VE presented a significantly lower value than the 100 ppm VE and control treatments due to a lower yellowness (b*) (data not shown). Andrés et al. (2013) did not show a significant effect on C* despite there were

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a* and b* differences, in agreement with the current results. Human evaluators are not able to differentiate individual L*a*b* coordinates but are able to understand real colour

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(H*) and L* (Ripoll, Joy, Muñoz, & Alberti, 2008). Thus, the differences observed in

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L* and H* would not have a great influence at a visual level up to 7d PT.

PT had a greater effect on colour compared to DS since all coordinates were significantly affected by this effect (Table 3). From 0 to 4d PT an L* increase was shown, then stabilizing from 4 to 7d PT. Following this, an additional L* increase from 7 to 10d PT was observed. In the studies of Ripoll et al. (2011, 2013), an increase in L* value was also observed throughout display although values were higher than in the current study due to differences in methodology. Nevertheless, all samples would be acceptable considering an L* value 0.1); t: tendency (p≤0.1); *: p≤0.05; **: p≤0.01; ***: p≤0.001; a-c: different letters in the same column indicate significant differences (p≤0.05); w-z: different letters in the same row indicate significant differences (p≤0.05).

ACCEPTED MANUSCRIPT Table 4. Effect (significance values) of diet supplementation and preservation time (days) on myoglobin forms (mean and standard error of the difference - SED). 0

4

7

10

SED

pvalue

100 ppm VE

19.97w

21.80cx

25.19y

28.93z

1.35

***

200 ppm VE

18.79x

20.23abcx

23.34y

27.77z

2.08

***

300 ppm VE

18.29x

20.19abcx

24.14y

30.30z

1.25

***

150 ppm PRF

18.39x

19.35ax

23.21y

26.96z

1.71

***

100 ppm VE + 100 ppm PRF

18.84x

21.05bcx

24.35y

28.97z

3.40

***

Control

18.93x

19.84abx

23.86y

28.62z

1.94

***

SED

1.03

1.05

1.38

2.51

p-value

ns

*

ns

ns

100 ppm VE

61.95z

36.75y

27.94ax

34.08y

4.60

***

200 ppm VE

62.80z

39.50y

33.92cx

38.35xy

3.73

***

300 ppm VE

32.39bcx

35.05xy

2.80

***

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% MetMb

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Effect/Variable

38.58y

150 ppm PRF

59.02z

41.00y

32.38bcw

36.19x

4.68

***

100 ppm VE + 100 ppm PRF

59.98z

40.30y

32.37bcx

34.86x

3.61

***

Control

63.66z

37.50y

30.53abx

35.57y

4.00

***

SED

4.54

2.66

2.01

2.39

p-value

ns

ns

**

ns

100 ppm VE

18.09x

41.44y

46.86bz

36.99y

4.69

***

200 ppm VE

18.41x

40.27z

42.75az

33.88y

3.25

***

300 ppm VE

24.60x

41.22z

43.46az

34.65y

2.65

***

150 ppm PRF

22.59x

39.65y

44.41abz

36.85y

4.11

***

100 ppm VE + 100 ppm PRF

21.18x

38.65y

43.28az

36.17y

3.98

***

Control

17.41x

42.66z

45.61abz

35.81y

3.37

***

SED

4.41

2.35

1.86

2.24

p-value

ns

ns

*

ns

57.10z

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% Mb

% OMb

VE: vitamin E; PRF: product rich in flavonoids (Evencit®); MetMb: Metmyoglobin; Mb: myoglobin; OMb: Oximyoglobin; ns: no significant (p≥0.1); *: p≤0.05; **: p≤0.01;***: p≤0.001; a-c: different letters in the same column indicate significant differences (p≤0.05); w-z: different letters in the same row indicate significant differences (p≤0.05).

ACCEPTED MANUSCRIPT Table 5. Effect (significance values) of diet supplementation and preservation time (days) on lipid oxidation (mg malonaldehyde/kg meat) (mean and standard error of the difference - SED). p-value

4

7

10

100 ppm VE

0.109bcw

0.527bx

1.193cy

1.678bz

0.29

***

200 ppm VE

0.085ax

0.201axy

0.359ay

0.702az

0.20

***

300 ppm VE

0.107abcx

0.171ax

0.276ax

0.725ay

0.17

***

150 ppm PRF

0.117cx

0.283ax

0.770by

1.428bz

0.26

***

100 ppm VE + 100 ppm PRF

0.115cw

0.551bx

1.403cy

2.154cz

0.27

***

Control

0.091abw

0.518bx

1.300cy

2.550cz

0.23

***

SED

0.03

0.27

0.19

0.31

-

-

p-value

*

***

***

-

-

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0

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SED

Effect/Variable

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VE: vitamin E; PRF: product rich in flavonoids (Evencit®); *: p≤0.05; ***: p≤0.001; a-c: different letters in the same column indicate significant differences (p≤0.05); w-z: different letters in the same row indicate significant differences (p≤0.05).

ACCEPTED MANUSCRIPT Table 6. Effect (significance values) of diet supplementation and preservation time (days) on lamb colour instensity1 (mean and standard error of the difference - SED). 150 ppm

100 + 100 ppm VE / PRF

Effect/Variabl e

100 ppm VE

200 ppm VE

300 ppm VE

PRF

Day 1

7.54z

7.66z

7.61z

7.64z

7.64z

7.71z

Day 2

7.63z

7.51z

7.47z

7.39z

7.46z

7.50z

Day 3

6.64y

6.79y

6.80y

6.50y

6.61y

6.86y

Day 4

5.27abx

6.23dx

6.19dx

5.17ax

5.86cd x

5.70bc x

Day 5

3.93ab w

5.77d w

5.80dx

4.97bw

4.39aw

Day 6

3.47av

5.03cv

4.04bv

3.33av

Day 7

2.57au

4.47cu

2.21av

3.57bu

2.24au

Day 8

2.47abu

3.76bt

4.04bv

1.99av

2.83bt

2.36ab u

Day 11

1.71at

3.11cs

3.34cu

1.77av

2.33bs

1.81at

Day 12

2.16atu

3.16cs

3.56cu

2.04av

2.60bt

1.74at

p-value

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SED

5.24c w 4.90c w

3.81a w 3.49a w

Control

SED

0.1 3 0.1 6 0.1 8 0.2 4 0.2 6 0.2 8 0.2 7 0.2 5 0.2 2 0.2 2

0.23

0.22

0.22

0.22

0.22

0.22

-

***

***

***

***

***

***

-

pvalu e ns ns ns *** *** *** *** *** *** *** -

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VE: vitamin E; PRF: product rich in flavonoids (Evencit®); ns: no significant; ***: p≤0.001; a-d: different letters in the same column indicate significant differences (p≤0.05); s-z: different letters in the same row indicate significant differences (p≤0.05). 1 Scale from 1 (low intensity) to 8 (high intensity).

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Highlights > This study evaluated diet supplementation (vitamin E/flavonoids/vit E. + flavonoids/no supplementation) effect on lamb quality > Quality was analyzed throughout preservation time up to 10-12 days > Supplementation had a great benefit on lipid oxidation, increased at higher doses > Supplementation influenced visual score after 4 days of display > Higher vitamin E doses showed higher stability and extended shelf-life.

Antioxidant diet supplementation and lamb quality throughout preservation time.

Diet supplementation (DS) (100, 200, 300ppm vitamin E -VE; 150ppm product rich in flavonoids-PRF; 100+100ppm VE-PRF; no supplementation) effect was ev...
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