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Heat Resistance of Salmonella spp., Listeria monocytogenes, Escherichia coli 0157:H7, and Listeria innocua M1, a Potential Surrogate for Listeria monocytogenes, in Meat and Poultry: A Review

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Heat Resistance of Salmonella spp., Listeria monocytogenes, Escherichia coli 0157:H7, and Listeria innocua M1, a Potential Surrogate for Listeria monocytogenes, in Meat and Poultry: A Review
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  Vol. 71, Nr. 3, 2006 —   JOURNAL OF FOOD SCIENCE R 23 Published on Web 3/28/2006 © 2006 Institute of Food Technologists Further reproduction without permission is prohibited     R    :    C    o    n    c    i    s    e    R    e    v    i    e    w    s    i    n    F    o    o    d    S    c    i    e    n    c    e  JFS R:Concise Reviews/Hypotheses in Food Science Heat Resistance of Salmonella spp., Listeria monocytogenes  ,  Escherichia coli  0157:H7,   and  Listeria innocua M1,   a PotentialSurrogate for Listeria monocytogenes, in Meat and Poultry: A Review CCCCC ORLISSORLISSORLISSORLISSORLISS  A. O’B A. O’B A. O’B A. O’B A. O’B RYANRYANRYANRYANRYAN , P, P, P, P, P HILIPHILIPHILIPHILIPHILIP  G. CG. CG. CG. CG. C RANDALLRANDALLRANDALLRANDALLRANDALL , E, E, E, E, E LIZABETHLIZABETHLIZABETHLIZABETHLIZABETH  M. MM. MM. MM. MM. M  ARTIN ARTIN ARTIN ARTIN ARTIN , C, C, C, C, C  ARL ARL ARL ARL ARL  L. GL. GL. GL. GL. G RIFFISRIFFISRIFFISRIFFISRIFFIS , , , , ,  AND AND AND AND AND  MMMMM ICHAELICHAELICHAELICHAELICHAEL  G. JG. JG. JG. JG. J OHNSONOHNSONOHNSONOHNSONOHNSON  ABSTRA  ABSTRA  ABSTRA  ABSTRA  ABSTRA CTCTCTCTCT: : : : : The heat-rThe heat-rThe heat-rThe heat-rThe heat-resistance data in meat and poultresistance data in meat and poultresistance data in meat and poultresistance data in meat and poultresistance data in meat and poultr y for v  y for v  y for v  y for v  y for v arararararious strious strious strious strious strains of ains of ains of ains of ains of SalmonellaSalmonellaSalmonellaSalmonellaSalmonella , , , , , LLLLListeriaisteriaisteriaisteriaisteria   monocytogenes monocytogenes monocytogenes monocytogenes monocytogenes  ,,,,,and and and and and Escherichia coli Escherichia coli Escherichia coli Escherichia coli Escherichia coli   O157:H7 as well as O157:H7 as well as O157:H7 as well as O157:H7 as well as O157:H7 as well as Listeria innocuaListeria innocuaListeria innocuaListeria innocuaListeria innocua  M1 are summarized. Heat resistance of these organ-M1 are summarized. Heat resistance of these organ-M1 are summarized. Heat resistance of these organ-M1 are summarized. Heat resistance of these organ-M1 are summarized. Heat resistance of these organ-isms is affected by many factors. Different strains of the same organism have different responses to heat. Heatisms is affected by many factors. Different strains of the same organism have different responses to heat. Heatisms is affected by many factors. Different strains of the same organism have different responses to heat. Heatisms is affected by many factors. Different strains of the same organism have different responses to heat. Heatisms is affected by many factors. Different strains of the same organism have different responses to heat. Heatresistance can also be influenced by the age of the culture, growth conditions, pH, and numerous other factors.resistance can also be influenced by the age of the culture, growth conditions, pH, and numerous other factors.resistance can also be influenced by the age of the culture, growth conditions, pH, and numerous other factors.resistance can also be influenced by the age of the culture, growth conditions, pH, and numerous other factors.resistance can also be influenced by the age of the culture, growth conditions, pH, and numerous other factors.Data from this review may prove useful to processors in validating their times and temperatures for thermalData from this review may prove useful to processors in validating their times and temperatures for thermalData from this review may prove useful to processors in validating their times and temperatures for thermalData from this review may prove useful to processors in validating their times and temperatures for thermalData from this review may prove useful to processors in validating their times and temperatures for thermalprprprprprocessing of meat and poultrocessing of meat and poultrocessing of meat and poultrocessing of meat and poultrocessing of meat and poultr y  y  y  y  y . . . . . The obThe obThe obThe obThe obvious gaps in the data will prvious gaps in the data will prvious gaps in the data will prvious gaps in the data will prvious gaps in the data will prooooovide rvide rvide rvide rvide researesearesearesearesearchers opporchers opporchers opporchers opporchers opportunities to fill thosetunities to fill thosetunities to fill thosetunities to fill thosetunities to fill thosegaps. In addition, it will encourage the development of surrogates, whether biological or otherwise, that will begaps. In addition, it will encourage the development of surrogates, whether biological or otherwise, that will begaps. In addition, it will encourage the development of surrogates, whether biological or otherwise, that will begaps. In addition, it will encourage the development of surrogates, whether biological or otherwise, that will begaps. In addition, it will encourage the development of surrogates, whether biological or otherwise, that will beable to be used in an actual processing environment.able to be used in an actual processing environment.able to be used in an actual processing environment.able to be used in an actual processing environment.able to be used in an actual processing environment.Keywords: thermal resistance, Keywords: thermal resistance, Keywords: thermal resistance, Keywords: thermal resistance, Keywords: thermal resistance, SalmonellaSalmonellaSalmonellaSalmonellaSalmonella , , , , , ListeriaListeriaListeriaListeriaListeria , , , , , E. coli E. coli E. coli E. coli E. coli   O157:H7, surrogatesO157:H7, surrogatesO157:H7, surrogatesO157:H7, surrogatesO157:H7, surrogates Introduction T hermal treatments are critical in controlling foodbornepathogens in many foods of animal srcin. Frequently, the coldchain of these foods is not reliable enough to prevent growth of pathogens if these products were under-processed. Changes inregulations occurred in 1999 to put in place lethality standards forready-to-eat (RTE) whole muscle foods of meat or poultry srcin(FSIS 1999). A 2nd proposed rule will extend these standards to vir-tually all RTE foods of meat or poultry srcin (FSIS 2001). Theseregulatory changes have placed the burden on processors of prov-ing through the use of scientific basis that a new or modified pro-cess will meet the performance standards. Many processors willlook for published D- and z-values to apply to their processes. Thisarticle summarizes some of the published data on the heat resis-tance of some important food borne pathogens, Salmonella spp., Listeria monocytogenes (LM), and Escherichia coli   O157:H7 ( E. coli  O157:H7), in meat and poultry products. Also included are data on Listeria innocua  M1 (LI), an organism that has been frequently usedas a nonpathogenic surrogate for LM. This strain of LI is resistant to50-ppm rifampicin and 250-ppm streptomycin so that it can easi-ly be enumerated on media containing these antibiotics on whichthe indigenous bacteria will not grow. Experimental conditions I t is important, when using D- and z-values from literature thatthe conditions under which the values were obtained be noted.The heating medium, the matrix used, heating conditions, and soforth, used to produce the inactivation parameters should not dif-fer in any significant way from the product or process parametersused by the processor. For this reason, we will briefly enumeratethe various conditions under which the reported values were ob-tained. Growth of test bacteria I n all reported experiments, bacteria were grown on conventional media under aerobic conditions. Salmonella  spp were grownaerobically in either tryptic soy broth (TSB) or brain heart infusion(BHI) at 35 °C to 37 °C for anywhere from 12 to 48 h.In most cases, LM was grown aerobically in either TSB plus 0.6 % yeast extract (TSBYE), plain TSB, or BHI at temperatures ranging from 25 °C to 35 °C. However, Gaze and others (1989) grew a 24-hculture of LM in nutrient broth (NB) at 30 °C. One-milliliter aliquotsof this culture were placed on 3 prepoured Tryptic soy agar with yeast extract (TSAYE) plates, and the plates were incubated at 30 °Cfor 72 h. A sterile spatula was used to harvest growth, which wasresuspended in 10 mL of maximum recovery diluent (MRD). E. coli   O157:H7 was grown aerobically in either TSB or BHI at35 °C to 37 °C for 18 to 24 h.LI was grown aerobically in TSBYE in 1 experiment with no add-ed antibiotics and in all other experiments with added antibiotics.The temperature at which cultures are grown affects the thermalresistance of the bacteria. Cultures grown at higher temperatureshave been shown to be more thermally resistant than those grownat lower temperatures (Bhaduri and others 1991; Juneja and Eblen1999). By the same token, length of incubation becomes importantbecause cells in the stationary phase of growth are generally moreheat resistant than cells in the logarithmic phase of growth (Lou and Yousef 1996).  MS 20050566 Submitted 9/19/05, Revised 10/17/05, Accepted 1/20/06. Au-thors O’Bryan, Crandall, and Johnson are with Dept. of Food Science, Univ.of Arkansas, 2650 Young Ave., Fayetteville, AR 72704. Authors Martin and Griffis are with Dept. of Biological and Agricultural Engineering, Univ. of  Arkansas, Fayetteville, Ark. Direct inquiries to author O’Bryan (E-mail:cobryan@uark.edu ).  R 24  JOURNAL OF FOOD SCIENCE —Vol. 71, Nr. 3, 2006 URLs and E-mail addresses are active links at www.ift.org  R  :    C   o  n   c  i    s   e  R   e  v  i    e  w  s  i   n  F    o   o   d    S   c  i    e  n   c   e   Heat resistance of foodborne pathogens . . . Inoculation Procedures I ndividual cultures of 6 or 8 species or strains of Salmonella  wereprepared and incubated under conditions as outlined previously.Equal aliquots of these cultures were mixed and the resulting “cock-tail” of species or strains was used to inoculate the food matrix. Smithand others (2001) centrifuged the mixed cultures and resuspendedthe resultant pellet in sterile 0.1% buffered peptone water (BPW).Juneja and others (2001a, 2001b) centrifuged the individual cultures,resuspended them in BPW, and then equal aliquots of the individu-al suspensions were mixed and used for inoculation of the meat. Thiscentrifugation and resuspending of the cultures, whether mixed orindividual, has the effect of removing any waste products as well asany nutrients that were still available from the incubated cultures.LM, whether used as a cocktail or as an individual culture, wasgenerally grown in broth and, if used as a cocktail, the aliquots were mixed and added to the meat. An exception was the study by Bolton and others (2000), who centrifuged a 16-h culture and resus-pended the cells into a 1:2 mixture of minced beef and distilled water. Gaze and others (1989) mixed their cell suspension (in MRD) with food homogenates that had been placed in universal bottlesin the water bath to reach temperature before inoculation. Walshand others (2001) soaked 300 g of beef cubes in 1000 mL of the in-oculum for 5 s, then drained and ground the inoculated beef piec-es. Bolton and others (2000) dipped 5- × 10-cm strips of beef intobacterial suspensions, then minced the beef. They also preparedsolid pieces of beef by cutting 5- × 5- × 2-cm squares of beef (about50 g) and injecting each square of beef with 1 mL of inoculum.In most cases, E. coli   O157:H7 cultures were grown as previously mentioned and used to inoculate meat either individually or ascocktails of equal volumes if more than 1 strain was used. Juneja(2003) was the exception; he centrifuged cultures and resuspendedcell pellets in BPW before inoculation.LI cultures were used directly after incubation to inoculate meatsamples. Heating Menstrua I ntrinsic properties of the product influence the heat resistanceof pathogens associated with the product. Most studies that have yielded D- and z-values have been done in meat slurries or on meatthat was inoculated on the surface. Virtually every study reportedhere, whether using fully cooked or raw product, was performed inground meat substrates. One exception is Murphy and others (2003a),in which cooked chicken leg quarters were injected with a cocktail of LM using a 24-gauge needle. Bolton and others (2000), as mentionedpreviously, used 50-g chunks of solid beef vacuum-packaged in bags. Heat Treatment  V  arious methods of heat treatment have been used in thestudies reported in this article. The preponderance of the exper-iments have been done with samples of ground meat, flattened in asterile bag to 0.5- to 1-mm thickness and heated in a controlled tem-perature water bath. Gaze and others (1989) used universal bottlesfilled with the heating menstruum that were placed in a shaking waterbath, allowed to reach the desired temperature then inoculated, mixedand held for the desired time at each temperature. Kotrola and Conner(1997) and Kotrola and others (1997) placed 1 g of inoculated meat intoa thermal death time (TDT) tube, sealed the tubes and placed themin a shaking oil bath. Bolton and others (2000) used vacuum bags forsolid pieces of beef and vacutainers for minced beef in laboratory  water baths, but they also processed vacuum-packaged beef minceand vacuum-packed solid beef pieces in a Barriquand Steriflow com-mercial retort. Murphy and others (2003a) vacuum-packed inoculatedcooked leg quarters and processed them in a Stein oven using steamimpingement at atmospheric pressure. Definite differences in results will be noted between experiments done in water baths and actual pro-cessing conditions. Murphy and others (1999) reported a 7-log reduc-tion of Salmonella  in ground chicken breast meat in a study that wasdone in a water bath. In the water bath studies, the temperaturethroughout the sample can be considered to be uniform. Murphy andothers (2001) subsequently studied thermal inactivation of Salmonella in ground chicken breast patties processed in a convection oven.There existed a definite temperature gradient throughout the patty during cooking. They also found that there was a higher survival of  Salmonella  in this study. Using the parameters from the water bathstudy would have resulted in an over prediction of thermal lethality for Salmonella  of 1.5 to 4.0 logs. Recovery of Heat-treated Bacteria S elective media are generally used to suppress the growth of extraneous bacteria and allow the growth and differentiation of only targeted bacteria. However, it is now known that selective chem-icals can inhibit the repair of sublethaly injured cells (Ray and Adams1984). Kang and Fung (2000) developed the thin agar layer (TAL)method to deal with the recovery of injured cells while keeping thedifferential and selective properties of media such as Modified Ox-ford Agar (MOX) or Xylose Lysine Desoxycholate Agar (XLD). Thegreat majority of the studies reported here used the TAL method forthe recovery and enumeration of the surviving bacteria. However,Bolton and others (2000) plated dilutions of heat treated LM on TSA and incubated these plates for 6 h at 25 °C. Plates were then overlaid with PALCAM agar and incubated at 30 °C for 48 h. Mazzotta and Go-mbas (2001) opened the heated pouches and added Listeria Enrich-ment Broth (LEB) and incubated the contents for 48 h at 30 °C.Pouches were then mixed, aseptically opened, and 0.1 mL of enrich-ment was plated on Oxford medium, which was incubated at 30 °C for24 h. Kotrola and Conner (1997) spiral plated E. coli   O157:H7 on phe-nol red agar containing 1% sorbitol. Juneja and others (2001a, 2001b)used irradiated meat so that there was no competitive microflora. Sur-vivors were enumerated by spiral plating on TSAYE agar with added1% sodium pyruvate. These plates were then incubated at 28 °C for48 h. The 28 °C incubation temperature was chosen by Juneja’sgroup because Katsui and others (1982) had previously determinedthat incubation at temperatures below the optimum growth temper-ature might enhance the repair of heat damaged cells. Smith andothers (2001) also used irradiated meat substrates and plated alldilutions on Petrifilm aerobic count plates at 37 °C for up to 36 h.Gaze and others (1989) used sterile food homogenates and used thepour plate technique with TSAYE. Orta-Ramirez and others (1997)plated both E. coli   O157:H7 and Salmonella   senftenberg   on Petrifilmcoliform count plates. They confirmed the sterility of their meat sam-ples by plating uninoculated samples onto both Petrifilm aerobiccount plates and Petrifilm coliform count plates. Summary of Data Listeria monocytogenes in meat and poultry Listeria monocytogenes in meat and poultry Listeria monocytogenes in meat and poultry Listeria monocytogenes in meat and poultry Listeria monocytogenes in meat and poultry  D and z values for LM in red meat are shown in Table 1; Table 2contains results for LM in poultry. It is obvious from the wide rangeof results that heat resistance can be affected by not only the strainof LM used, but also by the experimental conditions, the character-istics of the meat or poultry used in the tests, as well as prior growthconditions and treatment of the inoculum before testing.Most of the reported experiments were done on 1 type of product,making it difficult to state that LM is any more resistant to heat in 1 typeof meat over another. Mackey and others (1990) compared beef andchicken under the same test conditions using their most resistant  Vol. 71, Nr. 3, 2006 —   JOURNAL OF FOOD SCIENCE R 25 URLs and E-mail addresses are active links at www.ift.org      R    :    C    o    n    c    i    s    e    R    e    v    i    e    w    s    i    n    F    o    o    d    S    c    i    e    n    c    e Heat resistance of foodborne pathogens . . . Table 1—Thermal resistance of  Listeria monocytogenes in meat D-value (in min) at °Cz-StrainMedium4850525556586062646668ValueRef 10 strainsGround meat13.186.393.121.014.92 a 10 strainsMeat + cure50.016.77.061.283.50 a NCTC 11994 (4b)Minced beef32.73.40.314.9 b NCTC 11994 (4b)Minced beef36.13.20.154.2 c NCTC 11994 (4b)Minced beef65.821.33.05.9 d N7004, N7285, N7278,Hot dog batter14.63.20.655.9 e N7226, N7203, N7175N7004, N7285, N7278,Hot dog batter15.53.30.706.0 f N7226, N7203, N7175Pattern E (outbreak)Hot dog batter11.01.80.405.6 e Pattern E (outbreak)Hot dog batter8.11.80.235.2 f Scott A, MF27137, H7762,Ground beef, 25% fat27.699.634.186.10 g MF38521, MF46869Scott ABeef < 7% fat8.324.202.190.940.355.98 h 11994Beef < 7% fat6.272.902.210.930.275.98 h Strain 5Beef85213.80.937.2 i  (65) a Farber (1989) Inoculated ground meat placed in pouches in wire racks in water bath, phase of Listeria monocytogenes (LM) growth not stated. b Bolton and others (2000): Uninoculated minced beef in vacutainers, placed in a water bath, allowed to reach temp then inoculated with stationary phase cells. c Bolton and others (2000): Strips of beef inoculated with stationary phase cells minced, vacuum-packed, placed in water bath, allowed to reach temperature. d Bolton and others (2000): Strips of beef inoculated with stationary phase cells, minced, vacuum-packed, and processed in commercial retort. e Mazzotta and Gombas (2001): Batter prepared, inoculated with stationary phase cells, placed in pouches, sealed, rolled flat, placed in water bath. f Mazzotta and Gombas (2001): Batter prepared, inoculated with starved cells, placed in pouches, sealed, rolled flat, placed in water bath. g Juneja (2003): Ground beef inoculated, mixed, placed in pouches, rolled flat, heat sealed, placed in water bath, phase of growth of LM not stated. h Gaze and others (1989): Beef macerated, autoclaved, placed in universal bottles, allowed to reach temperature, inoculated with stationary phase cells,mixed and held. i Mackey and others (1990): Ground beef inoculated with stationary phase cells, mixed, placed in pouches, rolled flat, heat sealed, placed in water bath. Table 2—Thermal resistance of  Listeria monocytogenes  in poultry  D-value (in min) at °Cz-StrainMedium5557.5606262.564656667.56870ValueRef Scott A(4b), TN Scott A,Thigh and leg82.7526.547.782.51.070.40.115.28 a F4393 4b, F4260 (1/2b)meat with 4.8%F4263 (1/2a),Na LactateLCDC 81-861 (4b)Scott A(4b), TN Scott A,Thigh and leg38.949.672.041.010.30.10.045.28 a F4393 4b, F4260 (1/2b)meat, No NaF4263 (1/2a),LactateLCDC 81-861 (4b)Scott A(4b), TN Scott A,Thigh and leg38.949.672.041.010.30.10.045.08 b F4393 4b, F4260 (1/2b)meatF4263 (1/2a),LCDC 81-861 (4b)Scott A(4b), TN Scott A,Skin from thigh34.0510.193.951.370.410.130.055.27 b F4393 4b, F4260 (1/2b)and legF4263 (1/2a),LCDC 81-861 (4b)Scott A F4642Chicken breast5.292.511.560.680.380.166.72 c NCTC 11994Chicken breast5.022.211.840.950.410.27.39 c 5-strain cocktailCooked chicken51.0213.938.492.60.650.290.135.71 d breast5-strain cocktailCooked turkey119.0540.1616.74.541.290.460.215.29 d breastUSDA-ARS V105, V67,Chicken leg131.5823.649.842.230.930.420.115.76 e V72, V113, V125quarters meatUSDA-ARS V105, V67,Chicken leg82.6521.698.93.571.160.40.215.04 e V113, V125quarters skinStrain 5Chicken leg145.60.530.116.7 f Strain 5Chicken breast138.70.520.136.3 f a Murphy and others (2004b): Samples inoculated with stationary phase cells sealed in bag, rolled flat, placed in water bath at temperature for various times,assumed immediate come up. b Murphy and others (2004c): Samples inoculated with stationary phase cells sealed in bag, rolled flat, placed in water bath at temperature for various times,assumed immediate come up. c Gaze and others (1989): Samples placed in universal bottles, equilibrated to temperature in water bath, inoculated with stationary phase cells and held attemperature for various times. d Murphy and others (2003b): Samples inoculated with stationary phase cells, sealed in bag, rolled flat, placed in water bath at temperature for various times,assumed immediate come up. e Murphy and others (2003a): Cooked leg quarters inoculated with an “overnight culture” by injection, vacuum-packed, steamed in oven. f Mackey and others (1990): Chicken macerated, autoclaved, placed in universal bottles, allowed to reach temperature, inoculated with stationary phase cells,mixed, and held.  R 26  JOURNAL OF FOOD SCIENCE —Vol. 71, Nr. 3, 2006 URLs and E-mail addresses are active links at www.ift.org  R  :    C   o  n   c  i    s   e  R   e  v  i    e  w  s  i   n  F    o   o   d    S   c  i    e  n   c   e   Heat resistance of foodborne pathogens . . . strain of LM, but their results were inconclusive. At 50 °C, the beef sam-ples had a lower D value (85 min) than chicken leg (179 min) or chickenbreast (100 min), but at 55 °C, the beef D value was higher (21 min forbeef as opposed to 14 min for chicken leg or 13 min for chicken breast).Farber (1989) compared ground meat with ground meat containing a cure (nitrite, dextrose, lactose, corn syrup, and sodium chloride) andfound that the LM in the cured meat had greater heat resistance (D 58 = 50 min) than LM in plain ground beef (D 58  = 6.39 min). Similarly,Murphy and others (2004b) found that the addition of sodium lactateto ground thigh and leg meat increased the D values for a 6 strain cock-tail of LM by as much as 75%. These results are in direct contrast to thefindings of McMahon and others (1999) who found that adding sodi-um lactate to ground beef increased the sensitivity of LM to heat.No direct comparisons between raw and cooked meat were madeusing the same experimental conditions so it is not possible fromthese data to determine whether or not LM is more heat resistant incooked products than it is in raw meats. Fain and others (1991) com-pared LM D-values in low fat (2%) and high fat (30.5%) ground beef. At 135°F the D-value for LM was 5.8 min in the fatty beef as com-pared with 2.6 min in the lean beef, and at 145 °F the D value was 1.2min in the fatty beef as compared with 0.6 min in the lean beef. Theseresults suggest that fat lends some protection from thermal destruc-tion. Murphy and others (2004c) compared LM in chicken thigh andleg meat (10.3% fat) with LM in skin (47.4% fat) from the chicken thighand leg. They found that D values using the skin were higher thanthose in the meat for temperatures above 55 °C. For instance, the Dvalue in skin at 60 °C was 3.95 min as opposed to a value of 2.04 minfor the meat at the same temperature. Because the skin had a muchhigher level of fat, this can be seen as a confirmation that fat has aprotective role for pathogens under heat treatment.Bolton and others (2000) compared D- and z-values obtained in alaboratory water bath with those obtained using a commercial retort. Table 3—Thermal resistance of  Salmonella  spp in meat D-value (in min) at °Cz-StrainMedium5557.558606162.56364656667.570ValueRef Senftenberg, Heidelberg,Franks14.736.675.634.381.640.780.399.83 a Typhimurium, Mission,Montevideo, CaliforniaSenftenberg, Heidelberg,Beef patties9.097.704.802.400.970.570.259.14 a Typhimurium, Mission,Montevideo, CaliforniaSenftenberg, Heidelberg,Beef/turkey20.5812.894.422.041.030.710.378.35 a Typhimurium, Mission,pattiesMontevideo, CaliforniaSenftenberg, Heidelberg,Beef/turkey41.0215.155.602.070.760.280.105.83 b Typhimurium, Mission,linksMontevideo, CaliforniaSenftenberg ATCC 43854Ground beef21.793.380.920.344.51 c 19.1% fatTyphimurium DT104 (10127)Ground beef21.982.630.650.164.28 c 19.1% fatFSIS 120, H3527, H3502,Ground beef16.342.720.440.153.90 d H3380, MF 60404, 8457,19.1% fatFSIS 051, F5038BG1Senftenberg ATCC 43845Ground beef15.172.086.25 e FSIS 120, H3527, H3502,Ground beef18.663.390.570.204.08 f H3380, MF 60404, 8437,19.1% fatFSIS 051, F5038BG1Typhimurium DT104 (10127)Ground beef9.052.260.570.155.07 c 4.8% fatTyphimurium DT104 (10601)Ground beef10.552.150.410.074.13 e 4.8% fatTyphimurium DT104 (01071)Ground beef10.272.060.430.144.77 c 4.8% fatFSIS 120, H3527, H3502,Ground beef19.319.34.728.06 g H3380, MF 60404, 8437,25% fatFSIS 051, F5038BG1FSIS 120, H3527, H3502,Ground beef8.655.481.500.676.01 h H3380, MF 60404, 8437,12.5% fatFSIS 051, F5038BG1FSIS 120, H3527, H3502,Ground pork7.085.201.360.597.10 h H3380, MF 60404, 8437,7.0% fatFSIS 051, F5038BG1 a Murphy and others (2002b): Products blended with stationary phase culture, 8.5 g packed in thin wall metal containers, placed in water bath. b Murphy and others (2004a): Raw ground meat inoculated with stationary phase culture, mixed, placed in bags, vacuum-sealed, rolled flat, placed in water bath. c Smith and others (2001): Ground beef irradiated, inoculated, mixed, 1 g placed in bags, rolled flat, heat sealed, placed in water bath, phase of growth not stated. d Smith and others (2001): Ground beef irradiated, inoculated with log phase culture, mixed, 1 g placed in bags, rolled flat, heat sealed, placed in water bath,phase of growth not stated. e Orta-Ramirez and others (1997): Beef ground, inoculated with stationary phase culture, 1 g placed in TDT, sealed, placed in water bath at temperature. f Smith and others (2001): Ground beef irradiated, inoculated with stationary phase culture, mixed, 1 g placed in bags, rolled flat, heat sealed, placed in water bath. g Juneja (2003): Ground beef irradiated, inoculated, mixed, 3 g placed in bags, rolled flat, heat sealed, placed in water bath, phase of cell growth not stated. h Juneja and others (2001): Ground product irradiated, inoculated with stationary phase culture, mixed, 5 g placed in bags, rolled flat, heat sealed, placed in water bath.  Vol. 71, Nr. 3, 2006 —   JOURNAL OF FOOD SCIENCE R 27 URLs and E-mail addresses are active links at www.ift.org      R    :    C    o    n    c    i    s    e    R    e    v    i    e    w    s    i    n    F    o    o    d    S    c    i    e    n    c    e Heat resistance of foodborne pathogens . . . The D-value for minced beef in a vacuum package in the water bathat 55 °C was 3.2 min whereas the D-value in the commercial retort at56 °C was 3.0 min. The z-value for the mince in the water bath was4.2 °C whereas that in the retort was 5.9 °C. These differences in z-values between water bath and commercial retort processing ledthem to conclude that the data collected in laboratory settings, atleast for LM and Yersinia enterocolitica , may not be transferable toactual processing conditions. They believe that only data obtainedfrom commercial systems should be used to construct models. SalmonellaSalmonellaSalmonellaSalmonellaSalmonella  spp in meat and poultry spp in meat and poultry spp in meat and poultry spp in meat and poultry spp in meat and poultry  Table 3 reports the thermal resistance of Salmonella  spp in redmeat and Table 4 reports the thermal resistance of Salmonella  sppin poultry products.The comparison of Salmonella typhimurium  DT104 by Smithand others (2001) in ground beef with low fat (4.8%) and high fat(19.1%) yielded mixed results. At 55 °C, the D-value for strain 10127in the high fat beef was 21.98 min, over twice the value of 9.05 minin the low fat beef. However, the results at higher temperatures were not significantly different. Juneja and others (2000) have sug-gested that a higher fat level produces a survivor curve with a pro-nounced shoulder, which leads to higher D-values.FSIS/USDA (1999) issued a Final Rule specifying lethality perfor-mance standards for cooked and roast beef and cooked poultry products. This rule specified that any process for RTE whole musclefoods must achieve a 6.5-log reduction for Salmonella  in beef and a7.0-log reduction of Salmonella  in poultry. A proposed rule (FSIS/USDA 2001) would extend this approach to essentially all RTE prod-ucts containing meat and/or poultry. FSIS recommended that any challenge studies performed to validate processes should use acocktail of various serotypes of Salmonella , including relatively heat-resistant pathogenic serotypes or strains that have been implicated Table 4—Thermal resistance of  Salmonella  spp in poultry  D-value (in min) at °Cz-StrainMedium5557.558606262.56567.570ValueRef Senftenberg, Heidelberg, Typhimurium,Cooked Chicken24.0719.63.8281.5270.6090.2430.0976.262 a Mission, Montevideo, CaliforniaBreastSenftenberg, Heidelberg, Typhimurium,Raw chicken26.9714.558.093.981.390.610.327.6 b Mission, Montevideo, CaliforniapattiesSenftenberg, Heidelberg, Typhimurium,Raw chicken22.379.928.54.551.250.380.327.61 b Mission, Montevideo, CaliforniatendersSenftenberg, Heidelberg, Typhimurium,Roast duck28.5714.316.792.090.580.20.115.82 c Mission, Montevideo, CaliforniameatSenftenberg, Heidelberg, Typhimurium,Roast duck25.3214.474.32.461.210.490.177.01 c Mission, Montevideo, CaliforniaskinSenftenberg, Heidelberg, Typhimurium,Cooked turkey24.698.675.21.850.620.190.126.23 c Mission, Montevideo, CaliforniabreastSenftenberg, Heidelberg, Typhimurium,Cooked chicken24.079.63.831.530.610.240.16.26 c Mission, Montevideo, CaliforniabreastFSIS 120, H3527, H3502, H3380,Ground chicken7.384.831.140.4155.46 d MF 60404, 8457, FSIS 051, F5038BG1 2% fatFSIS 120, H3527, H3502, H3380,Ground chicken,7.334.681.160.5145.46 d MF 60404, 8457, FSIS 051, F5038BG16.3% fatFSIS 120, H3527, H3502, H3380,Ground chicken,8.545.401.160.5295.46 d MF 60404, 8457, FSIS 051, F5038BG19% fatFSIS 120, H3527, H3502, H3380,Ground chicken,9.045.501.300.5025.46 d MF 60404, 8457, FSIS 051, F5038BG112% fatFSIS 120, H3527, H3502, H3380,Ground turkey,7.504.561.530.5896.13 d MF 60404, 8457, FSIS 051, F5038BG11% fatFSIS 120, H3527, H3502, H3380,Ground turkey,7.714.941.850.5526.13 d MF 60404, 8457, FSIS 051, F5038BG17% fatFSIS 120, H3527, H3502, H3380,Ground turkey,6.915.131.450.5696.13 d MF 60404, 8457, FSIS 051, F5038BG110% fatFSIS 120, H3527, H3502, H3380,Ground turkey,7.415.431.780.5926.13 d MF 60404, 8457, FSIS 051, F5038BG112% fatSenftenberg, Heidelberg, Typhimurium,Chicken thigh/43.7613.665.721.620.550.190.075.46 e Mission, Montevideo, CaliforniaLeg meatSenftenberg, Heidelberg, Typhimurium,Chicken thigh/43.78134.761.770.660.20.085.46 e Mission, Montevideo, CaliforniaLeg meat withNa LactateSenftenberg, Heidelberg, Typhimurium,Chicken thigh/43.7613.665.721.620.550.190.075.34 f Mission, Montevideo, CaliforniaLeg meatSenftenberg, Heidelberg, Typhimurium,Chicken thigh/43.3314.097.312.210.790.230.095.56 f Mission, Montevideo, CaliforniaLeg skinFSIS 120, H3527, H3502, H3380,Ground turkey7.424.821.510.86.88 g MF 60404, 8457, FSIS 051, F5038BG19 % fatFSIS 120, H3527, H3502, H3380,Ground chicken7.085.21.360.596.11 g MF 60404, 8457, FSIS 051, F5038BG17 % fat a Murphy and others (2002a): Cooked chicken ground, inoculated with “actively growing” culture, 25 g placed in pouch, vacuum-sealed, rolled flat, placed in water bath. b Murphy and others (2002b): Raw product ground, inoculated with stationary phase culture, 8.5 g packed in thin-walled metal containers, placed in water bath. c Murphy and others (2003b): Cooked product ground, inoculated with stationary phase culture, 5 g placed in pouches, vacuum-packed, rolled flat placed in water bath. d Juneja and others (2001a): Product ground, inoculated with stationary phase cells, 5 g placed in bag, rolled flat, heat-sealed, placed in water bath. e Murphy and others (2004b): Product ground, inoculated with stationary phase culture, 10 g placed in pouch, vacuum-sealed, rolled flat, placed in water bath. f Murphy and others (2004c): Product ground, inoculated with stationary phase culture, 10 g placed in pouch, vacuum-sealed, rolled flat, placed in water bath. g Juneja and others (2001b): Ground meat irradiated, inoculated with stationary phase cells, 5 g placed in bag, pressed flat, heat-sealed, placed in water bath.
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