Effect of Curing Method and Freeze-Thawing on Subsequent Growth of Listeria Monocytogenes on Cold-Smoked Salmon
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1619 Journal of Food Protection, Vol. 75, No. 9, 2012, Pages 1619–1626 doi:10.4315/0362-028X.JFP-11-561 Copyright G, International Association for Food Protection Effect of Curing Method and Freeze-Thawing on Subsequent Growth of Listeria monocytogenes on Cold-Smoked Salmon JIHUN KANG, SILIN TANG, RUI HAI LIU, MARTIN WIEDMANN, KATHRYN J. BOOR, TERESA M. BERGHOLZ, AND SIYUN WANG* Department of Food Science, Cornell University, Ithaca, New York 14853, USA Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/9/1619/1686790/0362-028x_jfp-11-561.pdf by guest on 27 September 2021 MS 11-561: Received 23 December 2011/Accepted 15 April 2012 ABSTRACT The presence of the foodborne pathogen Listeria monocytogenes on cold-smoked salmon is a major concern for the seafood industry. Understanding processing and postprocessing handling factors that affect the ability of this pathogen to grow on cold- smoked salmon is critical for developing effective control strategies. In this study, we investigated the effect of curing method and freeze-thawing of cold-smoked salmon on (i) physicochemical properties and (ii) subsequent growth of genetically diverse strains of L. monocytogenes (inoculated after freeze-thawing) and endogenous lactic acid bacteria. The majority of the measured physicochemical properties were unaffected by freezing and thawing. Overall, wet-cured cold-smoked salmon had higher pH, water activity, and moisture, as well as lower fat, water-phase salt, and phenolic content compared with dry-cured cold-smoked salmon. The curing method and freeze-thawing did not affect growth of endogenous lactic acid bacteria. Freeze-thawing cold- smoked salmon prior to inoculation led to pronounced growth of L. monocytogenes at 7uC. The increase in cell density between days 0 and 30 was significantly (P ~ 0.0078) greater for cold-smoked salmon that was frozen and thawed prior to inoculation compared with nonfrozen cold-smoked salmon. On dry-cured, freeze-thawed cold-smoked salmon, L. monocytogenes had a lag phase ranging from 3.7 ¡ 0.1 to 11.2 ¡ 1.4 days compared with salmon that was wet cured and freeze-thawed, on which L. monocytogenes began to grow within 24 h. Variation in growth among L. monocytogenes strains was also observed, indicating the significance of assessing multiple strains. Further efforts to understand the impact of processing and postprocessing handling steps of cold-smoked salmon on the growth of genetically diverse L. monocytogenes will contribute to improved challenge study designs and data. This, in turn, will likely lead to more reliable and unbiased risk assessments and control measures. Listeria monocytogenes is a bacterial pathogen, which cooking (15). Cold-smoked salmon is produced through a causes a potentially severe foodborne disease that has the series of steps including curing, smoking, trimming, and third highest mortality rate among foodborne infections, vacuum packaging (40). Curing is commonly achieved by killing about 250 people annually in the United States (43). applying dry salt and sugar to the surface of salmon (dry While L. monocytogenes typically contaminates food at low cure) or by submerging salmon into or injecting salmon with levels that are unlikely to cause human disease, it can grow a brine solution (wet cure) (40). After curing, salmon fillets to levels that can lead to disease, during refrigerated storage are smoked at 20 to 30uC for 20 to 30 h. The final product of many ready-to-eat (RTE) foods (18). Consequently, U.S. is typically vacuum packaged, and is stored frozen or regulatory policy specifies zero tolerance (i.e., absence in refrigerated. In the United States, cold-smoked salmon is 25 g) for L. monocytogenes in RTE foods, including RTE distributed frozen or under refrigeration (16). In contrast, seafood. Control of L. monocytogenes represents a consid- cold-smoked salmon is distributed as frozen products in erable challenge for all food processors, as this pathogen is Canada if sealed in package without other means of commonly found in raw materials and in most environments preservation (10), while chilled distribution is the main (15, 37). Of all the U.S. Food and Drug Administration– means of distribution in Europe (7, 30). Among the regulated foods that were recalled because of L. monocy- processing procedures, salting, smoking, and freezing are togenes contamination from 1986 to 2006, seafood had the known to influence the survival and growth of L. highest proportion of recalls (21). monocytogenes (49) on cold-smoked salmon. The effect of L. monocytogenes is of particular concern in cold- freezing stress on the growth of L. monocytogenes has been smoked fish products (37, 41) because the heat applied assessed in cold-smoked salmon; in all cases, L. monocy- during processing is not sufficient to inactivate the togenes was inoculated onto cold-smoked salmon prior to organism, and the products are consumed without further freezing (5, 27, 31, 53). Aside from the effect of freezing on L. monocytogenes, freezing salmon before or after smoking * Author for correspondence. Tel: 607-255-1266; Fax: 607-254-4868; causes structural and chemical changes (39, 44). However, E-mail: [email protected]. there is limited knowledge on the effect of freezing on 1620 KANG ET AL. J. Food Prot., Vol. 75, No. 9 TABLE 1. Listeria monocytogenes strains Strain Common name Ribotype Lineage Serotype Source Reference FSL F2-237 1062D II 1/2a RTE salmon 42 FSL F6-366 H7858 1044A I 4b RTE meat 33 FSL L3-051 1042C I 1/2b RTE salmon 22 FSL X1-001 10403S 1030A II 1/2a Human skin lesion 8 physicochemical properties of cold-smoked salmon and salmon fillets were soaked in brine containing 5% sugar and 40% how the freezing-induced changes in cold-smoked salmon salt for 5 days for wet curing. Both curing methods were carried prior to inoculation affect subsequent growth of L. out at refrigeration temperatures (,4uC). Salmon from both curing methods were cold-smoked at 22uC for 26 h in a convection monocytogenes on cold-smoked salmon. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/9/1619/1686790/0362-028x_jfp-11-561.pdf by guest on 27 September 2021 The presence and potential growth of L. monocytogenes smoking oven. No nitrites or other preservatives except salt and sugar were incorporated into the curing process. Cold-smoked on cold-smoked salmon have been studied, and a complex salmon fillets were vacuum packaged and were transported at 4uC interplay of several physicochemical properties including to our laboratory. To evaluate the effect of freezing prior to pH, water-phase salt (WPS), water activity (aw), phenolic inoculation on subsequent growth potential of L. monocytogenes at content, and storage temperature, as well as the interaction 7uC, a portion of dry-cured and wet-cured cold-smoked salmon between these parameters and growth of lactic acid bacteria fillets was frozen at 220uC, while the rest of the cold-smoked (LAB), is known to have an impact on the growth of this salmon fillets were stored at 4uC for a maximum of 2 days prior to pathogen in vacuum-packed cold-smoked salmon (11, 17, inoculation experiments. 20, 23, 28). However, data on growth characteristics of L. monocytogenes strains representing different genetic back- Physicochemical analysis of cold-smoked salmon. From grounds are limited. It has been observed in a number of each batch of dry- and wet-cured cold-smoked salmon, three studies that different subtypes of L. monocytogenes vary in samples with a weight of approximately 50 g were used for physicochemical analyses. The samples were first homogenized in virulence (36, 52), as well as in ability to grow under a 10-speed blender for 45 s (Osterizer, Sunbeam Products, Inc., adverse conditions (6, 13, 25). Although research has been Boca Raton, FL) and analyzed for aw by using an aw meter (Aqua performed on the growth of different L. monocytogenes Lab Series 3TE, Decagon Devices, Inc., Pullman, WA). For pH strains in food matrices such as RTE frankfurters (38) and measurement, 10 g of salmon homogenate was mixed with 40 ml RTE mayonnaise-based salads (50), variation of growth of deionized water and measured with a pH meter (Accumet AR10, characteristics among different subtypes has not been well Fisher Scientific, Inc., Waltham, MA). The moisture, fat, and total studied in cold-smoked salmon. ash contents were determined with AOAC International methods Understanding the impact of different processing- 950.46, 960.39, and 923.03, respectively. The total phenolic postprocessing handling steps (e.g., freeze-thawing) on compounds were extracted as described previously (1), with some growth of L. monocytogenes and related structural, modifications. In brief, 5 g of salmon homogenate was mixed with chemical, and biological changes in cold-smoked salmon 30 ml of hexane to remove lipids. The sample was then extracted will be crucial for more accurate assessment of growth twice with 50 ml of chilled 80% acetone. The acetone fractions were pooled and evaporated at 45 Cto,1 ml. Phenolic potential of this pathogen on cold-smoked salmon. More- u compounds were dissolved in 70% ethanol to a final volume of over, it will also facilitate better design of challenge studies 10 ml. The extracts were stored at 240uC until further use. The and systematic comparison of L. monocytogenes growth total phenolic content of each extract was determined with the data across studies. Evaluation of multiple strains that method described by Singleton et al. (45) with modifications (14). represent genetic diversity will further allow for estimation In short, the extracts were oxidized with the Folin-Ciocalteu of the range of growth dynamics on cold-smoked salmon. reagent for 6 min, and the reaction was neutralized with sodium Thus, the objectives of this study were (i) to investigate carbonate.