Thermal Inactivation D- and z-Values of Multidrug-Resistant and Non–Multidrug-Resistant Salmonella Serotypes and Survival in Ground Beef Exposed to Consumer-Style Cooking

2008 ◽  
Vol 71 (3) ◽  
pp. 509-515 ◽  
Author(s):  
J. D. STOPFORTH ◽  
R. SUHALIM ◽  
B. KOTTAPALLI ◽  
W. E. HILL ◽  
M. SAMADPOUR
Keyword(s):  
Heat Resistance ◽  
Thermal Inactivation ◽  
Ground Beef ◽  
Antibiotic Use ◽  
Multidrug Resistant ◽  
Significant Difference ◽  
Salmonella Serotypes ◽  
D Values ◽  
Food Processes ◽  
Best Fit

There has been speculation that multidrug-resistant (MDR) strains are generated by subtherapeutic antibiotic use in food animals and that such strains result in increased resistance to lethality by food processes such as heat and irradiation. The objective of this study was to evaluate the heat resistance of 20 strains, namely an MDR and a non–multidrug-resistant (NMDR) strain of each of 10 Salmonella serotypes isolated from cattle or cattle environments. MDR and NMDR Salmonella serotypes studied included Montevideo, Typhimurium, Anatum, Muenster, Newport, Mbandaka, Dublin, Reading, Agona, and Give. For phase I, stationary-phase cultures of the strains were aliquoted into sterile capillary tubes and immersed in a temperature-controlled water bath at 55, 60, 65, and 70°C for appropriate times. Survivor curves were plotted for each temperature, and a best-fit linear regression was derived for each temperature. D-values (decimal reduction times) and z-values (changes in temperature required to change the D-values) were calculated for each strain. Although there was no overall significant difference in the heat resistance of MDR and NMDR serotypes, NMDR serotypes generally appeared to have slightly higher heat resistance than NMDR serotypes, especially at 55 and 60°C. The highest relative heat resistance (highest z-values) was exhibited by Salmonella Anatum. Notably, the relative heat resistance of NMDR Salmonella Agona was similar to that of NMDR Salmonella Anatum and had the highest D-values at all four temperatures. For phase II, three serotypes (regardless of resistance profile) with the highest relative heat resistance and their drug-resistant counterparts were selected for thermal inactivation in ground beef patties cooked to endpoint temperatures. Salmonella Agona was able to survive in ground beef cooked to an internal temperature of 71°C. Results of these studies suggest drug resistance does not affect the heat resistance of Salmonella and that serotype or strain is an important consideration in risk assessment of the pathogen with regard to survival at cooking temperatures.

Modeling the Effects of Temperature, Sodium Chloride, and Green Tea and Their Interactions on the Thermal Inactivation of Listeria monocytogenes in Turkey†

2014 ◽  
Vol 77 (10) ◽  
pp. 1696-1702 ◽  
Author(s):  
VIJAY K. JUNEJA ◽  
JIMENA GARCIA-DÁVILA ◽  
JULIO CESAR LOPEZ-ROMERO ◽  
ETNA AIDA PENA-RAMOS ◽  
JUAN PEDRO CAMOU ◽  
...  
Keyword(s):  
Listeria Monocytogenes ◽  
Sodium Chloride ◽  
Protective Effect ◽  
Heat Resistance ◽  
Green Tea ◽  
Thermal Inactivation ◽  
Heating Temperature ◽  
Lethal Effect ◽  
Interactive Effects ◽  
D Values

The interactive effects of heating temperature (55 to 65°C), sodium chloride (NaCl; 0 to 2%), and green tea 60% polyphenol extract (GTPE; 0 to 3%) on the heat resistance of a five-strain mixture of Listeria monocytogenes in ground turkey were determined. Thermal death times were quantified in bags that were submerged in a circulating water bath set at 55, 57, 60, 63, and 65°C. The recovery medium was tryptic soy agar supplemented with 0.6% yeast extract and 1% sodium pyruvate. D-values were analyzed by second-order response surface regression for temperature, NaCl, and GTPE. The data indicated that all three factors interacted to affect the inactivation of the pathogen. The D-values for turkey with no NaCl or GTPE at 55, 57, 60, 63, and 65°C were 36.3, 20.8, 13.2, 4.1, and 2.9 min, respectively. Although NaCl exhibited a concentration-dependent protective effect against heat lethality on L. monocytogenes in turkey, addition of GTPE rendered the pathogen more sensitive to the lethal effect of heat. GTPE levels up to 1.5% interacted with NaCl and reduced the protective effect of NaCl on heat resistance of the pathogen. Food processors can use the predictive model to design an appropriate heat treatment that would inactivate L. monocytogenes in cooked turkey products without adversely affecting the quality of the product.

Thermal Inactivation of Escherichia coli O157: H7, Salmonella senftenberg, and Enzymes with Potential as Time-Temperature Indicators in Ground Beef

1997 ◽  
Vol 60 (5) ◽  
pp. 471-475 ◽  
Author(s):  
ALICIA ORTA-RAMIREZ ◽  
JAMES F. PRICE ◽  
YIH-CHIH HSU ◽  
GIRIDARAN J. VEERAMUTHU ◽  
JAMIE S. CHERRY-MERRITT ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Thermal Inactivation ◽  
Ground Beef ◽  
Escherichia Coli O157 ◽  
E Coli ◽  
Triose Phosphate ◽  
Beef Products ◽  
Z Value ◽  
D Values ◽  
Salmonella Senftenberg

The USDA has established processing schedules for beef products based on the destruction of pathogens. Several enzymes have been suggested as potential indicators of heat processing. However, no relationship between the inactivation rates of these enzymes and those of pathogenic microorganisms has been determined. Our objective was to compare the thermal inactivation of Escherichia coli O157:H7 and Salmonella senftenberg to those of endogenous muscle proteins. Inoculated and noninoculated ground beef samples were heated at four temperatures for predetermined intervals of time in thermal-death-time studies. Bacterial counts were determined and enzymes were assayed for residual activity. The D values for E. coli O157:H7 were 46.10, 6.44, 0.43, and 0.12 min at 53, 58, 63, and 68°C, respectively, with a z value of 5.60°C. The D values for S. senftenberg were 53.00, 15.17, 2.08, and 0.22 min at 53, 58, 63, and 68°C, respectively, with a z value of 6.24°C. Apparent D values at 53, 58, 63, and 68°C were 352.93, 26.31, 5.56, and 3.33 min for acid phosphatase; 6968.64, 543.48, 19.61, and 1.40 min for lactate dehydrogenase; and 3870.97, 2678.59, 769.23, and 42.92 min for peroxidase; with z values of 7.41,3.99, and 7.80°C, respectively. Apparent D values at 53, 58, 63, and 66°C were 325.03, 60.07, 3.07, and 1.34 min for phosphoglycerate mutase; 606.72, 89.86, 4.40, and 1.28 min for glyceraldehyde-3-phosphate dehydrogenase; and 153.06, 20.13, 2.25, and 0.74 min for triose phosphate isomerase; with z values of 5.18, 4.71, and 5.56°C, respectively. The temperature dependence of triose phosphate isomerase was similar to those of both E. coli O157 :H7 and S. senftenberg, suggesting that this enzyme could be used as an endogenous time-temperature indicator in beef products.

Thermal Inactivation of Listeria monocytogenes in Chicken Gravy

1992 ◽  
Vol 55 (7) ◽  
pp. 492-496 ◽  
Author(s):  
I-PING D. HUANG ◽  
AHMED E. YOUSEF ◽  
ELMER H. MARTH ◽  
M. EILEEN MATTHEWS
Keyword(s):  
Heat Treatment ◽  
Listeria Monocytogenes ◽  
Heat Resistance ◽  
Thermal Inactivation ◽  
Refrigerated Storage ◽  
Department Of Agriculture ◽  
Large Numbers ◽  
Z Value ◽  
D Values ◽  
The U.S

Heat resistance of Listeria monocytogenes strains V7 and Scott A in chicken gravy and changes in heat resistance during refrigerated storage were studied. After chicken gravy was made, it was cooled to 40°C, inoculated with 105 CFU L. monocytogenes per ml of gravy, and then stored at 7°C for 10 d. Gravy was heated at 50, 55, 60, and 65°C immediately after inoculation and after 1, 3, 5, and 10 d of refrigerated storage. The D values for strains Scott A and V7 in gravy heated at 50°C at day 0 were 119 and 195 min and at day 10 they were 115 and 119 min, respectively, whereas at 65°C comparable values at day 0 were 0.48 and 0.19 min and at day 10 they were 0.014 and 0.007 min. Heat resistance (expressed as D values) was greater at day 0 than at the end of refrigerated storage. The z values ranged from 3.41 to 6.10°C and were highest at the early stages of chill storage and then decreased at the later stages. Strain V7 was more heat resistant than Scott A at 50°C. Strain Scott A always had a higher z value than did strain V7 at the same storage interval. A heat treatment greater than the 4-D process recommended by the U.S. Department of Agriculture was required to inactivate the large numbers of L. monocytogenes that developed in chicken gravy during refrigerated storage.

Evaluation of Microbiological Safety of Shrimp Cooked in a Microwave Oven

1995 ◽  
Vol 58 (7) ◽  
pp. 742-747 ◽  
Author(s):  
SRIKANTH GUNDAVARAPU ◽  
YEN-CON HUNG ◽  
ROBERT E. BRACKETT ◽  
P. MALLIKARJUNAN
Keyword(s):  
Mathematical Model ◽  
Listeria Monocytogenes ◽  
Heat Resistance ◽  
Constant Temperature ◽  
Microwave Power ◽  
Thermal Inactivation ◽  
Microwave Oven ◽  
D Values ◽  
Cooking Times ◽  
Temperature Water

The effect of different microwave power levels (240, 400, 560, and 800 W) on the survival of Listeria monocytogenes in inoculated shrimp was investigated. Thermal inactivation rates (D-values) of L. monocytogenes were determined using constant temperature water baths to establish the heat resistance of L. monocytogenes in shrimp. Shrimp were inoculated with approximately 5 × 105 CFU/g of a five-strain mixture of L. monocytogenes. One hundred grams of shrimp were cooked in the microwave oven at different power levels using cooking times predicted by a mathematical model as well as 20% longer times than those obtained from the model. No viable L. monocytogenes were detected in uninoculated shrimp after microwave cooking, but at least one replication of inoculated shrimp tested positive for the presence of Listeria. No viable L. monocytogenes were detected in shrimp cooked at 120% of predicted times.

Thermal Inactivation Kinetics of Sporolactobacillus nakayamae Spores, a Spoilage Bacterium Isolated from a Model Mashed Potato–Scallion Mixture

2016 ◽  
Vol 79 (9) ◽  
pp. 1482-1489
Author(s):  
HAYRIYE BOZKURT ◽  
JAIRUS R. D. DAVID ◽  
RYAN J. TALLEY ◽  
D. SCOTT LINEBACK ◽  
P. MICHAEL DAVIDSON
Keyword(s):  
Heat Resistance ◽  
Thermal Inactivation ◽  
Weibull Model ◽  
Inactivation Kinetics ◽  
Order Model ◽  
First Order ◽  
Different Temperatures ◽  
Spoilage Bacterium ◽  
D Values ◽  
Kinetics Of

ABSTRACT Sporolactobacillus species have been occasionally isolated from spoiled foods and environmental sources. Thus, food processors should be aware of their potential presence and characteristics. In this study, the heat resistance and influence of the growth and recovery media on apparent heat resistance of Sporolactobacillus nakayamae spores were studied and described mathematically. For each medium, survivor curves and thermal death curves were generated for different treatment times (0 to 25 min) at different temperatures (70, 75, and 80°C) and Weibull and first-order models were compared. Thermal inactivation data for S. nakayamae spores varied widely depending on the media formulations used, with glucose yeast peptone consistently yielding the highest D-values for the three temperatures tested. For this same medium, the D-values ranged from 25.24 ± 1.57 to 3.45 ± 0.27 min for the first-order model and from 24.18 ± 0.62 to 3.50 ± 0.24 min for the Weibull model at 70 and 80°C, respectively. The z-values determined for S. nakayamae spores were 11.91 ± 0.29°C for the Weibull model and 11.58 ± 0.43°C for the first-order model. The calculated activation energy was 200.5 ± 7.3 kJ/mol for the first-order model and 192.8 ± 22.1 kJ/mol for the Weibull model. The Weibull model consistently produced the best fit for all the survival curves. This study provides novel and precise information on thermal inactivation kinetics of S. nakayamae spores that will enable reliable thermal process calculations for eliminating this spoilage bacterium.

scholarly journals Predictive Thermal Inactivation Model for Effects of Temperature, Sodium Lactate, NaCl, and Sodium Pyrophosphate on Salmonella Serotypes in Ground Beef

2003 ◽  
Vol 69 (9) ◽  
pp. 5138-5156 ◽  
Author(s):  
Vijay K. Juneja ◽  
Harry M. Marks ◽  
Tim Mohr
Keyword(s):  
Heat Resistance ◽  
Survival Data ◽  
Thermal Inactivation ◽  
Ground Beef ◽  
Sodium Lactate ◽  
Sodium Pyrophosphate ◽  
Relative Reduction ◽  
Survival Curves ◽  
The Times ◽  
The Individual

ABSTRACT Analyses of survival data of a mixture of Salmonella spp. at fixed temperatures between 55°C (131°F) and 71.1°C (160°F) in ground beef matrices containing concentrations of salt between 0 and 4.5%, concentrations of sodium pyrophosphate (SPP) between 0 and 0.5%, and concentrations of sodium lactate (NaL) between 0 and 4.5% indicated that heat resistance of Salmonella increases with increasing levels of SPP and salt, except that, for salt, for larger lethalities close to 6.5, the effect of salt was evident only at low temperatures (<64°C). NaL did not seem to affect the heat resistance of Salmonella as much as the effects induced by the other variables studied. An omnibus model for predicting the lethality for given times and temperatures for ground beef matrices within the range studied was developed that reflects the convex survival curves that were observed. However, the standard errors of the predicted lethalities from this models are large, so consequently, a model, specific for predicting the times needed to obtained a lethality of 6.5 log10, was developed, using estimated results of times derived from the individual survival curves. For the latter model, the coefficient of variation (CV) of predicted times range from about 6 to 25%. For example, at 60°C, when increasing the concentration of salt from 0 to 4.5%, and assuming that the concentration of SPP is 0%, the time to reach a 6.5-log10 relative reduction is predicted to increase from 20 min (CV = 11%) to 48 min (CV = 15%), a 2.4 factor (CV = 19%). At 71.1°C (160°F) the model predicts that more than 0.5 min is needed to achieve a 6.5-log10 relative reduction.

Thermal Inactivation of Staphylococcus aureus in Retentates from Ultrafiltered Milk

1989 ◽  
Vol 52 (9) ◽  
pp. 631-637 ◽  
Author(s):  
JEFFREY L. KORNACKI ◽  
ELMER H. MARTH
Keyword(s):  
Staphylococcus Aureus ◽  
Heat Resistance ◽  
Thermal Inactivation ◽  
Thermal Protection ◽  
Skim Milk ◽  
Stationary Growth Phase ◽  
Plate Count ◽  
Mannitol Salt Agar ◽  
Whole Milk ◽  
D Values

Cells of Staphylococcus aureus strains 196E, 481, and 425 were thermally stressed at 56°C for 10 min in milk and enumerated on Plate Count Agar (PCA), Mannitol Salt Agar (MSA), and PCA with an overlay of MSA. PCA recovered more S. aureus 196E and 481 than did PCA/MSA, which recovered more than MSA. PCA/MSA recovered slightly more S. aureus 425 than did PCA, which recovered more than MSA. At 58°C, in order of decreasing heat resistance, the four strains of S. aureus originally isolated from food were 425 &gt; 100 and 481 &gt; 196E. Their D-values were 26,14,13, and 3.0 min, respectively. S. aureus 425 was more heat resistant in the stationary than in the log phase when heated at 58°C in whole milk. Heat resistance at 58°C increased overall during the stationary growth phase, but was fairly stable when the culture was from 17 to 25 h or from 41 to 49 h old. S. aureus 425 exhibited no consistent differences in heat resistance in concentrated (4X by volume) and unconcentrated skim or whole milk. Adjustments of protein (3.5–4.0% to 12.6–16%), milkfat (0.28–1.12% to 10%), and lactose (ca. 4.5–5.0% to ca. 14.5–15%) contents of milk and 4X (volume concentration) UF milk retentates afforded no significant thermal protection to S. aureus 425. Diafiltration of 4X skim milk reduced thermal protection of S. aureus 425 in the retentate over that of unconcentrated skim milk of the same lot when tested at 63 and 74°C. S. aureus 425 had greatest D-values (min) in skim milk (0.36 ± 0.05) and permeate (0.30 ± 0.14) followed by permeate from diafiltration (0.28 ± 0.06) when tested at 63°C.

Thermotolerance of Escherichia coli O157:H7 ATCC 43894, Escherichia coli B, and an rpoS-Deficient Mutant of Escherichia coliO157:H7 ATCC 43895 Following Exposure to 1.5% Acetic Acid

1998 ◽  
Vol 61 (9) ◽  
pp. 1184-1186 ◽  
Author(s):  
NICOLE C. WILLIAMS ◽  
STEVEN C. INGHAM
Keyword(s):  
Escherichia Coli ◽  
Acetic Acid ◽  
Heat Resistance ◽  
Acid Stress ◽  
Deficient Mutant ◽  
E Coli ◽  
Significant Difference ◽  
Stressed Cells ◽  
D Values ◽  
D Value

On a beef carcass, Escherichia coli may sequentially encounter acid- and heat-intervention steps. This study tested whether acid stress (1.5% [vol/vol] acetic acid, pH 4.0, 37°C, 15 min) would enhance subsequent heat resistance of E. coli. Initially, cells (E. coli O157:H7 ATCC 43894, nonpathogenic E. coli B [strain FRIK-124], and rpoS-deficient mutant 813-6 [derived from E. coli O157:H7 ATCC 43895]) were acid stressed and transferred to 54°C tiypticase soy broth (TSB), and survivors were immediately enumerated after at least three intervals of 12, 2, and 6 min, respectively, by plating. The ATCC 43894 and 813-6 strains survived the acid stress but strain FRIK-124 did not. Acid-stressed ATCC 43894 had significantly lower D values than the non-acid-stressed controls. Strain 813-6 had significantly lower D values than strain ATCC 43894, with no significant difference between acid-stressed and non-acid-stressed cells. In a second experiment, cooling of cells prior to plating resulted in an increased D value for acid-stressed ATCC 43894 cells, such that it was not significantly different from the D value for non-acid-stressed Controls. Using this protocol, there was no significant difference in D values between acid-stressed and non-acid-stressed ATCC 43894 cells in prewarmed TSB (54, 58, and 62°C), in prewarmed ground beef slurry (GBS; 58°C), or in TSB and GBS inoculated at 5°C and heated to 58°C. The acid stress tested does not enhance subsequent heat resistance of E. coli.

Thermal Inactivation of Escherichia coli O157:H7 Isolated from Ground Beef and Bovine Feces, and Suitability of Media for Enumeration

1998 ◽  
Vol 61 (3) ◽  
pp. 285-289 ◽  
Author(s):  
M. ROCELLE S. CLAVERO ◽  
LARRY R. BEUCHAT ◽  
MICHAEL P. DOYLE
Keyword(s):  
Escherichia Coli ◽  
Thermal Inactivation ◽  
Ground Beef ◽  
Treatment Temperature ◽  
Escherichia Coli O157 ◽  
E Coli ◽  
Polyethylene Bags ◽  
D Values ◽  
Bovine Feces

Rates of thermal inactivation of five strains of Escherichia coli O157:H7 isolated from ground beef implicated in outbreaks of hemorrhagic colitis and five strains isolated from bovine feces were determined. Ground beef (22% fat, 10 g), inoculated with individual test strains at populations ranging from 6.85 to 7.40 log10 CFU g−1 of beef, was formed into patties (0.3 cm thick and 8.0 cm in diameter) and sealed in polyethylene bags. For each strain and treatment temperature (54.4, 58.9, 62.8, 65.6, or 68.3°C), 6 bags were simultaneously immersed into a recirculating water bath. Viable cells in patties heated for various lengths of time were enumerated by plating diluted samples on sorbitol MacConkey agar supplemented with 4-methylumbelliferyl-β-d-glucuronide (MSMA) and modified eosin methylene blue (MEMB) agar. Regardless of strain or treatment temperature, higher numbers of E. coli O157:H7 cells were generally recovered on MEMB agar than on MSMA, indicating the inferiority of MSMA as a recovery medium for quantitative determination of E. coli O157:H7 cells in heat-processed ground beef. Significantly (P ≤ 0.05) higher D values when enumeration was done using MEMB agar compared with MSMA. Mean D values for combined strain data at 54.4, 58.9, 62.8, and 65.6°C from cultures on MEMB agar were 123.90, 6.47, 0.62, and 0.20 min, respectively, whereas D values of 25.5, 5.21, 0.57, and 0.18 min were obtained at the same temperatures from cultures on MSMA. Results suggest that cooking ground beef patties to an internal temperature of 68.3°C for 40 s will inactivate at least 99.99% of E. coli O157:H7 cells; z values of 4.0 and 5.1°C were calculated from mean D values obtained from MEMB agar and MSMA, respectively, as recovery media. Differences in D values and z values existed among strains but rates of thermal inactivation do not appear to be correlated with the sources of the isolates.

Thermal Inactivation of a Single Strain Each of Serotype O26:H11, O45:H2, O103:H2, O104:H4, O111:H−, O121:H19, O145:NM, and O157:H7 Cells of Shiga Toxin–Producing Escherichia coli in Wafers of Ground Beef†

2013 ◽  
Vol 76 (8) ◽  
pp. 1434-1437 ◽  
Author(s):  
J. B. LUCHANSKY ◽  
A. C. S. PORTO-FETT ◽  
B. A. SHOYER ◽  
J. PHILLIPS ◽  
D. EBLEN ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Shiga Toxin ◽  
Thermal Inactivation ◽  
Ground Beef ◽  
Sampling Time ◽  
Single Strain ◽  
E Coli ◽  
D Values ◽  
Cooking Times ◽  
Sterile Filter

For each of two trials, freshly ground beef of variable fat content (higher: 70:30 %lean:%fat; lower: 93:7 %lean:%fat) was separately inoculated with ca. 7.0 log CFU/g of a single strain of Escherichia coli serotypes O26:H11, O45:H2, O103:H2, O104:H4, O111:H−, O121:H19, O145:NM, and O157:H7. Next, ca. 3-g samples of inoculated beef were transferred into sterile filter bags and then flattened (ca. 1.0 mm thick) and vacuum sealed. For each temperature and sampling time, three bags of the inoculated wafers of beef were submerged in a thermostatically controlled water bath and heated to an internal temperature of 54.4°C (130°F) for up to 90 min, to 60°C (140°F) for up to 4 min, or to 65.6°C (150°F) for up to 0.26 min. In lower fat wafers, D-values ranged from 13.5 to 23.6 min, 0.6 to 1.2 min, and 0.05 to 0.08 min at 54.4, 60.0, and 65.6°C, respectively. Heating higher fat wafers to 54.4, 60.0, and 65.6°C generated D-values of 18.7 to 32.6, 0.7 to 1.1, and 0.05 to 0.2 min, respectively. In addition, we observed reductions of ca. 0.7 to 6.7 log CFU/g at 54.4°C after 90 min, ca. 1.1 to 6.1 log CFU/g at 60.0°C after 4 min, and 0.8 to 5.8 log CFU/g at 65.6°C after 0.26 min. Thus, cooking times and temperatures effective for inactivating a serotype O157:H7 strain of E. coli in ground beef were equally effective against the seven non-O157:H7 Shiga toxin–producing strains investigated herein.

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