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Martina Franca donkey meat quality: Influence of slaughter age and suckling technique
Meat Science 134 (2017) 128–134
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Martina Franca donkey meat quality: Influence of slaughter age and suckling technique
MARK
P. De Paloa, A. Tateoa, A. Maggiolinoa,⁎, R. Marinob, E. Cecia, A. Nisic, J.M. Lorenzod Department of Veterinary Medicine, University “Aldo Moro” of Bari, S.P. per Casamassima, km 3, 70010 Valenzano, BA, Italy Department of Agricultural Food and Environmental Sciences, University of Foggia, Via Napoli, 25-71121 Foggia, Italy c Free Lance DVM, Italy d Centro Tecnológico de la Carne de Galicia, rúa Galicia no 4, Parque Tecnológico de Galicia, San Cibrao das Viñas 32900, Ourense, Spain a
b
A R T I C L E I N F O
A B S T R A C T
Keywords: Donkey meat Artificial suckling Slaughter age Meat quality Rheological parameters
This work aimed to evaluate the effect of suckling technique and slaughter age on Martina Franca donkey meat quality. Twenty Martina Franca male foals were involved in the trial. Foals naturally assumed colostrum within 4 h from birth. Afterwards, 10 foals were partially artificially suckled (AS), and 10 foals were naturally suckled (NS). All the foals were weaned at 180 d, then housed indoors and fed the same diet. Ten donkeys were slaughtered at 12 months and the other 10 at the age of 18 months. Samples of Longissimus thoracis et lumborum (LTL) were taken from each foal for chemical analysis, then rheological parameters, oxidative profile, colorimetric parameters and fatty acid profile were assessed. Older donkeys (18 months) fed with natural milk presented the highest intramuscular fat (IMF) and meat protein content. From a dietary view point, IMF acid composition showed a more favourable profile in meat from artificially-reared donkeys compared to naturallysuckled ones.
1. Introduction Donkeys (Equus asinus) have been used worldwide since ancient times as draught animals in agriculture and for transporting people (Polidori, Pucciarelli, Ariani, Polzonetti, & Vincenzetti, 2015). Mechanization has reduced this need, leading to lower numbers of domestic equid, which has even led some asinine and horse breeds to become endangered. However, some donkey and horse breeds have been repositioned for milk (Centoducati, Maggiolino, De Palo, & Tateo, 2012) and meat (De Palo, Maggiolino, Lestingi, & Tateo, 2009) production. Moreover, male foals on dairy farms are mainly set aside for meat production in order to increase profits. The introduction of artificial suckling techniques, even in dairy equid breeding, could raise milk production figures and reduce foal fasting times. Indeed, the traditional technique for donkey's milk production involves separating foals from their dams for not < 4 h before each milking session (De Palo, Maggiolino, Milella, Centoducati, Papaleo, Tateo, 2016a). During this separation, foals are forced to fast as they are unable to assume enough solid feed to satisfy their nutritional requirements, especially during the first weeks of life. The artificial suckling system could thus be a way of lengthening the separation of foals from their dams, thus increasing the hours dedicated to milking over the course of the day (De
⁎
Corresponding author. E-mail address: [email protected] (A. Maggiolino).
http://dx.doi.org/10.1016/j.meatsci.2017.07.025 Received 30 March 2017; Received in revised form 31 July 2017; Accepted 31 July 2017 Available online 02 August 2017 0309-1740/ © 2017 Elsevier Ltd. All rights reserved.
Palo, Maggiolino, Milella et al., 2016a). In addition, these authors revealed that artificial suckling positively affects growth performance in donkey foals, with higher weight gain in the first 6 months of life, and higher final live weight and carcass weight at 12 and 18 months old. Consumer's interest in animal products is influenced by the perception of a food's “healthiness” which, in the case of meat, is largely related to intramuscular fat (IMF) content, fatty acid profile and cholesterol content (McAfee et al., 2010). Thus, taking account of all the above, the aim of this study was to assess the effect of artificial suckling and slaughtering age on the physicochemical parameters, rheological characteristics and fatty acid profile of Martina Franca donkey meat obtained from foals slaughtered at 12 and 18 months of age. 2. Materials and methods 2.1. Animal treatment and sampling This study was approved by the Ethics Committee for animal testing–CESA (process number 58337-X/10). Twenty Martina Franca jennies and their male foals were randomly included in the trial. At birth, all foals naturally suckled colostrum from their dams. Afterwards, foals were randomly assigned to two experimental groups: 10 were
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Fig. 1. Maximum amount of daily available artificial milk and mean milk intake.
partially artificially suckled (AS), and 10 were naturally suckled (NS) (Fig. 1). From 0800 h to 2000 h, both groups were separated from their mothers in order to allow the milking procedures to take place; the foals were kept in two different stalls, identical in size, environmental and structural conditions, with ad libitum fresh water, foal starter feed (2% DM of live body weight) and oat hay (ad libitum) (Martin-Rosset, 1990) in creep feeding trough. The AS group was kept in a stall equipped with an automatic calf-suckling machine (Urban CalfMom, Urban Gmbh & Co. KG, Wüsting, Germany) equipped with two suckling stations. Each station was modified for the foals' dimensions and by replacing calf teats with others measuring 6 cm in length and 3 cm in maximum diameter, as described by Tateo, Maggiolino, Padalino, and Centoducati (2013a). During these hours, each group was fed with foal starter feed, hay and water, but the AS group also had access to milk replacer. Initially, the AS foals were encouraged to drink milk from a bottle containing milk replacer, offered to them near the feeding station. This was done until the foals started independently consuming milk from the feeding station. This occurred within the first 12 h. A commercial calf milk replacer was used (Table 1) added with calcium carbonate (0.3%) and lactose (6%) (Martin-Rosset, Vermorel, Doreau, Tisserand, & Andrieu, 1994) to modify cow's milk in order to create a chemical composition similar to natural donkey milk. Milk powder was
Table 2 Fatty acid composition of natural and artificial milk (expressed as % of total fatty acid methyl esters).
Table 1 Composition of starter, oat hay and milk replacer offered to donkeys.
DM Protein Fat Fibre Ash Neutral detergent fibre Acid detergent fibre Acid detergent lignin Horse forage units, n/kg of DM Digestible protein, g/kg Sodium Vitamin A Vitamin D3 Vitamin E Vitamin C Iron (iron (II) sulphate) Zinc (zinc sulphate) Manganese (manganese sulphate) Copper (copper (II) sulphate) Iodine (calcium iodate) Selenium (sodium selenate)
Starter
Oat hay
Milk replacera
86.5% 17.1% 5.76% 10.4% 6.8% 27.7% 13.4% 2.6% 0.85% 108.4% – – – – – – – – – – –
88.8 11.4 2.75 34.2 10.8 55.4 38.9 7.1 0.48 20.4 – – – – – – – – – – –
– 26% 22% 0.05% 6.5% – – – – – 0.7% 50,000 IU/kg 5000 IU/kg 100 mg/kg 100 mg/kg 80 mg/kg 70 mg/kg 55 mg/kg 8 mg/kg 1 mg/kg 0.25 mg/kg
Fatty acids
Natural milk
Artificial milk
C11:0 C12:0 C13:0 C14:0 C14:1 C15:0 C15:1 C16:0 C16:1 C17:0 C17:1 C18:0 C18:1 trans C18:1 n − 9 C18:2 n − 6 C18:3 n − 3 C20:0 C20:3 n − 3 C20:3 n − 6 C20:5 n − 3 C21:0 C22:1 SFAa MUFAb PUFAc
1.59 11.02 0.08 8.28 0.64 0.54 0.26 25.31 4.89 0.59 0.47 2.94 0.05 27.12 15.24 0.44 0.05 0.28 0.05 0.03 0.05 0.08 50.45 33.51 16.04
1.62 9.75 0.25 6.38 0.97 0.67 0.58 21.97 2.72 0.12 0.74 11.84 0.36 33.49 7.27 0.48 0.06 0.17 0.08 0.15 0.14 0.19 52.8 39.05 8.15
a b c
SFA: saturated fatty acids. MUFA: monounsaturated fatty acids. PUFA: polyunsaturated fatty acids.
automatically diluted in warm water at 40 °C to a concentration of 6%. The fatty acid profile was analyzed in triplicate by sampling both kinds of milk (donkey milk and milk replacer) used for suckling, on samples collected every 30 days, and it is reported in Table 2. The feeding machine operated continuously. Both NS and AS groups were weaned at 182 ± 7 days (26 ± 1 week) of life. The AS group had milk replacer available during the daytime when they were separated from their dams until 180 days of life, while the NS group only had water and solid feed at their disposal. Each foal in the AS group was equipped with a transponder fixed to a lightweight collar round its neck, which was used by the automatic suckling machine to recognize individual animals. The machine was settable both for suckling frequency and for total daily amount of milk replacer available per foal. The frequency for all animals and during the entire trial was set at 1 suckling bout per hour, so the recorded and programmed total amount of milk replacer per foal was equally subdivided into the 12 daytime suckling bouts. The maximum amount of
a Composition: cow milk serum protein concentrate, whey without lactose, sweet whey, coconut oil, palm oil, wheat protein concentrate, wheat flour.
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source D65; Minolta Camera Co. Ltd., Osaka, Japan). Reflectance measurements were collected from a 0° viewing angle with A-pulsed xenon arc lamp with a reading surface of 8 mm diameter. For each sample of meat, three measurements were performed at three different points. Three measurements were obtained at each point, performed by rotating the detector system by 90° compared to the previous one, giving a total of nine measurements per sample. The colorimeter was calibrated on the Hunter-lab colour space system using a white title (L* = 99.2, a* = 1.0, b* = 1.9). The a* and b* values were used to determine chroma = (a2 + b2)1/2 and hue (°) = tan− 1 (b/a) according to De Palo, Maggiolino, Centoducati, and Tateo (2012). The pH was recorded using a portable pH meter with glass electrode shaped to easily penetrate meat (Carlo Erba pH 710; Carlo Erba Reagenti, Milano, Italy). Before each measurement, the pH meter was automatically calibrated for muscle temperature and using solutions with 4 and 7 pH values (Crison, Lainate, Italy). The water holding capacity (WHC), cooking losses and Warner-Bratzler shear force (WBSF) were measured as described by De Palo, Tateo, Maggiolino, and Centoducati (2014).
milk replacer available was decreased with increasing foal age (Fig. 1): 12 L from 1 to 59 days of age, 9 L from 60 to 89 days, 7 L from 90 to 119 days, 4 L from 120 to 159 days, 2 L from 160 to 180 days. The foal diet satisfied nutritional requirements for weight gain, according to Martin-Rosset et al. (1994). Management and solid feeding of foals in the NS group were identical to those in the AS group. During the night (from 2000 h to 0800 h), foals from both experimental groups were kept with their dams. After weaning, they were housed indoors in two different stables of equal size, environmental and structural characteristics and received the same diet. The composition of the feed administered was the same for both experimental groups (Table 1). Ten donkeys were randomly chosen for slaughter at the age of 12 months (12 M), and the other 10 at 18 months (18 M). Foals were transported and slaughtered at a European Community-approved abattoir in compliance with European Community laws on Animal Welfare in transport (1/2005EC) and the European Community regulation on Animal Welfare for slaughter of commercial animals (1099/ 2009EC). Foals were transported approximately 20 km to the abattoir and the journey time was less than one hour. Foals were stunned (by captive bolt gun), exsanguinated and dressed following commercial dressing-out procedures at the abattoir. No electrical stimulation was used. Immediately after slaughter, carcasses were chilled at 4 °C in a chilling room for 24 h. Afterwards, samples of Longissimus thoracis et lumborum (LTL) muscle between the 13th and 18th thoracic vertebra (about 500 g of each sample) were taken for analysis. Milk samples from jennies were collected every 30 days and analyzed for FAME profile. Samples were transported at 4 °C to the laboratory and started to be analyzed within 2 h of sampling.
2.5. Fatty acid profile Fatty acid methyl esters (FAME) were prepared by transesterification, as described by De Palo, Maggiolino, Centoducati, and Tateo (2015), using methanol in the presence of 3% hydrochloric acid in methanol (vol/vol). Fatty acids were determined with a Trace GC Thermo Quest Gas Chromatograph (Thermo Electron, Rodano, Milan, Italy) equipped with a flame ionization detector after their esterification with methanol in the presence of 3% hydrochloric acid in methanol (vol/vol). The derivatives were separated on a capillary column (Supelco SP-2380 fused-silica column, 60 m length, 0.25 mm internal diameter, and 0.20 mm film thickness). Injector and detector temperatures were held at 260 °C. Column oven program temperatures were as follows: T1 = 80 °C hold 1 min; T2 = 150 °C ramp at 15 °C/ min, hold 2 min; T3 = 220 °C ramp at 5 °C/min, hold 2 min; T4 = 250 °C ramp at 15 °C/min, hold 5 min. The flow rate of the carrier gas (He) was set at 0.8 mL/min. Identifications of fatty acid methyl esters (FAME) were based on the retention times of reference compounds (Sigma-Aldrich, St. Louis, MO, USA) and mass spectrometry. Fatty acid composition was expressed as the percentage of total FAME (standard: SupelcoTM 37 Component FAME Mix, Catalog Number 47885-U). Nutritional implications were assessed by calculating the amount of saturated fatty acids (SFA), monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), n − 3 and n − 6 fatty acids, as well as the SFA/UFA and the n − 6/n − 3 ratios. Moreover, atherogenic and thrombogenic indices were calculated according to these formulas (Ulbricht & Southgate, 1991):
2.2. Chemical composition Moisture was determined in an oven at 105 °C until a constant weight was reached, protein content was measured according to ISO 937:1978 (ISO, 1978), IMF was determined according to ISO 1443:1973 (ISO, 1973) and ash was calculated using ISO 936:1998 (ISO, 1998). Each muscle was homogenized with a mixture of chloroform and methanol (1:2, vol/vol) solution for the extraction of total lipids from IMF (De Palo, Maggiolino, Centoducati, Milella, Calzaretti, Tateo, 2016b). 2.3. Thiobarbituric acid reactive substances, protein carbonyls and hydroperoxides Meat samples (2 g) were homogenized in 20 mL of 100 mM phosphate buffer (pH 7.0) for 2 min using a homogeniser. An aliquot of homogenate (1 mL) was transferred to a glass tube for the determination of thiobarbituric acid reactive substances (TBARS), and added with 0.05 mL of butylated hydroxytoluene (7.2% in ethanol) and with 1950 mL of TBA/trichloracetic acid (TCA)/HCl (0.375% TBA, 15% TCA, and 0.25 N HCl). The sample solution was shaken and then incubated at 90 °C for 15 min in a thermostatic bath. After this period, the samples were cooled down to room temperature (15–30 °C) and then centrifuged at 2000 ×g for 15 min. Supernatant absorbance at 531 nm was measured against a blank containing 2 mL of TBA/TCA/HCl solution in 1 mL of distilled water. The TBARS were calculated compared with a standard curve constructed with 1,1,3,3-tetramethoxypropane, and the concentration of lipid oxidation was expressed as milligrams of malondialdehyde (MDA) per kg of meat (Buege & Aust, 1978). Protein carbonyl concentration and hydroperoxides were calculated according to De Palo, Maggiolino, Centoducati, and Tateo (2013a).
Atherogenic index (AI) = (C12: 0 + 4 × C14: 0 + C16: 0) [ΣMUFA +ΣPUFA(n − 6)and (n − 3)]
Thrombogenic index (TI) = (C14: 0 + C16: 0 + C: 18) [0.5ΣMUFA + 0.5ΣPUFA(n − 6) + 3ΣPUFA(n − 3) + (n − 6) (n − 3)] 2.6. Statistical analysis The data set was subjected to analysis of variance (ANOVA) using the GLM by SAS software (SAS, 2001), according to the following model:
2.4. Colour evaluation, pH, water holding capacity, cooking loss, postthawing loss and Warner-Bratzler shear force
yijk = μ + Si + Aj + (S × A)ij + εijk where yijk represents all the meat qualitative patterns as dependent variables; μ is the overall mean; S is the effect of the ith suckling system (i = 1, 2), A is the effect of the jth age (j = 1, 2), S × A is the effect of
The surface meat colour was determined according to the CIE L*, a*, b* (CIE, 1976) colour system using a Minolta CR-300 colorimeter (light 130
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Table 3 Effect of the interaction between age at slaughter (12 and 18 months) and suckling system (artificial and natural) on chemical composition and rheological parameters in donkey Longissimus thoracis et lumborum (LTL) (mean and SEM). Parameters
AS1
NS2
12M3 Moisture (g/100 g) Protein (g/100 g) IMF5 (g/100 g) Ash (g/100 g) pH WBSF6 on raw meat (kg/cm2) WBSF on cooked meat (kg/cm2) Water Holding Capacity (%) Cooking loss (%) Post-thawing loss (%) Hydroperoxides (micromoles/g) Protein carbonyls (nmoles DNPH7/mg prot) TBARS8 (mg MDA9/kg) Acid hematin (ppm) L10 a⁎,11 b⁎,12 Chroma Hue
18M4 A
74.32 20.45 1.67A 1.09A 6.10A 4.31 5.29 85.69 41.60A 3.18 1.59 1.63 0.45 239.07 39.68Aa 16.05A -2.16A 15.40A 0.39Aa
Means within a row with different superscripts differ (A, B: P < 0.01; ns = non-significant (P > 0.05). ⁎ P < 0.05. ⁎⁎ P < 0.01. ⁎⁎⁎ P < 0.001. 1 AS: donkeys fed with artificial milk. 2 NS: donkeys fed with natural milk. 3 12M: donkeys slaughtered at 12 months. 4 18M: donkeys slaughtered at 18 months. 5 Intramuscular fat. 6 Warner Blatzer Shear Force. 7 2,4-Dinitrophenyl hydrazine. 8 Thiobarbituric acid reactive substances. 9 Malondialdehyde. 10 Lightness. 11 Redness. 12 Yellowness.
12 M A
74.72 19.54A 1.84A 1.26B 6.00A 3.60 5.30 87.04 40.64 3.11 1.65 1.40 0.46 243.25 38.50ac 16.88a − 0.71B 17.99A 0.41A a, b
SEM 18 M A
75.44 19.83A 1.13B 1.27B 6.43B 3.50a 5.60 85.87 41.35A 2.84 1.49 1.53 0.46 260.09 36.64bc 16.96a −1.47a 17.56a 0.43b
P-value Suckling
B
72.64 21.35B 1.94A 1.24 B 6.11A 4.97b 5.23 86.17 39.49B 2.21 1.66 1.47 0.48 256.15 35.95Bb 18.23Bb − 0.63Bb 20.81Bb 0.47B
0.40 0.31 0.12 0.03 0.08 1.51 1.82 0.45 0.49 0.42 0.03 0.05 0.01 6.54 0.71 0.36 0.22 1.16 0.01
ns ns ns ⁎ ⁎⁎
ns ns ns ns ns ns ns ns ns ⁎⁎⁎ ⁎⁎
ns
Age
Suckling × age
⁎⁎
⁎
ns ns ns ⁎⁎ ⁎
ns ns ⁎⁎
ns ns ns ns ns ns ⁎⁎ ⁎⁎⁎
⁎⁎ ⁎⁎ ⁎⁎
ns ns ns ns ns ns ns ns ns ns ⁎ ⁎⁎
ns
⁎⁎
⁎
⁎⁎
⁎⁎⁎
⁎
⁎⁎
: P < 0.05).
the interaction of the ith suckling system and jth age, and εijk is the error term. A Bonferroni's test was applied for post hoc comparison to evaluate the differences between means (SAS, 2001). All the data were expressed as least squares mean. Significance was set as P < 0.05.
donkeys was lower than 18 M foals of both suckling systems (P < 0.01). Moreover, b* values of NS 12 M were lower than NS 18 M (P < 0.05). Chroma values observed on meat of NS 18 M donkeys were higher than AS donkeys of both ages (P < 0.01) and NS 12 M showed higher Chroma values than AS 12 M foals (P < 0.05). Hue values observed on NS 18 M meat are higher than AS foals of both ages (P < 0.01). Moreover, Hue values of meat of NS 12 M donkeys were higher than AS 12 M foals (P < 0.05). The effect of the interaction between slaughter age and suckling system on donkey meat fatty acid profile is shown in Table 4. The suckling system affect fatty acid composition. Animals of AS 18 M group showed higher values of C13:0 and C14:1 and lower values of C14:0 than NS 12 M (P < 0.05). Foals of NS 12 M group showed the lowest C11:0 values (P < 0.05) and lower C20:3n3 values than AS 12 M foals (P < 0.05). The AS 12 M foals showed lower C16:0 (P < 0.01), higher C17:0, C18:1 trans (P < 0.01) and C20:0 (P < 0.05) values than NS animals of both ages investigated. Animals of NS 18 M group showed the highest values of C16:1 (P < 0.05); foals of AS 18 M group showed C18:0 values higher than 12 M foals of both suckling systems (P < 0.05). AS groups showed lower C18:1n − 9 and higher n6/n3 ratio (P < 0.01) than Ns groups. Moreover, foals of AS 12 M group showed the highest values of c18:2n − 6, C20:3n6, total PUFA and total n6 (P < 0.01), the lowest values of TI (P < 0.01) C18:3n − 3 (P < 0.05). Foals of NS 12 M group showed lower C21:0 than AS foals of both ages considered (P < 0.01); moreover foals of NS 18 M group showed lower C21:0 values than AS 12 M foals (P < 0.05). The total SFA were lower in animals slaughtered at 12 M of both
3. Results Table 3 shows the results of analysis of variance and post hoc test of the binary interaction between age at slaughter and suckling system on chemical, rheological, oxidative and colorimetric parameters. Animals from the NS group slaughtered at 18 M produced meat with the lowest (P < 0.01) moisture content and the higher (P < 0.01) protein level. Meat from donkeys slaughtered at 12 M from the NS group showed the lowest IMF content (P < 0.01). Moreover, AS 12 M donkeys showed the lowest values of ash concentration (P < 0.01). Meat from donkeys slaughtered at 12 M from the NS group revealed the highest (P < 0.01) pH values in their meat. Animals of NS group 12 M showed lower values of WBSF on raw meat than NS 18 M donkeys. Meat from NS 18 M donkeys showed lower values of cooking loss compared to 12 M donkeys of both suckling groups. Also colour parameters are influenced by suckling system, slaughter age and their binary interactions. AS 12 M donkeys showed higher lightness (L*) values than NS 18 M (P < 0.01) and NS 12 M (P < 0.05). Moreover, AS 18 M animals showed higher L* values than NS 18 M group (P < 0.05). Redness (a*) on meat of NS 18 M foals was higher than AS 12 M (P < 0.01), AS 18 M and NS 12 M donkeys (P < 0.05) Yellowness (b*) registered on meat of AS 12 M 131
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Table 4 Effect of the interaction between age at slaughter (12 and 18 months) and suckling system (artificial and natural) on fatty acid composition (expressed as percentage of the total fatty acid methyl esters) in donkey Longissimus thoracis et lumborum (LTL) (mean and SEM). Fatty acid
C11:0 C12:0 C13:0 C14:0 C14:1 C15:0 C15:1 C16:0 C16:1 C17:0 C17:1 C18:0 C18:1 trans C18:1n − 9 C18:2n − 6 C18:3n − 3 C20:0 C20:3n − 3 C20:3n − 6 C20:5n − 3 C21:0 C22:1 SFA5 MUFA6 PUFA7 n3 n6 n6/n3 SFA/MUFA SFA/PUFA SFA/UFA AI8 TI9
AS1
NS2
SEM
12M3
18M4
12 M
18 M
a
a
b
a
0.54 1.07 0.47 2.62 0.21 0.61 1.41 22.08A 2.72a 1.44A 0.35 11.14a 1.71A 21.88A 22.60A 2.83a 1.12a 0.27a 1.45A 0.17 1.98Aa 2.55 40.75a 32.48 27.29A 3.46 22.06A 5.81A 1.27 1.39 0.69 0.57 0.37A
0.54 0.87 0.62a 2.27a 0.30a 0.36 1.23 25.37 2.64a 1.08 0.50 15.53b 0.99 21.88A 16.61B 3.57b 0.52 0.17 0.68B 0.20 1.46A 2.27 48.63b 31.26 21.03B 3.57 17.29B 5.83A 1.61 2.50 0.94 0.68 0.64B
0.12 1.15 0.21b 3.31b 0.06b 0.38 0.98 26.08B 2.91a 0.34B 0.27 12.01a 0.21B 28.06B 15.36B 3.49b 0.28b 0.02b 0.43B 0.19 0.50Ba 1.88 43.40a 35.05 19.84B 3.50 15.80B 4.41B 1.37 2.37 0.83 0.70 0.60B
Means within a row with different superscripts differ (A, B: P < 0.01; ns = non-significant (P > 0.05). ⁎ P < 0.05. ⁎⁎ P < 0.01. ⁎⁎⁎ P < 0.001. 1 AS: donkeys fed with artificial milk. 2 NS: donkeys fed with natural milk. 3 12 M: donkeys slaughtered at 12 months. 4 18 M: donkeys slaughtered at 18 months. 5 SFA: saturated fatty acids. 6 MUFA: monounsaturated fatty acids. 7 PUFA: polyunsaturated fatty acids. 8 AI: atherogenic index. 9 TI: thrombogenic index.
a, b
P-value Suckling
0.58 0.62 0.37 2.92 0.26 0.41 1.45 27.13B 4.16b 0.66B 1.37 12.78 0.44B 26.40B 16.28B 3.97b 0.40b 0.16 0.59B 0.16 1.15b 2.23 46.88b 36.15 19.26B 4.17 16.81B 4.59B 1.41 2.27 0.89 0.70 0.61B
0.09 0.18 0.12 0.29 0.08 0.07 0.21 0.91 0.36 0.15 0.47 1.02 0.25 1.59 1.06 0.42 0.19 0.06 0.18 0.04 0.21 0.28 1.60 1.81 1.28 0.43 1.06 0.84 0.12 1.36 0.06 0.05 0.04
ns ns ns ⁎
ns ns ns ⁎⁎ ⁎ ⁎⁎⁎
ns ns ⁎⁎⁎ ⁎⁎
Age
Suckling × age
⁎
⁎
ns ns ns ns ns ns
ns ns ns ns ns ns ns ns ns ns ns ns ns
⁎
ns ns ns ⁎
ns ns
⁎⁎⁎
⁎⁎
⁎
⁎
⁎
ns ⁎⁎
ns ⁎⁎⁎
ns ns ns ⁎⁎
ns ⁎⁎⁎ ⁎⁎
ns ns ns ns ⁎⁎
ns ns ns ns ns ns ⁎
ns ns ns
⁎⁎⁎
ns ns ns ⁎
ns ⁎
ns ns ns ns ns
⁎⁎
⁎⁎⁎
ns ns ns ns
ns ns ns ns ns
⁎⁎
⁎⁎
⁎
: P < 0.05).
Considering their rusticity and low growth rate, donkeys tend to convert energy first into bone and muscular tissue, rather than into fat (De Palo, Maggiolino, Milella et al., 2016a), so an effect on IMF content is recordable only in older animals (18 M). Regarding the suckling system, donkeys from the AS group slaughtered at 12 M presented similar IMF content to older animals. This could be due to the higher energy intake in donkeys that assumed ad libitum milk replacer and so had more energy available to be converted into muscle and fat (De Palo, Maggiolino, Milella et al., 2016a). However, IMF concentrations observed are in line with what reported by other authors in horse meat (De Palo, Maggiolino, Centoducati, & Tateo, 2013b; Tateo, De Palo, Ceci, & Centoducati, 2008), although higher than what observed by Franco & Lorenzo, 2014). Colour is a very important parameter affecting consumer perception of quality, because it is often associated with freshness (Lorenzo, Pateiro, & Franco, 2013). The colorimetric pattern is affected by myoglobin concentration, its chemical state, lipid oxidative status, muscle structure and its biochemical processes, its pH and marbling (De Palo
suckling systems (P < 0.05).
4. Discussion Some researchers have shown that there is an inverse relationship between IMF concentration and the amount of water in meat (Smith, Harris, Haneklaus, & Savell, 2011). In particular, if fat remains constant, moisture tends to decline until the animal body reaches chemical maturity; otherwise, if IMF increases, there is a decrease in moisture. These trends can also be observed in our results, even though they are not particularly evident, probably due to equid tendency to deposit fat principally in the subcutaneous district, inducing few intramuscular changes (Tateo, De Palo, Maggiolino, & Centoducati, 2013b). In our study, although equids tend to deposit lipids in the subcutaneous district, older donkeys showed higher IMF content. This outcome is in agreement with data reported by other authors (Domínguez, Crecente, Borrajo, Agregán, & Lorenzo, 2015; Polidori et al., 2015) who found higher IMF content in older animals. 132
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Acknowledgements
et al., 2012; Polidori, Cavallucci, Beghelli, & Vincenzetti, 2009). Lightness is influenced by chemical composition and in particular by IMF and water content (Mancini & Hunt, 2005). The high IMF content observed in young AS donkeys could explain these results. On the other hand, a* values were significantly affected by slaughter age and suckling system. Older donkeys presented the highest a* values (16.50 vs. 17.55 for animals slaughtered at 12 and 18 months, respectively), whereas the lowest a* values were observed in artificially-suckled animals (16.46 vs. 17.59 for AS and NS animals, respectively). Myoglobin concentration increases during the first 2 years of life, and decreases over the following ten (Badiani & Manfredini, 1994). The colour of meat from animals slaughtered at 6 months is less red due to the low levels of haem iron; however, meat from animals slaughtered at 18 M was very rich in myoglobin and darker in colour. Other authors (Domínguez et al., 2015) did not observe significant differences in a* values between animals slaughtered at different ages. Finally, only yellowness was significantly (P < 0.001) affected by slaughter age, since the lowest values were observed in younger donkeys. Concerning FAME, our findings are in disagreement with data reported by Domínguez et al. (2015), who found no significant differences in C16:0, C18:0 and SFA content between meat from foals slaughtered at 8 and 11 months. In addition, Polidori et al. (2015) observed that meat from foals slaughtered at 12 months had higher C18:2 and lower C18:3 content than animals slaughtered at 8 months, although they found no statistically significant differences. The n − 6/ n − 3 fatty acid ratio is regarded as an important healthiness parameter and should not exceed 4 (Simopoulos, 2004). The excessive consumption of n − 6 PUFA and very high n − 6/n − 3 PUFA ratio are associated with severe pathogenesis, such as inflammatory and autoimmune diseases, cancer and cardiovascular illness (McAfee et al., 2010). In our study, the mean n − 6/n − 3 ratio values ranged from 4.41 to 5.83. These results are in agreement with data reported by Lanza, Landi, Scerra, Galofaro, and Pennisi (2009) who found values from 6.7 to 4.1 in horse foals slaughtered at 15 months. Besides, the AI and TI indexes were calculated in order to reveal the health effect that FAME could have from a dietetic point of view for consumers (Lorenzo, Fuciños, Purriños, & Franco, 2010; Lorenzo et al., 2014). Besides, similar values of both indices have previously been observed by other authors (Lorenzo et al., 2010) in horse meat. According to Lorenzo et al. (2014), donkey meat is considered “dietetic” due to its low IMF and favourable fatty acid profile, characterized by significant proportions of unsaturated fatty acid. From a human health point of view, meat from younger donkeys fed with commercial milk replacers proved more suitable due to their higher PUFA and lower SFA content, AI and TI indices. Artificial suckling seems to improve the fatty acid quality of twelve month old donkey meat, increasing PUFA concentration and reducing SFA content and TI, improving meat quality for human health and consumption.
The authors want to thank Prof. Antony Green for providing language help. Moreover, authors want to thank Dr. Samoilis, Dr. Cornacchia, Dr. ssa Calzaretti and Mr. Giacummo for their technical assistance. References Badiani, A., & Manfredini, M. (1994). La produzione della carne di cavallo. Zootecnica e Nutrizione Animale, 20, 5–43. Buege, J., & Aust, S. D. (1978). Microsomial lipid peroxidation. Methods in Enzymology, 52, 302–310. Centoducati, P., Maggiolino, A., De Palo, P., & Tateo, A. (2012). Application of Wood's model to lactation curve of Italian Heavy Draft horse mares. Journal of Dairy Science, 95, 5770–5775. CIE (1976). Colorimetry: Official recommendations of the International Commission on Illumination. Paris, France: Comisión Internationale del'Eclairage. De Palo, P., Maggiolino, A., Lestingi, A., & Tateo, A. (2009). Comparison between carcasses of artificially suckled I.H.D.H. (Italian Heavy Draught Horse) foals slaughtered at 6 months and traditional carcasses obtained by foals slaughtered at 11 and 18 months. Italian Journal of Animal Science, 8, 700–702. De Palo, P., Maggiolino, A., Centoducati, P., & Tateo, A. (2012). Colour changes in meat of foals as affected by slaughtering age and post-thawing time. Asian-Australasian Journal of Animal Sciences, 25, 1775–1779. De Palo, P., Maggiolino, A., Centoducati, P., & Tateo, A. (2013a). Effects of two different packaging materials on veal calf meat quality and shelf life. Journal of Animal Science, 91, 2920–2930. De Palo, P., Maggiolino, A., Centoducati, P., & Tateo, A. (2013b). Slaughtering age effect on carcass traits and meat quality of Italian heavy draught horse foals. AsianAustralasian Journal of Animal Sciences, 26, 1637–1643. De Palo, P., Tateo, A., Maggiolino, A., & Centoducati, P. (2014). Effect of nutritive level on carcass traits and meat quality of IHDH foals. Animal Science Journal, 85, 780–786. De Palo, P., Maggiolino, A., Centoducati, P., & Tateo, A. (2015). Effects of different milk replacers on carcass traits, meat quality, meat color and fatty acids profile of dairy goats. Small Ruminant Research, 131, 6–11. De Palo, P., Maggiolino, A., Milella, P., Centoducati, N., Papaleo, A., & Tateo, A. (2016a). Artificial suckling in Martina Franca donkey foals: Effect on in vivo performances and carcass composition. Tropical Animal Health and Production, 48, 167–173. De Palo, P., Maggiolino, A., Centoducati, P., Milella, P., Calzaretti, G., & Tateo, A. (2016b). Is meat quality from Longissimus lumborum samples correlated with other cuts in horse meat? Animal Science Journal, 87, 428–438. Domínguez, R., Crecente, S., Borrajo, P., Agregán, R., & Lorenzo, J. M. (2015). Effect of slaughter age on foal carcass traits and meat quality. Animal, 9, 1713–1720. Franco, D., & Lorenzo, J. M. (2014). Effect of muscle and intensity of finishing diet on meat quality of foals slaughtered at 15 months. Meat Science, 96, 327–334. ISO International Organization for Standardization (1973). Determination of total fat content. ISOR-1443–1973. International standards meat and meat products. Genève, Switzerland: International Organization for Standardization. ISO International Organization for Standardization (1978). Determination of nitrogen content. ISOR-937–1978. International standards meat and meat products. Genève, Switzerland: International Organization for Standardization. ISO International Organization for Standardization (1998). Determination of ash content. ISOR-936–1998. International standards meat and meat products. Genève, Switzerland: International Organization for Standardization. Lanza, M., Landi, C., Scerra, M., Galofaro, V., & Pennisi, P. (2009). Meat quality and intramuscular fatty acid composition of Sanfratellano and Haflinger foals. Meat Science, 81, 142–147. Lorenzo, J. M., Fuciños, C., Purriños, L., & Franco, D. (2010). Intramuscular fatty acid composition of “Galician Mountain” foals breed: Effect of sex, slaughtered age and livestock production system. Meat Science, 86, 825–831. Lorenzo, J. M., Pateiro, M., & Franco, D. (2013). Influence of muscle type on physicochemical and sensory properties of foal meat. Meat Science, 94, 77–83. Lorenzo, J. M., Sarries, M. V., Tateo, A., Polidori, P., Franco, D., & Lanza, M. (2014). Carcass characteristics, meat quality and nutritional value of horsemeat: A review. Meat Science, 96, 1478–1488. Mancini, R. A., & Hunt, M. C. (2005). Current research in meat colour. Meat Science, 71, 100–121. Martin-Rosset, W. (Ed.), (1990). L'alimentation des chevaux. Paris: INRA. Martin-Rosset, W., Vermorel, M., Doreau, M., Tisserand, J. L., & Andrieu, J. (1994). The French horse feed evaluation systems and recommended allowances for energy and protein. Livestock Production Science, 40, 37–56. McAfee, A. J., McSorley, E. M., Cuskelly, G. J., Moss, B. W., Wallace, J. M., Bonham, M. P., ... Fearon, A. M. (2010). Red meat consumption: An overview of the risks and benefits. Meat Science, 84, 1–13. Polidori, P., Cavallucci, C., Beghelli, D., & Vincenzetti, S. (2009). Physical and chemical characteristics of donkey meat from Martina Franca breed. Meat Science, 82, 469–471. Polidori, P., Pucciarelli, S., Ariani, A., Polzonetti, V., & Vincenzetti, S. (2015). A comparison of the carcass and meat quality of Martina Franca donkey foals aged 8 or 12 months. Meat Science, 106, 6–10. SAS (2001). Applied statistics and the SAS programming language. Cary, NC, USA: SAS Institute Inc.
5. Conclusions Breeding Martina Franca donkeys for milk and meat production is a consolidate practice in Italy. Our results show that artificially suckling system, as innovative technique, and slaughter age had an effect on physicochemical parameters, rheological properties and fatty acid profile of Martina Franca donkey meat. Older donkeys fed with natural milk presented the highest IMF and protein concentrations. Moreover, meat from naturally-suckled donkeys was darker and slightly redder than those from animals fed milk replacer. From a dietetic point of view, intramuscular fatty acid composition showed a more suitable profile in meat from artificially-suckled foals. The present study represents a first step to improve the knowledge about the influence of an innovative milk suckling technique on donkey meat quality.
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Tateo, A., Maggiolino, A., Padalino, B., & Centoducati, P. (2013a). Behavior of artificially suckled foals. Journal of Veterinary Behaviour, 8, 162–169. Tateo, A., De Palo, P., Maggiolino, A., & Centoducati, P. (2013b). Post-thawing colour changes in meat of foals as affected by feeding level and post-thawing time. Archiv fur Tierzucht, 56, 293–302. Ulbricht, T. L. V., & Southgate, D. A. T. (1991). Coronary heart disease: Seven dietary factors. Lancet, 338, 985–992.
Simopoulos, A. P. (2004). Omega-6/Omega-3 essential fatty acid ratio and chronic diseases. Food Reviews International, 20, 77–90. Smith, A. M., Harris, K. B., Haneklaus, A. N., & Savell, J. W. (2011). Proximate composition and energy content of beef steaks as influenced by USDA quality grade and degree of doneness. Meat Science, 89, 228–232. Tateo, A., De Palo, P., Ceci, E., & Centoducati, P. (2008). Physicochemical properties of meat of Italian Heavy Draft horses slaughtered at the age of eleven months. Journal of Animal Science, 86, 1205–1214.
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Martina Franca donkey meat quality: Influence of slaughter age and suckling technique
MARK
P. De Paloa, A. Tateoa, A. Maggiolinoa,⁎, R. Marinob, E. Cecia, A. Nisic, J.M. Lorenzod Department of Veterinary Medicine, University “Aldo Moro” of Bari, S.P. per Casamassima, km 3, 70010 Valenzano, BA, Italy Department of Agricultural Food and Environmental Sciences, University of Foggia, Via Napoli, 25-71121 Foggia, Italy c Free Lance DVM, Italy d Centro Tecnológico de la Carne de Galicia, rúa Galicia no 4, Parque Tecnológico de Galicia, San Cibrao das Viñas 32900, Ourense, Spain a
b
A R T I C L E I N F O
A B S T R A C T
Keywords: Donkey meat Artificial suckling Slaughter age Meat quality Rheological parameters
This work aimed to evaluate the effect of suckling technique and slaughter age on Martina Franca donkey meat quality. Twenty Martina Franca male foals were involved in the trial. Foals naturally assumed colostrum within 4 h from birth. Afterwards, 10 foals were partially artificially suckled (AS), and 10 foals were naturally suckled (NS). All the foals were weaned at 180 d, then housed indoors and fed the same diet. Ten donkeys were slaughtered at 12 months and the other 10 at the age of 18 months. Samples of Longissimus thoracis et lumborum (LTL) were taken from each foal for chemical analysis, then rheological parameters, oxidative profile, colorimetric parameters and fatty acid profile were assessed. Older donkeys (18 months) fed with natural milk presented the highest intramuscular fat (IMF) and meat protein content. From a dietary view point, IMF acid composition showed a more favourable profile in meat from artificially-reared donkeys compared to naturallysuckled ones.
1. Introduction Donkeys (Equus asinus) have been used worldwide since ancient times as draught animals in agriculture and for transporting people (Polidori, Pucciarelli, Ariani, Polzonetti, & Vincenzetti, 2015). Mechanization has reduced this need, leading to lower numbers of domestic equid, which has even led some asinine and horse breeds to become endangered. However, some donkey and horse breeds have been repositioned for milk (Centoducati, Maggiolino, De Palo, & Tateo, 2012) and meat (De Palo, Maggiolino, Lestingi, & Tateo, 2009) production. Moreover, male foals on dairy farms are mainly set aside for meat production in order to increase profits. The introduction of artificial suckling techniques, even in dairy equid breeding, could raise milk production figures and reduce foal fasting times. Indeed, the traditional technique for donkey's milk production involves separating foals from their dams for not < 4 h before each milking session (De Palo, Maggiolino, Milella, Centoducati, Papaleo, Tateo, 2016a). During this separation, foals are forced to fast as they are unable to assume enough solid feed to satisfy their nutritional requirements, especially during the first weeks of life. The artificial suckling system could thus be a way of lengthening the separation of foals from their dams, thus increasing the hours dedicated to milking over the course of the day (De
⁎
Corresponding author. E-mail address: [email protected] (A. Maggiolino).
http://dx.doi.org/10.1016/j.meatsci.2017.07.025 Received 30 March 2017; Received in revised form 31 July 2017; Accepted 31 July 2017 Available online 02 August 2017 0309-1740/ © 2017 Elsevier Ltd. All rights reserved.
Palo, Maggiolino, Milella et al., 2016a). In addition, these authors revealed that artificial suckling positively affects growth performance in donkey foals, with higher weight gain in the first 6 months of life, and higher final live weight and carcass weight at 12 and 18 months old. Consumer's interest in animal products is influenced by the perception of a food's “healthiness” which, in the case of meat, is largely related to intramuscular fat (IMF) content, fatty acid profile and cholesterol content (McAfee et al., 2010). Thus, taking account of all the above, the aim of this study was to assess the effect of artificial suckling and slaughtering age on the physicochemical parameters, rheological characteristics and fatty acid profile of Martina Franca donkey meat obtained from foals slaughtered at 12 and 18 months of age. 2. Materials and methods 2.1. Animal treatment and sampling This study was approved by the Ethics Committee for animal testing–CESA (process number 58337-X/10). Twenty Martina Franca jennies and their male foals were randomly included in the trial. At birth, all foals naturally suckled colostrum from their dams. Afterwards, foals were randomly assigned to two experimental groups: 10 were
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Fig. 1. Maximum amount of daily available artificial milk and mean milk intake.
partially artificially suckled (AS), and 10 were naturally suckled (NS) (Fig. 1). From 0800 h to 2000 h, both groups were separated from their mothers in order to allow the milking procedures to take place; the foals were kept in two different stalls, identical in size, environmental and structural conditions, with ad libitum fresh water, foal starter feed (2% DM of live body weight) and oat hay (ad libitum) (Martin-Rosset, 1990) in creep feeding trough. The AS group was kept in a stall equipped with an automatic calf-suckling machine (Urban CalfMom, Urban Gmbh & Co. KG, Wüsting, Germany) equipped with two suckling stations. Each station was modified for the foals' dimensions and by replacing calf teats with others measuring 6 cm in length and 3 cm in maximum diameter, as described by Tateo, Maggiolino, Padalino, and Centoducati (2013a). During these hours, each group was fed with foal starter feed, hay and water, but the AS group also had access to milk replacer. Initially, the AS foals were encouraged to drink milk from a bottle containing milk replacer, offered to them near the feeding station. This was done until the foals started independently consuming milk from the feeding station. This occurred within the first 12 h. A commercial calf milk replacer was used (Table 1) added with calcium carbonate (0.3%) and lactose (6%) (Martin-Rosset, Vermorel, Doreau, Tisserand, & Andrieu, 1994) to modify cow's milk in order to create a chemical composition similar to natural donkey milk. Milk powder was
Table 2 Fatty acid composition of natural and artificial milk (expressed as % of total fatty acid methyl esters).
Table 1 Composition of starter, oat hay and milk replacer offered to donkeys.
DM Protein Fat Fibre Ash Neutral detergent fibre Acid detergent fibre Acid detergent lignin Horse forage units, n/kg of DM Digestible protein, g/kg Sodium Vitamin A Vitamin D3 Vitamin E Vitamin C Iron (iron (II) sulphate) Zinc (zinc sulphate) Manganese (manganese sulphate) Copper (copper (II) sulphate) Iodine (calcium iodate) Selenium (sodium selenate)
Starter
Oat hay
Milk replacera
86.5% 17.1% 5.76% 10.4% 6.8% 27.7% 13.4% 2.6% 0.85% 108.4% – – – – – – – – – – –
88.8 11.4 2.75 34.2 10.8 55.4 38.9 7.1 0.48 20.4 – – – – – – – – – – –
– 26% 22% 0.05% 6.5% – – – – – 0.7% 50,000 IU/kg 5000 IU/kg 100 mg/kg 100 mg/kg 80 mg/kg 70 mg/kg 55 mg/kg 8 mg/kg 1 mg/kg 0.25 mg/kg
Fatty acids
Natural milk
Artificial milk
C11:0 C12:0 C13:0 C14:0 C14:1 C15:0 C15:1 C16:0 C16:1 C17:0 C17:1 C18:0 C18:1 trans C18:1 n − 9 C18:2 n − 6 C18:3 n − 3 C20:0 C20:3 n − 3 C20:3 n − 6 C20:5 n − 3 C21:0 C22:1 SFAa MUFAb PUFAc
1.59 11.02 0.08 8.28 0.64 0.54 0.26 25.31 4.89 0.59 0.47 2.94 0.05 27.12 15.24 0.44 0.05 0.28 0.05 0.03 0.05 0.08 50.45 33.51 16.04
1.62 9.75 0.25 6.38 0.97 0.67 0.58 21.97 2.72 0.12 0.74 11.84 0.36 33.49 7.27 0.48 0.06 0.17 0.08 0.15 0.14 0.19 52.8 39.05 8.15
a b c
SFA: saturated fatty acids. MUFA: monounsaturated fatty acids. PUFA: polyunsaturated fatty acids.
automatically diluted in warm water at 40 °C to a concentration of 6%. The fatty acid profile was analyzed in triplicate by sampling both kinds of milk (donkey milk and milk replacer) used for suckling, on samples collected every 30 days, and it is reported in Table 2. The feeding machine operated continuously. Both NS and AS groups were weaned at 182 ± 7 days (26 ± 1 week) of life. The AS group had milk replacer available during the daytime when they were separated from their dams until 180 days of life, while the NS group only had water and solid feed at their disposal. Each foal in the AS group was equipped with a transponder fixed to a lightweight collar round its neck, which was used by the automatic suckling machine to recognize individual animals. The machine was settable both for suckling frequency and for total daily amount of milk replacer available per foal. The frequency for all animals and during the entire trial was set at 1 suckling bout per hour, so the recorded and programmed total amount of milk replacer per foal was equally subdivided into the 12 daytime suckling bouts. The maximum amount of
a Composition: cow milk serum protein concentrate, whey without lactose, sweet whey, coconut oil, palm oil, wheat protein concentrate, wheat flour.
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source D65; Minolta Camera Co. Ltd., Osaka, Japan). Reflectance measurements were collected from a 0° viewing angle with A-pulsed xenon arc lamp with a reading surface of 8 mm diameter. For each sample of meat, three measurements were performed at three different points. Three measurements were obtained at each point, performed by rotating the detector system by 90° compared to the previous one, giving a total of nine measurements per sample. The colorimeter was calibrated on the Hunter-lab colour space system using a white title (L* = 99.2, a* = 1.0, b* = 1.9). The a* and b* values were used to determine chroma = (a2 + b2)1/2 and hue (°) = tan− 1 (b/a) according to De Palo, Maggiolino, Centoducati, and Tateo (2012). The pH was recorded using a portable pH meter with glass electrode shaped to easily penetrate meat (Carlo Erba pH 710; Carlo Erba Reagenti, Milano, Italy). Before each measurement, the pH meter was automatically calibrated for muscle temperature and using solutions with 4 and 7 pH values (Crison, Lainate, Italy). The water holding capacity (WHC), cooking losses and Warner-Bratzler shear force (WBSF) were measured as described by De Palo, Tateo, Maggiolino, and Centoducati (2014).
milk replacer available was decreased with increasing foal age (Fig. 1): 12 L from 1 to 59 days of age, 9 L from 60 to 89 days, 7 L from 90 to 119 days, 4 L from 120 to 159 days, 2 L from 160 to 180 days. The foal diet satisfied nutritional requirements for weight gain, according to Martin-Rosset et al. (1994). Management and solid feeding of foals in the NS group were identical to those in the AS group. During the night (from 2000 h to 0800 h), foals from both experimental groups were kept with their dams. After weaning, they were housed indoors in two different stables of equal size, environmental and structural characteristics and received the same diet. The composition of the feed administered was the same for both experimental groups (Table 1). Ten donkeys were randomly chosen for slaughter at the age of 12 months (12 M), and the other 10 at 18 months (18 M). Foals were transported and slaughtered at a European Community-approved abattoir in compliance with European Community laws on Animal Welfare in transport (1/2005EC) and the European Community regulation on Animal Welfare for slaughter of commercial animals (1099/ 2009EC). Foals were transported approximately 20 km to the abattoir and the journey time was less than one hour. Foals were stunned (by captive bolt gun), exsanguinated and dressed following commercial dressing-out procedures at the abattoir. No electrical stimulation was used. Immediately after slaughter, carcasses were chilled at 4 °C in a chilling room for 24 h. Afterwards, samples of Longissimus thoracis et lumborum (LTL) muscle between the 13th and 18th thoracic vertebra (about 500 g of each sample) were taken for analysis. Milk samples from jennies were collected every 30 days and analyzed for FAME profile. Samples were transported at 4 °C to the laboratory and started to be analyzed within 2 h of sampling.
2.5. Fatty acid profile Fatty acid methyl esters (FAME) were prepared by transesterification, as described by De Palo, Maggiolino, Centoducati, and Tateo (2015), using methanol in the presence of 3% hydrochloric acid in methanol (vol/vol). Fatty acids were determined with a Trace GC Thermo Quest Gas Chromatograph (Thermo Electron, Rodano, Milan, Italy) equipped with a flame ionization detector after their esterification with methanol in the presence of 3% hydrochloric acid in methanol (vol/vol). The derivatives were separated on a capillary column (Supelco SP-2380 fused-silica column, 60 m length, 0.25 mm internal diameter, and 0.20 mm film thickness). Injector and detector temperatures were held at 260 °C. Column oven program temperatures were as follows: T1 = 80 °C hold 1 min; T2 = 150 °C ramp at 15 °C/ min, hold 2 min; T3 = 220 °C ramp at 5 °C/min, hold 2 min; T4 = 250 °C ramp at 15 °C/min, hold 5 min. The flow rate of the carrier gas (He) was set at 0.8 mL/min. Identifications of fatty acid methyl esters (FAME) were based on the retention times of reference compounds (Sigma-Aldrich, St. Louis, MO, USA) and mass spectrometry. Fatty acid composition was expressed as the percentage of total FAME (standard: SupelcoTM 37 Component FAME Mix, Catalog Number 47885-U). Nutritional implications were assessed by calculating the amount of saturated fatty acids (SFA), monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), n − 3 and n − 6 fatty acids, as well as the SFA/UFA and the n − 6/n − 3 ratios. Moreover, atherogenic and thrombogenic indices were calculated according to these formulas (Ulbricht & Southgate, 1991):
2.2. Chemical composition Moisture was determined in an oven at 105 °C until a constant weight was reached, protein content was measured according to ISO 937:1978 (ISO, 1978), IMF was determined according to ISO 1443:1973 (ISO, 1973) and ash was calculated using ISO 936:1998 (ISO, 1998). Each muscle was homogenized with a mixture of chloroform and methanol (1:2, vol/vol) solution for the extraction of total lipids from IMF (De Palo, Maggiolino, Centoducati, Milella, Calzaretti, Tateo, 2016b). 2.3. Thiobarbituric acid reactive substances, protein carbonyls and hydroperoxides Meat samples (2 g) were homogenized in 20 mL of 100 mM phosphate buffer (pH 7.0) for 2 min using a homogeniser. An aliquot of homogenate (1 mL) was transferred to a glass tube for the determination of thiobarbituric acid reactive substances (TBARS), and added with 0.05 mL of butylated hydroxytoluene (7.2% in ethanol) and with 1950 mL of TBA/trichloracetic acid (TCA)/HCl (0.375% TBA, 15% TCA, and 0.25 N HCl). The sample solution was shaken and then incubated at 90 °C for 15 min in a thermostatic bath. After this period, the samples were cooled down to room temperature (15–30 °C) and then centrifuged at 2000 ×g for 15 min. Supernatant absorbance at 531 nm was measured against a blank containing 2 mL of TBA/TCA/HCl solution in 1 mL of distilled water. The TBARS were calculated compared with a standard curve constructed with 1,1,3,3-tetramethoxypropane, and the concentration of lipid oxidation was expressed as milligrams of malondialdehyde (MDA) per kg of meat (Buege & Aust, 1978). Protein carbonyl concentration and hydroperoxides were calculated according to De Palo, Maggiolino, Centoducati, and Tateo (2013a).
Atherogenic index (AI) = (C12: 0 + 4 × C14: 0 + C16: 0) [ΣMUFA +ΣPUFA(n − 6)and (n − 3)]
Thrombogenic index (TI) = (C14: 0 + C16: 0 + C: 18) [0.5ΣMUFA + 0.5ΣPUFA(n − 6) + 3ΣPUFA(n − 3) + (n − 6) (n − 3)] 2.6. Statistical analysis The data set was subjected to analysis of variance (ANOVA) using the GLM by SAS software (SAS, 2001), according to the following model:
2.4. Colour evaluation, pH, water holding capacity, cooking loss, postthawing loss and Warner-Bratzler shear force
yijk = μ + Si + Aj + (S × A)ij + εijk where yijk represents all the meat qualitative patterns as dependent variables; μ is the overall mean; S is the effect of the ith suckling system (i = 1, 2), A is the effect of the jth age (j = 1, 2), S × A is the effect of
The surface meat colour was determined according to the CIE L*, a*, b* (CIE, 1976) colour system using a Minolta CR-300 colorimeter (light 130
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Table 3 Effect of the interaction between age at slaughter (12 and 18 months) and suckling system (artificial and natural) on chemical composition and rheological parameters in donkey Longissimus thoracis et lumborum (LTL) (mean and SEM). Parameters
AS1
NS2
12M3 Moisture (g/100 g) Protein (g/100 g) IMF5 (g/100 g) Ash (g/100 g) pH WBSF6 on raw meat (kg/cm2) WBSF on cooked meat (kg/cm2) Water Holding Capacity (%) Cooking loss (%) Post-thawing loss (%) Hydroperoxides (micromoles/g) Protein carbonyls (nmoles DNPH7/mg prot) TBARS8 (mg MDA9/kg) Acid hematin (ppm) L10 a⁎,11 b⁎,12 Chroma Hue
18M4 A
74.32 20.45 1.67A 1.09A 6.10A 4.31 5.29 85.69 41.60A 3.18 1.59 1.63 0.45 239.07 39.68Aa 16.05A -2.16A 15.40A 0.39Aa
Means within a row with different superscripts differ (A, B: P < 0.01; ns = non-significant (P > 0.05). ⁎ P < 0.05. ⁎⁎ P < 0.01. ⁎⁎⁎ P < 0.001. 1 AS: donkeys fed with artificial milk. 2 NS: donkeys fed with natural milk. 3 12M: donkeys slaughtered at 12 months. 4 18M: donkeys slaughtered at 18 months. 5 Intramuscular fat. 6 Warner Blatzer Shear Force. 7 2,4-Dinitrophenyl hydrazine. 8 Thiobarbituric acid reactive substances. 9 Malondialdehyde. 10 Lightness. 11 Redness. 12 Yellowness.
12 M A
74.72 19.54A 1.84A 1.26B 6.00A 3.60 5.30 87.04 40.64 3.11 1.65 1.40 0.46 243.25 38.50ac 16.88a − 0.71B 17.99A 0.41A a, b
SEM 18 M A
75.44 19.83A 1.13B 1.27B 6.43B 3.50a 5.60 85.87 41.35A 2.84 1.49 1.53 0.46 260.09 36.64bc 16.96a −1.47a 17.56a 0.43b
P-value Suckling
B
72.64 21.35B 1.94A 1.24 B 6.11A 4.97b 5.23 86.17 39.49B 2.21 1.66 1.47 0.48 256.15 35.95Bb 18.23Bb − 0.63Bb 20.81Bb 0.47B
0.40 0.31 0.12 0.03 0.08 1.51 1.82 0.45 0.49 0.42 0.03 0.05 0.01 6.54 0.71 0.36 0.22 1.16 0.01
ns ns ns ⁎ ⁎⁎
ns ns ns ns ns ns ns ns ns ⁎⁎⁎ ⁎⁎
ns
Age
Suckling × age
⁎⁎
⁎
ns ns ns ⁎⁎ ⁎
ns ns ⁎⁎
ns ns ns ns ns ns ⁎⁎ ⁎⁎⁎
⁎⁎ ⁎⁎ ⁎⁎
ns ns ns ns ns ns ns ns ns ns ⁎ ⁎⁎
ns
⁎⁎
⁎
⁎⁎
⁎⁎⁎
⁎
⁎⁎
: P < 0.05).
the interaction of the ith suckling system and jth age, and εijk is the error term. A Bonferroni's test was applied for post hoc comparison to evaluate the differences between means (SAS, 2001). All the data were expressed as least squares mean. Significance was set as P < 0.05.
donkeys was lower than 18 M foals of both suckling systems (P < 0.01). Moreover, b* values of NS 12 M were lower than NS 18 M (P < 0.05). Chroma values observed on meat of NS 18 M donkeys were higher than AS donkeys of both ages (P < 0.01) and NS 12 M showed higher Chroma values than AS 12 M foals (P < 0.05). Hue values observed on NS 18 M meat are higher than AS foals of both ages (P < 0.01). Moreover, Hue values of meat of NS 12 M donkeys were higher than AS 12 M foals (P < 0.05). The effect of the interaction between slaughter age and suckling system on donkey meat fatty acid profile is shown in Table 4. The suckling system affect fatty acid composition. Animals of AS 18 M group showed higher values of C13:0 and C14:1 and lower values of C14:0 than NS 12 M (P < 0.05). Foals of NS 12 M group showed the lowest C11:0 values (P < 0.05) and lower C20:3n3 values than AS 12 M foals (P < 0.05). The AS 12 M foals showed lower C16:0 (P < 0.01), higher C17:0, C18:1 trans (P < 0.01) and C20:0 (P < 0.05) values than NS animals of both ages investigated. Animals of NS 18 M group showed the highest values of C16:1 (P < 0.05); foals of AS 18 M group showed C18:0 values higher than 12 M foals of both suckling systems (P < 0.05). AS groups showed lower C18:1n − 9 and higher n6/n3 ratio (P < 0.01) than Ns groups. Moreover, foals of AS 12 M group showed the highest values of c18:2n − 6, C20:3n6, total PUFA and total n6 (P < 0.01), the lowest values of TI (P < 0.01) C18:3n − 3 (P < 0.05). Foals of NS 12 M group showed lower C21:0 than AS foals of both ages considered (P < 0.01); moreover foals of NS 18 M group showed lower C21:0 values than AS 12 M foals (P < 0.05). The total SFA were lower in animals slaughtered at 12 M of both
3. Results Table 3 shows the results of analysis of variance and post hoc test of the binary interaction between age at slaughter and suckling system on chemical, rheological, oxidative and colorimetric parameters. Animals from the NS group slaughtered at 18 M produced meat with the lowest (P < 0.01) moisture content and the higher (P < 0.01) protein level. Meat from donkeys slaughtered at 12 M from the NS group showed the lowest IMF content (P < 0.01). Moreover, AS 12 M donkeys showed the lowest values of ash concentration (P < 0.01). Meat from donkeys slaughtered at 12 M from the NS group revealed the highest (P < 0.01) pH values in their meat. Animals of NS group 12 M showed lower values of WBSF on raw meat than NS 18 M donkeys. Meat from NS 18 M donkeys showed lower values of cooking loss compared to 12 M donkeys of both suckling groups. Also colour parameters are influenced by suckling system, slaughter age and their binary interactions. AS 12 M donkeys showed higher lightness (L*) values than NS 18 M (P < 0.01) and NS 12 M (P < 0.05). Moreover, AS 18 M animals showed higher L* values than NS 18 M group (P < 0.05). Redness (a*) on meat of NS 18 M foals was higher than AS 12 M (P < 0.01), AS 18 M and NS 12 M donkeys (P < 0.05) Yellowness (b*) registered on meat of AS 12 M 131
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Table 4 Effect of the interaction between age at slaughter (12 and 18 months) and suckling system (artificial and natural) on fatty acid composition (expressed as percentage of the total fatty acid methyl esters) in donkey Longissimus thoracis et lumborum (LTL) (mean and SEM). Fatty acid
C11:0 C12:0 C13:0 C14:0 C14:1 C15:0 C15:1 C16:0 C16:1 C17:0 C17:1 C18:0 C18:1 trans C18:1n − 9 C18:2n − 6 C18:3n − 3 C20:0 C20:3n − 3 C20:3n − 6 C20:5n − 3 C21:0 C22:1 SFA5 MUFA6 PUFA7 n3 n6 n6/n3 SFA/MUFA SFA/PUFA SFA/UFA AI8 TI9
AS1
NS2
SEM
12M3
18M4
12 M
18 M
a
a
b
a
0.54 1.07 0.47 2.62 0.21 0.61 1.41 22.08A 2.72a 1.44A 0.35 11.14a 1.71A 21.88A 22.60A 2.83a 1.12a 0.27a 1.45A 0.17 1.98Aa 2.55 40.75a 32.48 27.29A 3.46 22.06A 5.81A 1.27 1.39 0.69 0.57 0.37A
0.54 0.87 0.62a 2.27a 0.30a 0.36 1.23 25.37 2.64a 1.08 0.50 15.53b 0.99 21.88A 16.61B 3.57b 0.52 0.17 0.68B 0.20 1.46A 2.27 48.63b 31.26 21.03B 3.57 17.29B 5.83A 1.61 2.50 0.94 0.68 0.64B
0.12 1.15 0.21b 3.31b 0.06b 0.38 0.98 26.08B 2.91a 0.34B 0.27 12.01a 0.21B 28.06B 15.36B 3.49b 0.28b 0.02b 0.43B 0.19 0.50Ba 1.88 43.40a 35.05 19.84B 3.50 15.80B 4.41B 1.37 2.37 0.83 0.70 0.60B
Means within a row with different superscripts differ (A, B: P < 0.01; ns = non-significant (P > 0.05). ⁎ P < 0.05. ⁎⁎ P < 0.01. ⁎⁎⁎ P < 0.001. 1 AS: donkeys fed with artificial milk. 2 NS: donkeys fed with natural milk. 3 12 M: donkeys slaughtered at 12 months. 4 18 M: donkeys slaughtered at 18 months. 5 SFA: saturated fatty acids. 6 MUFA: monounsaturated fatty acids. 7 PUFA: polyunsaturated fatty acids. 8 AI: atherogenic index. 9 TI: thrombogenic index.
a, b
P-value Suckling
0.58 0.62 0.37 2.92 0.26 0.41 1.45 27.13B 4.16b 0.66B 1.37 12.78 0.44B 26.40B 16.28B 3.97b 0.40b 0.16 0.59B 0.16 1.15b 2.23 46.88b 36.15 19.26B 4.17 16.81B 4.59B 1.41 2.27 0.89 0.70 0.61B
0.09 0.18 0.12 0.29 0.08 0.07 0.21 0.91 0.36 0.15 0.47 1.02 0.25 1.59 1.06 0.42 0.19 0.06 0.18 0.04 0.21 0.28 1.60 1.81 1.28 0.43 1.06 0.84 0.12 1.36 0.06 0.05 0.04
ns ns ns ⁎
ns ns ns ⁎⁎ ⁎ ⁎⁎⁎
ns ns ⁎⁎⁎ ⁎⁎
Age
Suckling × age
⁎
⁎
ns ns ns ns ns ns
ns ns ns ns ns ns ns ns ns ns ns ns ns
⁎
ns ns ns ⁎
ns ns
⁎⁎⁎
⁎⁎
⁎
⁎
⁎
ns ⁎⁎
ns ⁎⁎⁎
ns ns ns ⁎⁎
ns ⁎⁎⁎ ⁎⁎
ns ns ns ns ⁎⁎
ns ns ns ns ns ns ⁎
ns ns ns
⁎⁎⁎
ns ns ns ⁎
ns ⁎
ns ns ns ns ns
⁎⁎
⁎⁎⁎
ns ns ns ns
ns ns ns ns ns
⁎⁎
⁎⁎
⁎
: P < 0.05).
Considering their rusticity and low growth rate, donkeys tend to convert energy first into bone and muscular tissue, rather than into fat (De Palo, Maggiolino, Milella et al., 2016a), so an effect on IMF content is recordable only in older animals (18 M). Regarding the suckling system, donkeys from the AS group slaughtered at 12 M presented similar IMF content to older animals. This could be due to the higher energy intake in donkeys that assumed ad libitum milk replacer and so had more energy available to be converted into muscle and fat (De Palo, Maggiolino, Milella et al., 2016a). However, IMF concentrations observed are in line with what reported by other authors in horse meat (De Palo, Maggiolino, Centoducati, & Tateo, 2013b; Tateo, De Palo, Ceci, & Centoducati, 2008), although higher than what observed by Franco & Lorenzo, 2014). Colour is a very important parameter affecting consumer perception of quality, because it is often associated with freshness (Lorenzo, Pateiro, & Franco, 2013). The colorimetric pattern is affected by myoglobin concentration, its chemical state, lipid oxidative status, muscle structure and its biochemical processes, its pH and marbling (De Palo
suckling systems (P < 0.05).
4. Discussion Some researchers have shown that there is an inverse relationship between IMF concentration and the amount of water in meat (Smith, Harris, Haneklaus, & Savell, 2011). In particular, if fat remains constant, moisture tends to decline until the animal body reaches chemical maturity; otherwise, if IMF increases, there is a decrease in moisture. These trends can also be observed in our results, even though they are not particularly evident, probably due to equid tendency to deposit fat principally in the subcutaneous district, inducing few intramuscular changes (Tateo, De Palo, Maggiolino, & Centoducati, 2013b). In our study, although equids tend to deposit lipids in the subcutaneous district, older donkeys showed higher IMF content. This outcome is in agreement with data reported by other authors (Domínguez, Crecente, Borrajo, Agregán, & Lorenzo, 2015; Polidori et al., 2015) who found higher IMF content in older animals. 132
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Acknowledgements
et al., 2012; Polidori, Cavallucci, Beghelli, & Vincenzetti, 2009). Lightness is influenced by chemical composition and in particular by IMF and water content (Mancini & Hunt, 2005). The high IMF content observed in young AS donkeys could explain these results. On the other hand, a* values were significantly affected by slaughter age and suckling system. Older donkeys presented the highest a* values (16.50 vs. 17.55 for animals slaughtered at 12 and 18 months, respectively), whereas the lowest a* values were observed in artificially-suckled animals (16.46 vs. 17.59 for AS and NS animals, respectively). Myoglobin concentration increases during the first 2 years of life, and decreases over the following ten (Badiani & Manfredini, 1994). The colour of meat from animals slaughtered at 6 months is less red due to the low levels of haem iron; however, meat from animals slaughtered at 18 M was very rich in myoglobin and darker in colour. Other authors (Domínguez et al., 2015) did not observe significant differences in a* values between animals slaughtered at different ages. Finally, only yellowness was significantly (P < 0.001) affected by slaughter age, since the lowest values were observed in younger donkeys. Concerning FAME, our findings are in disagreement with data reported by Domínguez et al. (2015), who found no significant differences in C16:0, C18:0 and SFA content between meat from foals slaughtered at 8 and 11 months. In addition, Polidori et al. (2015) observed that meat from foals slaughtered at 12 months had higher C18:2 and lower C18:3 content than animals slaughtered at 8 months, although they found no statistically significant differences. The n − 6/ n − 3 fatty acid ratio is regarded as an important healthiness parameter and should not exceed 4 (Simopoulos, 2004). The excessive consumption of n − 6 PUFA and very high n − 6/n − 3 PUFA ratio are associated with severe pathogenesis, such as inflammatory and autoimmune diseases, cancer and cardiovascular illness (McAfee et al., 2010). In our study, the mean n − 6/n − 3 ratio values ranged from 4.41 to 5.83. These results are in agreement with data reported by Lanza, Landi, Scerra, Galofaro, and Pennisi (2009) who found values from 6.7 to 4.1 in horse foals slaughtered at 15 months. Besides, the AI and TI indexes were calculated in order to reveal the health effect that FAME could have from a dietetic point of view for consumers (Lorenzo, Fuciños, Purriños, & Franco, 2010; Lorenzo et al., 2014). Besides, similar values of both indices have previously been observed by other authors (Lorenzo et al., 2010) in horse meat. According to Lorenzo et al. (2014), donkey meat is considered “dietetic” due to its low IMF and favourable fatty acid profile, characterized by significant proportions of unsaturated fatty acid. From a human health point of view, meat from younger donkeys fed with commercial milk replacers proved more suitable due to their higher PUFA and lower SFA content, AI and TI indices. Artificial suckling seems to improve the fatty acid quality of twelve month old donkey meat, increasing PUFA concentration and reducing SFA content and TI, improving meat quality for human health and consumption.
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5. Conclusions Breeding Martina Franca donkeys for milk and meat production is a consolidate practice in Italy. Our results show that artificially suckling system, as innovative technique, and slaughter age had an effect on physicochemical parameters, rheological properties and fatty acid profile of Martina Franca donkey meat. Older donkeys fed with natural milk presented the highest IMF and protein concentrations. Moreover, meat from naturally-suckled donkeys was darker and slightly redder than those from animals fed milk replacer. From a dietetic point of view, intramuscular fatty acid composition showed a more suitable profile in meat from artificially-suckled foals. The present study represents a first step to improve the knowledge about the influence of an innovative milk suckling technique on donkey meat quality.
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