Physico-chemical and microbiological properties of raw fermented

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
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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
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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
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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.
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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
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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).
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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.
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