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Food Microbiology 30 (2012) 427e431

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Food Microbiology

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Thermal inactivation of Escherichia coli O157:H7 and Salmonella on catfishand tilapiaq

Kathleen T. Rajkowski*

Food Safety and Intervention Technologies Research Unit, Eastern Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, 600 East Mermaid Lane,Wyndmoor, PA 19038, USA

a r t i c l e i n f o

Article history:Received 22 September 2011Received in revised form22 November 2011Accepted 21 December 2011Available online 17 January 2012

Keywords:FinfishCatfishTilapiaEscherichia coli O157:H7SalmonellaThermal D-valuesZ-values

q Mention of trade names or commercial products ithe purpose of providing specific information and doeor endorsement by the U.S. Department of Agricultutunity provider and employer.* Tel.: þ1 215 233 6440; fax: þ1 215 233 6406.

E-mail address: Kathleen.rajkowski@ars.usda.gov.

0740-0020/$ e see front matter Published by Elseviedoi:10.1016/j.fm.2011.12.019

a b s t r a c t

Thermal inactivation kinetics of individual cocktails of Escherichia coli O157:H7, or of Salmonella meatisolates or seafood isolates were determined in catfish and tilapia. Determinations were done at 55, 60and 65 �C using a circulating-water bath and calculated using linear regression analysis. Salmonellaseafood and meat isolates D-10 values on the finfish were the same and ranged from 425 to 450, 27.1 to51.4, 2.04e3.8 s (z ¼ 4.3 �C) at 55, 60 and 65 �C, respectively. The E. coli O157:H7 D-10 values ranged from422 to 564, 45.2 to 55.5 and 3.3e4.2 s (z ¼ 4.3 �C) at 55, 60 and 65� C, respectively. The only statisticaldifference (P � 0.05) was found when comparing the D-10 values for E. coli O157:H7 at 55 �C on catfishand tilapia. The other D-10 values for the Salmonella at all temperatures and E. coli O157:H7 at 60 and65 �C on the catfish or tilapia showed no statistical difference. D-10 values for the catfish and tilapiawere significantly lower than the reported values in other food systems, but the z-values were withinthe literature reported range. These D-10 values can be used to determine cooking parameters of finfish.

Published by Elsevier Ltd.

1. Introduction

Globally fish consumption reached 115.1 million tonnes in 2008(17 kg/person) which can vary from 1 to 100 kg per capitadepending on geographical area and can even vary within theindividual country (FAO, 2007). Aquaculture contributed an esti-mated 50% of the available fish consumed and for some countriesthis can mean an increase of imported fish (Greenlees et al., 1998).Since 2001 aquaculture production has increased at an averageannual growth rate of 6.2% and in the United States fisheriesproduction averages about 10% for the aquaculture products (FAO,2007). Consumption of fish products has remained at about23 kg/capita (1996e2006) in North America.

Fish, as defined in Section 21 of the United States’ Code ofFederal Register part 123.3 (d), “means fresh or saltwater finfish,crustaceans, other forms of aquatic animal life (including, but notlimited to, alligator, frog, aquatic turtle, jellyfish, sea cucumber, andsea urchin and the roe of such animals) other than birds or

n this publication is solely fors not imply recommendationre. USDA is an equal oppor-

r Ltd.

mammals, and all mollusks, where such animal life is intended forhuman consumption” (CFR, 2008). Another term used to describefish is seafood which is divided into three categories: finfish,crustacean (shrimp) and mollusk (shellfish).

When the United States General Accounting Office (GAO) issueda report on the seafood safety program in 2004, they stated that80% of the consumed seafood (finfish, crustaceans and mollusk)was imported and that eating contaminated seafood resulted inabout 15% of the reported food borne outbreaks in the U.S. which “isa greater percent than either meat or poultry even through meatand poultry are consumed at 8 and 6 times the rate of seafood,respectively” (GAO, 2004). In 2006 the U.S. Center for DiseaseControl classified food vehicles implicated in outbreaks into 17 foodcommodities and determined that fish (47 outbreaks) was associ-ated with most outbreaks (CDC, 2009).

Bacterial pathogens were listed as the cause of the seafood-related illnesses (GAO, 2004).

In particular Salmonella can contaminate seafood fromharvest toconsumption and is the major cause of seafood-associated bacterialoutbreaks in the EU (EFSA, 2010), in the US (CSPI, 2009) and in othercountries worldwide. The United States Food and Drug Adminis-tration tested 11,312 imported and 768 domestic seafood samplesfrom 1990 to 1998 (GAO, 2004). They reported that overall 7.2% forimported and 1.3% for domestic seafoodwerepositive for Salmonella

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431428

and the Salmonella isolated were species identified from bothdomestic and imported fish and shellfish (Heinitz et al., 2000).Amagliani et al. (2011) reported that Salmonella contaminated fishand fish products are responsible for 1.4% of the outbreaks in the EU.

In their review of food borne microbial pathogens of seafoodaquaculture, Greenlees et al. (1998) identified Escherichia coli andSalmonella as inhabitants in pond water, whereas, E. coli wasisolated only from finfish harvested from those ponds (Greenleeset al., 1998; GAO, 2004). Andrews et al. (1977) surveyed retailfresh and frozen channel catfish (Ictalurus punctatus) for Salmonella.They isolated Salmonella from the samples and reported that thenumber of positive samples from the farm-raised catfish wereseasonal with a 0.9% incidence for JanuaryeMarch versus 5.7% forJulyeSeptember (Andrews et al., 1977). Huss et al. (2000)reviewed the hazards of consuming seafood (finfish and mollusk)and identified both Salmonella and E. coli O157:H7 as pathogenicbacterial contamination on seafood. In a survey of sushi (rawsalmon) sold frozen at retail and raw at sushi bars Salmonella andE. coli were isolated from the raw finfish used in sushi preparationand that the prevalence of E. coliwas higher in the fresh fish than inthe frozen fish (Atanassova et al., 2008). In their epidemiologicalreview of seafood-associated infections in the U.S., Iwamoto et al.(2010) reported that from 1973 to 2006 there were 10 outbreaksdue to salmonellosis, As more reports on the pathogenic contami-nation of raw finfish become available, there will be increasedemphasis on proper handling and cooking of seafood.

The three different types of seafood (finfish, crustacean andmollusk) would require different cooking parameters. In the FDAFood Code (2009), the cooking parameters for retail establishmentgives different time/temperatures for the seafood types (fish, crus-tacean,mollusk) and state a cooking time forfish of 15 s at 63 �C (FDA,2009). In the NACMCF’s (2008) report and Doyle and Mazzotta’s(2000) review, thermal inactivation data for the individual humanbacterial pathogens on seafood, particularly finfish, is lacking. Thisstudy was conducted to determine the thermal inactivation ofSalmonella and E. coliO157:H7 inoculated on fresh catfish and tilapia.

2. Materials and methods

2.1. Microorganisms

E. coli O157:H7 933, A9218-C1 and 45753.35 and Salmonellaenteritidis Enteritidis 13076, Senftenberg 8400, and Typhimurium14028 (meat isolates) were obtained from the Eastern RegionalResearch Center’s culture collection. Salmonella Schwarzengrund19535, Panama 19545, Bahrenfeld 19489 and Weltevreden 19493were obtained from the U.S. Food and Drug Administration and areseafood isolates (Zhao et al., 2006). Working stock cultures of eachstrain were maintained in brain-heart infusion broth (Becton,Dickinson and Co., Sparks, MD) and stored at 4 �C.

2.2. Inoculation preparation

The day before the procedure the isolates, either Salmonellameat,Salmonella seafood or E. coli O157:H7 for the individual cocktail weregrown separately overnight at 37 �C in tryptic soy broth (TSB, Becton,Dickinson and Co) to obtain an 18 h culture. The cocktail was madeby combining 5 ml of each overnight culture and centrifuging at3600 � g for 10 min (Sorvall Legend� RT centrifuge, Kendro Labo-ratory Products, Newtown, CT). The pellet was re-suspended inButterfield’s phosphate buffer (BPB-6.8 pH; Hardy Diagnostics, SantaMaria, CA) to the original cocktail volume. Three different cocktails,E. coli - meat, Salmonella e meat and Salmonella e seafood, wereprepared. The cell density of the cocktail was determined by serialdilution in 0.1% peptone water (PW, Becton, Dickinson and Co.) and

plating in duplicate on tryptic soy agar (TSA, Becton, Dickinson andCo.) The cocktail (107�9 CFU/ml) was used immediately to inoculatethe fish and discarded.

2.3. Sample preparation

Two finfish types were used to represent a high fat fish (catfishe 7.6% total lipid, 79.1%water and 15.2% protein/100 g) and a low fatfish (tilapia e 1.7% total lipid, 78.1% water and 20.1% protein/100 g)(NND, 2009).

Fresh channel catfish fillets (I. punctatus) were obtained fromthe catfish genetic laboratory of U.S.D.A. Agricultural ResearchService, Stoneville, MS. The catfish were caught, filleted and ship-ped by overnight express for arrival the next day. Upon arrival, thecatfish fillets were cut into smaller pieces before being homoge-nized in a sterile laboratory blender (Model 38BL54, Waring,Torrington, CT). Instant quick frozen (IQF) tilapia fillets werepurchased from a local supermarket, thawed and cut into smallerpieces before being homogenized.

Ten g of the homogenized catfish or tilapia samples wereweighed into a re-closable plastic bag (Zip-Pak�, Minigrip, Seguin,TX), frozen and irradiated frozen (�20 �C) with a dose of 10 kGysufficient to remove background microflora (Rajkowski, 2008). Theirradiation process was done in a self-contained 137Cs gammairradiator (Lockheed Georgia Co., Marietta, GA) with a sourcestrength of ca. 88,359 Ci (2.39 PBq). The samples were placedwithin a uniform area of the radiation field to minimize variationsin the absorbed dose, which is checked yearly for uniformity usingalanine dosimeters. Actual dose (dosimetry) was verified bymeasuring the free-radical signal of 5 mm diameter alaninedosimeter pellets (Bruker Biospin Corp. Billerica, MA) usinga Bruker EMS 104 EPR Analyzer. The irradiated samples were keptfrozen (�20 �C) until used. The pH of the thawed-irradiated samplewas measured using an Orion 520A meter (Orion Research Co.,Boston, MA).

2.4. Thermal destruct values

Fish samples (10 g) for the thermal destruction values study werethawed to room temperature andmixedwell with 0.1ml inoculationcocktail for a 1:100 dilution of the initial inoculum for a final cellconcentration of 106�7 CFU/g. One g sample was weighed intostomacher bags (200 ml, Whirl-Pak filter bags, Nasco, Fort Atkinson,WI) and the fish sample distributed in the bag to form a thin layerbefore being vacuumed heat sealed (Model A300/16), MULTIVAC,Sepp Haggenmüller GmbH & Co. KG, Wolfertschwenden, Germany).

The thermal destruct method as developed by Huang (2009)was used. The sample bags were placed in a rack constructed toprovide adequate contact with the hot water. All samples wereplaced simultaneously in a re-circulating hot water bath (ModelESRB-7, Techne, Burlington, NJ) which was fitted with a tempera-ture control unit (TU-20D, Techne). The temperature of the waterbath was monitored by inserting a temperature probe into thewater. The temperature of the water bath was set at one of threetemperatures: 55, 60 or 65 �C and the pull time intervals weredetermined during preliminary trials. A minimum of five timeintervals were used: 0, 120, 360, 600, 720, 960, and 1200 s at 55 �C;0, 10, 20, 40, 60, 80, and 100 s at 60 �C; and, 0, 2, 4, 6, 8, 10, 12 s at65 �C. The come-up time (lag time required for the food tempera-ture to reach bath temperature) was 4 s (Huang, 2009). At thedetermined time intervals (after correcting for the come-up time)the fish samples were removed from the hot water bath andimmediately immersed in iced water to stop the heating process.The fish samples remained chilled and recovery of survivors wasdone immediately. The thermal destruct study on the catfish and

Fig. 2. Thermal inactivation curves at 60 �C for E. coli O157:H7 and Salmonella meatand seafood isolates inoculated on catfish and tilapia.

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431 429

tilapia using the three cocktails at each temperature was repeatedtwo times.

2.5. Plating of samples

The bag containing the pre-weighed 1 g catfish or tilapiasamples was aseptically cleaned, opened and 9ml buffered peptonewater (Becton, Dickinson and Co.) added obtaining a 1:10 dilution.The samples were stomached for 2 min (Stomacher 400, TekmarCo., Cincinnati, OH) and serial diluted with PW before being surfaceplated on TSA to determine survivors. The plates were incubated for24 h at 37 � 1 �C before being hand counted.

2.6. Thermal D-10 and Z-values

The thermal D-10 value is the time required to reduce themicrobial population by 90% at a specific temperature (Pflug et al.,2001). Regression analysis was done on a minimum of five valuesfrom the linear portion of the survival plot using the DMFitprogram (Baranyi and Roberts, 1994). The thermal D-10 value wascalculated by taking the reciprocal of the slope (D-10 ¼ �1/slope).The Z-value is the change of temperature (�C) required for 1-logcycle change in D-10 values and was calculated using the formula(Pflug et al., 2001): z ¼ (T2 e T1)/(log D1 e log D2)

2.7. Statistical analysis

The D-10 and z-values were analyzed by ANOVA to determinethe effects and interactions of the fish type and temperature (Miller,1981).

3. Results and discussion

3.1. Thermal destruct procedure

Rajkowski (2008) reported that 10 kGy was sufficient to removebackground microflora and that the irradiation process did notaffect the lipid content of the catfish or tilapia as indicated by TBARvalues. This decision to remove the background microflora torecover on TSAwas supported by Clavero et al. (1998) who reported

Fig. 1. Thermal inactivation curves at 55 �C for E. coli O157:H7 and Salmonellameat andseafood isolates inoculated on catfish and tilapia.

that the use of selective medii (sorbitol MacConkey agar supple-mented with 4-methylumbelliferyl-b-D-glucouronid and modifiedeosin methylene blue agar) were inhibitory in recoveringsub-lethally heat-injured E. coli O157:H7 cells. Therefore TSA wasused to recover E. coli O157:H7 and Salmonella after the thermalprocessing.

3.2. Thermal destruct times and z-values for E. coli O157:H7

The thermal destruction curves for E. coli O157:H7 inoculated onthe catfish and tilapia at 55, 60 and 65 �C are illustrated in Figs. 1e3.There was no observed lag or tailing in any of the E. coli O157:H7survivor curves and such linear curves suggested that the cocktailpopulation was homogeneous. Listed in Table 1 are the calculatedE. coli O157:H7 D-10 values obtained at 55, 60 and 65 �C, and theregression curves had an r2 values of>0.92. The E. coli O157:H7 hada significantly higher (P � 0.05) D-10 value at 55 �C on tilapia thanon the catfish which was not observed at the higher temperatures.Ahmed et al. (1995) determined and compared the D-10 values forE. coli O157:H7 inoculated on various meats (chicken, turkey beef

Fig. 3. Thermal inactivation curves at 65 �C for E. coli O157:H7 and Salmonella meatand seafood isolates inoculated on catfish and tilapia.

Table 1Thermal destruct times in seconds and regression data for Escherichia coliO157:H7 isolates inoculated on catfish and tilapia as compared to literature values on ground beef andchicken.

Temperature E. coli E .coli

�C �F Catfish Tilapia Ground beefa Chickena

55 131 422 � 0.3b 564 � 0.7b 1267.8 710r2 ¼ 0.96 r2 ¼ 0.98

60 140 55.5 � 2.8 45.2 � 2.0 190.2 98r2 ¼ 0.97 r2 ¼ 0.98

65 149 4.2 � 0.09 3.3 � 0.04 23.4 22r2 ¼ 0.92 r2 ¼ 0.98

a Taken from Juneja et al. (1997).b Significantly different at P � 0.05.

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431430

and pork sausage) which had different fat content. They reportedthat at 50 and 55 �C, the higher fat-content meat samples hada higher D-10 value than the lower fat content meats. In this studyat 55 �C we obtained the opposite results. Comparison confirmeda statistically higher (P � 0.05) D-10 value at 55 �C for the E. coliO157:H7 inoculated on the tilapia which has a lower fat content(1.7%) compared to catfish with the higher fat content (7.6%) eventhough the pH of both finfish samples was 6.3 (NND, 2009). Ahmedet al. (1995) reported that therewas no significant difference for theD-10 values at 60 �C for turkey or beef samples and we also did notobserve any difference with the catfish and tilapia samples at boththe 60 and 65 �C.

It was reported that different D-10 values were obtained amongthe strains of E. coli O157:H7 (Clavero et al., 1998). We were able tocompare our E. coli O157:H7 D-10 results using catfish and tilapiawith literature values for ground beef and chicken, since ourcocktail contained some of the same strains used by Juneja et al.(1997) in their study. Also, the pH of both finfish was similar to thepH of the ground beef and chicken (Juneja et al., 1997). Forcomparison listed in Table 1 are their reported D-10 values usingground beef and chicken. The D-10 values for the catfish and tilapiawere much lower. It took twice as long to inactive the E. coliO157:H7 in the chicken compared to the finfish and about threetimes as long to inactive in the ground beef sample (Juneja et al.,1997). When researchers used different strains of E. coli O157:H7to determine the D-10 value in beef and poultry, their results werealso higher than those reported here for catfish and tilapia (Ahmedet al., 1995; Line et al., 1991).

The calculated z-values for E. coli O157:H7 on catfish and tilapiawas 4.3 �C. When compared with the z-values for E. coli O157:H7obtained using meat or poultry with the reported z-value obtainedusing catfish and tilapia, the z-values were found to be within thereported range of 4e6 �C (Juneja et al., 1997; Line et al., 1991;Sörqvist, 2003) regardless of the E. coli O157:H7 isolate used.

3.3. Thermal destruct times and z-values for Salmonella

Comparison of data for the thermal destruct values of Salmonellaon finfish (catfish or tilapia) with published reports is lacking. Doyle

Table 2Thermal destruct times in seconds and regression data for Salmonella meat and seafoodbeef.

Temperature Meat isolates

�C �F Catfish Tilapia

55 131 450 � 0.3 425.5 � 0.3r2 ¼ 0.96 r2 ¼ 0.97

60 140 51.4 � 2.2 27.1 � 0.7r2 ¼ 0.95 r2 ¼ 0.97

65 149 3.8 � 0.8 2.04 � 0.03r2 ¼ 0.98 r2 ¼ 0.94

a Taken from Juneja et al. (2001).

and Mazzatta (2000) in their review stated that thermal resistanceof Salmonella can vary between serotypes and the food used todetermine the D-10 value. Therefore to overcome this difficulty,isolates of Salmonella frommeat and seafood were used for the twodifferent cocktails to determine the D-10 values at 55, 60 and 65 �C.

Representative curves of the two Salmonella cocktails (meat andseafood) are given in Figs. 1e3 and listed in Table 2 are the D-10values. There was no significant difference (P � 0.05) in the D-10values between the meat isolate or seafood isolate cocktails, andthere was no significant difference (P � 0.05) between the Salmo-nella D-10 value between the catfish (pH 6.3) and tilapia (pH 6.3).Plaza and Gabriel (2008) used S. Typhimurium inoculated oystermeat (pH 6.0) and reported the D-10 value at 60 �C of 23.04 s, whichis within the range observed in this study.

When the Salmonella D-10 values for both the meat and seafoodisolates on the finfish were compared with the reported values incustard and chicken a la king, egg, liquids with D-10 values rangingfrom 180 to 4890 s at 60 �C (Angelotti et al., 1961; Doyle andMazzatta, 2000; Sörqvist, 2003) our results were lower rangingfrom 22 to 51 s at 60 �C. Juneja et al (2001) reported a range of289e399 s at 60 �C for beef, pork, turkey and chicken, whereas wefound that the D-10 value at 60 �C ranged from 22 to 51 s for thefinfish which is much lower. This wide range of reported D-10values for Salmonella most likely is due to strain differences andfor that reason those strains isolated from seafood appear to beless resistant to heat inactivation.

When liquids (egg, milk products, saline solutions, scaldingwater from chicken and pork plants) were used to determine thethermal destruct data, the reported z-value range varied from 3.24to 9.5 �C (Doyle andMazzatta, 2000; Sörqvist, 2003). The calculatedz-values for the Salmonella inoculated on the catfish and tilapiawere not different statistically (P � 0.05) and there was no differ-ences (P � 0.05) between the two cocktail used. Since there was nodifferences, the calculated z-values were averaged. The z-values forthe finfish calculated in this study ranged from 4.3 to 4.8 �C with anaverage value of 4.5 �C and falls within the range reported forliquids. However Juneja et al. (2001) reported the z-value rangingfrom 5.77 to 6.91 �C on meat samples and Angelotti et al. (1961)reported z-values ranging from 9.3 to 13.75 �C using custard and

isolates inoculated on catfish and tilapia as compared to literature values on ground

Seafood isolates 8 strain cocktail

Catfish Tilapia Ground beefa

497.7 � 20.0 337.3 � 5.7r2 ¼ 0.97 r2 ¼ 0.9729.5 � 2.1 22.9 � 0.8 328.8r2 ¼ 0.97 r2 ¼ 0.972.43 � 0.25 1.62 � 0.06 40.2r2 ¼ 0.98 r2 0.92

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431 431

chicken a la king to determine the D-10 value. In both of thesereports, the samples used had higher fat content that the finfishused in this study.

4. Conclusions

Overall, the fat content between the catfish and tilapia did notaffect the D-10 values. The D-10 values for both E. coli O157:H7 andSalmonella inoculated on finfish were lower than those reported forother food systems, particularly meats. However the z-values,which were low, did fall within the reported range.

Cooking, heat inactivation, is a way of destroying pathogens infoods and remains the primary means of protecting against foodborne illnesses. Knowing the rate of destruction, further studies areneeded to obtain cooking parameters for finfish. These results canbe used to provide safe cooking instructions to the consumer.

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