Abstract
There are health concerns with regard to the consumption of sodium. Excessive consumption of sodium is suspected to cause high blood pressure, among other things. Therefore, sodium should be reduced or replaced during the production of food. In the present study, in the first part, raw fermented sausages from pork and turkey meat, produced with reduced NaCl concentrations, were investigated. In a second part, the salts, potassium chloride, magnesium chloride, and calcium chloride were added to the sausages, replacing 50% of NaCl. To elucidate, if the reduction or replacement influences the quality of the sausages, physicochemical and microbiological parameters of the products were analyzed. The data show that a reduction of sodium chloride partly influences the hardness and water activity results of raw fermented sausages, made from pork and turkey meat, the redness and nitrite content of the pork sausages, and the ripening losses and total viable counts of the turkey products. Raw fermented sausages with potassium, magnesium, and calcium as partial substitutes for sodium had differing water activity, pH, hardness, and microbiological results using pork and differing pH, hardness, and microbiological results using turkey meat. A bactericidal effect was observed in raw fermented sausages with calcium chloride in inoculation tests with Listeria monocytogenes due to the pH reduction due to calcium. The results indicate that reduction and replacement of NaCl can influence the final products. Therefore, the producers should carefully evaluate before alteration the NaCl content, if this change influences the product acceptability.
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Introduction
For the production of raw (cured, fermented) sausages, sodium chloride (NaCl) is usually added due to its impact on the sensory and technological properties as well as the microbiological safety of the final products [1, 2]. However, there are health concerns with regard to the consumption of sodium salts. A risk analysis of the World Health Organization (WHO) indicates that a high sodium intake increases the incidence of high blood pressure and is associated with increased occurrence of (lethal) strokes and (fatal) heart diseases [3]. A higher risk of gastric cancer in relation to high salt intake was also shown [4]. Therefore, the WHO recommends that people should not consume more than 2 g sodium per day [3] which is nearly equivalent to 5 g NaCl/day. As raw fermented sausages are frequently consumed, decreasing the salt content in these products might be important with regard to the described health concerns.
In the last years, several studies have been published investigating the effect of a NaCl reduction on the physicochemical, sensory, and microbiological parameters of raw fermented sausages during ripening [5,6,7,8,9,10,11]. For example, Araya-Morice et al. [8] and Hu et al. [10] showed that NaCl reduction resulted in higher water activity (aw) results of the sausages. Lower shear force/hardness results due to the NaCl reduction were shown by Elias et al. [7], Araya-Morice et al. [8], and Hu et al. [11], whereas Corral et al. [5] found lower cohesiveness and chewiness values of NaCl-reduced sausages. After sensory analyses, reduced saltiness/salty taste, hardness perception, and overall quality in NaCl-reduced raw fermented sausages were obtained [5, 6, 8,9,10]. With regard to the microbiology, in some studies, reduction of NaCl in raw fermented sausages did not have an impact on the growth of specific bacteria, e.g., the total viable counts (TVC) or lactic acid bacteria (LAB) during storage of raw fermented sausages [5,6,7, 10]. In general, NaCl reduction influences the physicochemical and sensory parameters depending on the degree of sodium reduction and ripening time of the raw fermented sausages. However, several publications indicate that salt reduction in raw fermented sausages has no clear impact on the shelf life of the products, which is quite difficult to understand. NaCl influences microbial growth directly, as many bacteria species prefer lower salt contents for growth. Beside this, indirect influences due to alteration of the food (matrix) by the NaCl, e.g., the change of the aw values, are also very important, as higher aw values, usually found in NaCl-reduced raw fermented sausages, positively influence the growth of many bacteria species [12]. It could be suggested that the starter culture bacteria (e.g., LAB) in raw fermented sausages representing the primary bacteria species are not positively or negatively influenced by the NaCl alteration and the related impacts on the aw values.
The influence of a (partial) replacement of the sodium by ions like potassium or calcium in raw fermented sausages has also been investigated [5, 13,14,15,16]—for example, the use of potassium seems to reduce the risk of cardiovascular diseases [17]. Gimeno et al. [13] showed that at reduced sodium concentration and increasing potassium, calcium and magnesium content aw values were higher and pH values as well as sensory saltiness and overall acceptability were reduced. The sensory color intensity was higher in the sodium-reduced products, which is supported by the study of Ojangba et al. [15]. The authors found higher redness values of sodium-reduced/potassium-replaced raw fermented sausages. The pH value alteration was mainly due to the addition of magnesium and calcium, as other studies, where sodium was only (partly) replaced by potassium, showed no effect on the pH values [14, 16]. Corral et al. [5] found that (partly) replacing sodium by potassium reduced the instrumental chewiness and cohesiveness results and the sensory aroma, interestingly not the sensory tenderness, taste, and overall quality, whereas Chen et al. [14] found that reduction and replacement of sodium resulted in higher odor and bitter taste and reduced overall acceptability. Qin et al. [16] found a reduced sensory saltiness perception in sodium-reduced/potassium-replaced raw fermented sausages. Chen et al. [14] and Qin et al. [16] found no impact of (partly) sodium replacement by potassium on the TVC or LAB results.
Several studies with NaCl-reduced or sodium-replaced raw fermented sausages using pork and to a lesser extent beef have been published. However, as far as we know, no publications have been published that analyzed in this context, on the one hand, turkey raw fermented sausages, and, on the other hand, physicochemical and microbiological parameters of two different meat species for the production of the raw fermented sausages. Therefore, in the present study, in two independent parts (Study 1, Study 2), the effects of a reduction of the NaCl concentration and the replacement of a part of the sodium with other cations on the physicochemical and microbiological properties of raw fermented sausages, produced with pork ham and turkey breast, were analyzed. To elucidate the impact of a NaCl reduction and partial replacement of NaCl on the microbiological safety of the raw sausages during retail storage, we packaged sliced sausages, inoculated them with different bacteria species and stored these packages for up to 28 days. We considered bacteria species that might contaminate the products, e.g., during slicing and packaging, in pork and turkey food processing companies.
Materials and methods
Materials
For the production of the raw fermented sausages, the ham of hybrid slaughter pigs and the breast muscles (Musculus pectorals) of male turkeys of a fast-growing fattening turkey genetic (Aviagen Turkeys Ltd., United Kingdom) were used. For the production of the pork and turkey sausages, the fat source was always back fat of hybrid slaughter pigs. The hams/backfat were collected from pig slaughterhouses and the breast muscles from turkey slaughterhouses 24 h after slaughter and transported in a refrigerated truck to the Institute for Food Quality and Food Safety. During transport of the living animals to the slaughterhouse, lairage at the slaughterhouse, stunning and slaughter of the animals, all related animal welfare and food hygiene regulations of the European Union and of Germany were considered. Compliance with the regulations was regularly controlled by the German competent authorities. In the institute, the samples were grinded, portioned (ca. 2.5 kg pork and turkey meat, 1.0 kg pork backfat) and frozen at 20 °C until production of the raw fermented sausages 1 week after freezing at the latest.
In the first part of the study (Study 1), in three independent investigations, the frozen stored meat and backfat was thawed in a cold room at 4 °C 24 h before sausage production. The pork raw fermented sausages were produced considering the following principal recipe for the control samples (2.5 N): 70% pork ham, 30% pork back fat, 2.5% NaCl, 125 ppm NaNO2, 0.1% glucose, 0.15% sucrose, starter cultures Lactobacillus sakei, Staphylococcus carnosus, and Pediococcus acidilactici (25 g per 100 g meat); Bactoflavour BFL-F05 and Safe-Pro B-LC-20, Chr. Hansen Holding GmbH, Hoersholm, Denmark). In the NaCl-reduced raw fermented sausages, the concentration of NaCl was decreased to 2.0% (2.0 N) and 1.5% (1.5 N), whereas the other components of the recipe remain the same. The turkey raw fermented sausages were produced in the same way, with the only difference that the turkey breast was used instead of the pork ham. The components were carefully mixed using a cutter. After the mixing, the sausages were filled into R2L-D Naturin casings (Naturin Viscofan GmbH, Weinheim, Germany, thickness/diameter 5.0 cm, length 25 cm), marked with an individual label, and individually weighed to estimate the weight loss during ripening. The sausages were hanged and ripened in a ripening chamber (T1900 619, Fessmann GmbH und Co., Winnenden, Germany) until day 14. The humidity and the air temperature were continuously reduced from 96 to 84% and from 22 to 15 °C, respectively. The air circulation was between 55 and 65 m/s. On days 3, 6, and 11, the sausages were smoked in the same chamber for 10 min at 18 °C to 22 °C. On day 14, the sausages were transferred to a chilling room, hanged and stored until day 35 at 4 °C. On days 7, 14, 21, 28, and 35, from every group, two sausages were randomly collected and weighted for analysis of the ripening loss. The ripening losses were calculated as the percentual reduction of the sausage weights on the collection days in relation to the weight, directly after production. On days 7, 14, 21, 28, and 35, 5 g of each sausage for microbiological analysis of the TVC were removed (10 g in total). All sausages were cut perpendicular to the length of the sausage and pH as well as color values were determined on the inner perpendicular sausage surface. A sample for determination of the hardness was removed on days 7, 14, 21, 28, and 35. Samples for analysis of the concentrations of NaCl were collected on all ripening days and of nitrite on days 0, 21, and 35, homogenized for 1 min at 10,000 rounds per min (rpm, Grindomix GM 200, Retsch GmbH, Haan, Germany) and frozen at − 20 °C until analysis. A part of the homogenate was used for the water activity (aw) analysis (not day 0).
In the second part of the study (Study 2), in three independent investigations, raw fermented sausages were produced, as described in the paragraph above, with the following salt concentration: 2.5% NaCl (2.5 N), 1.5% NaCl (1.5 N), 1.5% NaCl + 1.0% KCl (1.5 N + 1.0 K), 1.5% NaCl + 1.0% MgCl2 (1.5 N + 1.0 Mg), 1.5% NaCl + 1.0% CaCl2 (1.5 N + 1.0 Ca). The samples were only ripened until day 28, and ripening loss, pH, aw, color, and TVC were analyzed on days 0, 14, 28 and hardness values on days 14 and 28. In addition, on all ripening days, the number of lactobacilli were analyzed. On day 28, samples were collected for analysis of fat, protein, and ash concentrations, homogenized for 1 min at 10,000 rpm (Retsch) and frozen at − 20 °C until analysis.
In an additional investigation of the Study 2, the raw sausages, previously ripened until day 28, were cut in slices, inoculated with Brochothrix (Br.) thermosphacta (pig, turkey) Listeria (L.) monocytogenes (pig), and Campylobacter (C.) jejuni (turkey), packed in modified atmosphere packages (MAP, 70% N2, 30% CO2) using a packaging machine T100 (Multivac Sepp Haggenmüller, GmbH & Co. KG) and stored up to day 28 at 4 °C. The MAP were opened on days 0 (day of inoculation and packaging), 14, and 28 and 10 g was removed for the microbiological analysis of the number of the specific bacteria species inoculated.
Methods
Physicochemical parameter
The pH value was determined using a portable pH meter (Portamess®, Knick GmbH, Berlin, Germany) equipped with a glass electrode (InLab 427, Mettler-Toledo, Urdorf, Switzerland) and a temperature sensor. Before measurement, the apparatus was calibrated with pH 4.0 and pH 7.0 standard solutions (Carl Roth GmbH + Co. KG, Karlsruhe, Germany). Each pH measurement was performed at three different points on the sample and the mean of the three measurements was used for statistical analysis.
The color values lightness (L*), redness (a*), and yellowness (b*) were analyzed on the inner sausage surface with a colorimeter (Minolta CR 400®, Konica-Minolta GmbH, Langenhagen, Germany, 2° Standard observer, D65 illuminant, 8 mm measuring field) after calibration of the apparatus with a specific white plate (Y = 84.0, x = 0.3226, y = 0.3392, Konica-Minolta GmbH). Color measurements were repeated at least five times on different points of the sausage slice and the mean of the measurements was used for statistical analysis.
The aw values of the sausage homogenates were determined once with an aw-cryometer (AWK-40, NAGY Messsysteme GmbH, Gäufelden, Germany) after calibration of the apparatus with a solution of 10% NaCl.
For hardness determination, a texture profile analysis (TPA) was performed. Sausages were cut perpendicular to the length of the sausage The samples with a diameter of 5.0 cm and height of 4.0 cm were analyzed using a texture analyzer (TA.XT.plus, Stable Micro Systems, Survey, United Kingdom) equipped with a 50 kg load cell and a round aluminum stamp (50 mm). The stamp moved down with a speed of 3 mm/s until 50% of the sample height was reached. The back speed was also 3 mm/s. The hardness was calculated by the software. The analysis was performed with four cylinder, cut from two sausages per group. The mean value was used for statistical analysis.
The NaCl concentrations of the sausages were determined potentiometrically with the Titro-Line 7800 (SI Analytics GmbH, Mainz, Germany). An amount of 1 g was weighed in a flask and filled up with 50 ml distilled water with a temperature of 40 °C. The solution was homogenized for 1 min at 15,000 rpm and the stator and rotor were then rinsed with distilled water to capture all NaCl residues. For further analysis, the flask was filled up to 75 ml with distilled water and 1 ml 4 mol/l nitric acid was added. 0.1 mol/l silver nitrate solution was titrated into the flask under continuous stirring until the equivalent point was reached. The measurements were performed in triplicates. A standard solution containing 2 g NaCl was also titrated as a control.
Nitrite was measured photometrically (Evolution 201-UV–VIS-Spectrophotometer, Thermo Scientific, Waltham, Massachusetts) according to ISO 6777. An amount of 5 g of the sausage was weighed in a 200 ml flask. 50 ml of distilled water with a temperature of 50–60 °C were added and the solution was homogenized for 1 min at 17,000 rpm and boiled for 15 min. After cooling down to room temperature, each 2 ml of the Carrez clarification solutions I and II (VWR) were added and the solution was filled up with distilled water to 200 ml. After filtration (Folded Filters Grade: 131, Sartorius), 5 ml of the filtrate was pipetted to a tube. After addition of one spoon of the nitrite-test kit (Spectroquant Nitrite Test, Merck KGaA, Darmstadt, Germany) and incubation at room temperature for 10 min, the solution was transferred to a 2.5 ml plastic cuvette and the absorption was measured at 540 nm. The standard solution was prepared with NaNO2 (0.1, 0.5, 1.0, 1.5, 2.0 mg/l). The measurements were performed in triplicates.
The concentrations of ash, fat, and protein in the sausages, ripened for 28 days, were determined with a NIR apparatus (FT-NIR-Spectrometers TANGO, Bruker Corporation, Billerica, MA, USA).
Microbiological parameter
To inoculate the sausage slice, at first the bacteria species Brochothrix thermosphacta (German Collection of Microorganisms and Cell Cultures (DSM) 20171, pork and turkey sausages), Listeria monocytogenes (DSM 20600, pork sausages), and Campylobacter jejuni (DSM 4688, turkey sausages) were used. The bacteria species for the inoculation were transferred to Columbia blood agar with sheep blood (Oxoid GmbH, Wesel, Germany), incubated at 37 °C for 24 h and colonies from the agar were transferred to sterile saline (0.9% NaCl). The solution was adjusted to McFarland turbidity standards of 3.0 using a densimat (BioMérieux SA France IDN 013615, Craponne). The total bacteria number in the solution after McFarland turbidity analysis was always analyzed on the inoculation day, as described below. The bacteria suspension was diluted to achieve an appropriate bacteria concentrations of 106 colony forming unit (cfu)/ml and 100 µl was applied to the perpendicular surface of the sausage. Then the solution was carefully spread with a spatula. The final concentration (fin. conc.) on the sausage was approximately 105 cfu.
For analysis of the TVC and lactobacilli during ripening, from two sausages each, 5 g were removed aseptically and transferred to a plastic bag (Stomacher 400 Strainer Bags, Seward Limited, Worthing, United Kingdom) and diluted 1:10 with a sterile saline solution (1% peptone, 0.85% NaCl, pH 7.0, VWR). The solution was homogenized for 2 min at 230 rpm with a stomacher (Stomacher 400 Circulator, Seward). Serial tenfold dilutions up to 106 were performed using again the sterile saline solution and for TVC analysis, 1 ml of the appropriate dilutions were pipetted into sterile Petri dishes. 12 to 15 ml plate count agar (Oxoid) were added. The agars were incubated for 72 h at 30 °C. For analysis of lactobacilli, 0.1 ml of the appropriate dilutions were pipetted on MRS agar (Oxoid) and distributed on the agar with a sterile spatula. The agars were incubated for 72 h at 25 °C.
An amount of the 10 g of the inoculated sausage surface was aseptically removed after opening of the MAP and transferred to a bag (Stomacher 400 Strainer Bags, Seward). Initial dilution (1:10), homogenization, and preparation of serial tenfold dilutions up to 106 were performed, as described in the TVC section. An amount of 0.1 ml of the appropriate dilutions were pipetted onto the particular agar plate, depending on the bacteria species, and distributed on the agar with a sterile spatula. For analysis of Br. thermosphacta Streptomycin-Inosit-Neutralrot-Agar (SIN) agar (Oxoid), for analysis of L. monocytogenes OCLA agar (Oxoid), and for analysis of C. jejuni CCDA agar (Oxoid) were used. Br. thermosphacta was incubated for 24 h at 25 °C, L. monocytogenes for 24 h at 37 °C and C. jejuni for 24 h at 42 °C using a specific gas combination (5–6% O2, 10% CO2, 84–85% N2).
For analysis of the number of bacteria inoculated on the sausage surface after McFarland turbidity analysis, serial tenfold dilutions up to 107 of the solution were performed using saline solution with peptone (0.85% NaCl and 0.1% peptone). 0.1 ml of the 105, 106, and 107 dilutions were pipetted on the appropriate agar plates and incubated, as presented above. The bacteria concentration was always approximately 108 cfu/ml.
The detection limits in the microbiological investigations were 1.0 log10 cfu/g sausage (TVC) and 2.0 log10 cfu/g sausage (Br. thermosphacta, L. monocytogenes, C. jejuni). If no colony was found on the agar plates with the initial dilution, the half detection limit (0.7 or 1.7 log10 cfu/g sausage) was used for statistical analysis.
Statistical analysis
The data were statistically analyzed using the software SAS Enterprise Guide 7.1 (SAS Institute Inc., North Carolina, USA). The following models were considered:
where Yi is the observation value; μ is the overall mean; Si is the fixed effect of the salt reduction group (1.5% NaCl, 2.0% NaCl, 2.5% NaCl); Ri is the fixed effect of the salt-replacement group (1.5% NaCl, 2.5% NaCl, 1.5% NaCl + 1% KCl, 1.5% NaCl + 1% MgCl2, 1.5% NaCl + 1% CaCl2); εi is the random error.
All data were statistically analyzed using ANOVA, if the data were normally distributed (Kolmogorov–Smirnov test) and variance homogeneous (Levene test). If the F value was significant (p ≤ 0.05), differences between the salt/salt-replacement groups were calculated with the TUKEY post hoc test. Data that were non-normally distributed and/or variance heterogeneous were analyzed using the Kruskal–Wallis test. If the Kruskal–Wallis test showed a p value below 0.05, for individual comparison of the data between the different salt/salt-replacement groups the Kruskal–Wallis test was applied. If the p value was below 0.05, the difference was considered significant.
Results
In the following sections, the results for NaCl reduction (Study 1) and NaCl reduction or NaCl replacement (Study 2) are presented separately, as this makes it easier to discuss the results in relation to these two main topics than a combined result presentation and discussion.
Study 1
Color, pH
The analysis of the physicochemical parameters resulted in no significant effects of the NaCl reduction in pork sausages on all ripening days on the L*, b*, and pH values. The L* values were between 56 and 60, the b* values between 6.0 and 9.2, and the pH values between 5.1 and 5.4 (data not shown). On days 7, 21, and 28, the a* values of the 1.5 N sausages were significantly higher compared to the other NaCl groups. On day 28, the 2.5 N products showed significantly lower a* results than the 2.0 N sausages (Table 1).
The analysis of the physicochemical parameters resulted in no significant effects of the NaCl reduction in turkey raw fermented sausages on the a* and b* values and in few significant effects on the L* and pH results. The a* and b* values were between 6.3 and 7.9 and between 6.2 and 8.5, respectively. L* values were between 57.2 and 62.8. On day 14, 1.5 N sausages had with 62.8 significantly higher L* values than the 2.0 N products (58.4), whereas the lightness results of the 2.5 N sausages (61.1) were comparable with those of the other NaCl groups. The pH values were between 5.2 and 5.4, whereas on day 0, sausages with 2.5% NaCl had with 5.4 significantly higher values than the other sausages that had both comparable pH results of 5.3 on this day of ripening (data not shown).
Ripening loss, a w values
The analysis of the physicochemical parameters resulted in no significant effects of the NaCl reduction in pork sausages on all ripening days on the ripening losses. The ripening losses were between 21.0 and 23.6% on day 7, between 33.5 and 34.2% on day 21, and between 38.2 and 38.9% on day 35 of ripening (data not shown). On days 14, 21, and 28, the aw values of the 1.5 N sausages were significantly higher compared to the 2.5N products. On days 14 and 21, the aw values of the 2.0 N sausages were comparable with the results of the other NaCl groups, whereas on day 28, the values were only comparable with those of the 2.5N products (Fig. 1a).
Mean and SD values of the aw values of pork (a) and turkey raw sausages (b) depending on the NaCl concentration and the ripening day (N = 3); abmean values with different letters on the same ripening day are significantly different (p ≤ 0.05)
The ripening losses of the 1.5 N turkey sausages were significantly higher compared to the raw fermented sausages with 2.5% NaCl on all ripening days, except on day 21. The ripening loss results of the 2.0 N sausages were comparable with the results of the other sausages on days 14, 28, and 35, whereas on day 7, the loss results of the 2.0 N products differed significantly from those of the low NaCl sausage group (Table 1).On nearly all ripening days, except day 28, the turkey sausages with 1.5% NaCl showed significantly higher aw values compared to the 2.5 N products. A significant difference of the aw values was also obtained between the 1.5 N and the 2.0 sausages on days 7 and 35, but not on the other ripening days. On all days, the sausages with 2.5% NaCl and 2.0% NaCl showed comparable aw values (Fig. 1b).
Texture (hardness)
With regard to the texture/hardness analysis on days 14, 28, and 35 for the pork sausages with 1.5% NaCl, significantly lower values could be determined. However, the sausages with 2.0% NaCl showed, on all these ripening days, hardness results, which were comparable with those of the 1.5 N and 2.5 N sausages (Fig. 2a).
Mean and SD values of the hardness values of pork (a) and turkey raw sausages (b) depending on the NaCl concentration and the ripening day (N = 3); abmean values with different letters on the same ripening day are significantly different (p ≤ 0.05)
On all ripening days, turkey sausages with 1.5% and with 2.5% NaCl had significantly lower hardness results, whereas the values of the low NaCl sausages were always lower. Considering the hardness results of the 2.0 N sausages, the values were nearly always comparable with those of the other NaCl groups, except day 21, where the 2.0 N sausages had significantly lower hardness values compared to the high NaCl sausages (Fig. 2b).
NaCl and nitrite
On all ripening days, the NaCl concentrations of the 1.5 N sausages were significantly lower than the results of the other sausages. In addition, the 2.0 N products had significantly lower NaCl contents compared to the 2.5 N products. The nitrite concentrations of the 1.5 N sausages were significantly lower compared to the 2.5 N sausages on days 0 and 35 of ripening, whereas the nitrite results of the 2.0 N products did not differ from the results of the other NaCl groups (Table 1).
Like in the pork sausages, on all ripening days, the NaCl concentrations of the 1.5 N turkey sausages were significantly lower than the results of the other sausages. In addition, the 2.0 N products had significantly lower NaCl contents than the 2.5 N products. The nitrite concentrations of the 1.5 N sausages were significantly lower compared to the 2.0 N and the 2.5 N sausages on day 0 of ripening, whereas the nitrite results of the 2.0 N and the 2.5 N products were comparable (Table 1).
TVC
The analysis of the microbiological parameters resulted in no significant effects of the NaCl reduction of the pork sausages on all ripening day on the TVC results. The values were between 7.6 and 8.4 log10 cfu/g sausages (data not shown).
The microbiological analysis resulted on days 0 and 14 in significant differences between the three NaCl turkey sausage groups. On day 0, the turkey sausages with 1.5% NaCl had significantly higher TVC values than the 2.0 N and 2.5 N products and the TVC results of the sausages with 2.0% NaCl were also significantly higher than the products with 2.5% NaCl. On day 14, the 1.5 N sausages showed significantly higher TVC results compared to the results of both other NaCl groups that had comparable TVC values on this day of ripening (Table 1).
Study 2
Color, pH
The reduction/replacement of the NaCl in the pork raw fermented sausages resulted in no significant effect on all ripening days on the color (L*a*b*) values. The L* results were between 52 and 57, the a* values were between 11.2 and 14.0%, and the b* results were between 6.2 and 8.5. The pH values of the 1.5 N + 1 Ca were significantly lower on days 14 and 28 compared to the products with 1.5% NaCl, 2.5% NaCl, and 1.5% NaCl + 1.0% KCl. The sausages with 1.0% MgCl2 were comparable with all other groups on day 14 and on day 28 with the 1.5 N + 1 Ca sausages (Table 2).
The reduction/replacement of the NaCl in the turkey raw fermented sausages resulted in no significant effect on all ripening days on the color (L*a*b*) values. The L* results were between 57.0 and 63.6, the a* values were between 7.3 and 10.0%, and the b* results were between 6.2 and 8.7 (depending on the ripening day). The pH values of the 1.5 N + 1 Ca turkey sausages on days 0 and 14 were significantly lower compared to the sausages with 1.5% NaCl, 2.5% NaCl, and 1.5% + 1.0% KCl. In addition, the 1.5 N + 1 Mg sausages had significantly lower pH values than the 2.5 N products. On day 28, the 1.5 N + 1 Mg and 1.5 N + 1 Ca sausages showed significantly lower pH values compared to the other sausage groups, which also had comparable pH values (Table 2).
Ripening loss, a w values
The reduction/replacement of the NaCl in the pork raw fermented sausages resulted in no significant effect on all ripening days on the ripening losses, which were between 32.8 and 41.1% (depending on the ripening day) (data not shown). On day 0, the products with 1.5% NaCl had significantly higher aw values than all other sausages. Beside this, the sausages with CaCl2 had significantly higher aw results than the products with MgCl2. On day 14, the sausages with KCl had significantly lower aw values than the products with MgCl2, whereas the sausages of the other groups had comparable aw, also not differing significantly from the 1.5 N + 1 K and 1.5 N + 1 Mg sausages (Table 2).
The reduction/replacement of the NaCl in the turkey raw fermented sausages resulted in no significant effect on all ripening days on the ripening losses and the aw values. The ripening losses were between 33.2 and 40.1% and the aw values were between 0.888 and 0.973 (depending on the ripening day) (data not shown).
Texture (hardness)
The hardness values of the sausages with MgCl2 and CaCl2 were significantly higher compared to the samples with 1.5% NaCl on days 14 and 28. The hardness values of the 2.5 N and 1.5 N + 1 K sausages were comparable with all other groups on day 14 and with the 1.5 N and 1.5 N + 1 Mg sausages on day 28 (Table 2).
The hardness values of the turkey sausages of the 1.5 N + 1 Ca group were significantly higher compared to the sausages with 1.5% NaCl, 2.5% NaCl and 1.5 N + 1 K on day 14 and the sausages with 1.5% NaCl and 2.5% NaCl. In addition, the 1.5 N sausages had significantly lower hardness values than the 1.5 N + 1 Mg and 1.5 N + 1 Ca sausages on day 14 and the 1.5 N + 1 K, 1.5 N + 1 Mg, and 1.5 N + 1 Ca sausages on day 28 (Table 2).
Fat, protein, ash
On day 28, the pork sausages of the different groups had comparable fat, protein, and ash concentrations with values between 31.4 and 33.6%, 25.7 and 27.9%, and 3.7 and 4.9%, respectively (data not shown).
On day 28, the turkey sausages of the different groups had comparable fat, protein, and ash concentrations with values between 28.6 and 32.1%, 24.8 and 27.8%, and 3.9 and 5.4%, respectively (data not shown).
TVC, Lactobacillus spp.
With regard to the microbiological investigations, the TVC results were only affected by the different pork sausage groups on day 14 with significantly higher values in the sausages with 1.5% NaCl compared to the products with 2.5% NaCl, 1.5% NaCl + 1.0% MgCl2, and 1.5% NaCl + 1.0% CaCl2. The sausages with 1.5% NaCl + 1.0% KCl differ significantly from the 1.0 N + 1 Ca products. An effect of the NaCl/replacement group on Lactobacillus spp. could be found on days 0 and 14 of ripening. On day 0, the 1.0 N + 1 Ca sausages had significantly lower values than the products with 1.5% NaCl, 2.5% NaCl, and 1.5% + 1.0% KCl, whereas the sausages with MgCl2 had only significantly lower results compared to the 1.5 N products. On day 14, the 1.0 N + 1 Ca sausages had significantly lower Lactobacillus spp. results than all other sausage groups, which all had comparable results of this bacteria group (Table 2).
With regard to the microbiological investigations, the TVC results in the turkey sausages were only affected by the different groups on day 14. Significantly higher TVC values in the sausages with 1.5% NaCl compared to the products with 1.5% NaCl + 1.0% KCl and 1.5% NaCl + 1.0% CaCl2 were found, whereas the results of the 2.5 N and 1.5 N + 1 Mg sausages were comparable with the results of all other NaCl/replacement groups (Table 2). On day 0, turkey sausages with 1.5% NaCl + 1.0% KCl had significantly higher Lactobacillus spp. results compared to the 1.5 N + 1 Ca sausages, whereas the results of the other sausage groups were comparable with the results of all other NaCl/replacement groups. On day 14, sausages with 1.5% NaCl and 2.5% NaCl had significantly higher Lactobacillus spp. values compared to the 1.5 N + 1 K products. The sausages with 1.5% NaCl + 1.0% MgCl2 and 1.5% NaCl + 1.0% CaCl2 had with the other groups comparable values (Table 2).
Br. thermosphacta, L. monocytogenes, C. jejuni (MAP storage)
During MAP storage of the inoculated pork sausage slices, no effect of the NaCl/replacement group on Br. thermosphacta on all storage days and on L. monocytogenes on days 0 and 28 was found. On day 14, the samples with 1.5% NaCl + 1.0% CaCl2 had significantly lower results of L. monocytogenes compared to the results of all other groups (Figs. 3, 4).
Mean and SD values of the number of Brochothrix thermosphacta on pork raw sausages, inoculated on ripening day 28, during storage in MAP (70% N2, 30% CO2) depending on the NaCl/replacement group concentration (1.5N/2.5 N = 1.5%/2.5% NaCl, 1 Ca = 1.0% CaCl2, 1 K = 1.0% KCl, 1 Mg = 1.0% MgCl2) and the storage day (N = 3)
Mean and SD values of the number of Listeria monocytogenes on pork raw sausages, inoculated on ripening day 28, during storage in MAP (70% N2, 30% CO2) depending on the NaCl/replacement group concentration (1.5 N/2.5 N = 1.5%/2.5% NaCl, 1 Ca = 1.0% CaCl2, 1 K = 1.0% KCl, 1 Mg = 1.0% MgCl2) and the storage day (N = 3); abmean values with different letters on the same ripening day are significantly different (p ≤ 0.05)
During MAP storage of the inoculated turkey sausage slices, no effect of the NaCl/replacement group on Br. thermosphacta and C. jejuni on all storage days was found (Figs. 5, 6).
Mean and SD values of the number of Brochothrix thermosphacta on turkey raw sausages, inoculated on ripening day 28, during storage in MAP (70% N2, 30% CO2) depending on the NaCl/replacement group concentration (1.5 N/2.5 N = 1.5%/2.5% NaCl, 1 Ca = 1.0% CaCl2, 1 K = 1.0% KCl, 1 Mg = 1.0% MgCl2) and the storage day (N = 3)
Mean and SD values of the number of Campylobacter jejuni on turkey raw sausages, inoculated on ripening day 28, during storage in MAP (70% N2, 30% CO2) depending on the NaCl/replacement group concentration (1.5 N/2.5 N = 1.5%/2.5% NaCl, 1 Ca = 1.0% CaCl2, 1 K = 1.0% KCl, 1 Mg = 1.0% MgCl2) and the storage day (N = 3)
Discussion
Study 1
Color, pH
The missing effect of the NaCl reduction on the L* and b* results in the pork sausages and on the L*, a* and b* results in the turkey sausages mainly agrees with the study of Corral et al. [5], Araya-Morice et al. [8], or Hu et al. [11] who compared pork sausages with 2.7 and 2.26% NaCl, 1.5 and 0.5% NaCl, or 2.5 and 1.75% NaCl, respectively. Studies that analyzed the color/appearance sensorically also found no effect of the NaCl alteration [5, 7], whereas Hu et al. [11] found that lower NaCl contents reduce the color perception by the sensory panel. In contrast to our pork sausage results, the studies found no impact of the NaCl reduction on the a* values. As in the present study, this effect was only found on three of six ripening days in pork sausages, it is difficult to explain and should not be overestimated. Interestingly, Hu et al. [11] only found an effect of the salt reduction on the L* values on one of four ripening days. In general, a direct impact of the NaCl on the sausage color could not be expected and therefore the mainly missing effect in the present study is comprehensible. However, although the NaCl alteration influences other physicochemical parameters like the water activity, as shown in the next section, this does not seem to influence the coloration of the product.
The pH results in the present study agree with different other publications that investigate NaCl-reduced raw pork sausages and also found no impact on the pH values [5,6,7,8]. This missing effect of the NaCl reduction is also understandable considering that NaCl has generally no direct pH changing properties. However, Olesen et al. [18] or Hu et al. [9, 10] found lower pH values during ripening in NaCl-reduced sausages explaining this by lower inhibition of the starter culture bacteria accompanied with reduced acidification of the product by, for example, lactic acid. This is comprehensible, but this effect is not seen with more pH and NaCl-tolerant starter culture species, which might be the case in the present and different other studies. For example, Vermeiren et al. [19] showed a high acid and salt tolerance of L. sakei strains, the same bacteria species that was used in the present study.
Ripening loss, a w values
The studies of Aaslyng et al. [6] and Araya-Morice et al. [8] agree with the missing effect of the NaCl reduction in our pork sausages on the ripening losses. The present results indirectly agree with studies that found comparable moisture percentages of normal and NaCl-reduced raw fermented sausages [5, 6]. For example, Olesen et al. found [18] a slight tendency of low salted sausages (1.5% NaCl) to a higher water loss. However, the higher ripening loss in the NaCl-reduced turkey sausages is more comprehensible, as NaCl increases the water-binding properties of the product by changing, for example, the solubility degree of the myofibrillar proteins [12]. The consequence is that water evaporates to a higher extent from the sausages, if the NaCl was reduced. However, why this presumed effect was only shown in the turkey sausages and not in pork sausages in our and other studies is difficult to discuss. Further studies, for example with chicken sausages, are under progress, as the meat species might affect the ripening loss results.
The higher aw values in NaCl-reduced sausages in the present study mainly agree with other publications [8,9,10, 18]. But there are also studies that found indifferent effects of a salt reduction on the aw values. For example, Elias et al. [7] found no significant aw differences of raw fermented sausages with 3.0 and 4.0% NaCl, Araya-Morice et al. [8] found higher aw results in low NaCl sausages at the beginning but not at the end of ripening. Corral et al. [5] also showed the latter results. Independent of these indifferent results, some review publications support our results indicating a negative correlation between NaCl content and aw values [1, 12, 20]. Water activity is defined as the ratio between the vapor pressure of a given food in relation to the vapor pressure of pure water at the same temperature [12]. As NaCl affects the water-binding properties, this should principally reduce the amount of water (or vapor pressure of the sausage) resulting in lower water activity values in sausages with “normal” NaCl concentrations.
Texture (hardness)
The hardness results with lower results in low NaCl sausages mainly agree with other publications [5, 7, 11, 21]. The published results only mainly agree with our results due to the fact that, like in the present study, significant differences in the other investigations were not found on all ripening days and other parameters of the TPA were significantly altered. For example, Corral et al. [5] found comparable hardness but significantly different chewiness and cohesiveness results. Results from sensory analysis also confirm our results. For example, Corral et al. [5] or Hu et al. [9, 11] found that NaCl-reduced sausages had higher juiciness or chewiness/hardness values, respectively. Interestingly, Araya-Morice et al. [8] found no effect of a salt reduction on the TPA and sensory chewiness/hardness values, whereas Elias et al. [7] found, despite a clear effect on the hardness analysis, no difference of the sensory hardness perception. This indicates again that effects of NaCl reduction are very much influenced by factors like the reduction degree or the ripening period. However, generally salt reduction can (negatively) influence the texture of the raw fermented sausages and this effect could be related to the aw values, as higher water activity values and higher water content reduce the firmness of the product.
NaCl, nitrite
The significant differences of the NaCl are as expected and need no further discussion, as we actively added the salt to the raw fermented sausages. The changes of the concentrations are related to the drying and the weight loss of the raw fermented sausages. However, in the present study, the NaCl content was analyzed potentiometrically by measuring the chloride content. We know that this analytical method does not reflect the real sodium content, but the method was also used in different other publications that analyzed NaCl-reduced raw fermented sausages [6,7,8].
With regard to the effect of the NaCl alteration on the nitrite results, the differences in the pork sausages on day 35 of ripening should not be overestimated. However, more interesting are the significant differences of the day 0 nitrite results in pork and turkey raw fermented sausages, as we added in the present study always the same concentration of sodium nitrite (125 ppm NaNO2). It seems that higher NaCl contents initially result in higher nitrite values or lower nitrite reduction and reduced nitrosomyoglobin formation. As far as we know, no comparable studies have been published. In the sausages, nitrite is reduced to nitric oxide which binds to myoglobin, thereby forming nitrosomyoglobin [22, 23]. This process is influenced, for example, by the starter culture bacteria like coagulase negative staphylococci [22], which were also added to the sausages in the present study (Staphylococcus carnosus), or the pH value. A reason for the differing nitrite reduction in the present study might be that higher NaCl contents negatively influence the growth of Staphylococcus carnosus. Müller et al. [24] showed in Brain Heart Infusion broth experiments that growth of Staphylococcus carnosus was influenced by the NaCl (at higher concentrations). The higher TVC results in the NaCl-reduced turkey sausages support this assumption, unfortunately not the pork sausage TVC results. However, an impact of the pH value on the bacteria growth or the nitrite reduction is unlikely, as the pH values were comparable in the different NaCl groups. A direct impact of the NaCl on the method for analysis of nitrite is also unlikely. In the analytical test, the nitrite ion specifically forms a diazonium salt with sulfanilic acid, which reacts with N-(1-naphthyl)-ethylenediamine dihydrochloride to form a red–violet azo dye and this reaction seems to be influenced by chloride [25]. Relating this assumption to the present results, higher chloride values would rather result in lower nitrite values, which is not the case in the present study. Further investigations might be useful to clarify this nitrite effect.
TVC
The TVC results showed quite high standard deviation values, which influenced the significant effects in the present study. As the TVC values mainly represent the number of the added starter culture bacteria species, we should have analyzed LAB as important starter culture bacteria species not only in the Study 2 but also in Study 1. However, the missing effects in the pork sausages agree with regard to the TVC with Elias et al. [7] and with regard to the LAB, although not analyzed in this study, with Aaslyng et al. [6], Elias et al. [7] or Hu et al. [10] indicating that the NaCl reduction does not affect bacterial (mainly LAB) growth. The significant effects in the turkey sausages on days 0 and 14 are difficult to discuss and should not be overestimated. Reale et al. [26] showed that different LAB strains had a good osmotolerance, as they grow similarly at 2, 3, and 4% NaCl in MRS broth. This supports the mainly low impact of the NaCl content in the present and other studies on the TVC results, which is mainly represented by the LAB in the raw fermented sausages at low pH values of around 5.2 in raw fermented sausages [6].
Study 2
Color, pH
The missing effect of the NaCl reduction and replacement by other salts on the color results principally agrees with the studies of Corral et al. [5, 28] or Campagnol et al. [27]. Gimeno et al. [33] found higher L*a*b* values, if NaCl was partly replaced in pork sausages by KCl and CaCl2, whereas Gimeno et al. [29] partly replaced NaCl by increasing concentrations of Ca-Ascorbate and found, depending on Ca-Ascorbat content, inconsistent decreasing L* and increasing a* and b* results. Ojangba et al. [15] replaced NaCl by 25 and 50% KCl and found during ripening up to day 28 comparable L* and b* (except day 0), but higher a* results with 50% NaCl replacement. The published results are not consistent, but a clear effect of a part NaCl replacement by other salts on the sausage color could not be found, insofar a direct color effect is unlikely.
The pH results with regard to the (part) replacement of NaCl by KCl principally agree with several other publications [5, 14, 16, 27, 30]. In contrast to these studies, Corral et al. [28] found a reduction and Guardia et al. [31] and Simsek et al. [32] an increase of the pH values after replacing NaCl with KCl in raw fermented sausages. The data from the present study and other studies indicate that KCl has no clear effect on the pH values. The reduction of the pH values in pork and turkey sausages with CaCl2 and to a lesser extent with MgCl2 agree with other publications [13, 32]. These results indicate a relation of the character of the divalent cations calcium and magnesium and the pH decrease.
Ripening loss, a w values
Other studies also found no impact of the NaCl reduction and/or replacement with KCl on the ripening losses [27, 28, 31]. As far as we know, no studies that partly replaced NaCl with MgCl2 and CaCl2 have been published. The results are comprehensible, also considering that reduction of the NaCl also had no impact on the ripening losses [6, 8].
The aw results partly disagree with regard to the described differences of the 1.5 N and 2.5 N sausages, especially in the turkey products. With regard to the NaCl replacement results, the results of the present study mainly agree with different publications that partly replaced KCl with NaCl [15, 27, 30]. However, other publications found higher aw results after partly replacing NaCl with KCl [28] or with KCl, MgCl2 and CaCl2, [13, 32]. These results disagree with the present study. We found rather lower aw values in pork raw fermented sausages with the salt alternatives. Further studies are necessary, as the water activity has an important impact on the shelf life [31], and therefore it is useful to know, how the replacement affects the water activity values of raw fermented sausages.
Texture (hardness)
The texture (hardness) values of the 1.5 N and 2.5 N pork and turkey raw fermented sausages were not significantly different in the Study 2 compared to the Study 1 and different other publications [5, 7, 11, 21]. However, there was a clear tendency to lower values of the 1.5 N products compared to the 2.5 N products. This discrepancy is difficult to explain. Considering other NaCl alternative results, the published data are quite inconsistent. For example, in some studies with raw fermented sausages, lower hardness values with CaCl2 [21], Ca-Ascorbate [29] or KCl and CaCl2 [33] were found. Similar values with or KCl [5] or KCl and KCl and CaCl2 [21] and higher values with KCl [28] were also found. In some studies, the texture (hardness) was also sensorically analyzed. For example, Guardia et al. [31] found higher hardness values in KCl sausages and other authors found comparable hardness values in sausages with KCl [5, 16, 27, 30]. The higher hardness of the pork and turkey sausages with CaCl2 compared to the 2.5 N products in the present study is difficult to discuss. As the effect was found during ripening in pork and turkey sausages, the results indicate a hardening effect of the CaCl2. This effect of the salt might be due to lower pH values of the calcium-containing sausages. This assumption is principally supported by Rigdon et al. [34] who found in fermented and subsequently cooked beef sausages, higher instrumental and sensory hardness values, if the sausages had a pH of 4.6 compared to 5.0 after fermentation and before cooking.
Fat, protein, ash
The raw nutrient analysis agrees with the data of Corral et al. [5] who found comparable fat and protein contents in raw fermented sausages with KCl, whereas Corral et al. [28] found similar fat but higher protein percentages in products with KCl. Several publications that analyzed the moisture content of raw fermented sausages indirectly support the present results, as they also found comparable results, if NaCl was partly replaced by KCl [5, 16, 28]] or KCl and CaCl2 [33]. Another study found (partly) lower moisture values after replacement of NaCl with KCl [31]. Chen et al. [14] found inconsistent moisture results with comparable results on days 0 and 6 of ripening, lower values of the KCl sausages on day 3, and higher results of these products on day 9 of ripening. Gimeno et al. [13] determined, after partly replacing NaCl with KCl, MgCl2, and CaCl2 on days 3 and 21, comparable moisture values and on days 7 and 15, lower values in the altered raw fermented sausages.
TVC, Lactobacillus spp.
In turkey sausages, no clear effect of the NaCl replacement was found, whereas in pork sausages, the addition of CaCl2 reduced the bacterial numbers during the first parts of the ripening period. However, the effects should not be overestimated, as the differences are quite low and quite inconsistent. In many studies, LAB were analyzed, as these bacteria are the main part of the starter cultures in raw fermented sausages. No clear effect of the NaCl replacement on the LAB number was also shown in other studies [5, 14, 16, 27, 28, 32],. It seems that especially the addition of CaCl2 and its impact on the pH values (Table 2) does not clearly influence the LAB, as they are quite resistant to lower pH values [26].
Br. thermosphacta, L. monocytogenes, C. jejuni (MAP storage)
As far as we know, no studies have been published that analyzed pork and especially turkey raw fermented sausages, in which NaCl is reduced and/or partly replaced with KCl, MgCl2 or CaCl2, during MAP storage. Independent of this, the MAP storage data principally agree with the previously discussed results that salt replacement has no (clear) effect on the LAB growth and the TVC. The single effect of the calcium-containing pork sausages on day 14 of storage on L. monocytogenes should not be overestimated. Considering also studies with other NaCl-reduced/-replaced meat products, the present results agree, for example, with the publications of Fougy et al. [35] or Dos Santos et al. [36]. Fougy et al. [35] found, in raw (not fermented) sausages. NaCl reduced from 2.0 to 1.5% and found no differing TVC results during MAP storage up to day 21. Dos Santos et al. [36] showed that reduction of NaCl from 4 to 2% in dry-cured ham, stored up to day 9, did not influence the bacteria number of L. monocytogenes. Further studies are necessary and under progress, as many reviews indicate that NaCl reduction/replacement might affect the shelf life of meat products like raw fermented sausages [2, 12, 37].
Data availability
All data supporting the findings of this study are available within the paper.
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Acknowledgements
The authors acknowledge all persons participating at the time-consuming experiments and analyses. This research was funded by the Fritz-Ahrberg Foundation, Hannover, Germany.
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Wagner, M., Ploetz, M. & Krischek, C. Impact of the reduction or replacement of NaCl during production and ripening of raw cured pork and turkey sausages. Eur Food Res Technol 250, 2161–2177 (2024). https://doi.org/10.1007/s00217-024-04528-6
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DOI: https://doi.org/10.1007/s00217-024-04528-6