Carcass characteristics and meat quality of male pigs submitted to surgical or immunological castration

Abstract

The objective of this study was to evaluate carcass characteristics and meat quality of surgically castrated and immunocastrated male pigs. Data were collected from 24 surgically castrated pigs and 24 immunocastrated male entire originating from the commercial line (Agroceres x Topigs), receiving isonutritive diets and were housed in the same experimental shed, slaughtered at 177 days old, with a slaughter weight of 127.8 (± 6.5) and 135.1 (± 7.8) kg, respectively. Carcass and meat quality characteristics such as carcass yield, lean meat yield, fat content, backfat thickness, muscle depth, pH, meat coloring and, drip, thawing and cooking loss, were evaluated. Immunocastrated pigs have heavier carcass, higher meat yield and lower fat thickness when compared to surgically castrated animals. Regarding meat quality, the immunocastrated presented a lighter meat, less reddness and less water holding capacity. In conclusion, this study confirmed that the carcass of male pigs, submitted immunocastration, has lower yield, however, more meat and less fat content, when compared to carcass of male pigs surgically castrated. Meat quality showed peculiar characteristics for immunocastrated pigs, and can be used more for sausage production, since it retains less water and have smaller redness color compared to surgically castrated pigs.

Key words
Castration methods; immunocastration; swine; surgically castrated; water holding capacity

INTRODUCTION

Castration is a widespread procedure in pig farming recommended preventing pig meat from having an unpleasant taste and odor to the human palate, which may cause a reduction in your consumption (Pauly et al. 2010). Normally, castration is performed in the early days of life and without the use of analgesics and or anesthetics. However, with the growing concern in relation to animal welfare, new alternatives have been increasingly used.

The immunocastration is an alternative technique to surgical castration, without anesthesia and or analgesia, it has gained space and popularity in the pig production industry (Martins et al. 2013). It is a procedure, where induces the formation of specific antibodies that bind to and neutralize GnRH, reducing activity in the hypothalamic-pituitary-gonadal axis (Thun et al. 2006). It usually consists of applying two doses of the vaccine, the first dose prepares the immune system, while the second dose stimulates the animal to produce specific antibodies (Dunshea et al. 2001).

The immunocastration vaccine contributes to improving animal welfare during its productive life and performance in the fattening period (Weiler et al. 2013, Muniz et al. 2019). Characteristics that indicate meat quality as shear force and color are similar between castrated and immunocastrated pigs (Gispert et al. 2010, Batorek et al. 2012). The carcass yield in immunocastrated pigs can be up to 3.0% lower than that observed in castrated pigs (Dunshea et al. 2013). However, immunocastration increases the amount of meat compared to surgically castrated pigs (Caldara et al. 2012).

However, it is known that immunocastration generally results in ranging between studies, for variables such as meat yield and carcass fat content, color of meat samples and water holding capacity (Batorek et al. 2012, Aluwé et al. 2013). Thus, the objective of this study was to evaluate carcass characteristics and meat quality of surgically castrated and immunocastrated male pigs.

MATERIALS AND METHODS

The experiment was carried out at the Setor de Suínos linked to the Zootechnics Department of the Federal University of Santa Maria, Rio Grande do Sul state, Brazil. The procedures adopted in the study was approved by the Ethics Committee on the Use of Animals (protocol number 2874110618), from the same institution.

Animals and feeding

Data were collected from 24 surgically castrated pigs, on the third day of life, and 24 immunocastrated male entire originating pigs from the commercial line (Agroceres x Topigs), receiving isonutritive diets and were housed in 24 pens separated according to sex and weight, in the same experimental shed, slaughtered at 177 days old, with a slaughter weight (SW) of 127.8 (± 6.5) and 135.1 (± 7.8) kg, respectively. The experimental design was in completely randomised, having two treatments, castrated surgically and immunologically. The animals received a diet plan consisting of four diets balanced according to (NRC 2012; Table I).

Table I
Composition and calculated nutritional values of the diets fed to pigs in the growing and finishing phases.

Ingredients	Diets, %
	G1	G2	F1	F2
Corn	64.48	68.13	69.74	75.14
Soyabean meal (46% CP)	30.41	27.03	25.46	21.83
Soya oil	1.94	1.79	1.73	0.40
L-Lysine	0.32	0.31	0.29	0.27
DL-Methionine	0.14	0.11	0.13	0.07
L-Threonine	0.11	0.09	0.10	0.07
Limestone	0.74	0.77	0.78	0.76
Dicalcium phosphate	1.33	1.20	1.19	0.92
Salt	0.43	0.48	0.48	0.45
Mineral premix1	0.05	0.05	0.05	0.05
Vitamin premix2	0.05	0.05	0.05	0.05
Composition nutritional and energy	G1	G2	F1	F2
Crude Protein, %	18.85	17.61	16.77	15.81
Metabolizable energy (ME), MJ.kg-1	13.82	13.82	13.82	13.60
SID lysine (Lys), %	1.00	0.92	0.88	0.79
Lys: ME, (g.MJ-1)	0.73	0.66	0.64	0.57
Calcium, %	0.70	0.67	0.64	0.59
Standardized phosphorus, %	0.35	0.33	0.32	0.28
Sodium, %	0.17	0.19	0.19	0.18

• G1– 24 days (30-50kg); G2– 28 days (50-80kg); F1– 25 days (80-105kg); F2– 26 days (105-130kg); ¹Composition per kg of product: calcium: 98.800mg; cobalt: 185mg; copper: 15.750mg; iron: 26.250mg; iodine: 1.470mg; manganese: 41.850mg; zinc: 77.999mg; selenium: 105mg; ² Composition per kg of product: folic acid: 116.55mg; pantothenic acid: 2.333mg; biotin: 5.28mg; niacin: 5.600mg; pyridoxine: 175mg; riboflavin: 933.3mg; thiamine: 175mg; Vit. A: 1.225.000 U.I.; Vit. D3: 315.000 U.I.; Vit. E: 1.400mg; Vit. K3: 700mg; Vit. B12: 6.825mg.

Castration’s management

The piglets, which underwent surgical castration, were sedated with administration of 4 mg.kg^-1 of tramadol and 1 mg.kg^-1 of midazolam, intramuscularly. After 10 minutes, the skin of the scrotal sac was cleaned and local anesthesia in each spermatic cord, using 0.5 ml of 2% lidocaine without epinephrine. The surgical procedure was performed 5 minutes after the application of the anesthetic, with the cleaning and disinfection of the skin of the scrotum with an iodine-based antiseptic solution, with a longitudinal cut and removal of the testicles. After surgical castration, no piglet had any complications, and it was not necessary to use anti-inflammatory or anti-biotic

The male pigs destined of the immunocastration, were vaccinated by a technical team (Vivax®, Zoetis, Brazil). The vaccination protocol consisted of the subcutaneous application of 2 ml (200 μh GnRH conjugated to protein per milliliter) of the vaccine, the first and second doses were performed eight and four weeks before slaughter, respectively. According to Dunshea et al. (2013), the first dose is of a sensitizing nature, where the animal will have contact with the anti-GnRH antigen, and the second dose will cause it to produce anti-GnRH antibodies.

Slaughter and data collection

The animals were fasted for eight hours before the transport. At the slaughterhouse, pigs were weighed individually, and housed in collective pens with free access to water. The time between transport and slaughter was approximately twelve hours. Using standard handling pre-slaughter to minimize stress, the pigs were stunned with electrical system, followed immediately by bleeding, scalding, mechanical depilation and evisceration. The carcass were weighed and divided lengthwise.

After were collected hot carcass weight (HCW) and cold carcass (CCW) (without head and feet); pH 45 minutes post-slaughter (pH-45) and pH 24 hours post-slaughter (pH-24), measured in the ham using the Testo-205® portable pH meter, this device compensates the temperature simultaneously due to an integrated sensor that allows accurate pH measurement.

The pH meter calibration was carried out by immersing his sensor in solutions with pH 4 and 7, according to the device manual. The gradient and displacement values were greater than 50 mV / pH and less than 60 mV, respectively, demonstrating that the electrode is functioning properly. Among the readings performed, the pH meter was packed in its cap, filled with KCl-based gel, to prevent disbalances.

In the region of the third and fourth ribs in the caudal-cranial direction, a cross section was performed, where the muscle depth (MD) of Longissimus lumborum and backfat thickness were measured, the entire area was drawn on butter paper for the calculation of loin eye area (LEA) and loin fat area (LFA). For the analysis of color, drip loss, thawing loss, cooking loss and shear force, samples of Longissimus lumborum muscle were collected from the left half-carcass. The carcass yield (CY) and carcass lean meat (CLM), were estimated through equations described by Irgang et al. (1998).

Post-slaughter analysis

The water-holding capacity was measured according to the methodology of Honikel (1987), comprising the sum of the variables, drip loss, thawing loss and cooking loss. Drip loss was determined using a 150 g meat sample approximately, suspended and wrapped with a plastic bag, without contact, in a cold chamber, being weighed at the beginning and after forty-eight hours. Samples of proportion similar to those used for drip loss (150 g), were submitted to freezing after twenty-four hours of the slaughter, for thawing loss determination (frozen samples weight – thawed samples weight). The samples of 150 g in natura were then cooked in an oven, until the internal temperature reached 70 ºC, and weighed, for cooking loss quantification (in natura samples weight - cooked samples weight).

The Shear force was determined, with a Warner-Bratzler Shear machine, in six cores 12.5 x 25.0 mm diameter and width, respectively, were removed parallel to the longitudinal orientation of the muscle fibers, per meat sample. A boxplot was used to identify and exclude outliers, results within normality were used to obtain the mean of each sample.

The color intensities (L, a* and b*) were evaluated with 2.5 cm thick samples. Three measurements were taken at different sample points, using the Minolta Sensing Spectrophotometer CR-400, with 10 grade of standard observer, D65 illuminant and 11-mm aperture, calibrated with a background white.

Statistical analyses

All statistical analyzes were performed in Minitab® 2018 statistical software. The qualitative and quantitative data of carcasses of swine, were submitted to analysis of variance by the General Linear Model procedure. Were analyzed, with sexual categories as fixed factor, and carcass weight as co-variable for the following variables carcass yield, carcass lean meat, loin fat area, backfat thickness, loin eye area and muscle depth. The differences between means were compared by the Fisher test and considered significant if P <0.05.

RESULTS

The carcass traits differed (P <0.05) among the sexual categories. The swine immunocastrated (IM) showed superiority, for hot carcass weight (HCW), cold carcass weight (CCW), carcass lean meat (CLM), loin eye area (LEA) and muscle depth (MD). While swine male surgically castrated (SC), were higher for carcass yield (CY), loin fat area (LFA), backfat thickness (Table II).

Table II
Carcass characteristics, meat quality and water holding capacity determined in the Longissimus lumborum muscle from swine male surgically castrated and immunocastrated.

	SC	IM	SEM	p-value
Carcass Characteristics (n)	24	24
Slaughter weight, Kg	127.80	135.10	1.475	0.001
Hot carcass weight, Kg	93.11	96.45	1.095	0.037
Cold carcass weight, Kg	88.51	92.01	1.065	0.025
Carcass yield, % sw*	72.88	71.38	0.240	0.001
Carcass lean meat, % sw*	57.88	59.93	0.413	0.001
Loin fat area, cm² sw*	24.13	20.23	0.792	0.001
Backfat thickness, mm sw*	16.18	12.89	0.651	0.001
Loin eye area, cm² sw*	56.52	60.63	1.190	0.019
Muscle depth, mm sw*	71.83	74.84	0.748	0.007
Meat Quality (n)	24	24
pH-45	6.49	6.54	0.053	0.493
pH-24	6.02	5.95	0.044	0.270
L*	52.86	55.65	0.619	0.004
a*	7.75	6.72	0.352	0.049
b*	12.94	12.64	0.309	0.496
Shear Force (N)	33.94	36.07	2.460	0.547
Water holding capacity (n)	24	24
Drip Loss (%)	2.21	2.92	0.203	0.019
Thawing loss (%)	5.06	7.28	0.544	0.008
Cooking loss (%)	23.22	25.91	0.903	0.044

• SC: Male surgically castrated, IM: Male submitted to immunocastration; SEM: Standard error mean; Backfat thickness: was measured in the region of the third and fourth ribs in the caudal-cranial direction; L*: Luminosity, a*: redness, b*: yellowness; pH-45: forty-five minutes after slaughter; pH-24: twenty-four hours after slaughter. ^SW*: Variables in which the slaughter weight was utilized with co-variable for analysis of variance.

The pH45, pH24 and shear force did not differ (P >0.05) between the castration groups. However, for meat coloration, only the variable b* (yellowness) did not differ statistically; L (luminosity) and a* (redness) were significantly different (P <0.05), indicating higher values for IM and SC, respectively (Table II). For the water-holding capacity variables, IM in relation to SC, obtained higher values (P < 0.05) for drip, thawing and cooking loss (Table II).

DISCUSSION

Quantitative and qualitative characteristics of pig carcasses are highly influenced by body weight, castration method and genetics (Kouba & Sellier 2011, Trefan et al. 2013). According to Pauly et al. (2009), the IM have higher intestine, kidney and liver weights. In addition, the total weight of the reproductive organs of the IM is greater, due to the presence of the testicles, and attached glands of the reproductive system, which have not yet reduced to the same proportion as in SC (Skrlep et al. 2010, Batorek et al. 2012). This accounts for the differences between sexual categories, for slaughter weight and hot carcass weight, resulting in as well the higher carcass yield for SC.

According to our results, IM were superior to SC for CLM, MD and LEA measurements, these variables have a positive correlation (Rehfeldt & Kuhn 2006). The likely explanation for this would be, male pigs submitted to immunocastration have greater anabolic potential, a result of the presence of gonadal hormones during most of the fattening period. Causing higher protein deposition in the carcass, resulting in value higher CLM after slaughter in relation to SC, that because they do not have testicles, they perform greater lipid deposition. (Pauly et al. 2009, Boler et al. 2012, Muniz et al. 2019).

The amount of fat in pig carcasses is influenced by the castration method, due to changes in the animal’s lipid metabolism (Kouba & Sellier 2011). Both forms of castration, surgical or vaccine-induced, reduce steroid hormones levels in the blood, resulting in increased lipid deposition (Schreurs et al. 2008, Fàbrega et al. 2010). However, in the IM increases the rate of lipid deposition after the second dose of the vaccine, 28 days before slaughter, (Lealiifano et al. 2011). Already SC, have this lipid metabolism from the third day of life, this may be the explanation for the presence the highest backfat thickness and loin fat area, resulting in a fatter carcass, for this sexual category.

Color is a subjective indication of meat quality for the consumer, although the color indicators described in the literature are inconsistent (Aluwé et al. 2013). The IM obtained lower pH-24 and higher drop in pH post-mortem, however, nothing statistically significant. The pH drop causes, electrostatic repulsion between myofilaments, increasing the distance between myofibrils, and with that the refraction of light (Swatland 2004), thus increasing the value for variable L, in samples this sexual category. For variable a*, the difference obtained can be explained by the slaughter weight. According to Tikk et al. (2008) the meat of heavier carcasses swines, tend to have a lower intensity of red, being confirmed by this study, where IM had higher slaughter weight and lower intensity of a* variable.

Batorek et al. (2012) demonstrated through meta-analytic study that entire male pigs have high values for shear force. The compensatory growth that occurs after the second dose of the vaccine in swines immunocastrated, produces a higher in vivo protein turnover, increasing post-mortem proteolysis which makes the meat from immunocastrated swine softer (Therkildsen et al. 2004, Lametsch et al. 2006). Generating similarity in the values found, for the variable shear force between IM and SC, as demonstrated in our study.

Unlike Boler et al. (2014), who state that immunocastration does not affect water-holding in the carcass. Our study found differences, in the variables that quantify water holding capacity between the sexual categories. The value found for CLM in our study, may be the explanation for the lower water holding capacity, obtained by IM. According to Schiavon & Emmans (2000), protein deposition retains more as, twice as much water as lipid deposition. With this, the IM has more water to be lost in industrial processes, such as cooling (drip loss), freezing followed by thawing (thawing loss) and cooking (cooking loss), validating the values found by our study.

The drop in pH post-mortem results in myofibrillar distancing, interfering with the loss of inter and intracellular water (Swatland 2004, Huff-Lonergan & Lonergan 2005). In a study by Bertram et al. (2002), the authors state that the water located outside the myofibrils, migrate towards the surface of the meat, contributing to the increase in water loss, during the storage and cooking processes. Caldara et al. (2012), submitted pork to cooking, finding higher losses of water by cooking in samples whose pH was less than 6.0. These higher losses found may be switched on to the acceleration of the denaturation process of myofibrillar proteins during cooking, due to pH and temperature, justifying for the values obtained for cooking loss in our study.

CONCLUSION

In conclusion, this study confirmed that the carcass of male pigs, submitted immunocastration, has a lower yield. However, immunocastrated pigs presented higher amounts of meat and less fat content when compared to carcass of male pigs surgically castrated. The meat of immunocastrated pigs retains less water and has smaller redness color compared to surgically castrated pigs, and therefore can be recommended for sausage production.

ACKNOWLEDGMENTS

This study was carried out with the support of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001 and the financial support of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, process 425055/2016-7).

REFERENCES

• ALUWÉ M, LANGENDRIES KCM, BEKAERT KM, TUYTTENS FAM, DE BRABANDER DL, DE SMET S & MILLET S. 2013. Effect of surgical castration, immunocastration and chicory-diet on the meat quality and palatability of boars. Meat Sci 94: 402-407.
• BATOREK N, CANDEK-POTOKAR M, BONNEAU M & VAN MILGEN J. 2012. Meta-analysis of the effect of immunocastration on production performance, reproductive organs and boar taint compounds in pigs. Animal 6(8): 1330-1338.
• BERTRAM HC, PURSLOW PP, & ANDERSEN HJ. 2002. Relationship between meat structure, water mobility, and distribution: a low-field nuclear magnetic resonance study. J Agr Food Chem 50: 824-829.
• BOLER DD, KILLEFER J, MEEUWSE DM, KING VL, MCKEITH FK & DILGER AC. 2012. Effects of slaughter time post-second injection on carcass cutting yields and bacon characteristics of immunologically castrated male pigs. J Anim Sci 90: 334-344.
• BOLER DD, PULS CL, CLARK DL, ELLIS M, SCHROEDER AL, MATZAT PD, KILLEFER J, MCKEITH FK & DILGER AC. 2014. Effects of immunological castration (Improvest) on changes in dressing percentage and carcass characteristics of finishing pigs. J Anim Sci 91: 359-368.
• CALDARA FR, SANTOS VMO, SANTIAGO JC, ALMEIDA PAZ ICL, GARCIA RG, VARGAS JUNIOR FM, SANTOS LS & NÄÄS IA. 2012. Propriedades físicas e sensoriais da carne suína PSE. Rev Bras Saúde Prod Ani 13(3): 815-824.
• DUNSHEA FR ET AL. 2013. The effect of immunization against GnRF on nutrient requirements of male pigs: A review. Animal 7(11): 1769-1778.
• DUNSHEA FR ET AL. 2001. Vaccination of boars with a GnRH vaccine (Improvac) eliminates boar taint and increases growth performance. J Anim Sci 79: 2524-2535.
• GISPERT M, OLIVER MA, VELARDE A, SUAREZ P, PÉREZ J & FONT-I-FURNOLS M. 2010. Carcass and meat quality characteristics of immunocastrated male, surgically castrated male, entire male and female pigs. Meat Sci 85: 664-670.
• HONIKEL. 1987. How to measure the water-holding capacity of meat? Recommendation of standardized methods. In: Tarrant PV et al. (Eds), Evaluation and control of meat quality in pigs, Dordrecht, The Netherlands: Martinus Nijhof, p. 129-142.
• HUFF-LONERGAN E & LONERGAN SM. 2005. Mechanisms of water-holding capacity of meat: The role of postmortem biochemical and structural changes. Meat Sci 71: 194-204.
• IRGANG R, GUIDONI AL, BERLITZ D & CORSO C. 1998. Medidas de espessura de toucinho e de profundidade de músculo para estimar rendimento de carne magra em carcaças de suínos. Rev Bras Zoot 27(5): 928-935.
• KOUBA M & SELLIER P. 2011. A review of the factors influencing the development of intermuscular adipose tissue in the growing pig. Meat Sci 88: 213-220.
• LAMETSCH R, KRISTENSEN L, LARSEN MR, THERKILDSEN M, OKSBJERG N & ERTBJERG P. 2006. Changes in the muscle proteome after compensatory growth in pigs. J Anim Sci 84: 918-924.
• LEALIIFANO AK, PLUSKE JR, NICHOLLS RR, DUNSHEA FR, CAMPBELL RG, HENNESSY DP, MILLER DW, HANSEN CF & MULLAN BP. 2011. Reducing the length of time between harvest and the secondary gonadotropin-releasing factor immunization improves growth performance and clears boar taint compounds in male finishing pigs. J Anim Sci 89: 2782-2792.
• MARTINS PC, ALBUQUERQUE MP, MACHADO IP & MESQUITA AA. 2013. Implicações da imunocastração na nutrição de suínos e nas características de carcaça. Arch Zootec 62: 105-118.
• MUNIZ HCM, ROCHA LT, KUNZLER JS, CERON MS, FRAGA BN, BOTTAN J, QUADROS ARB & OLIVEIRA V. 2019. Evaluation of factorial methods to estimate lysine requirements for barrows and immunocastrated pigs. Livest Sci 227: 68-74.
• NRC. 2012. Nutrient requirements of swine. 11th Rev ed. National Academies Press, Washington, DC.
• PAULY C, SPRING P, O’DOHERTY JV, KRAGTEN SA & BEE G. 2009. Growth performance, carcass characteristics and meat quality of group-penned surgically castrated, immunocastrated (Improvac®) and entire male pigs and individually penned entire male pigs. Animal 3(7): 1057-1066.
• PAULY C, SPRING P, O’DOHERTY JV, KRAGTEN SA, DUBOIS S, MESSADÈNE J & BEE G. 2010. The effects of method of castration, rearing condition and diet on sensory quality of pork assessed by a trained panel. Meat Science 86: 498-504.
• REHFELDT C & KUHN G. 2006. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 84: 113-123.
• SCHIAVON S & EMMANS GC. 2000. A model to predict water intake of a pig growing in a known environment on a known diet. Br J Nutr 84: 873-883.
• SCHREURS NM, GARCIA F, JURIE C, AGABRIEL J, MICOL D, BAUCHART D, LISTRAT A & PICARD B. 2008. Meta-analysis of the effect of animal maturity on muscle characteristics in different muscles, breeds, and sexes of cattle. J Anim Sci 86: 2872-2887.
• SKRLEP M, SEGULA B, ZAJEC M, KASTELIC M, KOSOROK S, FAZARINC G & CANDEK-POTOKAR M. 2010. Effect of immunocastration (Improvac ®) in fattening pigs I: growth performance, reproductive organs and malodorous com pounds. Slov Vet Res 47(2): 57-64.
• SWATLAND HJ. 2004. Progress in understanding the paleness of meat with a low pH. S Afr J Anim Sci 34 (Supplement 2): 1-7.
• THERKILDSEN M, VESTERGAARD M, BUSK H, JENSEN MT, RIIS B, KARLSSON AH, KRISTENSEN L, ERTBJERG P & OKSBJERG N. 2004. Compensatory growth in slaughter pigs – in vitro muscle protein turnover at slaughter, circulating IGF-1, performance and carcass quality. Livest Prod Sci 88: 63-75.
• THUN R, GAJEWSKI G & JANETT FF. 2006. Castration in male pigs: techniques and animal welfare issues. J Physiol Pharmacol 57: 189-194.
• TIKK K, LINDAHL G, KARLSSON AH & ANDERSEN HJ. 2008. The significance of diet, slaughter weight and aging time on pork color and color stability. Meat Sci 79: 806-816.
• TREFAN L, WILSON AD, ROOKE JA, TERLOW C & BÜNGER L. 2013. Meta-analysis of effects of gender in combination with carcass weight and breed on pork quality. J Anim Sci 91: 1480-1492.
• WEILER U, GOTZ M, SCHIMIDT A, OTTO M & MULLER S. 2013. Influence of sex and immunocastration on feed intake behavior, skatole and indole concentrations in adipose tissue of pigs. Animal 7(2): 300-308.

Publication Dates

• Publication in this collection
  27 Sept 2021
• Date of issue
  2021

History

• Received
  31 Jan 2020
• Accepted
  26 June 2020