Comparison of Carcass Traits,Meat Quality,and Chemical Composition of Tissues from Progeny Derived from Cloned and Noncloned Pigs

Abstract

Systematic studies of progeny derived from somatic cell nuclear transferred animals in their biophysical and biochemical characters are critical in assessing the safety of this kind of food. In this study, we compared the carcass traits and meat quality of 12 cloned and noncloned pigs, respectively, and chemical composition of tissues of 6 cloned and noncloned pigs, respectively. The carcass trait parameters, including body weight, carcass straight length, loin-eye area, backfat thickness at 10th and 11th interface, and rib number, were tested, and carcass yield was calculated. Meat quality parameters, such as meat color, marbling, temperatures, conductivity, and drip loss, were also tested. Finally, the gross chemical properties and the constitutions of fat acids, amino acids, and minerals in loin-eye muscle, omental fat, and liver from the two groups were tested. The results showed that the value for most parameters of these two groups was equivalent. In conclusion, these data indicated that the progeny of cloned pig were not different in the carcass traits, meat composition, and biochemical composition of tissues compared to the conventionally bred pigs, which further indicated the safety of products from cloned pigs.

Introduction

Somatic cell nuclear transfer (SCNT, clone) is a useful technique that can multiply elite animals faster and simpler than traditional breeding (Galli et al., 2012). Although the first cloned animal, namely dolly the sheep, was produced by this technique two decades ago (Wilmut et al., 1997), SCNT technique was still limited to therapeutic and basic research (Niemann and Lucas-Hahn, 2012), without widely used in animals producing. The U.S. Food and Drug Administration has concluded that meat and milk derived from clones of any species traditionally consumed as food are as safe to eat as food conventionally bred animals, which is supported by the risk assessment issued in December 2006, latest updated date on August 10, 2018 (https://www.fda.gov/ForConsumers/Consumer-Updates/ucm148768.htm).

Studies in cattle were in line with this conclusion, as the milk and meat produced by cloned cattle showed no significant difference in terms of their biochemical biophysical characters and the feeding biosafety with the conventionally bred cattle (Tian et al., 2005; Watanabe, 2013; Yang et al., 2007, 2011). However, a 2-year survey worldwide found that most countries have not approved meat and milk produced by cloned animals, but their progeny are entering the food supply (Hur, 2017). As a result, study in this field is in an urgent need to provide useful information and help acquiring understanding about the SCNT derived animal products for their safety concern.

Therefore, we carried out investigation in whether the carcass traits, the biological and biochemical characters of meat, and internal organs of progeny from SCNT derived pigs are safe and equivalent to the individuals of conventionally bred pigs.

The previous studies seem to contradict each other. On one hand, some malformation occurred more frequently in cloned animals, such as disorder of sex development and defects in the digestive, circulatory, reproductive, and musculoskeletal systems (Hill, 2014; Schmidt et al., 2015), which resulted in higher death rate in cloned animals. However, the higher death loss within 200 days of birth eliminated progeny that acquired congenital defects in cloned animals, so the survived ones were as healthy as the conventionally bred animals (Watanabe, 2013). Moreover, as mentioned above, several studies in cattle demonstrated that the products from cloned animals were safe and showed no difference in biophysical or biochemical characters with the noncloned animals (Tian et al., 2005; Yamaguchi et al., 2008; Yang et al., 2011).

On the other hand, some studies showed that there were significant differences between them, in terms of neutrophil counts, biochemical plasma concentration, and also the lipid metabolism in milk and muscles (Heyman et al., 2007).

In this study, we provided data on more than 20 parameters for carcass traits and more than 40 parameters for meat components and chemical constitution to compare the composition of meat and physical status of progeny of cloned and conventional reproduced pigs. Our results provided the first systematic data in comparing the carcass trait and the meat performance and chemical components of loin-eye muscle, omental fat, and liver from the progeny derived from SCNT pigs and conventional bred pigs.

Materials and Methods

Ethics statement

All research on animal was carried out in compliance with “The instructive Notions with Respect to Caring for Laboratory Animals,” issued by the Ministry of Science and Technology of China. All animals used in this study were reared and euthanized with the approval of the Institutional Animal Care and Use Committee of South China Agricultural University (Gu et al., 2019).

Animals

Twelve progeny of conventionally bred pigs were produced by artificial insemination (AI), and twelve cloned progeny were also produced by AI but with the semen from the cloned boars (Ao et al., 2019). Both group of pigs were raised under the same condition and received same diet formula.

Carcass trait measurements

Pigs were slaughtered at 6 months when they reached ∼110 kg by exsanguination after electrical stunning in an experimental slaughterhouse. The carcass traits were measured according to the protocol described by the Chinese technical regulation for testing carcass traits in lean-type pig (China MoAotPsRo, 2014).

Generally, hot carcass weight (the weight, including the head, kidneys, omental fat, and feet) was recorded after evisceration, so that the carcass yield can be calculated by hot carcass weight/preslaughter weight × 100%. The other carcass traits were tested, including carcass straight length (measured as the distance from the anterior edge of the first cervical vertebra to the anterior edge of the pubis), carcass sloping length (measured as the distance from the anterior edge of the first thoracic vertebra to the anterior edge of the pubis), loin-eye area (measured by tracing the outline of longissimus dorsi muscle at the 10th rib onto a transparent paper, and then the area within the outline was calculated by a planimeter), backfat thickness at the 10th and 11th rib interface, and rib numbers (Li et al., 2018).

Meat quality measurements

To compare the meat quality of cloned and noncloned progeny, the longissimus dorsi muscle was removed from 12 pigs in each group and ∼2.5 cm thick sections were cut from the anterior end for assessment of meat quality. Meat color was subjectively evaluated by comparing to the standard color cards (ranging from 1 to 6 with 1 = pale pinkish gray to white, 2 = grayish pink, 3 = reddish pink, 4 = dark reddish pink, 5 = purplish red, and 6 = dark purplish red) at 1 and 24 hours postmortem (Stoller et al., 2003). Marbling scores (ranging from 0 to 3 with 0 = devoid and 3 = overly abundant) were subjectively evaluated at 1 and 24 hours postmortem (Yin et al., 2017).

Body temperatures and pH values at 1, 6, and 24 hours postmortem were monitored with a handheld temperature probe (Thermo Scientific Orion). Meat conductivities at 1, 6, and 24 hours of slaughter were tested by LF-star (Matthaus, Germany), and drip loss was detected using pressing loss by the pressing machine (SOK Micro Motor Manufacturing, China).

Gross chemical composition, amino acids, fatty acids, and mineral constitution of meat, omental fat, and liver

After slaughter, one kilogram of loin-eye muscle, omental fat, and liver samples per animal were collected from six pigs of each group and were sent to the China National Analytical Center, Guangzhou (NACC) (www.fenxi.com.cn/client/centintroen/centintroen_list.jsp) for measurements of Gross chemical composition, amino acid, fatty acids, and mineral by standard methods.

Statistical analysis

All the data were processed by SPSS 18.0, and the student's t-test was used. All the data were presented in the form of mean ± standard error.

Results

Carcass traits

Carcass trait parameters, including preslaughter weight, carcass straight length, carcass sloping length, loin-eye area, backfat thickness at the 10th and 11th rib interface, and rib number, were determined. The majority of the carcass traits were similar between 12 progeny from cloned and noncloned pigs, respectively (Table 1), except that carcass yield of cloned progeny was significantly higher than noncloned progeny and the backfat thickness at the 10th and 11th rib interface was significantly higher too.

Table 1.

Carcass Trait Measurement of Progeny from Cloned and Noncloned Pigs

Parameters	Cloned (n = 12)	Noncloned (n = 12)
Preslaughter weight	110.75 ± 1.28	112.18 ± 0.94
Carcass yield (%)	86.08 ± 0.30^a	84.87 ± 0.37^b
Carcass straight length (cm)	102.58 ± 0.94	104.67 ± 1.41
Carcass sloping length (cm)	86.33 ± 0.69	87.08 ± 1.08
Loin-eye area (cm²)	61.10 ± 2.88	61.06 ± 2.911
Backfat thickness at the 10th and 11th rib interface (mm)	21.43 ± 1.38^a	17.41 ± 1.22^b
Rib number	15.00 ± 0.12	15.25 ± 0.18

a,b

Values with different superscripts within the same column differ significantly (p < 0.05).

Meat quality

Parameters for meat quality, including meat color, marbling, temperature, pH, conductivity, and drip loss, were determined at various checking time points. All the data for meat quality parameters showed that the meat collected from progeny of cloned and noncloned pigs was equivalent in all aspects that we tested (Table 2).

Table 2.

Meat Quality for the Loin-Eye Muscle of Progeny from Cloned and Noncloned Pigs

Parameters	Cloned (n = 12)	Noncloned (n = 12)
Meat color at 1 hour	2.71 ± 0.11	2.79 ± 0.18
Meat color at 24 hours	2.62 ± 0.13	2.38 ± 0.16
Marbling at 1 hour	1.50 ± 0.14	1.50 ± 0.12
Marbling at 24 hours	1.46 ± 0.10	1.50 ± 0.12
Temperature at 1 hour (°C)	33.57 ± 0.90	33.13 ± 0.50
Temperature at 6 hours (°C)	25.92 ± 1.10	24.96 ± 0.96
Temperature at 24 hours (°C)	3.34 ± 0.22	2.93 ± 0.15
pH at 1 hour	6.12 ± 0.08	6.07 ± 0.09
pH at 6 hours	5.72 ± 0.07	5.62 ± 0.06
pH at 24 hours	5.84 ± 0.05	5.75 ± 0.0.07
Conductivity at 1 hour	3.36 ± 0.77	2.67 ± 0.21
Conductivity at 6 hours	4.35 ± 0.88	3.76 ± 0.85
Conductivity at 24 hours	3.68 ± 0.67	5.46 ± 1.12
Drip loss	5.30 ± 0.74	4.13 ± 0.70

Gross chemical composition

The gross chemical composition was determined in the loin-eye muscle, omental fat, and livers from six progeny of cloned and noncloned pigs, respectively. The results demonstrated that there were no differences in all the three tissues of progeny from cloned and noncloned pigs, in terms of total amino acid, protein, crude fat, ash, moisture, and nitrogen free extract (Table 3).

Table 3.

Gross Chemical Composition for the Loin-Eye Muscle, Omental Fat, and Liver of Progeny from Cloned and Noncloned Pigs

Parameters	Loin-eye muscle (n = 6)		Omental fat (n = 6)		Liver (n = 6)
Parameters	Cloned	Noncloned	Cloned	Noncloned	Cloned	Noncloned
Total amino acid (g/100 g)	23.85 ± 0.40	24.05 ± 0.62	0.89 ± 0.08	0.85 ± 0.05	18.83 ± 0.23	19.18 ± 0.31
Protein (%)	23.43 ± 0.31	23.23 ± 0.33	1.08 ± 0.06	1.17 ± 0.06	20.98 ± 0.07	20.63 ± 0.42
Crude fat (%)	1.63 ± 0.17	1.73 ± 0.17	90.78 ± 0.12	90.65 ± 0.26	4.32 ± 0.32	4.35 ± 0.30
Ash (%)	1.20 ± 0.04	1.50 ± 0.28	<0.1	<0.1	1.35 ± 0.05	1.38 ± 0.03
Moisture (%)	71.48 ± 0.36	71.73 ± 0.53	7.12 ± 0.09	7.09 ± 0.34	70.48 ± 0.65	71.17 ± 0.32
Nitrogen free extract (%)	2.25 ± 0.17	1.80 ± 0.17	1.01 ± 0.06	1.05 ± 0.11	2.87 ± 0.40	2.88 ± 0.43

Fatty acid, amino acid, and mineral composition

Since the gross composition of loin-eye muscle, omental fat, and liver had no difference between the two groups, we further detected the detailed composition of them, including 14 parameters for fatty acid composition, 16 parameters for amino acid composition, and 12 parameters for mineral composition.

The results showed that main fatty acid compounds in all the tissues from the two groups were palmitic acid (C16:0), stearic acid (C18:0), oleic acid (C18:1), and linoleic acid (18:2), which accounted for ∼90% of all the fatty acids. And there were no differences in fatty acid composition in the loin-eye muscle, omental fat, and liver collected from progeny of cloned and noncloned pigs in Table 4.

Table 4.

Fatty Acid Composition for the Loin-Eye Muscle, Omental Fat, and Liver of Progeny from Cloned and Noncloned Pigs

Fatty acid (%)	Loin eye muscle (n = 6)		Omental fat (n = 6)		Liver (n = 6)
Fatty acid (%)	Cloned	Noncloned	Cloned	Noncloned	Cloned	Noncloned
C10: 0	0.10 ± 0.00	0.10 ± 0.00	0.08 ± 0.00	0.07 ± 0.01	0.00 ± 0.00	0.00 ± 0.00
C12: 0	0.08 ± 0.00	0.08 ± 0.00	0.08 ± 0.00	0.08 ± 0.00	0.00 ± 0.00	0.00 ± 0.00
C14: 0	1.35 ± 0.02	1.30 ± 0.04	1.32 ± 0.03	1.27 ± 0.05	0.42 ± 0.16	0.34 ± 0.06
C16: 0	24.42 ± 0.55	24.92 ± 0.59	27.00 ± 0.52	26.98 ± 1.22	18.50 ± 2.11	16.75 ± 0.84
C16: 1	3.77 ± 0.18	3.23 ± 0.19	1.72 ± 0.13	1.67 ± 0.09	1.02 ± 0.28	1.01 ± 0.13
C17: 0	0.12 ± 0.03	0.15 ± 0.03	0.24 ± 0.03	0.31 ± 0.03	0.40 ± 0.08	0.33 ± 0.03
C17: 1	0.16 ± 0.02	0.15 ± 0.01	0.14 ± 0.01	0.20 ± 0.02	0.00 ± 0.00	0.08 ± 0.04
C18: 0	12.58 ± 0.55	14.65 ± 0.81	19.40 ± 0.83	19.60 ± 1.40	29.97 ± 1.54	28.27 ± 2.25
C18: 1	47.28 ± 0.39	46.02 ± 0.66	34.55 ± 0.93	33.77 ± 0.98	21.55 ± 2.90	20.60 ± 1.59
C18: 2	7.35 ± 0.73	6.53 ± 0.84	13.00 ± 0.84	13.15 ± 2.35	14.12 ± 2.25	16.87 ± 0.63
C18: 3	0.41 ± 0.06	0.30 ± 0.07	0.96 ± 0.14	0.83 ± 0.22	0.45 ± 0.12	0.73 ± 0.11
C20: 1	0.69 ± 0.04	0.82 ± 0.03	0.53 ± 0.02	0.60 ± 0.04	0.00 ± 0.00	0.00 ± 0.00
C20: 2	0.31 ± 0.03	0.31 ± 0.04	0.42 ± 0.03	0.46 ± 0.08	0.00 ± 0.00	0.00 ± 0.00
C24: 1	0.24 ± 0.04	0.17 ± 0.03	0.13 ± 0.01	0.17 ± 0.02	1.33 ± 0.19	1.11 ± 0.16

The amino acids and the mineral compositions were also detected. There were also no differences in amino acids and mineral compositions in the loin-eye muscle, omental fat, and liver collected from progeny of cloned and noncloned pigs as shown in Supplementary Tables S1 and S2.

Discussion

To test the safety of food, there are several targeted analysis required, such as microbial content and composition of heavy metals, rather than analyzing every single constitution, which is impractical (Ramos-Miras et al., 2019; Sieg et al., 2019).

In this study, to fully assess the characters of progeny of cloned pigs, we investigated not only carcass traits and meat quality but also chemical composition of loin-eye muscle, omental fat, and liver of progeny derived from cloned and noncloned pigs, which collected data on 7 parameters in carcass traits, 14 parameters in meat quality, and more than 40 parameters in chemical composition. The reason we tested the omental fat and liver was that viscera organs were very popular in Chinese supermarkets (Xia et al., 2018). To our knowledge, this is the first investigation in the chemical constitution of the viscera organs of progeny derived from cloned and noncloned pigs.

We found no significant difference in these parameters except for two: one was carcass yield, which was higher in the progeny of the cloned pigs than noncloned pigs, and the other was the backfat thickness at 10th and 11th rib interface, which indicated that the higher carcass yield may be due to higher backfat thickness.

This is consistent with the results in cloned cattle, as consistently higher amounts of mesentery fat and fatty acids in meat/fat were also observed, compared to their genetic and breed comparators (Tian et al., 2005). The linear correlation between carcass yield and backfat thickness was also reported in the other studies as increasing dietary inclusions of camelina cake fed to pigs linearly decreased carcass weight and backfat thickness (Smit and Beltranena, 2017). Although the backfat thickness was higher in the progeny derived from cloned pigs (24.43 vs. 17.41 mm), it was similar or thinner than the data provided in the previous report, as the average backfat ranged from 24 to 34 mm when the pigs were reaching slaughter weight of about 100 kg (Li et al., 2018).

Meat color is a phenotypic indicator of meat quality, determined by the physical and biochemical characters of meat, as it is the direct indicator when the dark, firm, and dry or the pale, soft, and exudative meat occurred (Florowski et al., 2017; Warriss et al., 2006). In this study, the color of meat derived from progeny of cloned and noncloned pigs was similar with each other, indicating that the meat quality was similar in terms of color. pH value indicated level of glucose oxidation, which affected shelf-life of meat refrigerated and frozen (Echegaray et al., 2018). Marbling is a parameter positively correlated with the intramuscular fat content, which affected the favor, juiciness, cook loss, and tenderness of meat (Lee and Choi, 2019; Lowell et al., 2018). The study showed that the meat quality of progeny derived from both cloned and noncloned pigs was similar.

Furthermore, the detailed chemical composition, such as fatty acids, amino acids, and mineral composition detections, also confirmed that the constitution of the tissues derived from progeny of cloned and noncloned pigs was similar with each other. These results were consistent with the previous literatures. Walker et al. (2007) found that the parameters of loin sample composition from offspring of cloned were not different with the conventionally produced boars. Mir et al. (2005) found that the reproduction characters and the blood profile were similar in cloned and noncloned pigs.

In conclusion, the carcass traits and meat quality and the chemical composition of three tissues were similar between progeny derived from cloned and noncloned pigs.

Footnotes

Author Disclosure Statement

The authors declare that no conflicting financial interests exist.

Funding Information

This study was supported by the Natural Science Foundation of China (31802036; 31802033) and the Natural Science Foundation of Guangdong Province, China (2017A030310001; 2018B020203002).

Supplementary Material

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