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Poult Sci 2008. 87:1849-1859. doi:10.3382/ps.2007-00188
© 2008 Poultry Science Association
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PROCESSING, PRODUCTS, AND FOOD SAFETY

Slaughter Performance of Four Different Turkey Strains, with Special Focus on the Muscle Fiber Structure and the Meat Quality of the Breast Muscle

C. Werner1, J. Riegel and M. Wicke

Institute of Animal Breeding and Genetics, Georg-August University Goettingen, Albrecht-Thaer-Weg 3, D-37075 Goettingen, Germany

1 Corresponding author: carsten.werner{at}agr.uni-goettingen.de


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The increase in human consumption of turkey meat and the shift in the poultry market from whole birds to further processed meat products increases the visibility of meat alterations (e.g., heterogenic color, drip loss, petechial hemorrhages) at retail. Changes in poultry meat quality have been related to the intensive growth of the current turkey strains. Considering this, the main objective of this investigation was to evaluate the meat quality and muscle structure of commercially available turkey strains with different growth properties but similar breast yields. Toms (n = 120) of 4 different turkey strains (British United Turkeys Big 6, Kelly Broad-Breasted Bronze, Kelly Wrolstad, Kelly Super Mini; n = 30 per strain) were reared in an experimental barn under similar environmental and feeding conditions and were slaughtered at 22 wk of age in a commercial slaughterhouse. The strains Big 6 and Broad-Breasted Bronze belong to the fast-growing (FG) turkey strain and the other 2 to the slow-growing (SG) turkey strain. The carcass weights, as estimated by video imaging, differed significantly (P < 0.05) between the SG and FG groups. The breast yields (percentage of carcass weight) of the investigated strains were similar. Except for the significantly (P < 0.05) greater protein concentration in the musculus pectoralis superficialis of the SG birds, the musculus pectoralis superficialis had nearly similar fat and ash contents. Plasma lactate concentrations were similar in the investigated turkey strains but the creatine kinase activities were greater in the FG turkeys at the time of slaughter. Determination of the different meat quality parameters [pH, electrical conductivity, color (L*a*b*), drip loss, shear force] did not result in clear differences between the SG and FG turkey strains. There were larger muscle fibers in the FG in comparison with the SG strains, but no differences could be determined in the capillary density and incidence of degenerated or giant fibers, except for a higher rate in the Wrolstad strain. The present results are contradictory to the opinion that turkeys with faster growth have worse meat quality.

Key Words: turkey • commercial strain • growth • meat quality • muscle structure


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The shift in the poultry market from whole birds to further processed meat products increases the incidence of noticeable changes in physical appearance. Typical changes are myopathies, hemorrhages, or the appearance of pale, soft, and exudative (PSE)-like meat (Barbut, 1997; Dransfield and Sosnicki, 1999; Clark et al., 2002; Bianchi et al., 2006; Fraqueza et al., 2006). In some research reports, the authors have related these meat alterations to the intensive selection of poultry for increased live weights and breast yields (Berri et al., 2001; Alvarado and Sams, 2004; Branscheid et al., 2004). This assumption seems to be true with regard to the myopathies (Harper et al., 1983; Siller, 1985; Wilson et al., 1990; Velleman et al., 2003; Bianchi et al. 2006), but the impact of intensive selection for increased live and breast weight on the meat quality, especially on the incidence of PSE, is rather unclear. Some authors stated that these alterations are related to the rapid growth of the birds (Berri et al., 2001; Alvarado and Sams, 2004; Branscheid et al., 2004; Maltby et al., 2004). On the other hand, other researchers who have compared fast- and slow-growing birds of different species have reported that the incidence of PSE is independent of the growth velocity and the fiber diameter (Fernandez et al., 2001; Le Bihan-Duval et al., 2001; Baeza et al., 2002; Yost et al., 2002; Debut et al., 2003; Lonergan et al., 2003; Rammouz et al., 2004b; Updike et al., 2005).

However, PSE-like meat is a problem in the turkey population, as reported in different screening studies (Barbut, 1993, 1997; Owens and Sams, 2000; Taubert et al., 2002; Fraqueza et al., 2006). Pale, soft, and exudative-like meat is characterized by a paler color, a heterogeneous appearance, a poorer texture and cohesiveness, and a greater drip loss compared with unaffected poultry meat (Barbut, 1993, 1996, 1997). These alterations are not only unacceptable for consumers, but also give rise to problems in the poultry industry during processing. The phenomenon is similar to the homonymous meat quality problem in pork and is caused by a rapid pH decline postmortem, combined with high carcass temperatures and accelerated protein degeneration (Alvarado and Sams, 2004; Rehfeldt et al., 2004). Researchers have evaluated common meat quality parameters (e.g., pH, color) for the purpose of early and accurate prediction of PSE-type poultry meat (Owens and Sams, 2000; Van Laack et al., 2000; Le Bihan-Duval et al., 2001; Woelfel et al., 2002; Rammouz et al., 2004a; Fraqueza et al., 2006). Early and accurate prediction could be important for the poultry industry to be able to sort the meat before subsequent processing or packaging. Different authors (Van Laack et al., 2000; Le Bihan-Duval et al., 2001; Woelfel et al., 2002; Rammouz et al., 2004a; Fraqueza et al., 2006) have reported that determination of the pH value after initiation of rigor mortis (>3 h) is a good parameter to predict late postmortem meat characteristics, especially the brightness (L*) and redness (a*) values, the drip loss, or the cooking or grilling yield, with correlation coefficients between 0.3 and 0.7 in different poultry species.

Opponents of intensive poultry production, especially organic poultry producers, argue that the meat quality problems described can only be dealt with by reducing the growth rates and by improving the intensive husbandry conditions, but not by sorting of the meat after slaughter (Castellini et al., 2002). In the present study, 4 commercial turkey strains with different growth rates that had been selected for either intensive or organic production were reared and slaughtered under similar conditions to minimize any exogenic factors influencing the meat quality (e.g., stocking density, transport, stunning, chilling). The objective of the investigation was to compare the quality and chemical composition of the meat and the muscle structure in turkey strains with different growth rates.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Birds, Husbandry, and Feeding

Male turkey poults from midage laying hens (42 to 46 wk) were supplied by British United Turkeys (BUT Big 6, British United Turkeys Ltd., Tattenhall, UK) and Kelly Bronze [Kelly Broad-Breasted Bronze (Kelly BBB), Kelly Wrolstad, Kelly Super Mini; Kelly Turkey Farms, Danbury, UK]. The BUT Big 6 line is one common heavy turkey line for intensive production. The lines from Kelly Bronze differ in their growth rates and are selected for free-range or organic production, or both. All birds (n = 30 per strain) were reared according to the animal welfare recommendations of the Council of Europe (2001) in an experimental barn that provided good husbandry conditions (e.g., stocking density, litter, ventilation). The birds were raised under similar conditions in one barn. The different strains were separated by wooden walls. The birds had no access to the outdoor environment to minimize any disturbing influences. The temperature in the barn was 24°C at the beginning of the trial and the poults had access to extra radiant heaters. During the growth of the birds, the heaters were removed and the temperature was gradually reduced to 18°C. The light intensity at the beginning was 22 lx and was decreased gradually to 4 lx at the end of the growth period. The daily dark period was increased from 0 to 8 h within the first week and remained at this period of time until the end of the trial. The litter (chipped wood) was controlled daily (e.g., dirt, wetness), and additional material was added in case the birds were slightly dirty. At the end of the growth period, the stocking density did not exceed 45 kg/m2.

The turkeys were fed ad libitum during the growth period with 6 feed variants, depending on the age of the birds. The main components of the pellets (size depending on the age) were wheat, soy, and corn. In the diet the concentrations of protein (27 to 16.4%), calcium (1.4 to 0.75%), and phosphorus (1.0 to 0.45%) were decreased continuously. The energy content was increased from 11.4 to 13 MJ of ME/kg. After wk 5, phytase (Ronozyme, DSM Nutritional Products Europe Ltd., Basel, Switzerland) was added to the diet.

Collection and Physicochemical Evaluation of the Samples

In wk 22, a total of 120 birds (30 turkeys per strain) were transported within 1.0 h (including careful catching and loading) to a commercial turkey slaughterhouse. After careful unloading and hanging in randomized order, the birds were electrically stunned in a water bath. Immediately after stunning (150 mA, 300 Hz, 4 s), the bleeding was initialized by mechanical cutting of the arteria carotis communis. Slaughter blood was collected in heparinized tubes (Sarstedt AG & Co., Nürnbrecht, Germany) for determination of the creatine kinase (CK) activity and lactate concentration. After scalding (58 to 60°C, 45 s), the carcasses were de-feathered and automatically eviscerated, followed by a veterinary meat inspection. No carcasses were rejected during this inspection. The weight of the carcasses was determined by video image analysis with a VTS 2000 (e+v Technology GmbH, Oranienburg, Germany). This system had been validated by the responsible German authority (Hahn et al., 1998) and was calibrated daily or after longer slaughter breaks with specific "dummies" (e+v Technology GmbH). Before entering the chilling room, the left musculus pectoralis superficialis (MPS) and musculus supracoracoideus were completely removed from the carcass by an experienced slaughterhouse employee and transported immediately to a separate room.

After removal of the skin and separation of the MPS from the musculus supracoracoideus, both breast muscles were weighed. Only the MPS were used for further sample collection and analysis, as shown in Figure 1Go. The electrical conductivity (EC) and pH values were determined 20 min after stunning in the center of the MPS. The temperature was monitored at this time with a digital thermometer (Testo AG, Lenzkirch, Germany) to adjust the pH meter. Subsequently, the muscles were transported on ice to the laboratory.


Figure 1
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Figure 1. Positions for the determination of pH, electrical conductivity (EC), and color values, and intersection lines for the collection of samples for the analysis of meat quality, muscle structure, and chemical composition in the musculus pectoralis superficialis (MPS) of the turkey strains investigated. The image shows the ventral view of the MPS.

 
After 4 h, the EC, pH, and color (L*a*b*) values (Fraqueza et al., 2006) were determined in the center of the MPS (Figure 1Go). The different samples for analysis of the meat quality (e.g., drip loss, shear force), muscle structure, and chemical composition were collected as shown in Figure 1Go. For the muscle structure analysis, blocks (1 x 1 x 1 cm3) were rolled in talcum, frozen in liquid nitrogen, and stored at –80°C until analysis. The samples for the nutrient analysis were homogenized in a homogenizer (Grindomix GM 120, Retsch GmbH, Haan, Germany) and stored in portions at –20°C until analysis. The slaughter blood was centrifuged for 10 min at 1,900 x g (Macrofuge, Kendro Laboratory Products GmbH, Hanau, Germany), and the plasma was then removed and stored in portions at –20°C until analysis of the CK activity and lactate concentration.

Methods

EC. The EC was measured 20 min and 4 h after slaughter with an EC meter equipped with 2 parallel stainless steel electrodes (LF-Star, Matthäus GmbH, Poettmes, Germany; Taubert et al., 2002; Honikel, 2007). Before the measurement, the EC meter was calibrated with a specific calibration block (10 mS/cm; Matthäus GmbH). For the EC determination, the electrode was inserted in the center of the MPS (Figure 1Go). The accuracy of the instrument was regularly controlled by using the calibration block (10 mS/cm, Matthäus GmbH).

pH. The pH was measured 20 min and 4 h after slaughter with a portable pH meter (pH-Star, Matthäus GmbH) combined with a glass electrode (InLab 427, Mettler-Toledo, Urdorf, Switzerland; Taubert et al., 2002; Honikel, 2007). Before the measurement, the pH meter was calibrated with 2 pH standard solutions (pH 7.0, pH 4.0; Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany) and adjusted to the mean temperature of the meat samples [39°C (20 min); 7°C (4 h)]. For the pH measurement, the electrode was inserted in the center of the MPS (Figure 1Go). The accuracy of the instrument was regularly controlled by using the pH standard solutions (Sigma-Aldrich Chemie GmbH).

Color. The color was evaluated 4 h after slaughter on the cross-section of the MPS with a colorimeter (Minolta CR 300, Minolta GmbH, Langenhagen, Germany). The muscle was cut at the intersection lines (Figure 1Go) and exposed to air for 15 min at room temperature before determining the color at the intersection area of the muscle. Each value was a least squares mean of at least 4 measurements per cross-section.

Drip Loss. The drip loss was determined between 4 and 28 h after slaughter by the bag method (Christensen, 2003). From the caudal part of the MPS (approximately 200 g; Figure 1Go), a piece of the muscle was removed and trimmed of adjacent fat. After weighing, the sample was wrapped in gauze, transferred into a plastic bag, and sealed. The apparatus was hung in a refrigerator and stored at 2 to 4°C for 24 h. The meat was then removed from the sealed plastic bag and weighed again. The drip was calculated as the loss of weight during storage relative to the initial weight, expressed as a percentage.

Grill Loss. From the cranial part of the MPS (approximately 200 g; Figure 1Go), a piece of the muscle was removed and trimmed of adjacent fat. After weighing, the sample was wrapped in aluminum foil and grilled in a plate contact grill (Neumärker GmbH, Hemer, Germany) until the core temperature reached 73°C. The core temperature was controlled by inserting the electrode of a digital thermometer (Testo AG) into the center of the meat sample during the whole grilling process. After grilling, the sample was removed, cooled down to room temperature, and reweighed. The grill loss was calculated as the loss of weight during the heating process relative to the initial weight expressed as a percentage.

Shear Force. The samples prepared for the determination of the grill loss were subsequently used for the Warner-Bratzler shear force analysis according to Bratcher et al. (2005). Cores with a diameter of 1.27 cm were removed from the sample at different positions parallel to fiber orientation. Shear force determinations were conducted on an Instron universal testing machine (model 4301, Instron, High Wycombe, UK) equipped with a Warner-Bratzler shear force head perpendicular to the fiber direction. The shear velocity was 200 mm/min. Each value was an average of at least 6 measurements.

Hemorrhages. At the caudal side of all intersections (Figure 1Go), the number of hemorrhages was counted. Only hemorrhages with a clear structure were counted. Discolorations were not considered. Each value represents the number of hemorrhages from 4 intersection areas.

Lactate Concentration and CK Activity. In the plasma, the lactate concentration was determined photometrically with a Biosub Lab test kit (Biocon Diagnostics, Bangalore, India), and the CK activity was also determined photometrically with a Biozyme CK-MB test kit (Biocon Diagnostics).

Chemical Composition. The concentrations of fat, protein, and ash, and the DM was determined according to the AOAC (1990). The protein concentration was calculated by analysis of the nitrogen concentration after catalytic combustion by an elementary analysis apparatus (VarioMax CN, Elementar Analytical Systems GmbH, Hanau, Germany) and multiplying the result by 6.25. The ash concentration was analyzed after combustion (600°C, 24 h) of 1 to 2 g of material in a muffle furnace (Modell Thermicon T, Kendro Laboratory Products GmbH, Hanau, Germany). The dry mass concentration was calculated from the weight before and after drying the muscle sample in a drying oven (Kendro Laboratory Products GmbH) at 105°C for 24 h. Fat was determined after acid hydrolysis and extraction in a Soxtherm apparatus (Gerhardt Laboratory Systems GmbH, Koenigswinter, Germany) by calculating the weight before and after the procedure.

Histology. The cryopreserved muscle samples were transferred to a cryomicrotome (Cryocut CM 1900, Leica GmbH, Nussloch, Germany) and allowed to equilibrate to –20°C before being cut into slices of 12-µm thickness. The sections were stained according to Horak (1983) with slight modifications. First the reduced nicotinamide adenine dinucleotide-tetrazolium reductase activity was determined histochemically by incubating the slices for 60 min at 37°C in buffer A [25 mM NaH2PO4 (Sigma-Aldrich Chemie GmbH), 2 mM reduced nicotinamide adenine dinucleotide (Sigma-Aldrich Chemie GmbH), 333 µg/mL of nitro-blue-tetrazolium-chloride (Leica GmbH)]. This staining was followed by histochemical determination of the myofibrillar ATPase activity. After acid preincubation (pH 4.2), the slices were incubated in ATP solution [2.7 mM ATP (Sigma-Aldrich Chemie GmbH), 50 mM KCl (Sigma-Aldrich Chemie GmbH), 18 mM CaCl2 (Sigma-Aldrich Chemie GmbH), 0.1 M glycine (Sigma-Aldrich Chemie GmbH), pH 9.4] at 37°C for 20 min. The catalytically released phosphate ions react in several steps with CaCl2 (Sigma-Aldrich Chemie GmbH), Co3(PO4)2 (Sigma-Aldrich Chemie GmbH), and NH4S (Sigma-Aldrich Chemie GmbH). In the terminal step, insoluble, black-colored CoS2 precipitates are formed. In additional slices, the capillaries were visualized by amylase–periodic acid-Schiff staining according to Brocks et al. (2000). In brief, after fixation (80% ethanol, 15% chloroform, 5% acetic acid), the slices were first incubated for 15 min at 37°C in {alpha}-amylase solution (3 mg/mL), then transferred for 30 min to periodic acid (1%) and subsequently incubated in Schiff’s reagent (0.1% fuchsin, 1% Na2SO3). Between the different steps, the slices were intensively washed with distilled water. The slices were investigated with a stereomicroscope (Nikon GmbH, Duesseldorf, Germany) at a low magnification (4x), and several sections were transferred through a digital camera to a personal computer. In the pictures, the number of degenerated or giant fibers and the number of capillaries were counted and related to the total fiber number (>600 fibers) and to the fiber area, respectively. For determination of the cross-sectional diameters and areas, at least 200 type IIb muscle fibers were circumscribed and semi-automatically analyzed with Lucia software (Nikon GmbH).

Statistical Analysis

Statistical analysis of the data was performed with the software package Statistica 7.1 (StatSoft, 2005). Results for the individual birds were subjected to ANOVA by using one-way-ANOVA, considering the following statistical model:


Formula

where Si are turkey strains (i = BUT Big 6, Kelly BBB, Kelly Wrolstad, Kelly Super Mini). Statistical significance was calculated with Fisher’s least significant differences test (Hayter, 1986), considering a probability error of P < 0.05.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Slaughter Weights and Nutrient Composition of the MPS

The commercial lines BUT Big 6 and Kelly BBB exhibit fast-growing (FG) traits, as was observed with the carcass weights of 15.5 and 12.9 kg, respectively. The carcasses of the strains Kelly Wrolstad and Kelly Super Mini had lower weights (8.2 and 7.9 kg, respectively; P < 0.05), representing commercial slow-growing (SG) turkey strains. However, within the FG group the Big 6 birds were significantly heavier than the birds of the BBB strain, whereas in the SG group no significant differences were observed for the carcass weights (Table 1Go). The described differences in the carcass weights could be also found when considering the breast muscles (MPS and musculus supracoracoideus). The Big 6 strain had the heaviest breast weights, followed by the BBB strain—which differed significantly from the Big 6 line—and the Wrolstad and Super Mini strains. The weights of the SG turkeys did not differ significantly (P > 0.05). With regard to the breast muscle ratio, the 4 turkey strains had similar values of approximately 36.5%.


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Table 1. Least squares means (LSM) and SEM of the carcass characteristics and the musculus pectoralis superficialis (MPS) composition (protein, fat, ash), depending on the turkey strain investigated
 
Birds in the FG group had significantly lower protein concentrations than those in the SG group. Within the FG and SG groups, the protein values were similar (P > 0.05). With regard to the fat content of the MPS, the Big 6 birds had the greatest concentrations, followed by the Wrolstad and Super Mini strains. The BBB strain had the lowest pectoral fat concentration. Significant differences could be determined only between birds of the Big 6 and BBB strains. The ash content for the 4 strains was between 1.08% (BBB) and 1.15% (Super Mini), and these 2 were the only ones that were significantly different.

Plasma CK Activity and Lactate Concentration

The plasma CK activity was highest in the Big 6 strain (58.6 U/mL) and lowest in the Super Mini strain (22.3 U/mL; Figure 2Go). There were no significant differences between the FG and SG groups. There were significant differences between the Big 6 and both SG strains and between the Super Mini and the FG strains. Plasma lactate concentrations of the turkey strains were similar, with values of 6.4 mM (Big 6) to 7.5 mM (Super Mini).


Figure 2
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Figure 2. Least squares means and SEM of the lactate concentration (mg/dL) and the creatine kinase activity (U/mL) in the slaughter plasma of the 4 turkey strains. a–cColumns with different letters for the same property differ significantly (P < 0.05) between the turkey strains.

 
Meat Quality Parameters

The pH values of the MPS determined immediately after slaughter (pH20min) did not differ (P > 0.05) among the turkey strains. Within 4 h after slaughter, the pH in the breast muscle decreased significantly in all FG and SG birds. The birds of the Big 6 strain had significantly higher pH4h than the BBB and Super Mini strains. The pH4h of the Super Mini strain was significantly lower than in all other turkey strains (Table 2Go).


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Table 2. Least squares means (LSM) and SEM of the meat quality parameters and of intramuscular hemorrhages (petechia) of the musculus pectoralis superficialis (MPS) depending on the turkey strain investigated
 
The EC values determined shortly after slaughter (EC20min) were highest in the BBB strain, followed by the Big 6 and the small turkey strains. Significant differences were obtained between the BBB strain and all other turkey strains and additionally between the Big 6 and the Wrolstad strain. During 4 h of storage, the EC values (EC4h) increased significantly in all the turkey strains except for the Big 6 strain. The only difference in EC4h was between the BBB strain and the other 3 lines.

With regard to the color values, no significant differences (P > 0.05) existed between the different commercial turkey strains. The brightness (L*), redness (a*), and yellowness (b*) values were approximately 43.0, 6.0, and –1.9, respectively.

When the data on drip loss, grill loss, and shear force determinations among the turkey strains were compared, the grill loss values were similar (P > 0.05), with weight losses after grilling of approximately 21%. Only the birds of the BBB strain had significantly greater drip losses than the other turkey lines. The maximal shear force values differed significantly between the FG and the SG turkey strains, but not within the FG and SG groups.

The number of intrapectoral petechial hemorrhages (petechia), calculated at the 4 intersection lines of the left MPS and related to the weight of the muscle, were highest in the SG strains Super Mini and Wrolstad and lowest in the FG strains Big 6 and BBB. The values differed significantly between the FG and SG strains. The values also differ significantly between the Big 6 and BBB strains, but not between the Wrolstad and Super Mini strains.

Muscle Structure Parameters

The Big 6 strain had the highest mean fiber diameter, followed by the BBB, Wrolstad, and Super Mini strains. Significant differences were found only for birds within the FG and SG strains, but not between the FG and SG strains (Table 3Go).


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Table 3. Least squares means (LSM) and SEM of the histological muscle structure parameters of the musculus pectoralis superficialis (MPS) depending on the turkey strain investigated
 
The percentage of degenerated or giant fibers was lowest in the Big 6 birds, followed by the BBB, Super Mini, and Wrolstad strains. Only the turkeys from the Wrolstad strain had significantly greater percentages of degenerated or giant fibers.

To evaluate the blood supply of the muscle fibers, the capillary densities of all muscle samples were determined. The approximate numbers of capillaries per 10,000 µm2 were similar in the turkey strains, ranging between 1.69 (Big 6) and 1.81 (Super Mini; P > 0.05).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The selection of FG turkeys (Big 6, BBB) focuses on high growth intensities and correspondingly high yields of the breast muscles, whereas the SG birds (Wrolstad and Super Mini) are selected by reduced weights, slower growth rates, and being smaller birds at slaughter (Fernandez et al., 2001; Yost et al., 2002; Updike et al., 2005). One reason for the selection according to different growth properties might be the marketing attributes of the FG and SG carcasses. The small turkey strains are mainly sold as whole birds, for example, before Christmas and Thanksgiving, whereas the FG birds are usually processed further. Considering the production conditions of the turkeys, the FG birds are mainly used in intensive production, whereas SG turkeys are more favored by farmers for organic production. An argument for organic poultry production is that the reduced growth of the SG birds has a positive influence on the welfare of the birds and probably the quality of the meat (Castellini et al., 2002; Fanatico et al., 2005). Another reason is that the smaller birds are more suitable for outdoor access—an important prerequisite for organic animal production dictated by specific regulations, such as in the European Community and the United States (Castellini et al., 2002, 2006; Fanatico et al., 2005, 2006). However, with regard to the quality of the meat from SG birds, the presumed positive effect of the reduced growth is controversial (Berri et al., 2001; Fernandez et al., 2001; Le Bihan-Duval et al., 2001; Baeza et al., 2002; Yost et al., 2002; Debut et al., 2003; Lonergan et al., 2003; Alvarado and Sams, 2004; Branscheid et al., 2004; Maltby et al., 2004; Rammouz et al., 2004b; Updike et al., 2005).

The present study found no clear differences between the meat from FG and SG turkey strains. With regard to the proximate composition of the breast muscles investigated, the main results were the significantly (P < 0.05) greater protein concentrations in the SG strains and the lowest fat content in the BBB strain. Investigations of the chemical composition of turkey meat in relation to the growth capacity are rare. Fernandez et al. (2001) could not determine differences in the fat and ash concentrations in SG, intermediate-growing, and FG turkey strains. Only the protein content was significantly (P < 0.05) greater in the intermediate-growing strain. The authors stated that the differences could not be logically explained and have no practical influence on the quality of the breast muscle. For other poultry species, inconclusive results have been presented. Castellini et al. (2006) determined a greater fat concentration and similar protein, ash, and moisture contents in FG chickens, whereas Fanatico et al. (2005) determined only lower moisture in the breast muscle of FG chickens. In duck breast muscles, Baeza et al. (2002) determined lower protein and greater fat concentrations in unselected SG strains. When all these inconclusive results are taken into account, a clear influence of faster growth on the proximate composition of the breast muscles and a real practical influence on the product quality are not apparent (Fernandez et al., 2001).

The lactate concentrations and the CK activities in the slaughter blood of the different turkey strains were analyzed to determine the metabolic state (lactate) and the muscle activity and integrity (lactate, CK) before slaughter. A high activity of CK, a specific muscle enzyme in the blood, indicates disturbances of the muscle cell integrity leading to liberation of the enzyme from the muscle fibers (Apple and Rhodes, 1988; Barton-Gade and Christensen, 1998; Fabrega et al., 2002). Because of the similar blood lactate concentrations in the turkey strains, it could be suggested that the birds showed no differences in their response to preslaughter procedures, although a generally greater activity attributable to loading, transport, and unloading of the birds could be assumed. Fernandez et al. (2001) reported no differences in the muscle lactate content between the SG and FG turkey strains. It could be assumed that, similar to investigations in pigs (Soller et al., 2003), stress increases the muscle activity, accompanied by decreasing muscle pH caused by anaerobic glycolysis and increasing plasma lactate concentrations. Decreasing pH values, for example, because of preslaughter stress (loading, transport, unloading) can result in an altered muscle-to-meat transition and poorer quality of the meat, such as brighter color values (L*a*b*; Rammouz et al., 2004a). Some might suggest that the plasma lactate concentration has to be related to the muscularity of the birds, but we reported in another study that the plasma content of this metabolite is not related to the weight and age of the turkeys (Riegel et al., 2004). However, in contrast to the blood lactate, differences in the CK activities between the strains could indicate pathological alterations of the muscle tissue, especially in the FG strains. Muscle tissue and other organs, such as the heart or brain, release CK, especially when the cell membrane is disturbed by different pathological alterations (Wyss and Kaddurah-Daouk, 2000). Investigations of turkeys (Wilson et al., 1990; Riegel et al., 2004) and of humans (Apple and Rhodes, 1988; Deruisseau et al., 2004) have revealed that the plasma CK activity is positively correlated with the weight of the investigated animals or humans. Considering the muscularity of the different turkey strains (e.g., the breast muscle weight), the CK activities (in U/kg of breast muscle) are similar among nearly all the strains. Only the SG strain Super Mini had significantly lower CK activity values (7.4 U/kg of BW). This difference should not be overestimated because we have no information on the physiological CK activities in the different turkey strains, but assuming comparable physiological values, it could be suggested that the muscle tissue of the Super Mini birds was less affected by the preslaughter conditions.

From the pH values, which were similar early after slaughter (pH20min) but different at the late pH4h, especially with lower values in the BBB and Super Mini strains, a slightly accelerated lactacidosis in the latter turkey strains could be assumed. That this acceleration could have a negative influence on meat quality (e.g., on the drip loss or the brightness) has been reported by several investigators using turkeys and chicken (Owens and Sams, 2000; Van Laack et al., 2000; Le Bihan-Duval et al., 2001; Woelfel et al., 2002; Rammouz et al., 2004a; Fraqueza et al., 2006). In the present study, the variations in the pH4h values were less related to the quality parameters. The pH analysis is more problematic than other methods because the pH electrodes suffer from drift problems because of contamination with fat and muscle tissue or variation of the temperature. Considering this, frequent cleaning and recalibration during long-term investigations are necessary and the temperature of the tissue has to be controlled regularly, because determination of the pH depends on the temperature of the tissue (Karlsson and Rosenvold, 2002). Another problem, if this system were to be used in a plant, is the greater risk of breaking the glass electrode, accompanied by contamination of the meat. A better alternative for predicting meat quality is to determine the EC, because this measurement is less sensitive to disturbances and better related to meat quality failures such as drip loss [r = 0.29 (EC20min); r = 0.30 (EC4h)] and shear force [r = 0.34 (EC4h)].

Another interesting result of the study is the significantly lower shear force in the MPS of the SG birds. The shear force of poultry meat is positively correlated with the sensory attributes hardness/toughness and chewiness (Liu et al., 2004). Hardness/toughness is not a real quality problem in poultry meat in comparison with beef or pork, but the quality trait has to be considered, because in other farm animals such as pigs or cattle, a relationship to the muscle structure, especially the fiber diameter and composition, was estimated (Kirchofer et al., 2002; Gondret et al., 2006), and greater shear force values are related to other negative meat quality traits such as drip loss or redness (Rammouz et al., 2004a). However, the slight differences in the meat quality analysis should not be overestimated. It seems that the turkey strains had nearly identical meat quality traits. The presented results agree with the limited results by Updike et al. (2005), who also found greater shear force values in the FG line and similar pH values immediately and later after slaughter. However, considering the different publications that focus on the comparison of FG and SG poultry species, the meat quality results are quite inconclusive. Fernandez et al. (2001) also compared FG, SG, and crossbred turkeys and found different values between FG and SG turkey strains in some parameters such as brightness (L*) or drip loss. In their investigation, the SG birds had a significant brighter meat color 24 h after slaughter, whereas this difference disappeared 4 and 7 d after slaughter. Another difference was the greater drip loss and shear force of the meat in the SG birds. In broilers, Fanatico et al. (2005) found no significant differences in the brightness (L*), drip loss, and shear force values between the FG and SG strains, except for lower redness (a*) values in the SG birds. Berri et al. (2005) found a greater drip loss and lower late postmortem pH in SG broilers, and brighter and less red breast muscles in the FG birds. Castellini et al. (2006) reported greater brightness (L*) and redness (a*) values in SG chickens in comparison with FG birds that were reared with outdoor access. In Muscovy ducks, Baeza et al. (2002) found no clear differences between a selected FG strain and the control SG duck strain, except for brighter and less red breast muscle in the younger SG birds. A direct comparison of the previously published studies is difficult because the studies differed not only in the poultry species and strains used, but also in the husbandry conditions (e.g., outdoor access) and growing durations and age of the birds, as well as in the time points at which the different meat quality parameters were determined. For example, in the studies by Berri et al. (2005), Fanatico et al. (2005), and Updike et al. (2005), the birds differed in growth properties and age. Castellini et al. (2006) investigated broilers in an organic production system with outdoor access. Fernandez et al. (2001) used not only a commercial line, but also a local line and a crossbreed of these strains. In the present study, the focus was on the standardization of the bird material by using commercial turkey strains with great differences in their growth properties but similar carcass yields that were reared under the same husbandry conditions and slaughtered at the same age in a commercial abattoir to reduce the statistical effects of age, husbandry conditions, or carcass yields. The final analysis of the meat samples and the sample collection in the present study was performed 4 h after slaughter because the analysis and sampling at the abattoir and the transport to the laboratory took several hours. Some might argue that the second analysis and collection time was too early because the full color development is not manifested at 4 h after slaughter but increases for several days after slaughter of the birds (Petracci and Fletcher, 2002; Rammouz et al., 2004a). However, in most publications the color is determined several days before color manifestation. In the present study, the analysis and sampling time of 4 h after slaughter was chosen to prepare the samples for the histological, proximate, and drip loss analyses and to determine the pH, EC, and color values as soon as possible. The sampling time was chosen because the ultimate pH was already reached at this time (Owens and Sams, 2000; Alvarado and Sams, 2004), and in a previous investigation in our laboratory, a good correlation was shown between the brightness (L*) and redness (a*) values determined 4 and 48 h after slaughter (L*: r = 0.37; a*: r = 0.48).

Because high numbers of petechia in MPS are a major quality defect in slaughtered poultry (Kranen et al., 1998), the presented differences between the turkey strains have to be considered. Although until now no comparison has been presented of the incidence of hemorrhages with regard to the growth properties of the turkeys, Kranen et al. (1998) presumed a relationship between the growth intensity in broilers and the number of hemorrhages, which is in contrast to the results presented here for turkeys. Petechia result from the extravasation of blood from the muscle capillaries, and the red color is related to the hemoglobin that leaves the vascular system via intact erythrocytes or via the blood plasma (Kranen et al., 2000). Electrical stunning resulted in a greater number of petechia than gas stunning (Göksoy et al., 1999; Savenije et al., 2002). The high electrical currents that are necessary to anesthetize the birds can lead to muscle contractions and hemorrhaging by rupture of blood vessels and damage to muscle fibers (Savenije et al., 2002). Because the birds in the present study were electrically stunned, an effect of the current on the incidence of hemorrhaging of the SG birds could be assumed. One reason might be the greater resistance of the muscle tissue because of the reduced water content and smaller muscle fiber diameters or a slightly greater number of capillaries that could rupture, although the histological analysis revealed a similar capillary density in the 4 turkey strains. A random effect could be excluded because both SG strains showed a greater number of petechia.

In addition, the FG turkey strains had larger muscle fibers than the SG strains. This result is in agreement with several investigations in turkeys and other poultry species (Wilson et al., 1990; Dransfield and Sosnicki, 1999; Remignon et al., 2000; Baeza et al., 2002) and supports the assumption that growth occurs by an increase in the muscle fiber diameter and not by hyperplasia after the hatching or birth of poultry and mammals (Wilson et al., 1990; Dransfield and Sosnicki, 1999; Rehfeldt et al., 2004). However, the increased growth rates can lead to pathological muscle alterations and meat quality defects (Dransfield and Sosnicki, 1999; Remignon et al., 2000). These negative influences of hypertrophic growth on meat quality could not be shown in the present study and are, as already described, controversial with respect to different studies on poultry meat quality (Maltby et al., 2004). Deep pectoral myopathy, also known as "green muscle disease," is an ischemic necrosis of the deep pectoral muscle (musculus supracoracoideus or pectoralis minor), whereas focal myopathies affect the MPS of the birds (Harper et al., 1983; Siller, 1985; Wilson et al., 1990; Dransfield and Sosnicki, 1999). Because the musculus supracoracoideus was not analyzed histologically in the present study, deep pectoral myopathy could not be clearly excluded, although no macroscopic alterations were detected during preparation and separation of the breast muscles. In the MPS studied, the percentage of degenerated and giant fibers was determined, because different researchers using poultry and mammals reported a relationship between the incidence of these fibers—especially of giant fibers—and meat quality problems or muscle growth (Wilson et al., 1990; Solomon et al., 1991; Fiedler et al., 1999; Remignon et al., 2000; Fazarinc et al., 2002; Rehfeldt et al., 2004). The results presented here suggest that the giant fiber percentage did not differ significantly (P > 0.05) between the FG and SG strains, except for a greater incidence in the Wrolstad strain. This is opposite the results of Wilson et al. (1990), Dransfield and Sosnicki (1999), and Remignon et al. (2000), who reported greater giant fiber percentages in FG poultry species. Because the giant fibers are detected only postmortem and the frequency is related to pathological and degenerative alterations during the muscle-to-meat transition (Fiedler et al., 1999), the nearly similar results of the meat quality parameters and capillary densities in the present study might be the reason for these differences being absent in this study. However, the divergent result in the Wrolstad strain could not be explained. Independent of the fiber diameter and incidence of pathological muscle fibers, it is interesting to note that these strains seem to have no differences in the blood supply of the muscle tissue, as shown by the similar number of capillaries per muscle area. Because the frequency of pathological muscle fibers is related to the blood supply of the tissue and the occurrence of focal ischemic myopathies (Kranen et al., 1998; Dransfield and Sosnicki, 1999), it could be suggested that of the turkey strains investigated, independent of the growth properties, the predisposition to these muscular alterations is similar.

In conclusion, considering different quality parameters such as pH, EC, drip loss, shear force, and hemorrhages, meat of the FG turkey strains Big 6 and BBB did not differ in any major way from the SG lines Wrolstad and Super Mini. The greater BW and the larger muscle fibers of the FG strains had no negative impact on the postmortem muscle-to-meat transition process and the incidence of giant or degenerated fibers or of hemorrhages. The present results are contradictory to the widely held opinion that faster growth in turkeys negatively influences the meat quality.


    ACKNOWLEDGMENTS
 
We thank the Heidemark GmbH (Garrel, Germany) for the husbandry and slaughter of the turkeys. In addition, we thank all the people who participated in the sample collection and analysis.

Received for publication May 10, 2007. Accepted for publication May 11, 2008.


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 MATERIALS AND METHODS
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 DISCUSSION
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