Effects of a Starter Culture on Histamine Reduction, Nitrite

bs_bs_banner Journal of Food Safety ISSN 1745-4565 EFFECTS OF A STARTER CULTURE ON HISTAMINE REDUCTION, NITRITE DEPLETION AND OXIDATIVE STABILITY OF FERMENTED SAUSAGES XINHUI WANG1,3, HONGYANG REN2, WEI WANG1 and ZHEN JIAN XIE1 1Meat-Processing Application Key Lab of Sichuan Province, School of Biological Engineering, Chengdu University, Chengdu 610106, China 2State Key Laboratory of Oil and Gas Reservoir Geology and Exploitation, School of Chemistry and Chemical Engineering, Southwest Petroleum University, Chengdu, China 3Corresponding author. ABSTRACT TEL: +86-15882476156; FAX: 02884616062; A starter culture composed of Pediococcus pentosaceus, Lactobacillus sakei and EMAIL: [email protected] Staphylococcus xylosus isolated from Chinese-fermented sausages was used to manufacture fermented sausages. The effects of the starter culture on histamine Received for Publication April 21, 2015 accumulation, nitrite depletion, lipid oxidation and quality parameters including Accepted for Publication August 4, 2015 pH, water activity and total volatile base nitrogen (TVB-N), as well as the color doi: 10.1111/jfs.12227 and texture properties, were evaluated. The histamine accumulations were 0.32 and 8.85 mg/kg in fermented sausages inoculated with the starter culture and by a spontaneous fermentation, respectively. The levels of residual nitrite were 4.32 and 26.72 mg/kg in fermented sausages inoculated with the starter culture and by a spontaneous fermentation, respectively. The thiobarbituric acid reactive sub- stances test values reached up to 2.64 and 13.92 mg MDA/kg in fermented sausages inoculated with the starter culture and by a spontaneous fermentation, respectively. Additionally, the fermented sausages inoculated with the starter culture showed a stronger acidification and lower (P < 0.05) level of the TVB-N than that of spontaneous fermentation. The starter culture made a great contribu- tion to histamine reduction, nitrite depletion and oxidative stability in fermented sausages and was beneficial to improving hygienic quality and food safety of fermented sausages. PRACTICAL APPLICATIONS High levels of histamine, residual nitrite and lipid oxidation have been described in fermented sausages, which are major problems for public health and food safety. Thus, it is worthwhile to select favorable conditions to strict control histamine accumulation, residual nitrite content and lipid oxidation in fermented sausages. In this study, to meet the requirements of high-quality safe products, a starter culture composed of Pediococcus pentosaceus, Lactobacillus sakei and Staphylococcus xylosus isolated from Chinese-fermented sausages was used to manufacture fermented sausages. The effects of the starter culture on histamine accumulation, nitrite depletion, lipid oxidation and quality parameters including pH, water activity and total volatile base nitrogen (TVB-N), as well as the color and texture properties, were evaluated. These results indicate that addition of the starter culture was beneficial for histamine reduction, nitrite depletion and oxidative stability. Additionally, the batch inoculated with the starter culture showed a stronger acidification and lower level of TVB-N than that of the control. In con- clusion, the starter culture contributes to histamine reduction, nitrite depletion and oxidative stability of traditional fermented sausages. Journal of Food Safety •• (2015) ••–•• © 2015 Wiley Periodicals, Inc. 1 FOOD SAFETY OF FERMENTED SAUSAGES XH. WANG ET AL. INTRODUCTION the shelf life of meat foods. Several studies have reported that certain lactic acid bacteria (LAB), Staphylococcus ssp. Safety and quality are the basic requirements that must be and Pediococcus ssp. could contribute to lipid oxidation always satisfied in food products. High levels of histamine inhibition in fermented sausages (Martuscelli et al. 2000; have been detected in fermented sausages derived from raw Bover-Cid et al. 2001). materials with high protein content (Hu et al. 2007; Lu et al. In the study, a starter culture composed of P. pentosaceus, 2010). The presence of histamine in foods, particularly if L. sakei and S. xylosus isolated from Chinese-fermented sau- associated with tyramine or other biogenic amines, is the sages was used to manufacture fermented sausages. The risk of histamine poisoning, especially for the consumers effects of the starter culture on histamine accumulation, with reduced amine oxidase activity (González-Fernández nitrite depletion and oxidative stability of fermented sau- et al. 2006). In the U.S.A., 187 outbreaks of histamine poi- sages were evaluated. Quality parameters of fermented sau- soning occurred from 2000 to 2006 and 89 outbreaks were sages, namely pH, water activity and total volatile base reported from 1998 to 2008 in Japan (Toda et al. 2009). His- nitrogen (TVB-N), were also described. Additionally, the tamine poisoning is a major problem for public health and color and texture property evaluations of fermented sau- food safety. In recent years, controlling histamine accumula- sages were determined. tion in fermented foods has received increasing interests. It has been reported that inoculation of Pediococcus MATERIALS AND METHODS pentosaceus and Staphylococcus xylosus as starter cultures contributes to biogenic amine reduction in fermented sau- Starter Culture sages (Gardini et al. 2002; Komprda et al. 2004; Pons-Sanche-Cascado et al. 2005). The starter culture composed of P. pentosaceus, L. sakei and At present, the nitrite is still used as necessary curing S. xylosus were used to manufacture fermented sausages. agents in the production of fermented sausages for many These strains were isolated from Chinese-fermented sau- purposes, such as antimicrobial effects, fixing color and sages by Meat-Processing Application Key Lab of Sichuan texture improvement as well as a potent antioxidant (Gill Province in China. and Holley 2003; Honikel 2008). It has been reported that nitrite might react with amines to form nitrosamines that Sausages Formulation and Processing are related to an increasing risk of gastric, esophageal, naso- pharyngeal and bladder cancers (Lundberg et al. 2004). Fermented sausage formulation includes 750 g/kg lean pork Additionally, nitrite can oxidize reduced iron (Fe2+)in meat, 250 g/kg pork back fat, 25 g/kg NaCl, 0.5 g/kg glucose, 3+ hemoglobin to maximum oxidized state (Fe ), resulting in 0.5 g/kg sucrose, 150 mg/kg NaNO2 and 50 mg/kg ascorbic nitrite poisoning. Thus, despite the given advantages, exces- acid. The lean pork meat and pork back fat were ground sive intake of nitrite could induce the risk of cancer and through a 10.0 mm plate. Ground pork was mixed thor- nitrite poisoning. The National Hygiene Standards oughly with other ingredients at 4C for 10 min. The mixture (GB2760-2011) in China set a regulation of a maximum of was maintained at 4C for 24 h and then was divided into two 30 mg/kg nitrite residues in fermented sausages (Wang et al. batches, namely batch A with inoculation of the starter 2013). However, high levels of nitrite in several fermented culture (106 colony-forming unit/g) and batch B without sausages present in Chinese market have been reported addition of starter culture as the control. Each batch was (Gøtterup et al. 2008; Paik and Lee 2014). Recent discover- homogenized and stuffed into natural casings with a diam- ies pointed that Lactobacillus sakei and S. xylosus with nitrite eter of 5 cm. All sausages were placed in constant tempera- reductases contributed to nitrite depletion (Nassua et al. ture and constant humidity box (YTH-225, Yuanyao, China) 2003). under the same environmental conditions during fermenta- Fermented sausages are highly susceptible to lipid oxidation and ripening. Samples were fermented at 22–25C, tion and off-flavor development because of its high fatty 90–95% relative humidity (RH) for 3 days and ripening acid content and low water activity. Lipid oxidation is period was performed at 15–18C, 70–80% RH for 24 days. responsible for rancidity, which is regarded as one of the main causes for functional, sensory and nutritional quality Histamine Measurement deterioration in meat products. To control or minimize lipid oxidation, antioxidants were used to preserve fer- The content of histamine was analyzed by high- mented sausages. Because of the synthetic antioxidants that performance liquid chromatography (HPLC) as described have been found to exhibit various negative human health by Lu et al. (2010). For the histamine analysis of fermented effects, the meat industry is increasingly searching for sausages, 5 g of sample was homogenized in 15 mL of natural solutions to retard oxidative rancidity and extend 0.4 mol/L perchloric acid, incubated at 50C for 20 min and 2 Journal of Food Safety •• (2015) ••–•• © 2015 Wiley Periodicals, Inc. XH. WANG ET AL. FOOD SAFETY OF FERMENTED SAUSAGES centrifuged at 6000× g for 5 min at 4C. Then the superna- described by Cobb et al. (1973). Ten grams of sample was tant was filtered and placed in 50 mL volumetric flask. The homogenized in 90 mL distilled water for 2 min in a stom- remnant was extracted twice with 15 mL of 0.4 mol/L per- acher. Then the solution was centrifuged at 8000× g for chloric acid as described earlier. Finally, the volume of 5 min at 4C. Ten milliliters of supernatant was made of sample extract was adjusted to 50 mL with 0.4 mol/L per- alkaline by adding 10 mL of 10 g/L MgO and distilled for chloric acid for HPLC (Agilent 1100 series, Agilent Tech- 5 min using Kjeldahl distillation unit (Vapordest 30, nologies, Inc., Palo Alto, CA) analysis. Separation was Gerhardt, Germany). The distillate was absorbed by carried out on a Hypersil BDS C18 (4 × 125 mm) column 20 mL g/L boric acid and titrated with 0.02 mol/L HCl. The (Thermo Fisher Scientific, Waltham, MA). The column TVB-N content was expressed as mg N/kg fermented temperature was 40C, and the flow rate was 1.2 mL/min. sausage. The histamine peak was detected at 340 nm with fluores- cence detector. Standard histamine was purchased from Color Measurement and Texture Sigma (San Francisco, CA).

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