Control of Thermal Meat Processing

Carl L. Griffis and Tareq M. Osaili

Thermal Processing

The recent growth of the market for ready-to-eat (RTE) meat and poultry products has led to serious concern over foodborne illnesses due to the presence of pathogens, particularly Salmonella spp, Listeria monocytogenes and Escherichia coli O157:H7 in meat and poultry products. Emphasis has been placed on thermal processing since heat treatment is still considered the primary means of eliminating foodborne pathogens from raw meat and poultry products (Juneja, Eblen, & Ransom, 2001). Inadequate time/temperature exposure during cooking is a contributing factor in food poisoning outbreaks. Optimal heat treatment is required not only to destroy pathogenic microorganisms in meat and poultry products but also to maintain desirable food quality and product yield.

Thermal destruction of pathogens is a time-temperature-dependent process. The time-temperature relationship of the thermal inactivation of pathogens has long been expressed with the concept of decimal reduction time (D-value) and thermal resistance constant (z-value). The D-value is defined as the time required to cause a 90% reduction of the microbial population at a specific temperature. It reflects the tolerance of a pathogen to an increase in heating time at a specific temperature. D-value at each temperature is calculated from the linear regression model between log10 of the bacteria survivors and heating time. The D-value is the negative inverse slope of the survivor curve (Equation 9.1). The z-value is the temperature difference required for the thermal inactivation curve to cause one log10

This chapter summarizes some of the published data on the thermal inactivation of some important foodborne pathogens, Salmonella spp., Listeria monocytogenes, and Escherichia coli O157:H7 in meat and poultry products.

Department of Biology and Agricultural Engineering, University of Arkansas, Fayetteville AR 72701, USA e-mail: [email protected]

F. Toldra (ed.), Safety of Meat and Processed Meat,

Food Microbiology and Food Safety, DOI 10.1007/978-0-387-89026-5_9,

© Springer Science+Business Media, LLC 2009

reduction. It is correlated with the tolerance of a specific pathogen to the temperature changes in the product. The z-value is calculated by determining the linear regression between log10 of D-values and temperature. The z-value is the negative inverse slope of the thermal resistance curve (Equation 9.2). To calculate D- and z-values, microbial inactivation has traditionally been assumed to follow first order kinetics; i.e., at a certain temperature, the log10 reduction of bacteria is linear over time (Heldman & Hartel, 1997). This assumption is applicable if (1) the relationship of t{T, N} = g{T}.f{N} describes the thermal inactivation of microbes, where t = heating time at certain temperature (T), N = number of survivors at time t (Kormendy & Kormendy, 1997); (2) the sub-lethality injury phenomenon is ignored; and (3) the heating effect on the microorganisms in the food sample is homogenous (Moats, 1971).

where,

N0 is the survivors at time 0. N is the survivors at time t.

where,

D0 is the decimal reduction time (min) at temperature T0 (°C). D is the decimal reduction time at temperature T AT is the difference between T and T0 (T-T0) z is thermal resistant constant (°C).

Efforts have been increasing to prevent foodborne illnesses and make the food supply safe. The USDA-FSIS (1999) issued a final rule that requires each processing schedule in a meat or poultry industry to achieve 6.5-D reduction in the population of a cocktail of Salmonella serotypes in RTE beef products and 7-D reduction of a cocktail of Salmonella serotypes in fully cooked poultry products. The regulation applies to high heat-resistant strains as well as strains that have been implicated in foodborne outbreaks. Thus, thermal inactivation parameters (D- and z-values) for a certain microorganism are necessary to calculate process lethality (F).

where,

T(t) is the product temperature at a time t and T (ref) is a reference temperature. This equation makes clear that z-value should be known in order to calculate the process lethality during cooking. The regulation can be met if the time obtained from the process lethality is equal to or more than the performance standard.

Thermal Inactivation Studies

Most thermal inactivation studies of foodborne pathogens in meat and poultry products have been conducted in metal or glass tubes or in plastic bags. In tubes, the destruction of microorganisms at high temperature is achieved in the outer part of the sample close to the tube wall, but high temperatures do not reach the center of the tubes, and therefore, a majority of the sample does not reach the desired temperature (Orta-Ramirez, 2002). To produce isothermal destruction conditions and more homogeneous heat transfer to the sample, meat samples can be placed in aseptic plastic bags (Juneja, Eblen, & Ransom, 2001; Murphy, Beard, Martin, Duncan, & Marcy, 2004; Osaili et al., 2007). The thickness of the plastic bags has an effect on the thermal inactivation of pathogens in the food sample in the bag. Increasing the thickness of the plastic bag reduces the thermal inactivation rate of pathogens (Murphy, Duncan, Marcy, Berrang, & Driscoll, 2002).

Although thermal destruction of pathogens in food is assumed to be linear with time, deviations from linear destruction with time have been observed by some researchers. These reports indicate that survival curves exhibit a shoulder or tailing. Shouldering phenomena may be related to the ability of treated microorganism to repair the damage at early stages of the exposure to heat. Senhaji and Lincin (1977) reported that the tailing phenomenon shows a variation in thermal resistance within the bacterial strains or accumulation of protective substances released from the destroyed cells.

Factors Affecting Thermal Inactivation of Pathogens in Meat and Poultry Products

Product's Characteristics

Intrinsic properties of the product have an influence on the heat resistance of pathogens associated with the product. Researchers have found varying results concerning the effect of fat content on thermal inactivation of pathogens in meat and poultry products. Some found that fat decreased the thermal resistance of pathogens (Juneja & Eblen, 2000; Kotrola, Conner, & Mikel, 1997), some reported that fat had no effect (Kotrola & Conner, 1997) and most found that fat increased the thermal resistance (Ahmed, Conner, & Huffman, 1995;

Fain et al., 1991; Juneja, Eblen, & Marks, 2001; Line et al., 1991; Maurer, Ryser, Booren, & Smith, 2000). Juneja and Eblen (2000) found that the D-values of a cocktail of eight strains of Salmonella Typhimurium DT104 in ground beef decreased with increasing fat content. Kotrola and Conner (1997) found increasing the fat level from 3 to 11% in ground turkey did not have a significant effect on the D-value of E. coli O157:H7 heated at 52.5°C, 55°C, and 60°C. Maurer et al. (2000) reported that D-values of Salmonella Senftenberg in turkey thighs at temperatures of 58-64°C increased as the fat content increased from 5.3 to 7.4%. Fain et al. (1991) found that fat had a protective effect against L. monocytogenes Scott A in ground beef at temperatures of 51.7-62.8°C. They reported D-values ranged from 81.3 to 0.6 min, and 71.7 to 1.2 min for lean (2%) and fatty beef (30.5%), respectively. Line et al. (1991), Ahmed et al. (1995) and Smith, Maurer, Orta-Ramirez, Ryser, and Smith (2001) have studied the effect of fat content on thermal inactivation of E. coli O157:H7 in beef and poultry. Line et al. (1991) found that the D-values of E. coli O157:H7 increased from 78.2 to 115.5 min at 51.7°C, from 4.1 to 5.3 min at 57.2°C and from 0.3 to 0.5 min at 62.8°C when the fat content increased in ground beef from 2 to 30.5%. Ahmed et al. (1995) found that when the fat content increased from 3 to 11% in turkey and chicken meat, the D-values increased at temperatures of 50-60°C. For chicken, the D-value at 50°C increased from 65.24 to 105.5 min, at 55°C the value increased from 8.76 to 9.74 min, and at 60°C it increased from 0.38 to 0.55 min. For turkey, the D-value at 50°C increased from 70.41 to 115 min, at 55°C the value increased from 6.37 to 8.76 min, and at 60°C it increased from 0.55 to 0.58 min. Smith et al. (2001) reported that the E. coli O157:H7 was more heat stable in beef containing 19% fat than 4.8% fat. Theories behind increased heat resistance of microorganisms in food products with higher fat contents relate to lower heat conductivity or reduced water activity (aw) in fat portion.

The thermal resistance of foodborne pathogens in food increases with the addition of salt, curing salts, and food additives (Farber, Huges, Holley, & Brown, 1989; Mackey, Pritchet, Norris, & Mead, 1990; Juneja, 2003; Juneja & Eblen, 1999; Murphy, Osaili, Duncan, & Marcy, 2004a). Murphy et al (2004a) found that the D-value of L. monocytogenes in ground chicken thigh and leg meat with the addition of 4.8% sodium lactate was 53-75% higher than that in the meat without sodium lactate, but, the thermal resistance of a cocktail of Salmonella in meat was not affected with addition of sodium lactate. Juneja (2003) found that sodium lactate and sodium diacetate increased thermal resistance of L. monocytogenes in meat. The D-values of meat mixed with both 4.8% sodium lactate and 0.25% sodium diacetate at 60°C, 65°C, 71.1 °C, and 73.9°C increased from 4.67, 0.75, 0.17, and 0.04 min to 13.95, 1.81, 0.16, and 0.07 min, respectively. The D-values of L. monocytogenes in meat treated with 4.8% sodium lactate alone increased to 14.34, 2.23, 0.22, and 0.13 min at the relevant temperatures. The D-values of meat mixed with 0.25% sodium diacetate increased to 4.69, 0.85, 0.17, and 0.08 min at the relevant temperatures. Huang and Juneja (2003) reported that sodium lactate (up to 4.5%) had no effect on thermal inactivation at 55-65°C of E. coli O157:H7 in ground beef. Maurer et al. (2000) and Juneja and Eblen (1999) found that NaCl increased the thermal resistance of Salmonella in ground turkey and L. monocytogenes in beef gravy, respectively. The science behind decreased heat resistance of microorganisms in food products with addition of salts relates to decreases in water activity, aw. As the aw of the heated medium decreased, the thermal resistance of the cells increased (Carlson, Marks, Booren, Ryser, & Orta-Ramirez, 2005). Carlson et al. (2005) found that the thermal resistance of Salmonella decreased 64% when decreasing meat aw from 0.99 to 0.95. Juneja (2003) and Juneja and Eblen (1999) found that a reduction in aw of ground meat decreased the penetration of the heat through the food, thus increasing the resistance of the pathogens to heat.

Pathogen's Characteristics

The pathogen's characteristics include the type and the strain of the bacterial pathogen, its growth condition, and the exposure to stresses.

In general, Gram-positive bacteria are more heat resistance than Gramnegative bacteria. The temperature at which cultures were grown would have an effect on the thermal resistance of the bacteria. Cultures grown at higher temperatures have been shown to be more thermally resistant than those grown at lower temperatures (Juneja & Eblen, 1999). Furthermore, length of incubation has an effect on the thermal resistance of the bacteria; cells in the stationary phase of growth are generally more heat resistant than cells in the logarithmic phase of growth (Lou & Yousef, 1996). Smith et al. (2001) reported that a Salmonella cocktail in ground beef was more heat resistant during stationary growth phase than during logarithmic growth phase. The D-values at temperature 55-63°C were in the range of 18.66-0.20 min and 16.34-0.15 min for the pathogen in stationary and log phase, respectively.

Farber and Brown (1990) reported that L. monocytogenes that had been previously heat shocked at 48°C for 120 min showed a 2.4-fold increase in the D-value at 64°C. Wesche, Marks, and Ryser (2005) found that heat shock at 54°C for 30 min increased the thermal resistance of Salmonella in comminuted turkey. While cold shock at 4°C for 2 h decreased the thermal resistance of the cells. Similarly, Mackey and Derrick (1987) observed that heat shock at 48°C for 30 min increased the thermal resistance of Salmonella Thompson at 54°C and 60°C about 2.4- and 2.7-fold, respectively, in minced beef. Juneja, Klein, and Marmer (1998) reported that thermal resistance of E. coli O157:H7 in beef gravy and ground beef increased about 1.5-fold when the cells were pre-exposed to sub-lethal heat. Smith et al. (2001) reported that starvation of Salmonella in peptone water for 14 days at 4°C decreased the thermal resistance of the microbe at 55-63°C in ground beef. Miller, Bayles, and Eblen (2000) reported a reduction in the D-value at 60°C of L. monocytogenes inoculated onto the surface of frankfurter skin following cold shocking at 0°C for 3 h.

Thermal Inactivation ofFoodborne Pathogens in Meat and Poultry Products

Thermal Inactivation of Salmonella in Meat

Thermal inactivation kinetics of a cocktail of Salmonella in beef has been reported. Goodfellow and Brown (1978) determined the D-values for a cocktail of Salmonella at temperatures of 51.6-62.7°C. The D-values ranged from 62 to 0.6 min, and the z-value was 5.6°C. Orta-Ramirez et al. (1997) reported D-values of Salmonella Senftenberg in ground beef at 58°C and 64°C of 15.17 and 2.08 min, respectively, and z-value of 6.25°C. Juneja, Eblen, & Ransom (2001) found that the D-values of a cocktail of Salmonella in beef at temperatures of 58-65°C ranged from 8.65 to 0.67 min, and the z-value was 6.01 °C while in ground pork the values ranged from 6.68 to 0.87 min and the z-value was 7.10°C. Juneja and Eblen (2000) reported D-values at 58-65°C for eight strain cocktail of Salmonella Typhimurium DT104 in beef containing 7-24% fat. The D-values in beef containing 7%, 12%, 18%, and 24% fat ranged from 3.22 to 0.70 min, 2.46 to 0.34 min, 2.49 to 0.41 min, and 1.61 to 0.18 min, respectively. Smith et al. (2001) found that that the D-values of a cocktail of Salmonella at stationary phase at 55-63°C in high-fat (19.1%) ground beef ranged from 18.66 to 0.20 min, and the z-value was 4.08°C. Quintavalla, Larini, Mutti, and Barbuti (2001) compared among the thermal resistance of eight Salmonella strains (Salmonella Typhimurium strains (ATCC 14028,133 and I116), Salmonella Derby B4373, Salmonella Potsdam I133, Salmonella Menston I79, Salmonella Eppendorf I66, and Salmonella Kingston I124) in pork meat containing curing additives. They found that Salmonella Potsdam strain was the most resistant one, with D-values at 58-63°C ranged from 4.8 to 0.3 min, while the most sensitive strain was Salmonella Kingston, with D-values ranged from 2.79 to 0.24 min, at the same temperatures. Murphy, Duncan, Johnson, Davis, and Smith (2002) determined D- and z-values at temperatures of 55-70°C for a cocktail of Salmonella in different commercial meat products including beef patties and blended beef and turkey patties. The D-values in beef patties and blended beef and turkey patties ranged from 9.09 to 0.25 min and from 20.58 to 0.37 min, respectively, and the z-values were 9.14 and 8.35°C, for beef patties and blended beef and turkey patties, respectively. Murphy, Beard, Martin, Keener, and Osaili (2004) reported D-values for a cocktail of Salmonella in the range of 41.02-0.10 min in ground and formulated beef/turkey at 55-70°C. Murphy, Beard, Martin, Duncan, et al. (2004) and Murphy, Martin, Duncan, Beard, and Marcy (2004) reported D-values at 55-70°C for a cocktail of Salmonella in ground pork and ground beef in the range of 45.87-0.083 min and 37.05-0.066 min, respectively, and z-values of 5.89°C and 5.74°C, respectively. Osaili et al. (2007) and Osaili, Griffis, Martin, Beard, et al. (2006) reported that the D-values of a cocktail of Salmonella in chicken fried beef and breaded pork patties at 55-70°C ranged from 67.68 to 0.22 min and 69.48 to 0.29 min and the z-value of 6.0°C and 6.2°C, respectively.

The differences in the thermal inactivation parameters (D- and z-values) could be due to differences in methodology used for recovery of survivors, physiological condition of the cells sample size, or meat composition. Bigger samples might have longer come-up time leading to larger D-values.

Table 9.1 shows some of the reported D- and z-values for Salmonella in meat.

Thermal Inactivation of Salmonella in Poultry

Thermal inactivation kinetics of Salmonella in chicken breast and turkey meat has been studied. Hussemann and Buyske (1954) studied the thermal death temperature-time relationships of Salmonella Typhimurium in chicken muscle. Salmonella was mixed with ground chicken muscle and heated in glass test tubes in an oil bath to temperatures of 75°C, 80°C, 85°C, and 90°C for 3, 5,10,15,20, and 40 min. At 75°C for 5 min, 75% of the samples showed survivors of Salmonella. At 90°C for 15, 20, and 40 min, there were no survivors of Salmonella. Veeramuthu, Price, Davis, Booren, and Smith (1998) calculated the D-values of Salmonella Senftenberg in turkey thigh (4.35% fat) at temperatures of 55, 60, and 65°C. The values were 211.4-227.2 min, 13.2-13.6 min and 3.11-3.4 min, respectively, depending on the recovery method used, and z-values were 5.4-5.6°C. At temperatures of 56-63°C, Mazzotta (2000) found that the D-values of a cocktail of Salmonella in chicken breast meat ranged from 3.2 to 0.18 min and the z-value was 5.7°C. Juneja, Eblen, & Ransom (2001) found that the D-values of a cocktail of Salmonella at temperatures of 58-65°C ranged from 7.42 to 0.80 min in ground turkey (9% fat), and from 7.08 to 0.59 min in ground chicken (7% fat). The z-values in turkey and chicken were 6.88 and 6.11°C, respectively. At temperatures of 55-70°C, Murphy, Marks, Johnson, and Johnson (2000) and Murphy, Duncan, Berrang, Marcy, and Wolfe (2002) found the D-values for a cocktail of Salmonella in raw and fully cooked chicken breast meat were 30.10-0.24 min, 24.071-0.097 min, respectively, and the z-value was 6.53 and 6.26°C, respectively. Murphy, Duncan, Beard, and Driscoll (2003) compared among the thermal resistance of a cocktail of Salmonella in fully cooked poultry products including duck muscle meat, duck skin, and turkey breast meat. The D-values at 55-70°C in the relevant products ranged from 28.57 to 0.11 min, 25.32 to 0.17 min, 24.69 to 0.12 min, and 24.07 to 0.10 min, respectively. Murphy et al. (2000) and Murphy, Duncan, Johnson, et al. (2002) determined D- and z-values at temperatures of 55-70°C for a cocktail of Salmonella in ground chicken breast meat and in different commercial meat products including chicken patties and chicken tender. The D-values in the ground chicken breast, chicken patties, and chicken tender ranged from 30.1 to 0.238 min, 26.97 to 0.32 min, and 22.37 to 0.32 min, respectively, and the z-values were 6.53°C, 7.60°C, and 7.61°C for ground chicken breast, chicken patties, and chicken tender, respectively. Murphy, Martin, et al. (2004) reported D-values at 55-70°C for a cocktail of Salmonella in ground turkey in the range of 43.10-0.096 min and z-value of 5.96°C. Murphy et al. (2004a) and Murphy, Osaili, Duncan, and Marcy (2004b) studied

Table 9.1 D- and ^-values of Salmonella spp in meat uj

Temperature °C

Table 9.1 D- and ^-values of Salmonella spp in meat

Temperature °C

Medium

Strain

55.0

57.5

58.0

60.0

61.0

62.5

63.0

64.0

65.0

67.5

70.0

r-value

References

Beef

Cocktail

37.05

18.35

6.90

2.62

1.03

0.30

0.07

5.74

Murphy. Martin, et al. (2004)

Beef (12% fat)

Cocktail

2.46

1.43

0.24

0.34

5.66

Juneja and Eblen (2000)

Beef (12.5% fat)

Cocktail

8.65

5.48

1.50

0.67

6.01

Juneja. Eblen. and Ransom (2001)

Beef (18% fat)

Cocktail

2.49

0.48

1.98

0.41

5.47

Juneja and Eblen (2000)

Beef (19.1% fat)

Senftenberg

21.79

3.38

0.92

4.51

Smith et al. (2001)

Beef (19.1% fat)

DT104-10127

21.98

2.63

0.65

0.16

4.28

Smith et al. (2001)

Beef (24% fat)

Cocktail

1.61

0.48

2.35

0.18

6.99

Juneja and Eblen (2000)

Beef (4.8% fat)

DTI 04-01071

10.27

2.06

0.43

0.14

4.77

Smith et al. (2001)

Beef (7% fat)

Typhimurium

3.22

1.75

0.27

0.70

8.08

Juneja and Eblen (2000)

Beef patties

Cocktail

9.09

7.70

4.80

2.40

0.97

0.57

0.25

9.14

Murphy. Duncan. Johnson, et al. (2002)

(19% fat)

Beef (4.8% fat)

DT104-10127

9.05

2.26

0.57

0.15

0.15

5.07

Smith et al. (2001)

Beef (4.8% fat)

DT104-10601

10.55

2.15

0.41

0.07

4.13

Smith et al. (2001)

Beef/turkey

Cocktail

41.02

15.15

5.60

2.07

0.76

0.28

0.10

5.83

Murphy. Beard. Martin. Keener, et al.

(10% fat)

(2004)

Beef/turkey

Cocktail

20.58

12.89

4.42

2.04

1.03

0.71

0.37

8.35

Murphy. Duncan. Johnson, et al. (2002)

(20% fat)

Franks (24% fat)

Cocktail

14.73

6.67

5.63

4.38

1.64

0.78

0.39

9.83

Murphy. Duncan. Johnson, et al. (2002)

Beef (14.6% fat)

Cocktail

67.68

27.31

15.51

5.61

2.00

0.50

0.22

6.00

Osaili. Griffis, Martin. Beard, et al. (2006)

Beef

Senftenbery

15.17

2.08

6.25

Ort-Ramirez et al. (1997)

Beef (19.1% fat)

Cocktail

18.66

3.39

0.57

0.20

4.08

Smith et al. (2001)

Beef (25% fat)

Cocktail

19.31

9.30

4.72

8.06

Juneja (2003 )

Pork

Cocktail

45.87

26.67

5.07

2.56

1.91

0.36

0.08

5.89

Murphy. Beard. Martin. Duncan, et al. (2004)

Pork

Cocktail

69.48

29.99

15.20

7.71

2.64

0.61

0.29

6.20

Osaili et al. (2007)

Pork (8.5% fat)

Cocktail

6.68

6.65

1.62

0.87

7.10

Juneja. Eblen. and Ransom (2001)

in the thermal inactivation of a cocktail of Salmonella in ground chicken thigh/leg meat alone or mixed with 4.8% sodium lactate and in skin as varieties of value-added poultry products contain skin. They reported D-values of 43.76-0.07 min in the plain meat, 43.78-0.08 min in meat mixed with 4.8% sodium lactate, and 43.33-0.09 min in chicken skin at 55-70°C. The z-values were 5.46°C, 5.46°C, and 5.56°C in the relevant products. The D-values of Salmonella in meat were significantly different than that in skin at 60-70°C.

Table 9.2 shows some of the reported D- and z-values for Salmonella in poultry.

Thermal Inactivation of L. monocytogenes in Meat

Thermal inactivation kinetics of L. monocytogenes in beef meat has been calculated. Farber et al. (1989) determined the thermal resistance of a cocktail of L. monocytogenes at 56-64°C in pork-beef meat mixture (66% pork and 33% beef) and pork-beef mixture with cure. The D-values in plain meat at 56-62° C ranged from 14.18 to 1.01 min and the values in meat with cure at 58-64°C ranged from 50.0 to 1.28 min. Boyle, Sofos, and Schmidt (1990) found that D-values of L. monocytogenes Scott A in meat slurry at temperatures of 60-70°C were 2.54-0.23 min. Fain et al. (1991) found that the D-values for L. monocytogenes Scott A in lean beef at temperatures of 51.2-62.7°C were 81.3-0.6 min, respectively, and the value was 9.3F. Schoeni, Brunner, and Doyle (1991) determined the thermal resistance of a cocktail of L. monocyto-genes in ground beef roast and fermented beaker sausage. The D-values in ground beef roast at 54.4-62.8°C were in the range of 22.4-2.56 min and in fermented beaker sausage at 48.9-60°C were in the range of 98.6-9.13 min. Doherty et al. (1998) calculated the D-values for L. monocytogenes in minced beef heated in vacuum bags at temperatures of 50-60°C. The values ranged from 43.5 to 0.24 min. Murphy, Duncan, Johnson, et al. (2002) determined D- and z-values at temperatures of 55-70°C for L. innocua, which was developed as a heat resistance model for L. monocytogenes, in different commercial meat products including beef patties and blended beef and turkey patties. The D-values in beef patties and blended beef and turkey patties ranged from 19.52 to 0.29 min and from 46.08 to 0.18 min, respectively, and the z-values were 8.67 and 6.41°C, for beef patties and blended beef and turkey patties, respectively. Murphy, Beard, Martin, Duncan, et al. (2004) and Murphy, Martin, et al. (2004) reported D-values at 55-70°C for a cocktail of L. monocytogenes in ground pork and ground beef in the range of 47.17-0.085 min and from 36.91 to 0.063 min, respectively, and z-values of 5.92°C and 6.01°C, respectively. Murphy, Beard, Martin, Keener, et al. (2004) reported D-values for a cocktail of L. monocytogenes in the range of 50.35-0.13 min in ground and formulated beef/turkey at 55-70°C. Osaili, Griffis, Martin, Beard, et al. (2006) and Osaili et al. (2007) reported D-values in chicken fried beef and breaded pork patties at 55-70°C of 81.37-0.31 min and from 150.46 to 0.43 min and z-value of 6.1°C and 5.9°C, respectively.

Table 9.2 D- and ^-values of Salmonella spp in poultry

Temperature °C

Table 9.2 D- and ^-values of Salmonella spp in poultry

Temperature °C

Medium

Strain

55.0

56.0

57.5

58.0

60.0

62.0

62.5

63.0

65.0

67.5

70.0

r-value

References

Chicken

3.20

0.60

0.31

0.18

5.70

Mazzotta (2000)

Chicken

Cocktail

30.10

12.90

5.88

2.51

1.16

0.36

0.24

6.53

Murphy et al. (2000)

Chicken (meat)

Cocktail

43.76

13.66

5.72

1.62

0.55

0.19

0.07

5.34

Murphy. Osaili. Duncan, and Marcy (2004b)

Chicken (skin)

Cocktail

43.33

14.09

7.31

2.21

0.79

0.23

0.09

5.56

Murphy. Osaili. Duncan, and Marcy (2004b)

Chicken breast

Cocktail

0.29

0.18

Murphy et al. (1999)

Chicken thigh/leg

Cocktail

43.76

13.66

5.72

1.62

0.55

0.19

0.07

5.46

Murphy, Osaili, Duncan, and Marcy

meat

(2004a)

Chicken thigh/leg

Cocktail

43.78

13.00

4.76

1.77

0.66

0.20

0.08

5.46

Murphy, Osaili, Duncan, and Marcy

meat

(2004a)

Chicken (7% fat)

Cocktail

7.08

5.20

1.36

0.59

6.11

Juneja, Eblen, and Ransom (2001)

Cooked turkey breast

Cocktail

24.69

8.67

5.20

1.85

0.62

0.19

0.12

6.23

Murphy, Duncan, Beard, et al. (2003)

Cooked chicken

Cocktail

24.07

9.60

3.83

1.53

0.61

0.24

0.10

6.26

Murphy, Beard, Martin, Duncan, et al. (2004)

Cooked chicken breast

Cocktail

24.07

9.60

3.83

1.53

0.61

0.24

0.10

6.26

Murphy, Duncan, Beard, et al. (2003)

Chicken (12% fat)

Cocktail

9.04

5.50

1.30

0.50

Juneja, Eblen, and Marks (2001)

Chicken (2% fat)

Cocktail

7.38

4.83

1.14

0.41

Juneja, Eblen, and Marks (2001)

Chicken (6.3% fat)

Cocktail

7.33

4.68

1.16

0.51

Juneja, Eblen, and Marks (2001)

Chicken (9% fat)

Cocktail

8.54

5.40

1.16

0.53

Juneja, Eblen, and Marks (2001)

Turkey (1% fat)

Cocktail

7.50

4.56

1.53

0.59

Juneja, Eblen, and Marks (2001)

Turkey (10% fat)

Cocktail

6.91

5.13

1.45

0.57

Juneja, Eblen, and Marks (2001)

Turkey (12% fat)

Cocktail

7.41

5.43

1.78

0.59

Juneja, Eblen, and Marks (2001)

Turkey (7% fat)

Cocktail

7.71

4.94

1.85

0.55

Juneja, Eblen, and Marks (2001)

Raw chicken patties

Cocktail

26.97

14.55

8.09

3.98

1.39

0.61

0.32

7.60

Murphy, Duncan, Johnson, et al. (2002)

Raw chicken tenders

Cocktail

22.37

9.92

8.50

4.55

1.25

0.38

0.32

7.61

Murphy, Duncan, Johnson, et al. (2002)

Roast duck skin

Cocktail

25.32

14.47

4.30

2.46

1.21

0.49

0.17

7.01

Murphy, Duncan, Beard, et al. (2003)

Roast duck meat

Cocktail

28.57

14.31

6.79

2.09

0.58

0.20

0.11

5.82

Murphy, Duncan, Beard, et al. (2003)

Turkey (5.4% fat)

Cocktail

43.10

10.69

6.73

2.54

1.51

0.29

0.10

5.96

Murphy. Martin, et al. (2004)

Turkey (9% fat)

Cocktail

7.42

4.82

1.51

0.80

6.88

Juneja, Eblen, and Ransom (2001)

Table 9.3 shows some of the reported D- and z-values for L. monocytogenes in meat.

Thermal Inactivation of L. monocytogenes in Poultry

Murphy et al. (2000) and Murphy, Duncan, Berrang, et al. (2002) studied the thermal inactivation of L. innocua in raw and fully cooked chicken breast meat at temperatures of 55-70°C. The D-values ranged from 50.8 to 0.187 min and 56.169 to 0.126 min, respectively, and the z-values were 6.29 and 5.67 °C, respectively. Murphy, Duncan, Johnson, et al. (2002) determined the D- and z-values for L. innocua in different commercial meat products including chicken patties and chicken tenders at temperatures of 55-70°C. The D-values of chicken patties and chicken tenders ranged from 191.94 to 0.21 min and 128.21 to 0.29 min, respectively, and the z-values were 4.86°C and 5.55°C for chicken patties and chicken tenders, respectively. Murphy, Duncan, Beard, et al. (2003) compared among the thermal resistance of a cocktail of L. monocytogenes in fully cooked poultry products including duck muscle meat, duck skin, turkey breast meat, and chicken breast meat. The D-values at 55-70°C in the relevant products ranged from 131.58 to 0.11 min, 82.65 to 0.21 min, 119.05 to 0.21 min, and 51.02 to 0.13 min, respectively. Murphy, Martin, et al. (2004) reported D-values at 55-70°C for a cocktail of L. monocytogenes in ground turkey in the range of 33.11-0.12 min and z-value of 5.90°C. Murphy et al. (2004a, 2004b) studied the thermal inactivation of a cocktail of L. monocytogenes in ground chicken thigh/leg meat alone or with 4.8% sodium lactate and in skin and reported D-values at 55-70°C of 38.94-0.04 min in the plain meat, 82.75-0.11 min in the meat with 4.8% sodium lactate and 34.05-0.05 min in the skin. The z-values were 5.08°C, 5.28°C, and 5.27°C in the relevant products. The D-values of L. monocytogenes in meat were significantly different than those in skin at a temperature of 60-70°C.

Table 9.4 shows some of the reported D- and z-values for L. monocytogenes in poultry.

Thermal Inactivation of E. coli O157:H7 in Meat

Line et al. (1991) determined the D- and z-values of E. coli O157:H7 in the lean and fatty ground beef using plate count agar. They reported D-values at 51.7-62.7°C in the range of 78.2-0.30 min and 115.5-0.47 min in lean and fatty meat, respectively and z-values of 8.3 and 8.4f in lean and fatty meat, respectively. Ahmed et al. (1995) reported D-values for E. coli O157:H7 isolate 204P in the range of 55.34-0.45, 80.66-0.46 min and 92.67-0.47 min in beef containing 7%, 10%, and 20% fat, respectively, and D-values in the range of 49.50-0.37, 62.90-0.46, and 80.64-0.55 in pork sausage containing 7%, 10%, and 20% fat, respectively, at temperature range of 50-60°C. Also, they reported z-values of 4.78°C, 4.44°C, and 4.35°C for the pathogen in beef containing 7%, 10%, and 20% fat, respectively, and 4.72, 4.67, and 4.61 in pork sausage

Table 9.3 D- and ^-values of Listeria monocytogenes in meat

Temperature °C

Table 9.3 D- and ^-values of Listeria monocytogenes in meat

Temperature °C

Medium

Strain

55

57.5

58

60

62

62.5

64

65

66

67.5 68

70

r-value

References

Beef

Cocktail

21

3.8

0.93

7.2

Mackey et al. (1990)

Beef

Cocktail

36.91

11.28

3.91

2.4

1.41

0.39

0.063

6.01

Murphy. Martin, et al. (2004)

Beef (14.6%)

Cocktail

81.32

40.49

22.98

7.15

2.81

0.93

0.31

6.1

Osaili. Griffis, Martin. Beard, et al. (2006)

Beef (30.5% fat)

Scott A

1.2

11.4

Fain et al. (1991)

Beef (2% fat)

Scott A

0.6

9.3

Fain et al. (1991)

Beef «7% fat)

Cocktail

8.32

4.2

2.19

0.94

0.35

5.98

Gaze. Brown. Gaskell, and Banks (1989)

Beef «7% fat)

Cocktail

6.27

2.9

2.21

0.93

0.27

5.98

Gazeet al. (1989)

Beef/turkey

Cocktail

50.35

18.6

6.87

2.54

0.94

0.35

0.13

5.9

Murphy. Beard. Martin. Keener, et al. (2004)

Beef roast

Cocktail

4.47

Schoeniet al. (1991)

Beef (25% fat)

Cocktail

27.69

9.63

4.18

6.1

Juneja (2003)

Ground meat

Cocktail

6.39

3.12

1.01

4.92

Farber et al. (1989)

Meat + cure

Cocktail

50

16.7

7.06

1.28

3.5

Farber et al. (1989)

Hot dog batter

Cocktail Cocktail

14.6 15.5

3.3

0.65 0.7

5.9 6

Mazzotta and Gombas (2001) Mazzotta and Gombas (2001)

Hot dog batter

Cocktail

11

1.8

0.4

5.6

Mazzotta and Gombas (2001)

Hot dog batter

Cocktail

8.1

1.8

0.23

5.2

Mazzotta and Gombas (2001)

Meat slurry (1.23%)

Scott A

2.54

0.75

0.23

Boyle et al. (1990)

Minced beef

Cocktail

3.4

0.31

4.9

Bolton et al. (2000)

Minced beef

Cocktail

3.2

0.15

4.2

Bolton et al. (2000)

Minced beef

Cocktail

5.9

Bolton et al. (2000)

Beef

Cocktail

1.62

Schoeniet al. (1991)

Pork (40.2% fat)

Cocktail

47.17

22.32

5.61

2.87

1.5

0.44

0.085

5.92

Murphy. Beard. Martin. Duncan, et al. (2004)

Pork (23% fat)

Cocktail

150.46

55.08

20.61

10.64

3.08

1.15

0.43

5.9

Osaili et al. (2007)

Sausage

Cocktail

9.13

Schoeniet al. (1991)

Table 9.4 D- and ^-values of Listeria monocytogenes in poultry

Temperature °C

Table 9.4 D- and ^-values of Listeria monocytogenes in poultry

Temperature °C

Medium

Strain

55

57.5

60

62

62.5

64

65

66

67.5

68

70

^-value

References

Chicken (thigh/leg)

Cocktail

38.94

9.67

2.04

1.01

0.30

0.10

0.04

5.08

Murphy, Osaili, Duncan, and Marcy (2004b)

Chicken (47.4% fat,

Cocktail

34.05

10.19

3.95

1.37

0.41

0.13

0.05

5.27

Murphy, Osaili, Duncan, and

skin)

Marcy (2004b)

Chicken breast

Cocktail

5.29

2.51

1.56

0.68

0.38

0.16

6.72

Gaze et al. (1989)

Chicken breast

Cocktail

5.02

2.21

1.84

0.95

0.41

0.20

7.39

Gaze et al. (1989)

Chicken breast

Cocktail

13.00

8.70

0.52

0.13

6.30

Mackey et al. (1990)

Chicken leg

Cocktail

14.00

5.60

0.53

0.11

6.70

Mackey et al. (1990)

Chicken leg quarter

Cocktail

131.58

23.64

9.84

2.23

0.93

0.42

0.11

5.76

Murphy, Driscoll, et al. (2003)

meat

Chicken leg quarter

Cocktail

82.65

21.69

8.90

3.57

1.16

0.40

0.21

5.04

Murphy, Driscoll, et al. (2003)

skin

Cooked chicken

Cocktail

51.02

13.93

8.49

2.60

0.65

0.29

0.13

5.71

Murphy, Duncan, Beard, et al.

breast

(2003)

Cooked turkey

Cocktail

119.05

40.16

16.70

4.54

1.29

0.46

0.21

5.29

Murphy, Duncan, Beard, et al.

breast

(2003)

Duck muscle

Cocktail

131.58

23.64

9.84

2.23

0.93

0.42

0.11

5.04

Murphy, Duncan, Beard, et al. (2003)

Duck skin

Cocktail

82.65

21.69

8.90

3.57

1.16

0.40

0.21

5.76

Murphy, Duncan, Beard, et al. (2003)

Thigh and leg meat

Cocktail

82.75

26.54

7.78

2.50

1.07

0.40

0.11

5.28

Murphy, Osaili, Duncan, and Marcy (2004a)

Thigh and leg meat

Cocktail

38.94

9.67

2.04

1.01

0.30

0.10

0.04

5.28

Murphy, Osaili, Duncan, and Marcy (2004a)

Turkey

Cocktail

33.11

17.09

8.05

2.88

0.92

0.28

0.12

5.90

Murphy, Martin, et al. (2004)

containing 7%, 10%, and 20% fat, respectively. Juneja, Snyder, and Marmer (1997) reported D-values in the range of 21.13-0.39 min at 55-65°C in beef and z-value of 5.98°C. Smith et al. (2001) reported D-values in low-fat beef (4.8%) in the range of 20.08-0.16 min and in high-fat beef (19.1%) in the range of 22.47-0.18 min at 55-63°C. The z-values in high- and low-fat beef were 3.79°C and 3.60°C, respectively. Byrne, Bolton, Sheridan, Blair, and McDowell (2002) found that commercial production and product formulation had an effect on the heat resistance of E. coli O157:H7 (NCTC 12900) in beefburger. They found that the D-values at 55-65°C in quality formulations subjected to freezing ranged from 9.3 to 0.5 min compared with 20.8 to 0.6 min in unfrozen sample. While the D-values in unfrozen economy formulation samples ranged from 41.1 to 0.7 min and in frozen samples ranged from 11.7 to 0.6 min at 55°C, 60°C, and 65°C, respectively. Huage and Juneja (2003) reported D-values in lean ground beef containing 0, 1.5, 3.0, and 4.5 sodium lactate in the range of 11.13-0.75, 11.16-0.73, 10.91-0.71, and 11.02-0.73, respectively, at 55-65°C. Murphy, Beard, Martin, Duncan, et al. (2004) and Murphy, Martin, et al. (2004) and Murphy, Davidson, and Marcy (2004) reported D-values for a cocktail of E. coli O157:H7 in ground pork, raw formulated frank (containing beef, pork, and chicken), fully cooked frank, and ground beef in the range of 33.44-0.048 min, 21.36-0.031 min, 24.91-0.038 min, and 21.56-0.055 min, respectively, at 55-70°C and z-values of 4.94°C, 5.07°C, 5.08°C, and 5.43°C, respectively. Murphy, Beard, Martin, Keener, et al. (2004) reported D-values for a cocktail of E. coli O157:H7 in the range of 23.23-0.03 min in ground and formulated beef/turkey at 55-70°C. Osaili, Griffis, Martin, Beard, et al. (2006) and Osaili et al. (2007) reported D-values in chicken fried beef and breaded pork patties at 55-70°C of 27.62-0.04 min and 32.11-0.08 min and z-values of 5.2°C and 5.4°C, respectively.

Table 9.5 shows some of the reported D- and z-values for E. coli O157:H7 in meat.

Thermal Inactivation of E. coli O157:H7 in Poultry

Ahmed et al. (1995) reported D-values for E. coli O157:H7 isolate 204P in the range of 65.24-0.38 and 105.5-0.55 min in chicken containing 3% and 11% fat, respectively, and D-values in the range of 70.41-0.55 and 115.0-0.58 min in turkey containing 3% and 11% fat, respectively, at temperature range of 50-60°C. They reported z-value of 4.48°C and 4.38°C for the pathogen in chicken containing 3 and 11% fat, respectively, and 4.74 and 4.35 in turkey containing 3 and 11% fat, respectively. Kotrola and Conner (1997) reported D-values at 52-60°C in low- (3%) and high-fat (11%) content turkey meat with or without 8% NaCl, 4% sodium lactate or a mixture of 8% NaCl, 4% sodium lactate and 0.5% polyphosphate. The D-values ranged from 42.3 to 0.9 min, 83.6 to 1.4 min, 75.1 to 0.9 min, and -103.3 to 2.4 min in plain low-fat meat, meat with NaCl, meat with sodium lactate, and meat with salt mix, respectively. In plain high-fat meat, meat with NaCl, meat with sodium lactate, and meat

Table 9.5 D- and ^-values of Escherichia coli 0157:H7 in meat

Temperature °C

Table 9.5 D- and ^-values of Escherichia coli 0157:H7 in meat

Temperature °C

Medium

Strain

50

52

55

57.5

58

60

61

62.5

63

65

67.5

+1 0

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