Effects of different tomato products on the lipid oxidation, color, and texture of uncured cooked pork sausages in storage

Nana Mikami; Yoshitaka Yamashiro; Shiho Nagaoka; Yuzuki Akamatsu; Hayato Maeda; Kenichiro Shimada

doi:10.3136/fstr.FSTR-D-23-00016

Abstract

Tomato products containing lycopene can improve the quality of meat products during storage. However, few studies have compared the effects of different tomato products, including tomato paste (PAS), tomato powder (POW), and strained tomato, on meat quality. Herein, under two storage conditions (5 days at 37 °C under fluorescent light and 15 days at 4 °C), thiobarbituric acid values associated with lipid oxidation decreased in sausages prepared using all three tomato products compared to control sausages without tomato products. Tomato products also increased the redness of sausages stored at 4 °C. Texture analysis showed that only sausages prepared with POW and PAS exhibited decreased hardness and increased springiness compared to the control on day 10. Tomato products comparably improved the quality of cooked sausages regarding lipid oxidation and discoloration during storage whereas the texture depended on the product type, suggesting the use of tomato products as natural food additives in meat products.

Introduction

The total meat consumption and market values of processed meat have been dramatically increasing worldwide (Fiala, 2008)ⁱ⁾. Meat and meat products are essential for nutrition because they are rich in proteins, fats, vitamins (B complex vitamins), and minerals (iron, zinc, and phosphorus) (Pereira and Vicente, 2013). Various meat products are frequently used in daily meals; therefore, meat quality maintenance is crucial. Meat quality is affected by several factors. Lipid oxidation is a major cause of quality deterioration in processed meat products (Olsen et al., 2005). Moreover, unpleasant tastes and odors, as well as changes in color and rheological properties, are caused by the oxidative deterioration of oils and fats (Addis and Park, 1989). To preserve meat product quality, nitrite and nitrate are added as food additives, and their safety is ensured based on regulations (e.g., Food Sanitation Act, Japan). However, health-conscious consumers prefer additives that will not only improve the quality of meat products but also provide health benefits.

Tomato is a popularly consumed vegetable worldwide and is generally used in the form of pastes, sauces, powders, and concentrates (Bergougnoux, 2014). Tomatoes contain various health-promoting compounds, such as vitamins, minerals, dietary fibers, and non-nutritive phytochemicals (carotenoids and polyphenols) (Chaudhary et al., 2018)ⁱⁱ⁾. In particular, lycopene, a carotenoid mainly responsible for the red color of tomatoes, is highly abundant in tomatoes and their products, as well as in other vegetables and fruits (Omoni and Aluko, 2005). Lycopene exhibits several in vivo and in vitro effects, including anti-oxidative (Hu et al., 2017; Zheng et al., 2019), anti-carcinogenic (Livny et al., 2002; Tang et al., 2005), and anti-atherogenic effects (Kumar et al., 2017; Martin et al., 2000). Furthermore, epidemiological studies have shown that lycopene consumption is associated with a lower risk of human diseases, especially prostate cancer (Chen et al., 2015; Wang et al., 2015).

Lycopene-rich tomato products improve the quality of meat products (Dominguez et al., 2020). Candogan (2002) has reported that the addition of tomato pastes to beef patties reduces lipid oxidation under refrigerated conditions, suggesting the beneficial role of lycopene in tomatoes. Similarly, Østerlie and Lerfall (2005) have also reported that the addition of sundried tomatoes and tomato paste to minced meat reduces rancidity and increases storage stability. Moreover, tomato products increase the redness, hardness, and chewiness of meat, and improve the consumer acceptability of meat products (Candogan, 2002; Deda et al., 2007; Savadkoohi et al., 2014). Thus, various tomato products have considerable positive effects on meat product quality. However, it is unclear how the different types of tomato products affect meat quality. In the present study, we evaluated and compared the effects of three common tomato products (tomato powder, tomato paste, and strained tomato) on the physicochemical properties of cooked pork sausages during storage.

Materials and Methods

Materials　We used minced pork thigh meat purchased from Yamasa Meat Co., Ltd. (Hokkaido, Japan). The pork thigh meat was purchased from Tokachino Pork raised in Nakasatsunai village in Hokkaido (LWD cross-bred pigs, the live weight was approximately 110 kg). Collagen casing (#320, 28–29 mm in diameter; Nippi, Inc., Tokyo, Japan) was obtained to prepare the sausages. Three types of tomato products (Fig. 1) were purchased from Kagome Co., Ltd. (Aichi, Japan). Tomato powder, tomato paste, and strained tomato were approximately eighteen, six, and two times the concentration of raw tomato, respectively. Lycopene contents in tomato powder, tomato paste, and strained tomato were approximately 167, 56, and 26 mg/100 g products (w/w), respectively (Table 1).

Fig. 1.

Appearance of tomato products. (A) tomato powder, (B) tomato paste, and (C) strained tomato.

Table 1 Composition of tomato products.

Proximate composition (per 100 g, w/w)	POW	PAS	STR
Moisture (g)	2.4	70.1	83.8
Protein (g)	15.5	3.9	2.3
Fat (g)	1.6	0–0.6	0
Carbohydrate (g)	71.7	23.3	12.3
Salt equivalent (g)	0.2	0.028–0.222	0–0.2
Lycopene (mg)	167^*	56	26

^* estimated value.

Pork Sausage Manufacturing　We used cooked pork sausage as a model meat product in this study because sausage is commonly consumed around the world and its quality can be evaluated using a homogeneous mixture of fat and minced pork meat. Pork sausages were manufactured at the meat processing plant of the Obihiro University of Agriculture and Veterinary Medicine under strict hygienic conditions. Five batches of sausages were produced using different formulations, with and without tomato products. Briefly, uncured frankfurter pork sausages with four treatments were prepared: control (CON group; tomato product-free), tomato powder (2 % w/w; POW group), tomato paste (5 % w/w; PAS group), and strained tomato (11 % w/w; STR group). We produced model sausages with only salt and lard as controls. We added different types of tomato products containing the same amount of lycopene to the sausages, as shown in Table 2. The 3-mm minced pork meat was mixed with salt (2 % w/w) and lard (20 % w/w) using a food processor (MK-K60-W, Panasonic Corporation, Tokyo, Japan) and was maintained at approximately 4 °C. Then, each tomato product was added based on the weight of the minced meat. The mixture was manually stuffed into collagen casings by a stuffer (DK-9; Ohmichi Sangyo Co., Ltd., Gunma, Japan) and cooked at a core temperature of 63 °C for 30 min in Smokehouse (Ohmichi SUB-800C; Ohmichi Sangyo Co., Ltd.). The cooked sausages were cooled down to 5 °C in Smokehouse and stored in polyethylene bags (Tancho-duru polyethylene bag, HDPE, Hokuryo Chemical Corporation, Hokkaido, Japan) in a refrigerator at 4 °C until the next day (defined as day 0).

Table 2 Composition of tomato product-supplemented pork sausages.

Ingredients (wt %)	CON	POW	PAS	STR
Minced pork meat	100	100	100	100
Lard	20	20	20	20
Salt	2	2	2	2
Tomato powder	-	2	-	-
Tomato paste	-	-	5	-
Strained tomato	-	-	-	11
Estimated lycopene contents (mg/100 g sausage)	-	3.3	2.8	2.9

CON: control sausages; POW: tomato powder-supplemented pork sausages; PAS: tomato paste-supplemented pork sausages; STR: strained tomato-supplemented pork sausages.

Lycopene Analysis　The lycopene fraction was extracted from 10 g of raw sausages supplemented with tomato products with 20 mL of acetone overnight in the dark at room temperature (20–25 °C). The supernatant was obtained by centrifugation for 5 min at 600 × g. The extraction was repeated 5–6 times until the pellet became colorless. The collected supernatant was evaporated and dissolved in acetone (10 mL). Five milliliters of the acetone solution were added to 10 mL of 30 mg/mL pyrogallol-ethanol and mixed. The solution was saponified by adding 1 mL of 600 mg/mL potassium hydroxide and incubating it at 70 °C for 30 min. Then, 20 mL of 10 mg/mL sodium chloride and 12 mL of n-hexane/ethyl acetate (9/1, v/v) were added, and the solution was shaken for 5 min. After centrifugation at 600 × g for 5 min, the supernatant was collected, and the procedure was repeated twice. The collected supernatant was evaporated and dissolved in 10 mL of 1 mg/mL butylhydroxytoluene-ethanol. The sample was applied to a liquid chromatography system composed of ACQUITY UPLC H-Class (Waters, Wilmslow, UK) and ACQUITY UPLC HSS T3 column (1.8 μm, 2.1 mm i.d. × 100 mm; Waters). The ultra-high-performance liquid chromatography (UPLC) mobile phases were solvent A (acetonitrile/methanol/methyl-tert-butyl ether, 70/20/10 v/v) and solvent B (10 mM ammonium acetate). Elution was performed as follows: 0 min, 40 % B; 0–1 min, 25 % B; 4–12 min, 0 % B; and 12–15 min, 2 % B. The flow rate was maintained at 0.5 mL/min at 45 °C. Lycopene was detected at 450 nm, and lycopene content in the sausages was quantified using a standard curve.

Lipid Oxidation　The effect of different tomato products on lipid oxidation in sausages was evaluated using the thiobarbituric acid reactive substances (TBARS) method as described by Jayawardana et al. (2011). TBARS is a commonly utilized indicator of lipid oxidation in foods (Ghani et al., 2017). We measured the thiobarbituric acid (TBA) values of sausages stored under two different conditions: (1) sausages on days 0, 1, 2, 3, and 5 incubated at 37 °C under fluorescent light (approximately 3 310 lx); and (2) sausages on days 0, 5, 10, and 15 refrigerated at 4 °C in the dark.

Color Properties　The color properties of the Committee Internationale de l'Eclairage (CIE) L* (lightness), a* (redness), b* (yellowness), and hue angle (tone of color) of cooked pork sausages with tomato products were evaluated using a Chroma Meter Minolta CM-2600d spectrophotometer (Konica Minolta, Tokyo, Japan) on days 0, 5, 10, and 15 of storage at 4 °C. Prior to the measurements, calibration was performed with a white tile of known reflectance; the light source D₆₅ and the standard observer angle of 10° were used (Mikami et al., 2021).

Texture Properties　The texture properties of cooked pork sausages with tomato products were evaluated using a Texture Analyzer (TA.HDplusC; Stable Micro Systems, Surrey, UK) on the sausages stored at 4 °C (the assessment was limited only to days 0 and 10 because we took priority to the measurement of TBARS and color evaluations during storage in this study). Samples of 1 cm thickness were taken from the central part of the model sausages of each treatment group. Textural properties (hardness, adhesiveness, springiness, gumminess, chewiness, cohesiveness, and elasticity) were calculated by plotting a curve using time and shear force plots when the center of the sample was punctured twice with a cylindrical plunger (5 mm diameter, depression speed = 5 mm/s, up to a depth of 5 mm) at room temperature (20–25 °C).

Statistical Analysis　Data are presented as the means ± standard deviation of 4 or 5 independent experiments (except those of the color analysis on day 15, which were obtained from 3 independent experiments). All data were analyzed using one-way analysis of variance and Tukey's multiple comparison tests with the JMP 13 software (SAS Institute Inc., NC, USA). Statistical significance was set at p < 0.05.

Results and Discussion

Lycopene Content　We referred to the amount of tomato products supplemented in a previous report, which showed the suppressive effect of lipid oxidation (Candogan, 2002) and produced pork sausages supplemented with tomato products (POW; 2 % w/w, PAS; 5 % w/w, STR; 11 % w/w) containing almost equal amounts of lycopene and 15 % lard. Actual lycopene content was determined in the raw sausages using UPLC analysis. The lycopene level was 1.75, 1.30, and 1.23 mg/100 g sausages in the POW, PAS, and STR groups, respectively. There was no significant difference in the lycopene content of the sausages containing the added tomato products, although the content in POW was detected to be slightly higher.

Lipid Oxidation　We evaluated the effect of the different tomato products on TBA values in uncured cooked pork sausages during storage under two specified conditions. In the initial storage period, the values were not different among the four groups under either condition (Fig. 2A and 2B). Under storage at 37 °C with fluorescent light exposure, the values in the CON group were markedly increased on day 1 and continued to increase until day 5 (Fig. 2A). Because light is a factor that accelerates lipid oxidation (Ahmed et al., 2016), the fluorescent light may have contributed to the increase in the TBA values in the CON sausages in our study. In contrast, the TBA values were significantly suppressed in all three tomato groups throughout the storage period compared to those in the CON group (Fig. 2A; p < 0.05), and the magnitude of the effect was not different among the three types of tomato products. Additionally, under storage conditions of 4 °C in the dark, the TBA values rapidly increased in the CON group as the storage days progressed, and significant differences were detected on days 5, 10, and 15 across the three tomato product groups (Fig. 2B, p < 0.05). These results indicate that the tomato products exerted a suppressive effect on lipid oxidation in cooked sausages even under refrigerated storage conditions. Our results were consistent with those reported by other researchers who observed suppression of lipid oxidation by tomato products in meat products during storage (Eyiler and Öztan, 2011; Kim et al., 2013; Østerlie and Lerfall, 2005). Furthermore, previous studies have reported that the lycopene in tomato products suppresses malondialdehydes in meat products (Doménech-Asensi et al., 2013; Sánchez-Escalante et al., 2003). Malondialdehyde is a product of lipid oxidation and likely contributes to oxidative rancidity in meat products (Ghani et al., 2017). Lycopene content in three sausage groups was not statistically different; however, it varied between 1.23 and 1.75 mg/100 g sausages. This variation does not indicate the degree of suppressive effect of lipid oxidation. The effect of lycopene could be attributed to saturated or antioxidant components other than lycopene, such as rutin, prunin, and naringenin (Uto-Kondo et al., 2018).

Fig. 2.

Effects of different types of tomato products on lipid oxidation (thiobarbituric acid [TBA] value) in cooked pork sausages stored at (A) 37 °C with fluorescent light and (B) 4 °C.

TBA values were measured at days 0, 1, 2, 3, and 5 in (A), and days 0, 5, 10, and 15 in (B) of the storage period. Values are expressed as the mean ± standard deviation of four independent experiments (n = 5). Significant differences (p < 0.05) between treatments within a day of storage are denoted by different letters. CON: control group; POW: tomato powder supplemented-sausages; PAS: tomato paste-supplemented sausages; STR: strained tomato-supplemented sausages; MDA: malondialdehyde.

Color Properties　We investigated the effect of tomato products on the color properties of cooked pork sausages during storage at 4 °C. As shown in Fig. 3, the orange color of sausages supplemented with tomato products (POW, PAS, and STR groups) was easily recognizable compared to the meat color of CON sausages both on days 0 and 10 (Fig. 3). The CIE L* (lightness) and a* (redness) color values of tomato groups were lower in L* and higher in a* than those of CON group on day 0, and this trend was maintained until day 15 (Table 3). Although the a* value of the CON sausages gradually decreased during the storage period, supplementation with the three tomato products maintained the meat redness without discoloration. The b* (yellowness) values were significantly higher in the sausages supplemented with tomato products on days 0, 5, and 15, whereas no change was observed among the CON and tomato product groups on day 10. Deda et al. (2007) have reported that frankfurters formulated with tomato paste had higher a* (redness) and b* (yellowness) values and lower L* (lightness) values than control sausages; additionally, the a* value was maintained without discoloration. Another study has reported that lycopene-rich tomato pulp suppresses the discoloration of beef patties (Sánchez-Escalante et al., 2003). Therefore, our results are consistent with these previous findings. In contrast, we did not detect any difference between the three tomato products in terms of color properties in the sausages (Table 3). Although three different types of tomato products were used in this study, the content of lycopene (a red pigment) in the sausages was adjusted to be equal and the L*a*b* values did not differ among the three groups during the study period. Taken together, our results suggest that the degree of L*a*b* value may depend on lycopene content, even if the types of added tomato products were different.

Fig. 3.

Cross-sectional images of different types of tomato product-supplemented sausages stored for 0 and 10 days. CON: control sausages; POW: tomato powders-supplemented sausages; PAS: tomato paste-supplemented sausages; STR: strained tomato-supplemented sausages.

Table 3 Effects of different types of tomato products on instrumental color (Committee Internationale de l'Eclairage lab L*, a*, and b*) in cooked pork sausages during storage at 4°C.

	L*	a*	b*
Day 0
CON	67.19 ± 2.93^a	1.42 ± 0.55^b	10.82 ± 0.62^b
POW	60.00 ± 3.37^b	14.32 ± 2.34^a	21.06 ± 3.38^a
PAS	60.52 ± 3.24^b	13.40 ± 1.96^a	20.47 ± 2.95^a
STR	61.25 ± 2.81^ab	14.14 ± 1.87^a	21.35 ± 1.95^a
Day 5
CON	67.81 ± 1.64^a	0.43 ± 0.30^b	12.14 ± 2.10^b
POW	60.86 ± 2.12^b	12.53 ± 1.84^a	19.67 ± 1.32^a
PAS	60.90 ± 2.03^b	11.89 ± 1.86^a	20.84 ± 3.82^a
STR	60.81 ± 2.47^b	12.83 ± 0.38^a	20.63 ± 3.21^a
Day10
CON	70.25 ± 0.52^a	0.18 ± 0.50^b	11.25 ± 1.00
POW	60.53 ± 1.49^b	12.35 ± 2.28^a	19.90 ± 4.69
PAS	61.97 ± 1.30^b	11.27 ± 1.87^a	18.15 ± 3.26
STR	62.60 ± 0.53^b	11.41 ± 1.65^a	17.82 ± 3.36
Day 15
CON	69.32 ± 0.41^a	−0.16 ± 0.15^b	12.91 ± 0.98^b
POW	59.86 ± 1.16^b	11.22 ± 1.92^a	21.92 ± 2.71^a
PAS	61.16 ± 0.86^b	10.90 ± 2.15^a	22.00 ± 2.61^a
STR	60.75 ± 1.53^b	11.17 ± 0.63^a	22.04 ± 1.35^a

L*, a*, and b* values were measured on days 0, 5, 10, and 15 in storage. The values are expressed as the mean ± standard deviation (n = 10) of three or four independent experiments. Significant differences (p < 0.05) among treatments within a day of storage are denoted by different letters. Each item is as follows: L*, lightness; a*, redness; b*, yellowness. CON: control sausages; POW: tomato powder-supplemented pork sausages; PAS: tomato paste-supplemented pork sausages; STR: strained tomato-supplemented pork sausages.

Texture Properties　To investigate the textural properties of the sausages supplemented with tomato products, we examined seven parameters, namely, hardness, adhesiveness, elasticity, cohesiveness, springiness, gumminess, and chewiness, during storage at 4 °C for 10 days. Differences were observed in hardness, springiness, and gumminess across the CON and tomato product groups but not in the other parameters (Table 4). In terms of hardness, the value for sausages in the PAS group was significantly lower than that for sausages in the CON group on day 0. Furthermore, on day 10, the values for POW and PAS sausages were significantly lower than those for CON sausages. Supplementation with the tomato products tended to soften the texture of the pork sausages during storage, which was especially considerable in the POW and PAS groups. As shown in Table 1, there was a little difference between the composition of three tomato products. Lower moisture and higher fat contents were observed in the sausages of POW and PAS groups than in those of CON and STR groups (moisture contents (%): 50.8, 51.0, 53.1, 54.6, fat contents (%): 30.8, 31.4, 26.6, 26.8, POW, PAS, CON, STR, respectively, data not shown in Fig. and Table). Moisture and fat contents in sausages were shown to be negatively and positively correlated with hardness, respectively (Garcia et al., 2002). However, our results were not consistent with the previous report. Although a decrease of pH also softened the hardness of sausages (Wang et al., 2018), a decrease of hardness was detected in day 0 in the POW and PAS sausages without the decrease of pH (pH: 6.14 ± 0.15, 6.18 ± 0.15 and 6.28 ± 0.21, POW, PAS and CON, respectively). Springiness did not differ among the four sausage groups on day 0 but increased in the POW and PAS groups compared to those in the CON group on day 10. Additionally, gumminess values were lower in PAS (day 0) and POW (day 10) groups than in the CON group. Consistent with our findings, a previous study has also shown that the addition of tomato paste softens the hardness of mortadella (Doménech-Asensi et al., 2013). A previous study has shown that tomato pomace, mainly consisting of tomato seeds and skin, hardens the texture of beef frankfurter owing to the presence of fiber and hydrocolloids (lignin and cellulose) in the tomato pomace (Savadkoohi et al., 2014). In our study, among the tomato products, only STR partly contained tomato skin; however, it did not harden the sausages in the STR group compared to those in the CON group. Although there was no difference in the texture among the three tomato product-supplemented sausages on days 0 and 10, the effect of tomato products on the texture varied depending on the type of tomato product. Hence, tomato powder and tomato paste may potentially be used to modify sausage textures. However, in the present study, the same amount of tomato products was not added to the pork sausages because we mainly focused on the effects of lycopene in tomato products. Therefore, further research is needed to evaluate the effects of tomato products on the textural properties.

Table 4 Effects of different types of tomato products on instrumental textural properties of cooked pork sausages during storage at 4 °C.

	Hardness (N)	Adhesiveness (N s)	Elasticity (s)	Cohesiveness (ratio)	Springiness (cm)	Gumminess (N ratio)	Chewiness (N cm)
Day 0
CON	4.43 ± 0.45^a	−0.03 ± 0.03	0.94 ±	0.57 ± 0.09	1.11 ± 0.15	2.54 ± 0.46^a	2.87 ± 0.86
POW	3.10 ± 0.66^ab	−0.03 ± 0.02	0.97 ±	0.53 ± 0.08	1.25 ± 0.10	1.65 ± 0.42^ab	2.05 ± 0.50
PAS	2.79 ± 1.12^b	−0.01 ± 0.06	0.96 ±	0.50 ± 0.07	1.23 ± 0.14	1.42 ± 0.70^b	1.76 ± 0.97
STR	3.35 ± 1.07^ab	0.03 ± 0.12	0.95 ±	0.52 ± 0.06	1.24 ± 0.10	1.75 ± 0.61^ab	2.16 ± 0.78
Day
CON	4.86 ± 0.44^a	0.06 ± 0.19	0.95 ±	0.60 ± 0.12	1.12 ± 0.04^b	2.97 ± 0.80^a	3.33 ± 0.97
POW	3.09 ± 0.94^b	−0.01 ± 0.04	0.94 ±	0.52 ± 0.13	1.31 ± 0.05^a	1.68 ± 0.77^b	2.13 ± 1.01
PAS	3.06 ± 0.59^b	−0.02 ± 0.01	0.96 ±	0.55 ± 0.09	1.28 ± 0.09^a	1.71 ± 0.48^ab	2.20 ± 0.69
STR	3.33 ± 1.22^ab	−0.03 ± 0.02	0.94 ±	0.55 ± 0.09	1.22 ± 0.09^ab	1.82 ± 0.68^ab	2.20 ± 0.82

Values are expressed as the mean ± standard deviation of five independent experiments (n = 8).

Significant differences (p < 0.05) between treatments within a day of storage are denoted by different letters. CON: control group; POW: tomato powder-supplemented pork sausages; PAS: tomato paste-supplemented pork sausages; STR: strained tomato-supplemented pork sausages.

Conclusion

This study concluded that the supplementation of tomato products suppressed lipid oxidation and provided red color in cooked pork sausages during storage compared with the control. These effects were not significantly different among the three tomato products tested. Tomato powder and tomato paste affected the hardness, springiness, and gumminess of the sausages during storage at 4 °C for 10 days. In addition, the effect of the supplementation on textural properties was slightly different depending on the type of tomato product. Thus, tomato products could be used as natural food additives with variations in pigments, antioxidants, and texture-modifying substances.

Acknowledgements　We would like to thank Editage (www.editage.com) for their assistance with English language editing.

Conflict of interest　There are no conflicts of interest to declare.

References

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