Physico-chemical and microbiological properties of raw fermented sausages are not influenced by color differences of turkey breast meat J. Popp,* C. Krischek,*1 S. Janisch,† M. Wicke,† and G. Klein* *Institute of Food Quality and Food Safety, Foundation University of Veterinary Medicine, D-30173 Hannover, Germany; and †Department of Animal Sciences, Quality of Food of Animal Origin, Georg-August-University Goettingen, D-37075 Goettingen, Germany ABSTRACT It has been suggested that the color of turkey breast meat influences both physico-chemical and microbiological properties of raw fermented sausages. In this study, raw fermented sausages were produced with turkey breast meat in 3 different colors (pale, normal, or dark), which were obtained from 2 fast-growing-genetic-line toms at 2 slaughterhouses. Prior to the sausage production, the breast muscles were sorted into color groups according to the lightness values determined at 24 h postmortem. This meat was subsequently processed to raw fermented sausages using 1.5 or 2.5% curing salt (CS). The pale meat had higher lightness, electrical conductivity, and drip loss, whereas the dark meat showed a darker color only. The physico-chemical (pH, water activity), visual (lightness, redness), and microbial (total plate count) properties of the sausages were not influenced by the color of the turkey breast meat. The sausage made with 2.5% CS had lower aw and higher ash and hardness values than the sausages produced with 1.5% CS. In conclusion, processing of differently colored turkey meat to raw fermented sausages does not influence the quality characteristics of the products. Based on these findings, there is no reason for the sausage producer to separate turkey breast muscles by color before producing raw fermented sausages. Key words: turkey meat, color, raw fermented sausage, physico-chemical property, microbiological characteristic 2013 Poultry Science 92:1366–1375 http://dx.doi.org/10.3382/ps.2012-02724 INTRODUCTION The quality of raw fermented sausage is influenced by various factors such as raw meat quality, cure ingredients, starter cultures, fermentation, and smoking/ ripening conditions (Kijowski and Niewiarowicz, 1978; Ruusunen et al., 2003). Quality and color of the final products are influenced by endogenic factors (e.g., pH, electrical conductivity) of raw meat (Townsend et al., 1980; Honkavaara, 1988). Furthermore, it has been shown that microbiological and biochemical properties in poultry and swine were influenced by their muscle color and endogenic factors (Allen et al., 1998; Fraqueza et al., 2008; Holmer et al., 2009). Because poultry meat can show alterations such as pale, soft, and exudative (PSE) or dark, firm, and dry meat (although rare), the color of raw muscle is closely related with muscle pH, drip loss, and visual appearance, which influence the quality of raw fermented sausages (Barbut, 2009; Owens et al., 2009; Petracci et al., 2009; Werner et al., ©2013 Poultry Science Association Inc. Received August 29, 2012. Accepted January 15, 2013. 1 Corresponding author: [email protected] 2009; Sheard et al., 2012). In raw pork sausage, the use of PSE meat compared with normal meat resulted in lower fat content, less product yield, and more lipid oxidation (Townsend et al., 1980; Honkavaara, 1988). The aim of this study was to evaluate the influence of different turkey meat colors on the quality of raw sausages. MATERIALS AND METHODS Preparation of Raw Meat and Fermented Sausages Breast muscles from turkey toms (mean age: 149 d) of 2 fast-growing genetics (Aviagen Turkeys Ltd., Chester, UK) were collected from 2 commercial slaughterhouses (n = 25 per genetic). Before chilling, the carcasses were randomly removed from the slaughter line and weighed. Thereafter, breast muscles were carefully excised by a trained person and weighed after removal of the skin. Both breast muscles were individually packed and stored in a chilling room. Twenty-four hour postmortem (p.m.), pH, electrical conductivity (EC), and color values of the left breast muscles were measured. Color was determined on the bone surface of the muscle. For the measurement of drip loss, grill 1366 TURKEY MEAT COLOR AND RAW SAUSAGE PROPERTIES yield, and shear force, breast samples were prepared in the following way. The right breast muscle was cut in pieces (approximately 3 × 3 cm), individually packed in plastic bags, vacuumed, and stored at −20°C up to 6 mo until sausage production. The least squares means (LSM) and SD results of all breast muscle L* values, analyzed at 24 h p.m., were considered to sort the meat into dark (LSM − 1 SD, n = 14), normal (LSM, n = 22), and pale color groups (LSM + 1 SD, n = 14). On 4 different days within a 6-mo storage period, raw fermented sausages were produced from the frozen meat, as shown below. On all production days, pale (n = 13), normal (n = 13), and dark raw meat (n = 13) with comparable mean L*24 h p.m. values was used. In each of the experiments, 3 or 4 breast muscles per color group, with a total weight of 5 to 7 kg, were removed from the freezing room shortly before sausage production. In the meat technological unit of the Institute of Food Quality and Food Safety, a raw sausage batter consisting of approximately 69% turkey meat, 29.5% pork backfat, 0.15% glucose, 0.1% dextrose, and 0.05% starter culture mixture (Bactoflavor BFL-F05 and SafePro, Chr. Hansen GmbH, Pohlheim, Germany) was produced. Initially, the appropriate amount of dark, normal, and pale frozen meat and frozen fat were thawed for 15 min. Then the components were minced with a meat grinder (Typ WD 114, Seydelmann GmbH, Stuttgart, Germany) equipped with a 10-mm cutting plate. The minced meat and fat of each color group were separated into 2 equal amounts of batters and individually transferred to a cutter (SL-11, ADE, Hamburg, Germany). After adding glucose, dextrose, and the starter culture mixture, 1.5% curing salt (CS, 99.5% NaCl, 0.5% NaNO2) was added to the first dark, normal, and pale sausage batters, whereas 2.5% CS was added to the second, resulting in initial sodium nitrite concentrations of 75 and 125 mg/kg of NaNO2, respectively. The 6 batters (dark/1.5% CS, dark/2.5% CS, normal/1.5% CS, normal/2.5% CS, pale/1.5% CS, pale/2.5% CS) were then separately homogenized in the cutter for 2 min. Subsequently, the raw sausage batters were filled into artificial (collagen) casings (Naturin R2, 50 mm diameter, Naturin-Viscofan GmbH, Weinheim, Germany). On the production day, all sausages (n = 11 to 19 per color group) were weighed (250 to 300 g) and then ripened in a climate chamber for 28 d (RH decrease from 96 to 84%, temperature from 22 to 15°C, air circulation between 55 and 65 m/s). On d 3, 6, and 11, the sausages were smoked for 10 min at 18 to 22°C. On d 1, 7, 14, 21, and 28, at least 2 sausages per group were weighed and homogenized (Grindomix GM 120, Retsch GmbH, Haan, Germany). The homogenates were either directly used for aw and pH value determination, or frozen in plastic bags (−20°C) for analysis of TBA reactive substances (TBARS) and raw nutrients (only d 14 samples). Prior to the homogenization, samples (10 g) were removed for microbiological analysis. After that the color was determined on the cutting surface of the 1367 sausage. On d 14, one additional sausage was used for texture analysis. Methods Color. The lightness (L*), redness (a*), and yellowness (b*) values of the meat and sausages were evaluated by using a colorimeter (Minolta CR 400, KonicaMinolta GmbH, Langenhagen, Germany) on the medial surface (bone side) of the left breast muscle and the cutting area of the sausage. The surface of the muscle and sausage was exposed to air at room temperature for 30 min before determining the color. Each value was an average of at least 6 (meat) respectively 4 (sausage) measurements. pH Value. The pH values of the meat and sausage were measured by using a portable pH meter (Portamess, Knick GmbH, Berlin, Germany) combined with a glass electrode (InLab 427, Mettler-Toledo, Urdorf, Switzerland). Before measurement, the pH meter was adjusted to the mean temperature of the meat samples (4°C). For the pH determination, the electrode was inserted in the center of the left breast muscle and the homogenates of the sausages. EC. The EC (mS/cm) of the meat was measured with an EC meter equipped with 2 parallel stainless steel electrodes (LF-Star, Matthäus GmbH, Poettmes, Germany). Before the measurement, the EC meter was calibrated with a specific calibration block (10 mS/cm; Matthäus GmbH, Poettmes, Germany). For the EC determination, the electrode was inserted in the center of the left breast muscle. Drip Loss. The right breast muscle was weighed 24 h and 72 h after slaughter, and the drip loss was calculated as the loss of weight and expressed in percent. Between the measurements, the muscle was stored in an individual plastic container at 4°C. Grill Loss. After the drip loss analysis, the breast muscle was weighed and wrapped in aluminum foil before it was grilled in a plate contact grill (Neumärker GmbH, Hemer, Germany) until the core temperature reached 73°C. This process was controlled by inserting the electrode of a digital thermometer (Testo AG, Lenzkirch, Germany) 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 and expressed in percent. Shear Force. The meat 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). At least 5 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 1368 Popp et al. vertical to the fiber direction. The shear velocity was 200 mm/min. Each value (in N) was an average of at least 5 measurements. aw Value. The aw values of the sausages were determined by using the aw-Cryometer AWK 10 (Nagy GmbH, Gaeufelden, Germany). TBARS. The concentrations of TBARS in the sausages were measured photometrically according to Bruna et al. (2001). One gram of the sausage homogenate was minced in 10 mL of trichloroacetic acid (20%) for 2 min. After the addition of 0.5 mL of butylated hydroxytoluene (0.19 M) and centrifugation for 6 min at 3,000 × g (Hermle Z383 K, Hermle GmbH, Wehingen, Germany), the solution was filtered through filter paper (MN 613, Macherey-Nagel GmbH, Dueren, Germany). To 0.7 mL of the filtrate, the same volume of TBA (0.02 M) was added and heated for 30 min at 100°C (LAT GmbH, Garbsen, Germany). After cooling for 10 min, the TBARS concentration was determined at 532 nm (Helios β, Unicam Chromatography GmbH, Kassel, Germany). All experiments were performed in triplicates, and results were expressed as micrograms of malondialdehyde (MDA) per gram of sample. Texture Analysis. The hardness (in N) of the sausages was determined by using a TA.XTPlus Texture Analyzer (Stable Micro Systems, Surrey, UK) with a aluminum stamp (50 mm) connected to a 5-kg block. From each sausage, at least 5 cylinders with a diameter of a 50 mm and a thickness of 20 mm were cut and compressed twice to 50% of their original height. The up- and down speed was 0.8 mm/s. For hardness determination, the computer program Texture Expert, version 1.1G (Stable Micro Systems) was used. Raw Nutrients. The concentrations of protein, fat, ash, and DM in sausages were determined according to the AOAC (1990). The protein concentration was calculated by analyzing the nitrogen concentration of the material (approximately 1 g) using the Kjeldahl method (Vapodest 50s, Gerhardt Laboratory Systems GmbH, Koenigswinter, Germany) and multiplying the result by 6.25. Fat was determined after acid hydrolysis of the material (5 to 10 g) and extraction in a Soxleth equipment (LAT GmbH) by calculating the weight before and after this procedure. The ash concentration was analyzed from the weight difference before and after combustion (600°C, 4 h) of the material (3 to 5 g) in a muffle furnace (Carbolite, LAT GmbH). The DM concentration was calculated from the weight before and after drying the muscle sample (3 to 5 g) in a drying oven (Binder GmbH, Tuttlingen, Germany) at 105°C for 4 h. All experiments were performed in triplicate. Total Bacterial Plate Count. The total bacterial plate count (TPC) of the sausage samples (10 g) was determined on total mesophilic aerobic counts using plate count agar (Oxoid GmbH, Wesel, Germany) at 30°C for 2 d. Counts were expressed as log cfu per gram. Statistical Analysis The data were analyzed with the software Statistica 10.0 (StatSoft, Hamburg, Germany) considering the independent variables color group and curing salt concentration. The Kolmogorov-Smirnov-test was used to ensure the data were normally distributed. These data were analyzed using ANOVA and the Tukey post hoc test. A probability error of 0.05 was taken into account. Differences of the sausage weights as well as the pH, aw, L*, a*, TPC, and TBARS values between d 1, 7, 14, 21, and 28 were calculated with the t-test for dependent measures considering P < 0.05. RESULTS AND DISCUSSION Slaughter Characteristics of the Turkeys Turkey breast yield ranged from 29.6 to 30.8%, which was calculated from the turkey slaughter weight (15.7 to 17.4 kg) and dressed breast weight (4.8 to 5.2 kg). None of those values significantly influenced breast surface colors for dark, normal, and pale (P > 0.05, data not shown), which corresponds to previous reports (Havenstein et al., 2007; Sarica et al., 2009; Werner et al., 2009; Aviagen, 2012). Quality Characteristics of the Turkey Meat Turkey meat of the dark, normal, and pale color groups, used for the production of the sausages, differed significantly (P < 0.05) with regard to the L*, EC, and drip loss results. No significant differences were seen in muscle pH at 20 min and 24 h p.m., color (a*, b*) values at 24 h p.m., grill loss, and shear force after grilling. Pale turkey meat had higher L* and drip loss values (P < 0.05) than normal and dark meat and higher EC results in comparison with the dark meat. The EC values of the normal meat were comparable with the dark and pale samples (Table 1). A general comparison of meat quality data among laboratories is difficult due to differences in sample preparation, instruments, and measurement conditions (Bianchi and Fletcher, 2002). It could only be stated that the presented data and their variation are within the range of already published results about turkey meat quality (Fernandez et al., 2001; Hahn et al., 2001; Updike et al., 2005; Fraqueza et al., 2006; Werner et al., 2008, 2009; Eadmusik et al., 2011; Janisch et al., 2012; Mikulski et al., 2012). The presented differences among the color groups mainly correspond with other publications in turkeys. However, in contrast to the present study, other investigations showed lower pH values at 24 h p.m. in pale meat and higher results in dark meat (McKee et al., 1998; Owens et al., 2000; Fraqueza et al., 2006, 2008). A reason for the discrepancy might be that in the present study the L*24 h p.m. differences between the pale, normal, and dark meat were clearly lower than in these investigations. 1369 TURKEY MEAT COLOR AND RAW SAUSAGE PROPERTIES Table 1. Six different quality parameters (color, pH, electrical conductivity, drip loss, grill loss, and shear force) of turkey breast meats with 3 different colors (dark, normal, pale) Dark (n = 13)1 Item LSM L* 24 h p.m.2 a* 24 h p.m.2 b* 24 h p.m.2 48.50c pH 20 min p.m. pH 24 h p.m. EC3 24 h p.m. Drip loss4 (%) Grill loss5 (%) Maximum shear force6 (kg) 4.70 3.59 6.62 5.66 9.82b 0.96b 22.13 30.26 Normal (n = 13)1 SD LSM 1.62 0.89 1.08 0.21 0.18 2.24 0.50 1.79 9.26 50.93b 5.29 4.45 6.59 5.71 10.17ab 0.97b 22.44 27.75 Pale (n = 13)1 SD LSM SD 0.90 1.02 1.48 0.15 0.09 2.11 0.63 3.07 2.70 53.69a 1.18 1.00 1.02 0.26 0.07 2.46 0.77 2.85 5.12 4.69 4.60 6.60 5.67 11.32a 1.42a 23.05 26.59 a–cValues with different letters in a row differ significantly (P < 0.05). birds/breast muscles used for sausage production are considered. LSM = least squares means. 2Lightness (L*), redness (a*), and yellowness (b*) values of the turkey meat, determined 24 h after slaughter [24 h postmortem (p.m.)] on the bone surface. 3EC = electrical conductivity in mS/cm. 4Drip loss determined between 24 h and 72 h after slaughter (p.m.). 5Grill loss values determined with the drip loss samples. 6Maximal shear force values determined using the grill loss samples. 1The Quality Characteristics of the Turkey Sausages In the present study, the frozen meat used for the production of raw fermented sausages was stored for different periods within the 6 mo. Although frozen meat is commonly used for sausage production and although it was only thawed for a short period (15 min) before the initial mincing, it cannot be excluded that the varying freezing periods affected the color of the meat differently. The consequence might be that the color values after thawing were not related to the L*24 h p.m., considered for the sorting of the meat. Lee et al. (2008) presented color and texture differences between unfrozen and frozen broiler meat, as well as between frozen breast muscles stored for 2, 4, and 6 mo. In pork, Hansen et al. (2004) also found influences of freezing (30 mo) on the lightness values of the meat. However, the study also showed that the L* values of dark and pale pork before and after freezing were related to each other. Although these results indicate that the L*24 h p.m. values are related to the results of the dark, normal, and pale turkey meat after freezing, further investigation is necessary. The initial weight of sausages decreased significantly (P < 0.05) during the ripening period until d 28 (Figure 1), regardless of the color group. But the CS concentration had an impact on the weight results. On d 28, normal-colored sausages with 2.5% CS had higher weights (P < 0.05) in comparison with 1.5% CS (Figure 2). The weight loss of fermented sausage during ripening is common and already reported by others (Townsend et al., 1980; Blom et al., 1996; Muguerza et al., 2002; Ruiz-Capillas et al., 2012) in pork sausages. In contrast to the present data, Townsend et al. (1980) or Honkavaara (1988) showed that PSE pork meat, used for the sausage production, resulted in higher weight losses in comparison with normal meat. However, different colors of turkey breast in this study seemed to have no effect on sausage weight change. The aw of all sausages decreased significantly (P < 0.05) during 28 d of ripening, whereas the pH values were comparable between d 1 and 7 and then increased (P < 0.05) up to d 28 of storage (Figure 1). The aw results were significantly (P < 0.05) influenced by the CS concentration during the 28 d of ripening, except for d 14. The aw were lower in the sausages with 2.5% CS than in the 1.5% CS products. On d 1, 1.5% CS sausages had lower pH values than the 2.5% CS products. Neither the aw nor the pH values differed among the color groups during the entire ripening period (Table 2). The reduction of the aw values was also shown in different other publications with pork sausages and is related to the drying of the sausages during ripening (Townsend et al., 1980; Maijala et al., 1995; Fernández-López et al., 2008; Campagnol et al., 2011; RuizCapillas et al., 2012). Other studies also showed the initial decrease and following increase of the pH values (Maijala et al., 1995; Marco et al., 2006; FernándezLópez et al., 2008; Ercoskun and Oezkal, 2011; RuizCapillas et al., 2012). The decrease of the pH results was caused by the increasing lactate production by the starter culture bacteria, whereas the following pH increase could be explained by the accumulation of nonprotein nitrogen and amino acid catabolism products (Montel et al., 1993; Fernández-López et al., 2008). The effect of higher salt concentrations on the aw values was also shown by Olesen et al. (2004) or Stollewerk et al. (2012). Higher salt content, for example of sodium chloride, increases the polarity and the waterholding properties of the proteins by binding chloride ions (Ruusunen et al., 2003). This reduces the amount of free, unbound water and the related water activity (aw value), as shown in the present study. The influence 1370 Popp et al. Figure 1. General changes of raw fermented turkey sausages during the ripening for 28 d on weight (a), pH/aw (b), lightness (L*)/redness (a*) (c), and total plate count (TPC)/TBA reactive substances (TBARS) (d). Data points with different letters (v–z) between the ripening days differ significantly (P < 0.05). Figure 2. Weight changes (%) of raw fermented turkey sausages during 28 d of ripening after manufacture with 3 different color meats (dark, normal, pale) and 2 varying curing salt (CS) concentrations (1.5%, 2.5%). Columns with different letters (a,b) on the same ripening day differ significantly (P < 0.05). 1371 TURKEY MEAT COLOR AND RAW SAUSAGE PROPERTIES Table 2. Change of aw (water activity) and pH in raw fermented turkey sausages during 28 d of ripening after manufacture with 3 different color meats (dark, normal, pale) and 2 varying curing salt (CS) concentrations (1.5%, 2.5%) Dark (n = 4)1 Normal (n = 4)1 Pale (n = 4)1 P-value2 Item 1.5% CS3 2.5% CS3 1.5% CS 2.5% CS 1.5% CS 2.5% CS CG CC CG × CC aw d 1 0.97a 0.96b 0.97a 0.96b 0.97a 0.96b 0.48 <0.05 0.84 0.80 <0.05 0.55 0.38 0.16 0.46 0.95 <0.05 0.95 0.77 <0.05 0.77 0.78 <0.05 0.76 0.36 0.24 0.69 0.71 0.68 0.90 0.50 0.85 0.83 0.84 0.69 0.94 aw d 7 aw d 14 aw d 21 aw d 28 pH d 1 pH d 7 pH d 14 pH d 21 pH d 28 0.002 0.95a 0.004 0.92 0.019 0.91a 0.011 0.90a 0.004 5.29b 0.05 5.38 0.07 5.44 0.10 5.53 0.10 5.61 0.16 0.005 0.94b 0.006 0.92 0.005 0.90ab 0.011 0.87b 0.019 5.38a 0.15 5.38 0.13 5.44 0.07 5.57 0.19 5.60 0.22 0.004 0.95a 0.004 0.92 0.021 0.91a 0.017 0.90a 0.005 5.26b 0.08 5.35 0.12 5.42 0.09 5.50 0.14 5.57 0.16 0.003 0.94b 0.004 0.92 0.004 0.89b 0.014 0.88b 0.014 5.42a 0.10 5.30 0.11 5.39 0.09 5.46 0.16 5.56 0.22 0.003 0.95a 0.002 0.93 0.006 0.91a 0.022 0.90a 0.007 5.29b 0.11 5.36 0.11 5.42 0.14 5.50 0.13 5.58 0.16 0.002 0.94b 0.003 0.92 0.005 0.89b 0.014 0.88b 0.007 5.45a 0.13 5.26 0.06 5.40 0.04 5.46 0.10 5.50 0.13 a,bValues with different letters in a line differ significantly (P < 0.05). were produced with dark (L* = 48.5), normal (L* = 50.9), and pale turkey meat (L* = 53.7). 2Effects of color group (CG), curing salt concentration (CC), or interaction (CG × CC) are significant if P < 0.05. 3CS = curing salt [0.5% sodium nitrite (NaNO ), 99.5% sodium chloride (NaCl)], 1.5% CS = 15 g of NaCl or 75 mg of NaNO per kg of sausage, 2 2 2.5% CS = 25 g of NaCl or 125 mg of NaNO2 per kg of sausage. 1Sausages of the higher salt concentration on the pH values was also shown by Olesen et al. (2004) or Stollewerk et al. (2012) and is related to the inhibition of the growth or metabolic activity (or both) of the starter culture bacteria (Olesen et al., 2004). This could also be seen in the significant (P < 0.05) or tendency for lower TPC values in the 2.5% CS sausages on d 1, 21, or 28 of ripening in the present study. The L* values of all sausages increased significantly (P < 0.05) between d 1 and 7 followed by a decrease (P < 0.05) up to d 21. The L* results on d 21 and 28 were comparable. The a* values increased significantly (P < 0.05) between d 1 and 28 (Figure 1). With regard to the color group and the curing salt concentrations, no effects of these groups on the L* and a* values of the sausages could be obtained at all ripening days (Table 3). The presented alterations of the L* and a* results during storage of raw fermented sausages were also shown by Acton and Dick (1977), Townsend et al. (1980), Muguerza et al. (2002), Nassu et al. (2003), or Ercoskun and Oezkal (2011). The reduction of the L* and increase of the a* values might be caused by the formation of nitroso-myoglobin, which is related to the characteristic red color of dry fermented sausages (Wirth, 1986). Klettner and Troeger (2000) and Sammet (2004) found no influence of the CS concentration, especially the nitrite concentration, on the color results of raw fermented sausages. Townsend et al. (1980) found no color differences between pork sausages produced with PSE and normal meat. The formation of nitroso-myoglobin in the sausages seemed to eliminate the clear differences of the lightness values of the turkey meat. The TPC values decreased (P < 0.05) between d 7 and 14 and remained on comparable levels during the rest of ripening days. The TPC values on d 1 differed significantly (P < 0.05) from the results determined on d 14, 21, and 28, but not in comparison with d 7 (Figure 1). As shown in Table 4, the TPC results were significantly influenced or had a tendency to be influenced by the CS concentrations only on d 1 (P = 0.08), 21 (P < 0.05), and 28 (P = 0.09). On these days, the sausages with 2.5% CS had lower TPC values. The color group did not influence the TPC results on all storage days. The reduction of the TPC values during advanced storage was also presented by Trevino et al. (1997), Gimeno et al. (1998), Muguerza et al. (2002), Moretti et al. (2004), Lu et al. (2010), or Ercoskun and Oezkal (2011). The marginal influences of the CS on the TPC results might be related to the inhibitory effects of the higher CS content on the growth, metabolic activity, or both of the starter culture bacteria (Olesen et al., 2004), also influenced by the lower aw values in these sausages (Gençcelep et al., 2007). Kuo and Chu (2003) found no differences of the lactic acid bacteria content between PSE and non-PSE pork sausages. The concentrations of TBARS, as an indicator for the degradation of lipids (lipid oxidation), increased significantly (P < 0.05) from d 1 to 7, followed by a decrease (P < 0.05) during further storage of the sausages (Figure 1). However, neither the color of the turkey meat nor the CS concentration had any impact on the 1372 Popp et al. Table 3. Change of lightness (L*) and redness (a*) in raw fermented turkey sausages during 28 d of ripening after manufacture with 3 different color meats (dark, normal, pale) and 2 varying curing salt (CS) concentrations (1.5%, 2.5%) Dark (n = 4)1 Item L* d 1 L* d 7 L* d 14 L* d 21 L* d 28 a* d 1 a* d 7 a* d 14 a* d 21 a* d 28 Normal (n = 4)1 Pale (n = 4)1 1.5% CS3 2.5% CS3 1.5% CS 2.5% CS 1.5% CS 2.5% CS 59.83 4.89 61.36 4.92 58.45 4.31 56.10 2.79 57.56 3.14 6.74 0.62 7.32 0.40 7.52 0.84 8.31 0.89 8.33 0.64 59.05 7.01 60.66 5.52 57.54 6.54 56.69 3.81 57.31 2.73 6.87 0.74 7.43 0.78 7.89 1.31 8.32 0.82 8.83 0.67 60.19 3.61 61.61 3.90 57.77 3.70 57.41 3.00 57.64 3.00 6.75 0.57 7.23 0.92 7.79 0.79 8.02 0.59 8.56 0.38 59.13 2.96 61.43 3.75 58.45 4.31 57.62 2.71 57.86 3.06 6.53 0.70 7.12 0.86 7.93 1.01 8.10 0.46 8.46 0.39 59.51 2.08 60.77 2.93 57.81 2.18 57.33 1.72 56.65 0.28 6.60 0.43 7.38 0.42 7.67 0.48 7.88 0.59 8.17 0.42 59.28 3.28 60.76 1.99 58.86 2.00 57.74 1.41 57.34 2.08 6.01 1.05 7.19 0.67 7.48 0.88 7.92 0.68 8.29 0.33 P-value2 CG CC CG × CC 0.99 0.69 0.98 0.92 0.86 0.98 0.98 0.88 0.88 0.63 0.72 0.99 0.88 0.86 0.95 0.38 0.45 0.60 0.84 0.82 0.91 0.82 0.78 0.83 0.48 0.88 0.99 0.45 0.46 0.58 1Sausages were produced with dark (L* = 48.5), normal (L* = 50.9), and pale turkey meat (L* = 53.7). of color group (CG), curing salt concentration (CC), or interaction (CG × CC) are significant if P < 0.05. 3CS = curing salt [0.5% sodium nitrite (NaNO ), 99.5% sodium chloride (NaCl)], 1.5% CS = 15 g of NaCl or 75 mg of NaNO per kg of sausage, 2 2 2.5% CS = 25 g of NaCl or 125 mg of NaNO2 per kg of sausage. 2Effects Table 4. Change of total plate count (TPC) and TBA reactive substance (TBARS) concentrations in raw fermented turkey sausages during 28 d of ripening after manufacture with 3 different color meats (dark, normal, pale) and 2 varying curing salt (CS) concentrations (1.5%, 2.5%) Dark (n = 4)1 Item TPC4 d 1 TPC d 7 TPC d 14 TPC d 21 TPC d 28 TBARS5 d 1 TBARS d 7 TBARS d 14 TBARS d 21 TBARS d 28 a,bValues Normal (n = 4)1 Pale (n = 4)1 1.5% CS3 2.5% CS3 1.5% CS 2.5% CS 1.5% CS 2.5% CS 8.43 0.42 8.12 0.61 8.37 0.12 7.85ab 0.44 7.97 0.21 0.31 0.09 0.55 0.25 0.37 0.17 0.50 0.39 0.39 0.28 7.88 0.87 8.27 0.66 7.84 0.54 7.28b 0.06 7.32 0.41 0.34 0.04 0.54 0.23 0.40 0.29 0.35 0.18 0.42 0.24 8.30 0.59 8.35 0.83 7.93 0.84 8.11a 0.10 7.74 0.56 0.30 0.08 0.61 0.28 0.31 0.15 0.34 0.14 0.40 0.18 7.83 1.16 8.41 0.67 7.58 1.05 7.53ab 0.29 7.46 0.49 0.34 0.05 0.66 0.35 0.37 0.22 0.47 0.23 0.32 0.19 8.55 0.22 8.68 0.26 7.87 0.83 7.82ab 0.09 7.79 0.44 0.33 0.07 0.55 0.22 0.38 0.26 0.36 0.22 0.38 0.20 7.96 0.72 8.64 0.39 7.39 0.92 7.75ab 0.37 7.69 0.14 0.37 0.19 0.57 0.37 0.55 0.42 0.35 0.22 0.43 0.26 P-value2 CG CC CG × CC 0.87 0.08 0.98 0.36 0.82 0.95 0.56 0.22 0.97 0.24 <0.05 0.21 0.83 0.09 0.49 0.79 0.82 0.40 0.80 0.86 0.98 0.63 0.45 0.86 0.75 0.54 0.78 0.93 0.99 0.84 with different letters in a line differ significantly (P < 0.05). were produced with dark (L* = 48.5), normal (L* = 50.9), and pale turkey meat (L* = 53.7). 2Effects of color group (CG), curing salt concentration (CC), or interaction (CG × CC) are significant if P < 0.05. 3CS = curing salt [0.5% sodium nitrite (NaNO ), 99.5% sodium chloride (NaCl)], 1.5% CS = 15 g of NaCl or 75 mg of NaNO per kg of sausage, 2 2 2.5% CS = 25 g of NaCl or 125 mg of NaNO2 per kg of sausage. 4TPC in log cfu per g of sample. 5TBARS in µg/g of sample. 1Sausages 1373 TURKEY MEAT COLOR AND RAW SAUSAGE PROPERTIES Table 5. Change of DM, proximate concentrations (protein, fat, ash), and hardness in raw fermented turkey sausages during 28 d of ripening after manufacture with 3 different color meats (dark, normal, pale) and 2 varying curing salt (CS) concentrations (1.5%, 2.5%) Dark (n = 4)1 Item DM (%) Protein (%) Fat (%) Ash (%) Hardness (N) Normal (n = 4)1 Pale (n = 4)1 P-value2 1.5% CS3 2.5% CS3 1.5% CS 2.5% CS 1.5% CS 2.5% CS 62.03 1.50 30.13 2.66 28.63 2.83 3.63 0.40 10.94b 3.53 62.13 0.71 29.50 3.21 28.43 2.97 4.50 0.36 17.47ab 4.88 61.23 1.47 29.03 3.10 29.37 3.78 3.53 0.23 10.23b 3.82 62.17 0.85 27.77 3.95 29.90 4.90 4.83 0.32 20.49a 7.10 61.17 1.23 28.47 2.49 29.13 4.38 3.67 0.29 10.14b 3.12 59.70 0.98 27.87 2.31 27.53 3.93 4.47 0.91 18.47ab 3.95 CG CC CG × CC 0.07 0.79 0.23 0.60 0.56 0.98 0.82 0.82 0.89 0.88 <0.05 0.62 0.85 <0.05 0.72 a,bValues with different letters in a line differ significantly (P < 0.05). were produced with dark (L* = 48.5), normal (L* = 50.9), and pale turkey meat (L* = 53.7). 2Effects of color group (CG), curing salt concentration (CC), or interaction (CG × CC) are significant if P < 0.05. 3CS = curing salt [0.5% sodium nitrite (NaNO ), 99.5% sodium chloride (NaCl)], 1.5% CS = 15 g of NaCl or 75 mg of NaNO per kg of sausage, 2 2 2.5% CS = 25 g of NaCl or 125 mg of NaNO2 per kg of sausage. 1Sausages TBARS concentrations on all storage days (Table 4). In pork sausages, TBARS values similarly increased during the first days of storage and decreased later again (Bruna et al., 2001; Nassu et al., 2003; Marco et al., 2006; Olivares et al., 2011). Additionally, Nassu et al. (2003) and Marco et al. (2006) also showed decreasing TBARS values during further storage. A possible reason for this effect is that MDA, interacting within the TBARS reaction with TBA, binds to sausage proteins and no longer interacts with TBA. These bindings of the MDA to proteins have also been presented by Rittié et al. (2002). However, in comparison with the present study, TBARS reduction in pork sausages was observed during a later stage of storage (Nassu et al., 2003; Marco et al., 2006). We also found a TBARS reduction in pork sausages in a later storage period (unpublished data). Other studies found no impact of differing CS concentrations on the TBARS content either (Sammet, 2004; Coutinho de Oliveira et al., 2012). Kuo and Chu (2003) found no differences of the TBARS concentrations between PSE and non-PSE pork sausages. In contrast to the present study, Townsend et al. (1980) found higher TBARS concentrations in PSE pork sausages. However, studies with turkey meat have not been published yet. Both color group and CS concentration had no impact on the DM, protein, and fat content of the turkey sausages, except for the higher ash values in the 2.5% CS products. The same effect was seen with regard to the hardness of the sausages (Table 5). The higher ash content could be explained either by the increasing salt concentrations or by the lower aw values (Stollewerk et al., 2012). However, the lower aw values and associated higher ash contents were not accompanied by higher DM concentrations. In contrast to the present results, lower fat, higher protein, and moisture were found in PSE pork sausages (Townsend et al., 1980; Honkavaara, 1988; Kuo and Chu, 2003). The differences to the PSE pork sausages might be related to the general lower fat and higher protein content in PSE pork meat (Ewan et al., 1979; Oliver et al., 1994). In contrast to this, pale broiler meat had slightly lower protein and comparable fat contents (Qiao et al., 2002), whereas in turkeys color-related raw nutrient results have not been published until now. However, turkey nutrient data from our laboratory support the study in broilers (unpublished data). In conclusion, production of raw fermented sausages from pale, normal, and dark turkey meat has no impact on the physico-chemical and microbiological properties of the products, especially the color or TPC results. There seems to be no practical reason to separate turkey breast muscles by color before producing raw fermented sausages. The curing salt content influenced the water activity and TPC as well as the ash and hardness results. ACKNOWLEDGMENTS This study was funded by the Ahrberg Foundation, Hannover, Germany. The authors gratefully acknowledge Peter Ludewig, Ruth Wigger (Georg-August-University Goettingen, Goettingen, Germany), Dietmar Koeke, Bettina Engel-Abe, Manuela von Ahlen (Foundation University of Veterinary Medicine, Hannover, Germany), and all the people participating the timeconsuming meat collections, sausage production, and analyses. REFERENCES Acton, J. C., and R. L. Dick. 1977. Cured color development during fermented sausage processing. J. Food Sci. 42:895–897. Allen, C. D., D. L. Fletcher, J. K. Northcutt, and S. M. Russell. 1998. The relationship of broiler breast color to meat quality and shelf-life. Poult. Sci. 77:361–366. 1374 Popp et al. AOAC. 1990. Official Methods of Analysis. 15th ed. Assoc. Off. Anal. Chem., Arlington VA. Aviagen. 2012. Big 6 and Big 7 commercial performance goals. Accessed Feb. 19, 2013. http://www.aviagenturkeys.com/gb/products/but.aspx. Barbut, S. 2009. Pale, soft, and exudative poultry meat—Reviewing ways to manage at the processing plant. Poult. Sci. 88:1506– 1512. Bianchi, M., and D. L. Fletcher. 2002. Effects of broiler breast meat thickness and background on color measurements. Poult. Sci. 81:1766–1769. Blom, H., B. F. Hagen, B. O. Pedersen, A. L. Holck, L. Axelsson, and H. Naes. 1996. Accelerated production of dry fermented sausage. Meat Sci. 43(Suppl. 1):229–242. Bratcher, C. L., D. D. Johnson, R. C. Littell, and B. L. Gwartney. 2005. The effects of quality grade, aging, and location within muscle on Warner-Bratzler shear force in beef muscles of locomotion. Meat Sci. 70:279–284. Bruna, J. M., J. A. Ordonez, M. Fernandez, B. Herranz, and L. de la Hoz. 2001. Microbial and physico-chemical changes during the ripening of dry fermented sausages superficially inoculated with or having added an intracellular cell-free extract of Penicillium aurantiogriseum. Meat Sci. 59:87–96. Campagnol, P. C. B., B. A. dos Santos, R. Wagner, N. N. Terra, and M. A. R. Pollonio. 2011. The effect of yeast extract addition on quality of fermented sausages at low NaCl content. Meat Sci. 87:290–298. Coutinho de Oliveira, T. L., S. Malfitano de Carvalho, R. de Arajo Soares, M. A. Andrade, M. G. Cardoso, E. M. Ramos, and R. H. Piccoli. 2012. Antioxidant effects of Satureja montana L. essential oil on TBARS and color of mortadella-type sausages formulated with different levels of sodium nitrite. LWT Food Sci. Technol. 45:204–212. Eadmusik, S., C. Molette, X. Fernandez, and H. Remignon. 2011. Are one early muscle pH and one early temperature measurement sufficient to detect PSE breast meat in turkeys? Br. Poult. Sci. 52:177–188. Ercoskun, H., and S. G. Oezkal. 2011. Kinetics of traditional Turkish sausage quality aspects during fermentation. Food Contr. 22:165–172. Ewan, R. C., D. G. Topel, and K. Ono. 1979. Chemical composition of chops from pale, soft, exudative (PSE) and normal pork loins. J. Food Sci. 44:678–680. Fernandez, X., V. Sante, E. Baeza, E. Le Bihan-Duval, C. Berri, H. Remignon, R. Babile, G. Le Pottier, N. Millet, P. Berge, and T. Astruc. 2001. Post mortem muscle metabolism and meat quality in three genetic types of turkey. Br. Poult. Sci. 42:462–469. Fernández-López, J., E. Sendra, E. Sayas-Barberí, C. Navarro, and J. A. Perez-Alvarez. 2008. Physico-chemical and microbiological profiles of salchicon (Spanish dry-fermented sausage) enriched with orange fiber. Meat Sci. 80:410–417. Fraqueza, M. J., A. S. Cardoso, M. C. Ferreira, and A. S. Barreto. 2006. Incidence of pectoralis major turkey muscles with light and dark color in a Portuguese slaughterhouse. Poult. Sci. 85:1992–2000. Fraqueza, M. J., M. C. Ferreira, and A. S. Barreto. 2008. Spoilage of light (PSE-like) and dark turkey meat under aerobic or modified atmosphere package: Microbial indicators and their relationship with total volatile basic nitrogen. Br. Poult. Sci. 49:12–20. Gençcelep, H., G. Kaban, and M. Kaya. 2007. Effects of starter cultures and nitrite levels on formation of biogenic amines in sucuk. Meat Sci. 77:424–430. Gimeno, O., I. Astiasaran, and J. Bello. 1998. A mixture of potassium, magnesium, and calcium chlorides as a partial replacement of sodium chloride in dry fermented sausages. J. Agric. Food Chem. 46:4372–4375. Hahn, G., M. Malenica, W. D. Muller, E. Taubert, and T. Petrak. 2001. Turkey breast meat—Glycolysis post-mortem and technological properties. Fleischwirtschaft 81:120–122. Hansen, E., D. Juncher, P. Henckel, A. Karlsson, G. Bertelsen, and L. H. Skibsted. 2004. Oxidative stability of chilled pork chops following long term freeze storage. Meat Sci. 68:479–484. Havenstein, G. B., P. R. Ferket, J. L. Grimes, M. A. Qureshi, and K. E. Nestor. 2007. Comparison of the performance of 1966- versus 2003-type turkeys when fed representative 1966 and 2003 turkey diets: growth Rate, liveability, and feed conversion. Poult. Sci. 86:232–240. Holmer, S. F., R. O. McKeith, D. D. Boler, A. C. Dilger, J. M. Eggert, D. B. Petry, F. K. McKeith, K. L. Jones, and J. Killefer. 2009. The effect of pH on shelf-life of pork during aging and simulated retail display. Meat Sci. 82:86–93. Honkavaara, M. 1988. Influence of PSE pork on the quality and economics of cooked, cured ham and fermented dry sausage manufacture. Meat Sci. 24:201–207. Janisch, S., M. Wicke, and C. Krischek. 2012. Mitochondrial respiratory and antioxidative enzyme activities in turkey meat. Animal 6:346–352. Kijowski, J., and A. Niewiarowicz. 1978. Effect of initial pH in broiler breast muscles on gel forming capacity of meat proteins and on rheological characteristics of Frankfurter-type sausage. J. Food Technol. 13:461–468. Klettner, P. G., and K. Troeger. 2000. Technology of processing fermented sausage and cooked sausage with reduced nitrite addition. Fleischwirtschaft 80:82–85. Kuo, C. C., and C. Y. Chu. 2003. Quality characteristics of Chinese sausages made from PSE pork. Meat Sci. 64:441–449. Lee, Y., A. Saha, R. Xiong, C. Owens, and J. Meullenet. 2008. Changes in broiler breast fillet tenderness, water-holding capacity, and color attributes during long-term frozen storage. J. Food Sci. 73:E162–E168. Lu, S., X. Xu, G. Zhou, Z. Zhu, Y. Meng, and Y. Sun. 2010. Effect of starter cultures on microbial ecosystem and biogenic amines in fermented sausage. Food Contr. 21:444–449. Maijala, R., S. Eerola, S. Lievonen, P. Hill, and T. Hirvi. 1995. Formation of biogenic amines during ripening of dry sausages as affected by starter culture and thawing time of raw materials. J. Food Sci. 60:1187–1190. Marco, A., J. L. Navarro, and M. Flores. 2006. The influence of nitrite and nitrate on microbial, chemical and sensory parameters of slow dry fermented sausage. Meat Sci. 73:660–673. McKee, S. R., B. M. Hargis, and A. R. Sams. 1998. Pale, soft, and exudative meat in turkeys treated with succinylcholine. Poult. Sci. 77:356–360. Mikulski, D., J. Jankowski, Z. Zdunczyk, J. Juskiewicz, and B. Slominski. 2012. The effect of different dietary levels of rapeseed meal on growth performance, carcass traits, and meat quality in turkeys. Poult. Sci. 91:215–223. Montel, M. C., R. Talon, J. L. Berdague, and M. Cantonnet. 1993. Effects of starter cultures on the biochemical characteristics of French dry sausages. Meat Sci. 35:229–240. Moretti, V. M., G. Madonia, C. Diaferia, T. Mentasti, M. A. Paleari, S. Panseri, G. Pirone, and G. Gandini. 2004. Chemical and microbiological parameters and sensory attributes of a typical Sicilian salami ripened in different conditions. Meat Sci. 66:845–854. Muguerza, E., G. Fista, D. Ansorena, I. Astiasaran, and J. G. Bloukas. 2002. Effect of fat level and partial replacement of pork backfat with olive oil on processing and quality characteristics of fermented sausages. Meat Sci. 61:397–404. Nassu, R. T., L. A. G. Goncalves, M. A. A. P. da Silva, and F. J. Beserra. 2003. Oxidative stability of fermented goat meat sausage with different levels of natural antioxidant. Meat Sci. 63:43–49. Olesen, P. T., A. S. Meyer, and L. H. Stahnke. 2004. Generation of flavour compounds in fermented sausages—The influence of curing ingredients, Staphylococcus starter culture and ripening time. Meat Sci. 66:675–687. Olivares, A., J. L. Navarro, and M. Flores. 2011. Effect of fat content on aroma generation during processing of dry fermented sausages. Meat Sci. 87:264–273. Oliver, M. A., P. Gou, M. Gispert, A. Diestre, J. Arnau, J. L. Noguera, and A. Blasco. 1994. Comparison of 5 types of pig crosses. 2. Fresh meat quality and sensory characteristics of drycured ham. Livest. Prod. Sci. 40:179–185. Owens, C. M., C. Z. Alvarado, and A. R. Sams. 2009. Research developments in pale, soft, and exudative turkey meat in North America. Poult. Sci. 88:1513–1517. Owens, C. M., E. M. Hirschler, S. McKee, R. Martinez-Dawson, and A. R. Sams. 2000. The characterization and incidence of pale, TURKEY MEAT COLOR AND RAW SAUSAGE PROPERTIES soft, exudative turkey meat in a commercial plant. Poult. Sci. 79:553–558. Petracci, M., M. Bianchi, and C. Cavani. 2009. The European perspective on pale, soft, exudative conditions in poultry. Poult. Sci. 88:1518–1523. Qiao, M., D. L. Fletcher, J. K. Northcutt, and D. P. Smith. 2002. The relationship between raw broiler breast meat color and composition. Poult. Sci. 81:422–427. Rittié, L., J. C. Monboisse, M. C. Gorisse, and P. Gillery. 2002. Malondialdehyde binding to proteins dramatically alters fibroblast functions. J. Cell. Physiol. 191:227–236. Ruiz-Capillas, C., M. Triki, A. M. Herrero, L. Rodriguez-Salas, and F. Jimenez-Colmenero. 2012. Konjac gel as pork backfat replacer in dry fermented sausages: Processing and quality characteristics. Meat Sci. 92:144–150. Ruusunen, M., J. Vainionpaa, E. Puolanne, M. Lyly, L. Lahteenmaki, M. Niemisto, and R. Ahvenainen. 2003. Physical and sensory properties of low-salt phosphate-free frankfurters composed with various ingredients. Meat Sci. 63:9–16. Sammet, K. 2004. Assessment of the anti-oxidative potential of dietary supplemented alpha-tocopherol in nitrite reduced salami type sausages. PhD Thesis. Foundation University of Veterinary Medicine, Hannover, Germany. Sarica, M., N. Ocak, N. Karacay, U. Yamak, C. Kop, and A. Altop. 2009. Growth, slaughter and gastrointestinal tract traits of three turkey genotypes under barn and free-range housing systems. Br. Poult. Sci. 50:487–494. 1375 Sheard, P. R., S. I. Hughes, and M. H. Jaspal. 2012. Colour, pH and weight changes of PSE, normal and DFD breast fillets from British broilers treated with a phosphate-free, low salt marinade. Br. Poult. Sci. 53:57–65. Stollewerk, K., A. Jofre, J. Comaposada, J. Arnau, and M. Garriga. 2012. The effect of NaCl-free processing and high pressure on the fate of Listeria monocytogenes and Salmonella on sliced smoked dry-cured ham. Meat Sci. 90:472–477. Townsend, W. E., C. E. Davis, C. E. Lyon, and S. E. Mescher. 1980. Effect of pork quality on some chemical, physical, and processing properties of fermented dry sausage. J. Food Sci. 45:622–626. Trevino, E., D. Beil, and H. Steinhart. 1997. Formation of biogenic amines during the maturity process of raw meat products, for example of cervelat sausage. Food Chem. 60:521–526. Updike, M. S., H. N. Zerby, J. C. Sawdy, M. S. Lilburn, G. Kaletunc, and M. P. Wick. 2005. Turkey breast meat functionality differences among turkeys selected for body weight and/or breast yield. Meat Sci. 71:706–712. Werner, C., S. Janisch, U. Kuembet, and M. Wicke. 2009. Comparative study of the quality of broiler and turkey meat. Br. Poult. Sci. 50:318–324. Werner, C., J. Riegel, and M. Wicke. 2008. Slaughter performance of four different turkey strains, with special focus on the muscle fiber structure and the meat quality of the breast muscle. Poult. Sci. 87:1849–1859. Wirth, F. 1986. Curing: Color formation and color retention in frankfurter-type sausages. Fleischwirtschaft 66:354–358.
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