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Acta Veterinaria Scandinavica

  • Original article
  • Open Access

Heat Resistance in Liquids of Enterococcus spp., Listeria spp., Escherichia coli, Yersinia enterocolitica, Salmonella spp. and Campylobacterspp

  • 1
Acta Veterinaria Scandinavica200344:1

https://doi.org/10.1186/1751-0147-44-1

©  The Author(s) 2002

Received: 11 September 2002

Accepted: 28 October 2002

Published: 31 March 2003

Abstract

The aim of the work was to collect, evaluate, summarize and compare heat resistance data reported for Campylobacter, Enterococcus, Escherichia, Listeria, Salmonella and Yersinia spp. The work was limited to resistance in liquids with pH values 6–8. Results obtained under similar experimental conditions were sought. Thermal destruction lines for the various bacterial groups studied were constructed using log10 D values and treatment temperatures. There was a good linear relationship between log10 D and temperature with Escherichia coli, listerias and salmonellas. For campylobacters, enterococci and yersinias the relationships were weaker but, nevertheless, present. Using the slopes of the lines and their 95% confidence limits, z values and their 95% confidence limits were calculated. z values were compared with z values obtained from reports. The equations for the lines were also used for calculation of predicted means of D values at various treatment temperatures. 95% confidence limits on predicted means of D values and on predicted individual D values were also calculated. Lines and values are shown in figures and tables. Differences in heat resistance noted between and within the bacterial groups studied are discussed.

Keywords

  • Campylobacter jejuni/coli
  • Enterococcus faecalis
  • Enterococcus faecium
  • Escherichia coli
  • Listeria innocua
  • Listeria ivanovii
  • Listeria monocytogenes
  • Listeria seeligeri
  • Listeria welshimeri
  • Salmonella
  • Yersinia enterocolitica
  • thermal resistance
  • influencing factors
  • methods of determination
  • differences between species
  • differences between strains.

Sammanfattning

Värmeresistens i vätskor hos Enterococcus-, Listeria-, Escherichia-, Yersinia- , Salmonella- and Campylobacter-arter.

Introduction

Microbiologists now and then need heat resistance data for various microorganisms. In the literature, data of this kind are frequently based on reports from few investigations. To collect the data required, however, may be a laborious and time-consuming task for the individual user. The literature is generally extensive and many factors that may have influenced the results reported must be taken into consideration (for general information on influencing factors, see e.g. [71, 163, 137]). Furthermore, the presentations of results often differ essentially.

The aim of the present work was to collect, summarize, evaluate and compare heat resistance data reported for Campylobacter, Enterococcus, Escherichia, Listeria, Salmonella and Yersinia spp. As it was well known that considerably more heat resistance results were published from investigations with liquids than from those with other heating menstrua, it was considered appropriate to base the work on results obtained in liquids. Moreover, results of this kind could be expected to reflect the inherent heat resistance of the bacteria investigated better than those obtained in more complex heating menstrua.

Reports published until 2000 were studied. Data produced under experimental conditions as similar as possible were sought. This meant that results from some kinds of experiments were excluded. The various types of excluded data are given below under the different subheadings in Experimental conditions. It should be mentioned here that extensive reviews of heat resistance data reported for Escherichia coli O157:H7, Listeria monocytogenes and Salmonella spp. have been published recently by [162, 43] and [42], respectively. However, the aims and the selections and analyses of data in these reviews differ from those in the present work.

Bacteria

The work deals with the following bacteria: Campylobacter jejuni/coli, Enterococcus faecalis, Enterococcus faecium, Escherichia coli, Listeria innocua, Listeria ivanovii, Listeria monocytogenes, Listeria seeligeri, Listeria welshimeri, Salmonella spp. and Yersinia enterocolitica. Some of these bacteria are well-known food-associated human pathogens, others are utilized – enterococci and E. coli – or proposed – L. innocua [56, 48] – as indicators. Some types of E. coli also appear as food-linked human pathogens [119, 121, 122, 27, 29, 86, 10, 174, 62, 93] and enterococci have recently emerged as one of the leading causes of nosocomial, non-food-associated, infections [94].

Experimental conditions

Growth of test bacteria

In most cases the bacteria were grown in conventional media. In some investigations the growth media were milk, liquid egg products or clarified cabbage juice. The pH values of the media were given in some cases. The values varied from 5.6 to 7.4. Enterococci, E. coli, listerias and salmonellas were incubated aerobically at 30–37°C and Y. enterocolitica aerobically at 25–37°C. Campylobacters were grown microaerobically at 35–43°C. In the great majority of cases the bacteria were incubated for 12–48 h, i.e. they could be considered to have reached the late logarithmic or stationary growth phase. At stationary growth phase, bacterial heat resistance is at a maximum [46, 173, 99, 102, 9, 125, 77, 86, 105, 93, 131, 132].

Heat resistance results obtained for bacteria grown under carbon, glucose or nitrogen starvation or other stress conditions (see e.g. [125, 87, 105]) were not used in the present work.

Conditions between growth and heat treatment

Results recorded for bacteria subjected to stress conditions prior to heat treatment were not used: sublethal heat shock (see e.g. [108, 110, 111, 19, 20, 121, 122, 12, 82, 54, 53, 153], alkaline stress [81, 84], acid stress [49, 103, 175], osmotic stress [89] or other types of stress (see e.g. [12, 54, 53]).

Heating menstrua

Heating menstrua used were milk and liquid milk products, broths, physiological saline and other salt solutions, liquid egg products, diluted soups, scalding waters used at chicken or pig slaughter, and some other liquids. Heat resistance results obtained in menstrua with pH values of approx. 6–8 were used in the present work, as the bacterial species investigated are known to have their maximum heat resistances in this pH range (see e.g. [5, 99, 174, 60, 80, 148, 128, 10, 131, 138]). Results from experiments where salts, fats, carbohydrates, proteins or other substances were added to the heating menstrua with the aim of influencing the heat resistance of the test bacteria were excluded (see e.g. [100, 22, 5, 66, 170, 31, 3, 133, 10, 96]).

Heat treatment

Various methods of heat treatment were applied, e.g. heating in water baths using glass capillary tubes, sealed glass tubes, glass ampoules or polythene pouches completely immersed in the water, test tubes placed with the water level to the bases of the test tube plugs, flasks or cups placed with the menstruum levels under the water level and in some cases shaken, and heating using pasteurizers, two-phase slug flow heat exchangers [15, 18, 21, 20, 97, 29], submerged-coil heating apparatuses [3, 89, 88, 10, 90], thermoresistometers [141, 131, 132] and an "attemperated dilution blank method" [113, 114].

Results from experiments using rising heating temperatures [169, 109, 140, 161] were excluded.

Recovery of heat-treated bacteria

In the great majority of cases the recovery of heat-treated bacteria was performed on agar plates. Enterococci and E. coli were incubated aerobically at 30–37°C for 24 h-7 days, listerias, salmonellas and Y. enterocolitica aerobically at 25–37°C for 24 h-7 days and campylobacters microaerobically at 37–43°C for 24–72 h. In some studies anaerobic recovery was used: L. monocytogenes [95, 63], E. coli [121, 122, 58, 10, 63, 62] and salmonellas [177, 10, 63]. Most Probable Number (MPN) techniques were applied in some investigations. Procedures for repair of heat-injured bacteria were studied by [1, 127, 116, 157, 158, 63].

Results from experiments where heat-treated bacteria were recovered on selective or other media known to inhibit growth of heat-injured cells were excluded.

Types of collected data and statistical analysis

D and z values were collected from the studied literature. The D value is the time of heat treatment required at a certain temperature to destroy 90% of the bacterial cells, and the z value is the number of degrees of temperature change needed to change the D value by a factor of 10 [163]. When not reported, D values were, where possible, calculated from bacterial counts and periods of time of heat treatment given in texts, tables or figures. Some z values were worked out from reported or calculated D values and reported treatment temperatures.

For each of the bacterial species/groups studied, the log10 of D values recorded were plotted vs temperature and a thermal destruction line [163] was fitted using the method of least squares [30]. The equation for the line is log10 D = a - bt, where D is the decimal reduction time in s, a the intercept, -b the slope and t the treatment temperature in °C. The degree of linear relationship between the temperatures used and the logarithms of D values recorded was expressed by the coefficient of correlation, r [30]. Using the absolute and inverse values of the slope and its 95% confidence limits, the z value and its 95% confidence limits were calculated [163, 30].

95% confidence limits on predicted means [30] of D values were calculated (the predicted mean is the same as D in the equation). 95% confidence limits on predicted individual D values [30] were also figured out (From a practical point of view it may be more interesting to know these limits than those on predicted means).

Summaries of data

Reported z values are summarized in Table 1. Reported and calculated z values taken together are given in Table 2, where z values figured out in the work by means of the equation mentioned, etc. are also shown. Thermal destruction lines for the bacteria studied, except those for L. innocua, L. ivanovii, L. seeligeri and L. welshimeri, are depicted in Figures 1, 2, 3, 4, 5, 6, 7, where 95% confidence limits on predicted individual log10 D values are also illustrated graphically. In Table 3, some D values at these limits are shown for the seven bacterial groups and also for L. innocua. Equations for the thermal destruction line of L. innocua and that of L. ivanovii, L. seeligeri and L. welshimeri taken together, are given below under the headings Listeria innocua and Listeria ivanovii, L. seeligeri and L. welshimeri, respectively.
Table 1

z values reported from investigations where the experimental conditions laid down in this study were fulfilled.

Bacterium/Bacterial group

z* values (°C)

References

 

Range

Mean ± SD

No. of values

 

Enterococcus faecium

3.63–12.82

8.4 ± 2.5

14

[148, 113, 140, 68, 154, 120]

Enterococcus faecalis

2.24–9.06

6.0 ± 2.5

10

[59, 148, 113, 140]

Listeria innocua

4.65–6.9

5.8 ± 0.8

8

[138, 56, 48, 133]

Listeria monocytogenes

4.30–11.45

6.1 ± 1.2

85

[15, 16, 17, 8, 18, 21, 40, 45, 101, 138, 55, 104, 56, 139, 48, 157, 158, 7, 133, 123, 149, 23, 131, 147, 96]

Listeria ivanovii

6.3–6.6

6.5 ± 0.2

2

[17]

Listeria seeligeri

6.4–6.9

6.7 ± 0.3

2

[17]

Listeria welshimeri

6.1–6.9

6.5 ± 0.5

2

[17]

Escherichia coli

3.4–6.0

5.1 ± 0.8

11

[143, 39, 119, 29, 10, 175]

Yersinia enterocolitica

4.0–5.78

4.8 ± 0.6

10

[106, 156, 159, 132]

Salmonella spp. (except Salm. senftenberg 775W)

3.24–9.5

5.5 ± 1.7

36

[4, 61, 39, 64, 14, 159, 151, 177, 176, 133, 10, 149, 74, 117]

Salm. senftenberg 775W

5.3–6.8

6.0 ± 0.4

13

[4, 166, 5, 64]

Campylobacter jejuni/coli

2.8–5.81

4.8 ± 0.7

14

[11, 171, 156, 159]

* The z value is the number of degrees of temperature change needed to change the D value by a factor of 10 (The term D value, see Table 3).

Table 2

z values obtained using the slopes of thermal destruction lines constructed in the study and their 95% confidence limits and, for comparison, summaries of reported and calculated z values.

Bacterium/Bacterial group

z values (°C)*

 

Obtained value and its 95% confidence interval

Reported and calculated** values

  

Range

Mean ± SD

No. of values

Enterococcus faecium

9.6 (8.8 – 10.5)

3.63 – 14.3

10.2 ± 3.3

24

Enterococcus faecalis

9.5 (8.5 – 10.8)

2.24 – 14.2

8.1 ± 3.2

36

Listeria innocua

5.0 (4.5 – 5.6)

4.65 – 7.3

6.0 ± 0.9

9

Listeria monocytogenes

5.7 (5.6 – 5.9)

4.30 – 11.45

6.3 ± 1.3

103

Listeria ivanovii, L. seeligeri, L. welshimeri †

6.4 (6.1 – 6.7)

6.1 – 6.9

6.5 ± 0.3

6

Escherichia coli

6.0 (5.9 – 6.1)

3.2 – 9.1

5.4 ± 1.5

33

Yersinia enterocolitica

6.7 (6.0 – 7.7)

4.0 – 13.7

6.6 ± 2.7

20

Salmonella spp. (except Salm. senftenberg 775W)

5.2 (5.1 – 5.3)

3.24 – 9.5

5.1 ± 1.6

63

Salmonella senftenberg 775W

5.8 (5.4 – 6.4)

4.5 – 9.1

6.2 ± 1.1

16

Campylobacter jejuni/coli

6.4 (5.8 – 7.0)

2.8 – 8.0

5.5 ± 1.1

24

** Calculated z values were figured out from reported or calculated D values (see Types of collected data and statistical analysis) and reported treatment temperatures.

† Listeria ivanovii, L. seeligeri and L. welshimeri are taken together.

Table 3

Heat resistance values at 4 temperatures for bacteria studied in the work. The values are based on results reported from investigations where the experimental conditions laid down in the work were fulfilled.

  

D* values (s)

   

95% confidence interval

Bacterium/Bacterial group**

Temperature (°C)

Mean

For the mean

For a predicted individual value

Enterococcus faecium

55

3813

3095–4697

1041–13969

 

60

1150

1017–1300

317–4166

 

65

347

315–381

96–1254

 

72

65

53–79

18–237

Enteroccus faecalis

55

1393

1089–1783

220–8816

 

60

415

361–476

66–2593

 

65

123

108–141

20–771

 

72

23

17–30

3.5–144

Listeria innocua

55

1635

1050–2549

474–5644

 

60

162

127–207

50–529

 

65

16

13–20

5.0–52

 

72

0.6 †

0.4–1.0

0.2–2.2

Listeria monocytogenes

55

643

577–715

150–2754

 

60

87

81–93

20–371

 

65

12

11–13

2.7–50

 

72

0.7

0.6–0.8

0.2–3.0

Escherichia coli

55

266

239–297

53–1338

 

60

39

35–42

8–194

 

65

5.6

5.1–6.2

1.1–28

 

72

0.4

0.3–0.5

0.1–1.9

Yersinia enterocolitica

55

168

124–227

23–1244

 

60

30

24–37

4.1–221

 

65

5.4

4.0–7.4

0.7–40

 

72

0.5

0.3–0.9

0.1–3.9

Salmonella spp. (except Salm. senftenberg 775W)

55

222

208–237

64–771

 

60

24

23–26

7.0–84

 

65

2.6

2.3–2.9

0.8–9.1

 

72

0.1

0.1–0.2

0.1–0.4

Campylobacter jejuni/coli

55

50

44–57

13–190

 

60

8.2

6.5–10

2.1–32

 

65

1.3 †

0.9–2.0

0.3–5.4

 

72

0.1 †

0.1–0.2

0.1–0.5

* The D value is the time of heat treatment required at a certain temperature to destroy 90% of the bacterial cells.

** The bacteria are arranged according to their mean heat resistances at 60 and 65°C.

† Extrapolated value.

Figure 1
Figure 1

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Enterococcus faecium. The equation for the line is log10 D = 9.3080 - 0.10412t (r = -0.84748; total number of log10 D values = 195). The 95% confidence limits on predicted individual log10 D values are shown by (- -). The figure is based on data from: [69, 179, 85, 170, 148, 113, 114, 140, 68, 98, 136, 154, 94, 120, 144].

Figure 2
Figure 2

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Enterococcus faecalis. The equation for the line is log10 D = 8.9359 - 0.10531t (r = -0.72968; total number of log10 D values = 244). The 95% confidence limits on predicted individual log10 D values are shown by (- -). The figure is based on data from: [145, 172, 99, 173, 179, 9, 26, 85, 152, 170, 33, 35, 59, 148, 113, 114, 140, 12, 94, 54, 53].

Figure 3
Figure 3

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Listeria monocytogenes. The equation for the line is log10 D = 12.3787 - 0.17401t (r = -0.95631; total number of log10 D values = 474). The 95% confidence limits on predicted individual log10 D values are shown by (- -). The figure is based on data from: [15, 8, 18, 40, 16, 41, 52, 21, 50, 67, 127, 160, 45, 51, 101, 138, 164, 13, 19, 55, 95, 104, 112, 3, 17, 56, 97, 115, 139, 20, 49, 73, 116, 48, 157, 158, 161, 7, 89, 88, 133, 134, 105, 123, 135, 149, 23, 63, 90, 131, 147, 96].

Figure 4
Figure 4

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Escherichia coli. The equation for the line is log10 D = 11.6471 - 0.16768t (r = -0.97349; total number of log10 D values = 332). The 95% confidence limits on predicted individual log10 D values are shown by (- -). Data used are from: [46, 92, 155, 24, 142, 102, 143, 22, 47, 66, 35, 39, 169, 1, 91, 178, 37, 87, 119, 121, 122, 58, 2, 27, 28, 29, 86, 165, 10, 174, 175, 63, 62, 93, 150]. Thermal destruction line for an unusually heat-resistant strain of E. coli reported by [72] is also shown (- • -).

Figure 5
Figure 5

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Yersinia enterocolitica. The equation for the line is log10 D = 10.4176 - 0.14896t (r = -0.86082; total number of log10 D values = 88). The 95% confidence limits on predicted individual log10 D values are shown by (- -). The figure is based on data from: [70, 57, 126, 106, 37, 156, 159, 168, 153, 132].

Figure 6
Figure 6

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Salmonella spp. The equation for the line is log10 D = 12.9511 - 0.19282t (r = -0.92147; total number of log10 D values = 647). The 95% confidence limits on predicted individual log10 D values are shown by (- -). Data used are from: [155, 4, 130, 100, 38, 124, 166, 32, 141, 60, 61, 125, 5, 47, 66, 146, 31, 34, 118, 39, 64, 31, 167, 75, 80, 108, 128, 14, 36, 109, 110, 6, 19, 77, 76, 111, 159, 81, 151, 82, 84, 103, 177, 176, 83, 133, 134, 123, 165, 10, 149, 63, 74, 117]. Thermal destruction line for the extremely heat-resistant Salm. senftenberg 775W is also shown (- • -) ; for references, see text.

Figure 7
Figure 7

Heat resistance data (Mean ± SD) recorded at the different treatment temperatures used and fitted thermal destruction line (-) for Campylobacter jejuni/coli. The equation for the line is log10 D = 10.3432 - 0.15717t (r = -0.89853; total number of log10 D values = 112). The 95% confidence limits on predicted individual log10 D values are shown by (- -). The figure is based on data from: [44, 65, 11, 25, 171, 129, 78, 128, 79, 37, 156, 159].

Comments and further information

D and r values

The order of death of bacteria subjected to heat at a constant lethal temperature is often logarithmic [71, 163, 137], i.e. when the logarithm of survivors is plotted against the time of heating, the curve obtained, the survivor curve, is a straight line. The D value can then easily be calculated using the slope of the line. Deviations from the logarithmic order of death, however, are rather frequent and non-logarithmic survivor curves of some different types are obtained [71, 163, 137]. Deviations of this kind often make determinations of D values difficult.

The r values, varying from -0.92147 to -0.99405, obtained for Salmonella spp., E. coli and the 3 Listeria groups indicate very good linear relationships [30] between the log10 D values recorded and the treatment temperatures used. The r values, varying from -0.72968 to -0.89853, recorded for Ent. faecalis, Ent. faecium, Y. enterocolitica and Camp. jejuni/coli indicate weaker but, nevertheless, good linear relationships [30]. The following should be noted here: The number of Y. enterocolitica strains investigated is low. The results reported, however, indicate that great variation in heat resistance exists between strains of this species. As to enterococci, non-logarithmic survivor curves were reported in several works [179, 33, 35, 148, 113, 68, 12].

Listeria monocytogenes

[107] published a similar review of the heat resistance of L. monocytogenes. Equations were given for heat treatments in: (a) various menstrua and (b) milk. The treatments in (b) had been performed by a sealed tube method (b1) or a slug flow heat exchanger (b2). The equations for (a), (b1) and (b2) were log10 D = 10.888 - 0.14519t, log10 D = 11.931 - 0.1635t and log10 D = 10.126 - 0.1348t (D is in s in the equations). The means of D values obtained by the 3 equations for 55, 60, 65 and 72°C are shown in Table 4. The means in (a), (b1) and (b2) except that in (b2) for 55°C are higher than the corresponding ones (c) recorded for L. monocytogenes in the present work (Table 3). The differences between (a) and (c) may, at least to some extent, be explained by the fact that some of the heating menstrua in (a) were solids. The differences between (b1) or (b2) and (c) are therefore of greater interest, as all data for these 3 groups were obtained in liquids. A probable explanation of these differences is that heat resistance data for several "new" strains have been published later than the review by [107] and have thus been included in the present work. Furthermore, the methods of determining the heat resistance of bacteria have been widely discussed in recent years and some improvements or new procedures have been introduced. Factors of this kind may also have contributed to the differences.
Table 4

D values for Listeria monocytogenes according to the review by [107].

Heating menstruum(-a)/(s) Treatment method(s)

D** value (s)

 

55°C

60°C

65°C

72°C

(a) Various/Various

799*

150*

28*

2.7*

(b1) Milk/ST

868

132

20

1.4†

(b2) Milk/SF

515‡

109

23

2.6

** The D value is the time of heat treatment required at a certain temperature to destroy 90% of the bacterial cells.

ST, sealed tubes; SF, slug flow heat exchanger.

*, †, ‡ Value calculated using the equation given by the authors for (a), (b1) and (b2) respectively.

Listeria innocua

The non-pathogenic L. innocua is of special interest as it has, as mentioned, been proposed to be used as an indicator organism to evaluate thermal processes for lethality to L. monocytogenes. To function satisfactorily in this respect it is desirable that the indicator has heat resistance equal to or greater than the average heat resistance of L. monocytogenes or, more desirably, has heat resistance equal to that of the most resistant strains of this species. In the present work, heat resistance results for L. innocua were found in 5 reports [138, 112, 56, 48, 133]. The equation for the thermal destruction line constructed was log10 D (D in s) = 14.2559 - 0.20077t (r = -0.95519). The average heat resistance values at 55, 60 and 65°C calculated for L. innocua were greater than those for L. monocytogenes (Table 3), but none of analysed differences between means of D values were statistically significant. As to L. innocua, however, only 36 D values were reported totally and the D values obtained at the individual treatment temperatures used were few, 1–4. The most heat-resistant strain of the L. innocua strains investigated was reported by [138]. D values determined at 58, 60, 63 and 65°C using a culture medium as heating menstruum were 2.7 to 5.4 times greater than the average D values found in the present work for L. monocytogenes at these temperatures. [56] tested L. innocua strain ATCC 33091 in buffer and in skim milk at 56, 60 and 66°C. In buffer, the D values were lower at 56 and 60 but higher at 66°C than the corresponding average values for L. monocytogenes. When L. innocua PFEI (strain ATCC 33091 containing a plasmid which did not alter its heat resistance) was tested in skim milk, all D values obtained at these temperatures were higher, 1.5 to 2.1 times, than the values mentioned for L. monocytogenes. [133] determined D values for a L. innocua strain isolated from raw egg. The tests were performed in egg yolk. D values obtained at 61.1, 63.3 and 64.4°C were 2.5 to 2.9 times longer than the corresponding average values for L. monocytogenes. The results reported indicate that L. innocua may have greater average heat resistance than L. monocytogenes. However, as mentioned, only few heat resistance results are reported for L. innocua and more research on this matter is required.

Listeria ivanovii, L. seeligeri and L. welshimeri [17] studied the heat resistance of L. ivanovii, L. seeligeri and L. welshimeri. One strain of each species was tested in milk at 52.2, 57.8, 63.3 and 68.9°C. The equation for the 3 species taken together is log10 D (D in s) = 11.3419 - 0.15713t; r = -0.99405. All means of D values obtained for the 4 treatment temperatures were lower than the corresponding means noted in the present work for L. monocytogenes. The differences between the means were statistically significant for the values obtained at 52.2 and 57.8°C (p < 0.05 and < 0.001) but not for those obtained at 63.3 and 68.9°C. In view of the low number of D values, 24, reported for L. ivanovii, L. seeligeri and L. welshimeri and the fact that only one strain of each of these species was tested, no conclusion, however, should be drawn about differences in average heat resistance between these species and L. monocytogenes.

Salmonella

[124] studied the heat resistance of 300 Salmonella isolates and gave D57°C values for 123 strains. The well-known extremely heat-resistant Salm. senftenberg 775W and 19 other strains of Salm. senftenberg were among the tested isolates. The resistance of the 19 strains was similar to that of the majority of isolates. Ng concluded that strains of salmonellae as resistant to heat as Salm. senftenberg 775W are rare. A similar conclusion was drawn by [146] who compared the heat resistance of Salm. senftenberg 775W with that of 20 strains of Salm. senftenberg isolated from herring meal.

The heat resistance of Salm. senftenberg 775W was also tested by [4, 130, 38, 166, 32, 141, 60, 125, 5, 66, 33, 34, 64, 31, 77] and [10]. The thermal destruction line fitted to the data (number of D values = 54) reported by the investigators mentioned is shown in Fig. 6. The equation for the line is log10 D (D in s) = 12.8001 - 0.17111t (r = -0.94992).

In a screening of 221 Salmonella isolates, [5] found that 2 strains, one of Salm. senftenberg tested earlier by [38] and one of Salm. bedford, had D60°C values similar to that of Salm. senftenberg 775W. Baird-Parker et al. considered it possible, although unlikely, that the Salm. senftenberg strain was identical to Salm. senftenberg 775W (the strain was isolated from home-killed meat in the United Kingdom and Salm. senftenberg 775W from dried eggs in the United States). The authors determined D values in heart infusion broth for the Salm. bedford strain and for Salm. senftenberg 775W. D values obtained at 50, 55 and 60°C were 350, 18.8 and 4.3 min for the Salm. bedford strain and 268, 36.2 and 6.3 min for Salm. senftenberg 775W. For comparison, it may be mentioned that the D values obtained for Salm. senftenberg 775W using the equation constructed in the present study are 293, 40.8 and 5.7 min at these temperatures.

Escherichia coli

[72] investigated an E. coli strain noted for its heat resistance. Tests were performed in milk. The thermal destruction line based on the data (number of D values = 22) reported by Holland and Dahlberg is shown in Fig. 4. The equation for the line is log10 D (D in s) = 14.7478 - 0.19777t (r = -0.99403). The z value is 5.1°C. The author of the present work is unaware of whether this E. coli strain has been subjected to further heat resistance studies.

Concluding remarks

The design of the present study required that some differences in composition, etc. of heating menstrua used and in methods used for heat treatment and for recovery of heat-treated bacteria had to be accepted when heat resistance data were collected from the literature. This meant that experimental factors of varying character might have influenced the magnitude of heat resistance values used in the work. Statistical analyses of the results of these fairly numerous influences could not be achieved on the basis of available information. Scrutiny of heat resistance values chosen according to the stipulations laid down in the study, however, indicated that value differences probably caused by differences in experimental conditions were, in most cases, small or moderate.

The summary heat resistance values recorded -especially those for L. monocytogenes, E. coli and salmonellas which are based on large numbers of data – may give useful information on what is at present known about the heat resistance that the bacteria reviewed show in liquid heating menstrua with pH values of approx. 6–8. It should, however, be emphasized that they may, and often do, show heat resistance of different magnitude in other types of heating menstrua.

Notes

Declarations

Acknowledgements

The author thanks the Swedish Society for Veterinary Research for a grant from the Ivar and Elsa Sandberg Research Foundation which made this study possible. He also thanks Professor Marie-Louise Danielsson-Tham and Associate Professor Wilhelm Tham for their stimulating interest in this work and for their help with collecting the literature, and Susanne Broqvist for excellent clerical assistance in the preparation of the manuscript.

Authors’ Affiliations

(1)
Department of Food Hygiene, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Uppsala, Sweden

References

  1. Ahmad M, Srivastava BS, Agarwala SC: Effect of incubation media on the recovery of Escherichia coli K12 heated at 52°C. J Gen Microbiol. 1978, 107: 37-44.PubMedGoogle Scholar
  2. Ahmed NM, Conner DE: Evaluation of various media for recovery of thermally-injured Escherichia coli O157:H7. J Food Prot. 1995, 58: 357-360.Google Scholar
  3. Anderson WA, Hedges ND, Jones MV, Cole MB: Thermal inactivation of Listeria monocytogenes studied by differential scanning calorimetry. J Gen Microbiol. 1991, 137: 1419-1424.PubMedGoogle Scholar
  4. Anellis A, Lubas J, Rayman MM: Heat resistance in liquid eggs of some strains of the genus Salmonella. Food Res. 1954, 19: 377-395.Google Scholar
  5. Baird-Parker AC, Boothroyd M, Jones E: The effect of water activity on the heat resistance of heat sensitive and heat resistant strains of salmonellae. J Appl Bacteriol. 1970, 33: 515-522.PubMedGoogle Scholar
  6. Baker RC: Survival of Salmonella enteritidis on and in shelled eggs, liquid eggs and cooked egg products. Dairy Food Environ Sanit. 1990, 10: 273-275.Google Scholar
  7. Bartlett FM, Hawke AE: Heat resistance of Listeria monocytogenes Scott A and HAL 957E1 in various liquid egg products. J Food Prot. 1995, 58: 1211-1214.Google Scholar
  8. Beuchat LR, Brackett RE, Hao DY-Y, Conner DE: Growth and thermal inactivation of Listeria monocytogenes in cabbage and cabbage juice. Can J Microbiol. 1986, 32: 791-795.PubMedGoogle Scholar
  9. Beuchat LR, Lechowich RV: Survival of heated Streptococcus faecalis as affected by phase of growth and incubation temperature after thermal exposure. J Appl Bacteriol. 1968, 31: 414-419.PubMedGoogle Scholar
  10. Blackburn C de W, Curtis LM, Humpheson L, Billon C, McClure PJ: Development of thermal inactivation models for Salmonella enteritidis and Escherichia coli O157:H7 with temperature, pH and NaCl as controlling factors. Int J Food Microbiol. 1997, 38: 31-44. 10.1016/S0168-1605(97)00085-8.Google Scholar
  11. Blankenship LC, Craven SE: Campylobacter jejuni survival in chicken meat as a function of temperature. Appl Environ Microbiol. 1982, 44: 88-92.PubMed CentralPubMedGoogle Scholar
  12. Boutibonnes P, Giard JC, Hartke A, Thammavongs B, Auffray Y: Characterization of the heat shock response in Enterococcus faecalis. Antonie van Leeuwenhoek. 1993, 64: 47-55. 10.1007/BF00870921.PubMedGoogle Scholar
  13. Boyle DL, Sofos JN, Schmidt GR: Thermal destruction of Listeria monocytogenes in a meat slurry and in ground beef. J Food Sci. 1990, 55: 327-329. 10.1111/j.1365-2621.1990.tb06754.x.Google Scholar
  14. Bradshaw JG, Peeler JT, Corwin JJ, Barnett JE, Twedt RM: Thermal resistance of disease-associated Salmonella typhimurium in milk. J Food Prot. 1987, 50: 95-96.Google Scholar
  15. Bradshaw JG, Peeler JT, Corwin JJ, Hunt JM, Tierney JT, Larkin EP, Twedt RM: Thermal resistance of Listeria monocytogenes in milk. J Food Prot. 1985, 48: 743-745.Google Scholar
  16. Bradshaw JG, Peeler JT, Corwin JJ, Hunt JM, Twedt RM: Thermal resistance of Listeria monocytogenes in dairy products. J Food Prot. 1987, 50: 543-544. 556Google Scholar
  17. Bradshaw JG, Peeler JT, Twedt RM: Thermal resistance of Listeria spp. in milk. J Food Prot. 1991, 54: 12-14. 19Google Scholar
  18. Bunning VK, Crawford RG, Bradshaw JG, Peeler JT, Tierney JT, Twedt RM: Thermal resistance of intracellular Listeria monocytogenes cells suspended in raw bovine milk. Appl Environ Microbiol. 1986, 52: 1398-1402.PubMed CentralPubMedGoogle Scholar
  19. Bunning VK, Crawford RG, Tierney JT, Peeler JT: Thermotolerance of Listeria monocytogenes and Salmonella typhimurium after sublethal heat shock. Appl Environ Microbiol. 1990, 56: 3216-3219.PubMed CentralPubMedGoogle Scholar
  20. Bunning VK, Crawford RG, Tierney JT, Peeler JT: Thermotolerance of heat-shocked Listeria monocytogenes in milk exposed to high-temperature, short-time pasteurization. Appl Environ Microbiol. 1992, 58: 2096-2098.PubMed CentralPubMedGoogle Scholar
  21. Bunning VK, Donnelly CW, Peeler JT, Briggs EH, Bradshaw JG, Crawford RG, Beliveau CM, Tierney JT: Thermal inactivation of Listeria monocytogenes within bovine milk phagocytes. Appl Environ Microbiol. 1988, 54: 364-370.PubMed CentralPubMedGoogle Scholar
  22. Calhoun CL, Frazier WC: Effect of available water on thermal resistance of three nonsporeforming species of bacteria. Appl Microbiol. 1966, 14: 416-420.PubMed CentralPubMedGoogle Scholar
  23. Casadei MA, Esteves de Matos R, Harrison ST, Gaze JE: Heat resistance of Listeria monocytogenes in dairy products as affected by the growth medium. J Appl Microbiol. 1998, 84: 234-239. 10.1046/j.1365-2672.1998.00334.x.PubMedGoogle Scholar
  24. Chambers CW, Tabak HH, Kabler PW: Effect of Krebs cycle metabolites on the viability of Escherichia coli treated with heat and chlorine. J Bacteriol. 1957, 73: 77-84.PubMed CentralPubMedGoogle Scholar
  25. Christopher FM, Smith GC, Vanderzant C: Effect of temperature and pH on the survival of Campylobacter fetus. J Food Prot. 1982, 45: 253-259.Google Scholar
  26. Clark CW, Witter LD, Ordal ZJ: Thermal injury and recovery of Streptococcus faecalis. Appl Microbiol. 1968, 16: 1764-1769.PubMed CentralPubMedGoogle Scholar
  27. Clavero MRS, Beuchat LR: Suitability of selective plating media for recovering heat- or freezestressed Escherichia coli O157:H7 from tryptic soy broth and ground beef. Appl Environ Microbiol. 1995, 61: 3268-3273.PubMed CentralPubMedGoogle Scholar
  28. Clavero MRS, Beuchat LR: Survival of Escherichia coli O157:H7 in broth and processed salami as influenced by pH, water activity, and temperature and suitability of media for its recovery. Appl Environ Microbiol. 1996, 62: 2735-2740.PubMed CentralPubMedGoogle Scholar
  29. Clementi F, Parente E, Ricciardi A, Addario G, Moresi M: Heat resistance of Escherichia coli in goat milk: a comparison between the sealed capillary tube technique and a laboratory slug flow heat exchanger. Ital J Food Sci. 1995, 7: 235-243.Google Scholar
  30. Colton T: Statistics in Medicine. 1974, Little Brown, Boston, 191-202. 207–211, 1Google Scholar
  31. Corry JEL: The effect of sugars and polyols on the heat resistance of salmonellae. J Appl Bacteriol. 1974, 37: 31-43.PubMedGoogle Scholar
  32. Corry JEL, Barnes EM: The heat resistance of salmonellae in egg albumen. Brit Poult Sci. 1968, 9: 253-260. 10.1080/00071666808415716.Google Scholar
  33. Dabbah R, Moats WA, Edwards VM: Survivor curves of selected Salmonella enteritidis serotypes in liquid whole egg homogenates at 60°C. Poultry Sci. 1971, 50: 1772-1776.Google Scholar
  34. Dabbah R, Moats WA, Edwards VM: Heat survivor curves of food-borne bacteria suspended in commercially sterilized whole milk. I Salmonellae J Dairy Sci. 1971, 54: 1583-1588.PubMedGoogle Scholar
  35. Dabbah R, Moats WA, Edwards VM: Heat survivor curves of food-borne bacteria suspended in commercially sterilized whole milk. II. Bacteria other than salmonellae. J Dairy Sci. 1971, 54: 1772-1779.PubMedGoogle Scholar
  36. D'Aoust J-Y, Emmons DB, McKellar R, Timbers GE, Todd ECD, Sewell AM, Warburton DW: Thermal inactivation of Salmonella species in fluid milk. J Food Prot. 1987, 50: 494-501.Google Scholar
  37. D'Aoust J-Y, Park CE, Szabo RA, Todd ECD, Emmons DB, McKellar RC: Thermal inactivation of Campylobacter species, Yersinia enterocolitica and hemorrhagic Escherichia coli O157:H7 in fluid milk. J Dairy Sci. 1988, 71: 3230-3236.PubMedGoogle Scholar
  38. Davidson CM, Boothroyd M, Georgala DL: Thermal resistance of Salmonella senftenberg. Nature. 1966, 212: 1060-1061. 10.1038/2121060a0.PubMedGoogle Scholar
  39. Dega CA, Goepfert JM, Amundson CH: Heat resistance of salmonellae in concentrated milk. Appl Microbiol. 1972, 23: 415-420.PubMed CentralPubMedGoogle Scholar
  40. Donnelly CW, Briggs EH: Psychrotrophic growth and thermal inactivation of Listeria monocytogenes as a function of milk composition. J Food Prot. 1986, 49: 994-998.Google Scholar
  41. Donnelly CW, Briggs EH, Donnelly LS: Comparison of heat resistance of Listeria monocytogenes in milk as determined by two methods. J Food Prot. 1987, 50: 14-17,20.Google Scholar
  42. Doyle ME, Mazzotta AS: Review of studies on the thermal resistance of salmonellae. J Food Prot. 2000, 63: 779-795.PubMedGoogle Scholar
  43. Doyle ME, Mazzotta AS, Wang T, Wiseman DW, Scott VN: Review. Heat resistance of Listeria monocytogenes. J Food Prot. 2001, 64: 410-429.PubMedGoogle Scholar
  44. Doyle MP, Roman DJ: Growth and survival of Campylobacter fetus subsp. jejuni as a function of temperature and pH. J Food Prot. 1981, 44: 596-601.Google Scholar
  45. El-Shenawy MA, Yousef AE, Marth EH: Thermal inactivation and injury of Listeria monocytogenes in reconstituted nonfat dry milk. Milchwissenschaft. 1989, 44: 741-745.Google Scholar
  46. Elliker PR, Frazier WC: Influence of time and temperature of incubation on heat resistance of Escherichia coli. J Bacteriol. 1938, 36: 83-98.PubMed CentralPubMedGoogle Scholar
  47. Evans DA, Hankinson DJ, Litsky W: Heat resistance of certain pathogenic bacteria in milk using a commercial plate heat exchanger. J Dairy Sci. 1970, 53: 1659-1665.PubMedGoogle Scholar
  48. Fairchild TM, Foegeding PM: A proposed non-pathogenic biological indicator for thermal inactivation of Listeria monocytogenes. Appl Environ Microbiol. 1993, 59: 1247-1250.PubMed CentralPubMedGoogle Scholar
  49. Farber JM, Pagotto F: The effect of acid shock on the heat resistance of Listeria monocytogenes. Lett Appl Microbiol. 1992, 15: 197-201.Google Scholar
  50. Farber JM, Sanders GW, Speirs JI, D'Aoust J-Y, Emmons DB, McKellar R: Thermal resistance of Listeria monocytogenes in inoculated and naturally contaminated raw milk. Int J Food Microbiol. 1988, 7: 277-286. 10.1016/0168-1605(88)90054-2.PubMedGoogle Scholar
  51. Fedio WM, Jackson H: Effect of tempering on the heat resistance of Listeria monocytogenes. Lett Appl Microbiol. 1989, 9: 157-160.Google Scholar
  52. Fernández Garayzabal JF, Domínguez Rodríguez L, Vázques Boland JA, Rodríguez Ferri EF, Briones Dieste V, Blanco Cancelo JL, Suárez Fernández G: Survival of Listeria monocytogenes in raw milk treated in a pilot plant size pasteurizer. J Appl Bacteriol. 1987, 63: 533-537.PubMedGoogle Scholar
  53. Flahaut S, Frere J, Boutibonnes P, Auffray Y: Relationship between the thermotolerance and the increase of DnaK and GroEL synthesis in Enterococcus faecalis ATCC 19433. J Basic Microbiol. 1997, 37: 251-258. 10.1002/jobm.3620370404.PubMedGoogle Scholar
  54. Flahaut S, Hartke A, Giard J-C, Benachour A, Boutibonnes P, Auffray Y: Relationship between stress response towards bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol Lett. 1996, 138: 49-54. 10.1111/j.1574-6968.1996.tb08133.x.PubMedGoogle Scholar
  55. Foegeding PM, Leasor SB: Heat resistance and growth of Listeria monocytogenes in liquid whole egg. J Food Prot. 1990, 53: 9-14.Google Scholar
  56. Foegeding PM, Stanley NW: Listeria innocua transformed with an antibiotic resistance plasmid as a thermal-resistance indicator for Listeria monocytogenes. J Food Prot. 1991, 54: 519-523.Google Scholar
  57. Francis DW, Spaulding PL, Lovett J: Enterotoxin production and thermal resistance of Yersinia enterocolitica in milk. Appl Environ Microbiol. 1980, 40: 174-176.PubMed CentralPubMedGoogle Scholar
  58. Gadzella TA, Ingham SC: Heat shock, anaerobic jar incubation and fluid thioglycollate medium have contrasting effects on D-values of Escherichia coli. J Food Prot. 1994, 57: 671-673.Google Scholar
  59. Gardner GA, Patton J: A note on the heat resistance of a Streptococcus faecalis isolated from a "soft core" in canned ham. Proc 21st Europ Meet Meat Res Workers, Bern. 1975, 52-54.Google Scholar
  60. Garibaldi JA, Ijichi K, Bayne HG: Effect of pH and chelating agents on the heat resistance and viability of Salmonella typhimurium Tm-1 and Salmonella senftenberg 775W in egg white. Appl Microbiol. 1969, 18: 318-322.PubMed CentralPubMedGoogle Scholar
  61. Garibaldi JA, Straka RP, Ijichi K: Heat resistance of Salmonella in various egg products. Appl Microbiol. 1969, 17: 491-496.PubMed CentralPubMedGoogle Scholar
  62. George SM, Peck MW: Redox potential affects the measured heat resistance of Escherichia coli O157:H7 independently of oxygen concentration. Lett Appl Microbiol. 1998, 27: 313-317. 10.1046/j.1472-765X.1998.00466.x.PubMedGoogle Scholar
  63. George SM, Richardson LCC, Pol IE, Peck MW: Effect of oxygen concentration and redox potential on recovery of sublethally heat-damaged cells of Escherichia coli O157:H7, Salmonella enteritidis and Listeria monocytogenes. J Appl Microbiol. 1998, 84: 903-909. 10.1046/j.1365-2672.1998.00424.x.PubMedGoogle Scholar
  64. Gibson B: The effect of high sugar concentrations on the heat resistance of vegetative micro-organisms. J Appl Bacteriol. 1973, 36: 365-376.PubMedGoogle Scholar
  65. Gill KPW, Bates PG, Lander KP: The effect of pasteurization on the survival of Campylobacter spedies in milk. Brit Vet J. 1981, 137: 578-584.Google Scholar
  66. Goepfert JM, Iskander IK, Amundson CH: Relation of the heat resistance of salmonellae to the water activity of the environment. Appl Microbiol. 1970, 19: 429-433.PubMed CentralPubMedGoogle Scholar
  67. Golden DA, Beuchat LR, Brackett RE: Inactivation and injury of Listeria monocytogenes as affected by heating and freezing. Food Microbiol. 1988, 5: 17-23. 10.1016/0740-0020(88)90004-4.Google Scholar
  68. Gordon CLA, Ahmad MH: Thermal susceptibility of Streptococcus faecium strains isolated from frankfurters. Can J Microbiol. 1991, 37: 609-612.PubMedGoogle Scholar
  69. Greenberg RA, Silliker JH: Evidence for heat injury in enterococci. Food Res. 1961, 26: 622-625.Google Scholar
  70. Hanna MO, Stewart JC, Carpenter ZL, Vanderzant C: A research note. Heat resistance of Yersinia enterocolitica in skim milk. J Food Sci. 1977, 42: 1134, 1136-Google Scholar
  71. Hansen N-H, Riemann H: Factors affecting the heat resistance of nonsporing organisms. J Appl Bacteriol. 1963, 26: 314-333.Google Scholar
  72. Holland RF, Dahlberg AC: The effect of the time and temperature of pasteurization upon some of the properties and constituents of milk. New York State Agricultural Experiment Station, Technical Bulletin No. 254. 1940, 18-22. 39–55,Google Scholar
  73. Holsinger VH, Smith PW, Smith JL, Palumbo SA: Thermal destruction of Listeria monocytogenes in ice cream mix. J Food Prot. 1992, 55: 234-237.Google Scholar
  74. Humpheson L, Adams MR, Anderson WA, Cole MB: Biphasic thermal inactivation kinetics in Salmonella enteritidis PT4. Appl Environ Microbiol. 1998, 64: 459-464.PubMed CentralPubMedGoogle Scholar
  75. Humphrey TJ: The effects of pH and levels of organic matter on the death rates of salmonellas in chicken scald-tank water. J Appl Bacteriol. 1981, 51: 27-39.PubMedGoogle Scholar
  76. Humphrey TJ: Heat resistance in Salmonella enteritidis phage type 4: the influence of storage temperatures before heating. J Appl Bacteriol. 1990, 69: 493-497.PubMedGoogle Scholar
  77. Humphrey TJ, Chapman PA, Rowe B, Gilbert RJ: A comparative study of the heat resistance of salmonellas in homogenized whole egg, egg yolk or albumen. Epidemiol Infect. 1990, 104: 237-241.PubMed CentralPubMedGoogle Scholar
  78. Humphrey TJ, Cruickshank JG: Antibiotic and deoxycholate resistance in Campylobacter jejuni following freezing or heating. J Appl Bacteriol. 1985, 59: 65-71.PubMedGoogle Scholar
  79. Humphrey TJ, Lanning DG: Salmonella and campylobacter contamination of broiler chicken carcasses and scald tank water: the influence of water pH. J Appl Bacteriol. 1987, 63: 21-25.PubMedGoogle Scholar
  80. Humphrey TJ, Lanning DG, Beresford D: The effect of pH adjustment on the microbiology of chicken scald-tank water with particular reference to the death rate of salmonellas. J Appl Bacteriol. 1981, 51: 517-527.PubMedGoogle Scholar
  81. Humphrey TJ, Richardson NP, Gawler AHL, Allen MJ: Heat resistance of Salmonella enteritidis PT4: the influence of prior exposure to alkaline conditions. Lett Appl Microbiol. 1991, 12: 258-260.Google Scholar
  82. Humphrey TJ, Richardson NP, Statton KM, Rowbury RJ: Effects of temperature shift on acid and heat tolerance in Salmonella enteritidis phage type 4. Appl Environ Microbiol. 1993, 59: 3120-3122.PubMed CentralPubMedGoogle Scholar
  83. Humphrey TJ, Slater E, McAlpine K, Rowbury RJ, Gilbert RJ: Salmonella enteritidis phage type 4 isolates more tolerant of heat, acid, or hydrogen peroxide also survive longer on surfaces. Appl Environ Microbiol. 1995, 61: 3161-3164.PubMed CentralPubMedGoogle Scholar
  84. Humphrey TJ, Wallis M, Hoad M, Richardson NP, Rowbury RJ: Factors influencing alkali-induced heat resistance in Salmonella enteritidis phage type 4. Lett Appl Microbiol. 1993, 16: 147-149.Google Scholar
  85. Ienistea C, Chitu M, Roman A: Heat resistance in milk of some strains of group D streptococci from pasteurized milk and the influence exerted on their growth by selective media. Zbl Bakt, I Abt Orig. 1970, 215: 173-181.Google Scholar
  86. Jackson TC, Hardin MD, Acuff GR: Heat resistance of Escherichia coli O157:H7 in a nutrient medium and in ground beef patties as influenced by storage and holding temperatures. J Food Prot. 1996, 59: 230-237.PubMedGoogle Scholar
  87. Jenkins DE, Schultz JE, Matin A: Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol. 1988, 170: 3910-3914.PubMed CentralPubMedGoogle Scholar
  88. Jørgensen F, Panaretou B, Stephens PJ, Knøchel S: Effect of pre- and post-heat shock temperature on the persistence of thermotolerance and heat shock-induced proteins in Listeria monocytogenes. J Appl Bacteriol. 1996, 80: 216-224.PubMedGoogle Scholar
  89. Jørgensen F, Stephens PJ, Knøchel S: The effect of osmotic shock and subsequent adaptation on the thermotolerance and cell morphology of Listeria monocytogenes. J Appl Bacteriol. 1995, 79: 274-281.Google Scholar
  90. Juneja VK, Foglia TA, Marmer BS: Heat resistance and fatty acid composition of Listeria monocytogenes: effect of pH, acidulant, and growth temperature. J Food Prot. 1998, 61: 683-687.PubMedGoogle Scholar
  91. Katsui N, Tsuchido T, Takano M, Shibasaki I: Effect of preincubation temperature on the heat resistance of Escherichia coli having different fatty acid compositions. J Gen Microbiol. 1981, 122: 357-361.PubMedGoogle Scholar
  92. Katzin LI, Sandholzer LA, Strong ME: Application of the decimal reduction time principle to a study of the resistance of coliform bacteria to pasteurization. J Bacteriol. 1943, 45: 265-272.PubMed CentralPubMedGoogle Scholar
  93. Kaur J, Ledward DA, Park RWA, Robson RL: Factors affecting the heat resistance of Escherichia coli O157:H7. Lett Appl Microbiol. 1998, 26: 325-330. 10.1046/j.1472-765X.1998.00339.x.PubMedGoogle Scholar
  94. Kearns AM, Freeman R, Lightfoot NF: Nosocomial enterococci: resistance to heat and sodium hypochlorite. J Hosp Infect. 1995, 30: 193-199. 10.1016/S0195-6701(95)90314-3.PubMedGoogle Scholar
  95. Knabel SJ, Walker HW, Hartman PA, Mendonca AF: Effects of growth temperature and strictly anaerobic recovery on the survival of Listeria monocytogenes during pasteurization. Appl Environ Microbiol. 1990, 56: 370-376.PubMed CentralPubMedGoogle Scholar
  96. Knight KP, Bartlett FM, McKellar RC, Harris LJ: Nisin reduces the thermal resistance of Listeria monocytogenes Scott A in liquid whole egg. J Food Prot. 1999, 62: 999-1003.PubMedGoogle Scholar
  97. Konvincic I, Mrdjen M, Komnenov-Pupovac V, Vujicic IF, Vulic M, Svabic-Vlahovic M, Tierney JT: Heat resistance of Listeria monocytogenes in naturally infected and inoculated cow's milk. Acta Microbiol Hung. 1991, 38: 3-6.Google Scholar
  98. Kornacki JL, Marth EH: Thermal inactivation of Enterococcus faecium in retentates from ultrafiltered milk. Milchwissenschaft. 1992, 47: 764-769.Google Scholar
  99. Krishna Iyengar MK, Laxminarayana H, Iya KK: Studies on the heat-resistance of some streptococci. Indian J Dairy Sci. 1957, 10: 90-99.Google Scholar
  100. Lategan PM, Vaughn RH: The influence of chemical additives on the heat resistance of Salmonella typhimurium in liquid whole egg. J Food Sci. 1964, 29: 339-344. 10.1111/j.1365-2621.1964.tb01741.x.Google Scholar
  101. Lemaire V, Cerf O, Audurier A: Thermal resistance of Listeria monocytogenes. Ann Rech Vét. 1989, 20: 493-500.PubMedGoogle Scholar
  102. Lemcke RM, White HR: The heat resistance of Escherichia coli cells from cultures of different ages. J Appl Bacteriol. 1959, 22: 193-201.Google Scholar
  103. Leyer GJ, Johnson EA: Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl Environ Microbiol. 1993, 59: 1842-1847.PubMed CentralPubMedGoogle Scholar
  104. Linton RH, Pierson MD, Bishop JR: Increase in heat resistance of Listeria monocytogenes Scott A by sublethal heat shock. J Food Prot. 1990, 53: 924-927.Google Scholar
  105. Lou Y, Yousef AE: Resistance of Listeria monocytogenes to heat after adaptation to environmental stresses. J Food Prot. 1996, 59: 465-471.Google Scholar
  106. Lovett J, Bradshaw JG, Peeler JT: Thermal inactivation of Yersinia enterocolitica in milk. Appl Environ Microbiol. 1982, 44: 517-519.PubMed CentralPubMedGoogle Scholar
  107. Mackey BM, Bratchell N: A review. The heat resistance of Listeria minocytogenes. Lett Appl Microbiol. 1989, 9: 89-94.Google Scholar
  108. Mackey BM, Derrick CM: Elevation of the heat resistance of Salmonella typhimurium by sublethal heat shock. J Appl Bacteriol. 1986, 61: 389-393.PubMedGoogle Scholar
  109. Mackey BM, Derrick CM: Changes in the heat resistance of Salmonella typhimurium during heating at rising temperatures. Lett Appl Microbiol. 1987, 4: 13-16.Google Scholar
  110. Mackey BM, Derrick CM: The effect of prior heat shock on the thermoresistance of Salmonella thompson in foods. Lett Appl Microbiol. 1987, 5: 115-118.Google Scholar
  111. Mackey BM, Derrick C: Heat shock protein synthesis and thermotolerance in Salmonella typhimurium. J Appl Bacteriol. 1990, 69: 373-383.PubMedGoogle Scholar
  112. Mackey BM, Pritchet C, Norris A, Mead GC: Heat resistance of Listeria: strain differences and effects of meat type and curing salts. Lett Appl Microbiol. 1990, 10: 251-255.Google Scholar
  113. Magnus CA, Ingledew WM, McCurdy AR: Thermal resistance of streptococci isolated from pasteurized ham. Can Inst Food Sci Technol J. 1986, 19: 62-67.Google Scholar
  114. Magnus CA, McCurdy AR, Ingledew WM: Evaluation of four media for recovery of heat-stressed streptococci. J Food Prot. 1988, 51: 895-897.Google Scholar
  115. McKenna RT, Patel SV, Cirigliano MC: Thermal resistance of Listeria monocytogenes in raw liquid egg yolk. J Food Prot. 1991, 54: 816-Google Scholar
  116. Meyer DH, Donnelly CW: Effect of incubation temperature on repair of heat-injured Listeria in milk. J Food Prot. 1992, 55: 579-582.Google Scholar
  117. Michalski CB, Brackett RE, Hung Y-C, Ezeike GOI: Use of capillary tubes and plate heat exchanger to validate U.S. Department of Agriculture pasteurization protocols for elimination of Salmonella enteritidis from liquid egg products. J Food Prot. 1999, 62: 112-117.PubMedGoogle Scholar
  118. Moats WA, Dabbah R, Edwards VM: Survival of Salmonella anatum heated in various media. Appl Microbiol. 1971, 21: 476-481.PubMed CentralPubMedGoogle Scholar
  119. Morgan JN, Lin FJ, Eitenmiller RR, Barnhart HM, Toledo RT: Thermal destruction of Escherichia coli and Klebsiella pneumoniae in human milk. J Food Prot. 1988, 51: 132-136.Google Scholar
  120. Mulak V, Tailliez R, Eb P, Becel P: Heat resistance of bacteria isolated from preparations based on seafood products. J Food Prot. 1995, 58: 49-53.Google Scholar
  121. Murano EA, Pierson MD: Effect of heat shock and growth atmosphere on the heat resistance of Escherichia coli O157:H7. J Food Prot. 1992, 55: 171-175.Google Scholar
  122. Murano EA, Pierson MD: Effect of heat shock and incubation atmosphere on injury and recovery of Escherichia coli O157:H7. J Food Prot. 1993, 56: 568-572.Google Scholar
  123. Muriana PM, Hou H, Singh RK: A flow-injection system for studying heat inactivation of Listeria monocytogenes and Salmonella enteritidis in liquid whole egg. J Food Prot. 1996, 59: 121-126.Google Scholar
  124. Ng H: Heat sensitivity of 300 Salmonella isolates. U.S. Department of Agriculture, Agricultural Research Service ARS 74-37. 1966, 39-41.Google Scholar
  125. Ng H, Bayne HG, Garibaldi JA: Heat resistance of Salmonella: the uniqueness of Salmonella senftenberg 775W. Appl Microbiol. 1969, 17: 78-82.PubMed CentralPubMedGoogle Scholar
  126. Norberg P: Yersinia i opastöriserad mjölk (Yersinia enterocolitica in raw milk). Vår Föda. 1981, 33: 45-51. (In Swedish, summary in English)Google Scholar
  127. Northolt MD, Beckers HJ, Vecht U, Toepoel L, Soentoro PSS, Wisselink HJ: Listeria monocytogenes: heat resistance and behaviour during storage of milk and whey and making of Dutch types of cheese. Neth Milk Dairy J. 1988, 42: 207-219.Google Scholar
  128. Okrend AJ, Johnston RW, Moran AB: Effect of acetic acid on the death rates at 52°C of Salmonella newport, Salmonella typhimurium and Campylobacter jejuni in poultry scald water. J Food Prot. 1986, 49: 500-503.Google Scholar
  129. Oosterom J, de Wilde GJA, de Boer E, de Blaauw LH, Karman H: Survival of Campylobacter jejuni during poultry processing and pig slaughtering. J Food Prot. 1983, 46: 702-706. 709Google Scholar
  130. Osborne WW, Straka RP, Lineweaver H: Heat resistance of strains of Salmonella in liquid whole egg, egg yolk, and egg white. Food Res. 1954, 19: 451-463.Google Scholar
  131. Pagán R, Mañas P, Alvarez I, Sala FJ: Heat resistance in different heating media of Listeria monocytogenes ATCC 15313 grown at different temperatures. J Food Safety. 1998, 18: 205-219. 10.1111/j.1745-4565.1998.tb00215.x.Google Scholar
  132. Pagán R, Mañas P, Raso J, Trepat FJS: Heat resistance of Yersinia enterocolitica grown at different temperatures and heated in different media. Int J Food Microbiol. 1999, 47: 59-66. 10.1016/S0168-1605(99)00008-2.PubMedGoogle Scholar
  133. Palumbo MS, Beers SM, Bhaduri S, Palumbo SA: Thermal resistance of Salmonella spp. and Listeria monocytogenes in liquid egg yolk and egg yolk products. J Food Prot. 1995, 58: 960-966.Google Scholar
  134. Palumbo MS, Beers SM, Bhaduri S, Palumbo SA: Thermal resistance of Listeria monocytogenes and Salmonella spp. in liquid egg white. J Food Prot. 1996, 59: 1182-1186.Google Scholar
  135. Patchett RA, Watson N, Fernandez PS, Kroll RG: The effect of temperature and growth rate on the susceptibility of Listeria monocytogenes to environmental stress conditions. Lett Appl Microbiol. 1996, 22: 121-124.PubMedGoogle Scholar
  136. Patel SS, Wilbey RA: Thermal inactivation of γ-glutamyltranspeptidase and Enterococcus faecium in milk-based systems. J Dairy Res. 1994, 61: 263-270.PubMedGoogle Scholar
  137. Pflug IJ, Holcomb RG: Principles of thermal destruction of microorganisms. Disinfection, Sterilization, and Preservation. Edited by: Block SS. 1983, Lea & Febiger, Philadelphia, 751-810. 3Google Scholar
  138. Quintavalla S, Barbuti S: Resistenza termica di Listeria innocua e di Listeria monocytogenes isolate da carne suina (Heat resistance of Listeria innocua and Listeria monocytogenes isolated from pork). Industria Conserve. 1989, 64: 8-12. (In Italian, summary in English)Google Scholar
  139. Quintavalla S, Campanini M: Effect of rising temperature on the heat resistance of Listeria monocytogenes in meat emulsion. Lett Appl Microbiol. 1991, 12: 184-187.Google Scholar
  140. Quintavalla S, Campanini M, Miglioli L: Effetto della velocità di riscaldamento sulla resistenza termica di Streptococcus faecium (Effect of heating rate on the heat resistance of Streptococcus faecium). Industria Conserve. 1988, 63: 252-256. (In Italian, summary in English)Google Scholar
  141. Read RB, Bradshaw JG, Dickerson RW, Peeler JT: Thermal resistance of salmonellae isolated from dry milk. Appl Microbiol. 1968, 16: 998-1001.PubMed CentralPubMedGoogle Scholar
  142. Read RB, Norcross NL, Hankinson DJ, Litsky W: Come-up time method of milk pasteurization. III. Bacteriological studies. J Dairy Sci. 1957, 40: 28-36.Google Scholar
  143. Read RB, Schwartz C, Litsky W: Studies on thermal destruction of Escherichia coli in milk and milk products. J Appl Microbiol. 1961, 9: 415-418.Google Scholar
  144. Renner P, Peters J: Resistance of enterococci to heat and chemical agents. Zbl Hyg Umweltmed. 1998, 202: 41-50.Google Scholar
  145. Richards T, White HRB: The heat disinfection of Streptococcus faecalis. Proc Soc Appl Bacteriol. 1949, 2: 61-65.Google Scholar
  146. Rossebø L: Undersøkelser over resistens overfor fuktig varme hos stammer av Salmonella senftenberg isolert fra sildemel (Wet heat resistance in strains of Salmonella senftenberg isolated from herring meal). Nord Vet-Med. 1970, 22: 631-633. (In Norwegian, summary in English)Google Scholar
  147. Rowan NJ, Anderson JG: Effects of above-optimum growth temperature and cell morphology on thermotolerance of Listeria monocytogenes cells suspended in bovine milk. Appl Environ Microbiol. 1998, 64: 2065-2071.PubMed CentralPubMedGoogle Scholar
  148. Sanz Pérez B, López Lorenzo P, García ML, Hernández PE, Ordoñez JA: Heat resistance of enterococci. Milchwissenschaft. 1982, 37: 724-726.Google Scholar
  149. Schuman JD, Sheldon BW: Thermal resistance of Salmonella spp. and Listeria monocytogenes in liquid egg yolk and egg white. J Food Prot. 1997, 60: 634-638.Google Scholar
  150. Semanchek JJ, Golden DA: Influence of growth temperature on inactivation and injury of Escherichia coli O157:H7 by heat, acid, and freezing. J Food Prot. 1998, 61: 395-401.PubMedGoogle Scholar
  151. Shah DB, Bradshaw JG, Peeler JT: Thermal resistance of egg-associated epidemic strains of Salmonella enteritidis. J Food Sci. 1991, 56: 391-393. 10.1111/j.1365-2621.1991.tb05287.x.Google Scholar
  152. Shannon EL, Reinbold GW, Clark WS: Heat resistance of enterococci. J Milk Food Technol. 1970, 33: 192-196.Google Scholar
  153. Shenoy K, Murano EA: Effect of heat shock on the thermotolerance and protein composition of Yersinia enterocolitica in brain heart infusion broth and ground pork. J Food Prot. 1996, 59: 360-364.Google Scholar
  154. Simpson MV, Smith JP, Ramaswamy HS, Simpson BK, Ghazala S: Thermal resistance of Streptococcus faecium as influenced by pH and salt. Food Res Int. 1994, 27: 349-353. 10.1016/0963-9969(94)90190-2.Google Scholar
  155. Solowey M, Sutton RR, Calesnick EJ: Heat resistance of Salmonella organisms isolated from spray-dried whole-egg powder. Food Technol. 1948, 2: 9-14.Google Scholar
  156. Sörqvist S: Heat resistance of Campylobacter and Yersinia strains by three methods. J Appl Bacteriol. 1989, 67: 543-549.PubMedGoogle Scholar
  157. Sörqvist S: Heat resistance of Listeria monocytogenes by two recovery media used with and without cold preincubation. J Appl Bacteriol. 1993, 74: 428-432.PubMedGoogle Scholar
  158. Sörqvist S: Heat resistance of different serovars of Listeria monocytogenes. J Appl Bacteriol. 1994, 76: 383-388.Google Scholar
  159. Sörqvist S, Danielsson-Tham M-L: Survival of Campylobacter, Salmonella and Yersinia spp. in scalding water used at pig slaughter. Fleischwirtsch. 1990, 70: 1451-1454.Google Scholar
  160. Steinmeyer S: Untersuchungen zu Pathogenität, Hitzeresistenz und Acriflavinempfindlichkeit von Listerienstämmen (Investigations of pathogenicity, heat resistance and acriflavine sensitivity of Listeria strains). Dissertation, Munich. 1988, 60-75. (In German)Google Scholar
  161. Stephens PJ, Cole MB, Jones MV: Effect of heating rate on the thermal inactivation of Listeria monocytogenes. J Appl Bacteriol. 1994, 77: 702-708.PubMedGoogle Scholar
  162. Stringer SC, George SM, Peck MW: Thermal inactivation of Escherichia coli O157:H7. J Appl Microbiol Symposium Supplement. 2000, 88: 79S-89S.Google Scholar
  163. Stumbo CR: Thermobacteriology in Food Processing. 1973, Academic Press, New York, 70-120. 2Google Scholar
  164. Suárez Fernández G, Suárez Rodríguez M, Fernández Garayzabal F, Domínguez Rodríguez L: Termorresistencia de Listeria monocytogenes (Thermal resistance of Listeria monocytogenes). Alimentaria. 1989, 200: 51-53. (In Spanish, summary in English)Google Scholar
  165. Teo Y-L, Raynor TJ, Ellajosyula KR, Knabel SJ: Synergistic effect of high temperature and high pH on the destruction of Salmonella enteritidis and Escherichia coli O157:H7. J Food Prot. 1996, 59: 1023-1030.Google Scholar
  166. Thomas CT, White JC, Longrée K: Thermal resistance of salmonellae and staphylococci in foods. Appl Microbiol. 1966, 14: 815-820.PubMed CentralPubMedGoogle Scholar
  167. Thompson WS, Busta FF, Thompson DR, Allen CE: Inactivation of salmonellae in autoclaved ground beef exposed to constantly rising temperatures. J Food Prot. 1979, 42: 410-415.Google Scholar
  168. Toora S, Budu-Amoako E, Ablett RF, Smith J: Effect of high-temperature short-time pasteurization, freezing and thawing and constant freezing, on the survival of Yersinia enterocolitica in milk. J Food Prot. 1992, 55: 803-805.Google Scholar
  169. Tsuchido T, Takano M, Shibasaki I: Effect of temperature-elevating process on the subsequent isothermal death of Escherichia coli K-12. J Ferment Technol. 1974, 52: 788-792.Google Scholar
  170. Vrchlabsky J, Leistner L: Hitzeresistenz der Enterokokken bei unterschiedlichen aw-Werten. (Heat resistance of enterococci at different aw values). Fleischwirtsch. 1970, 50: 1237-1238. (In German, summary in English)Google Scholar
  171. Waterman SC: The heat-sensitivity of Campylobacter jejuni in milk. J Hyg Camb. 1982, 88: 529-533.PubMed CentralPubMedGoogle Scholar
  172. White HR: The heat resistance of Streptococcus faecalis. J Gen Microbiol. 1953, 8: 27-37.PubMedGoogle Scholar
  173. White HR: The effect of variation in pH on the heat resistance of cultures of Streptococcus faecalis. J Appl Bacteriol. 1963, 26: 91-99.Google Scholar
  174. Williams NC, Ingham SC: Changes in heat resistance of Escherichia coli O157:H7 following heat shock. J Food Prot. 1997, 60: 1128-1131.Google Scholar
  175. Williams NC, Ingham SC: Thermotolerance of Escherichia coli O157:H7 ATCC 43894, Escherichia coli B, and an rpoS -deficient mutant of Escherichia coli O157:H7 ATCC 43895 following exposure to 1.5% acetic acid. J Food Prot. 1998, 61: 1184-1186.PubMedGoogle Scholar
  176. Wolfson LM, Sumner SS: Antibacterial activity of the lactoperoxidase system against Salmonella typhimurium in trypticase soy broth in the presence and absence of a heat treatment. J Food Prot. 1994, 57: 365-368.Google Scholar
  177. Xavier IJ, Ingham S: Increased D-values for Salmonella enteritidis resulting from the use of anaerobic enumeration methods. Food Microbiol. 1993, 10: 223-228. 10.1006/fmic.1993.1024.Google Scholar
  178. Yamamori T, Yura T: Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc Natl Acad Sci USA. 1982, 79: 860-864. 10.1073/pnas.79.3.860.PubMed CentralPubMedGoogle Scholar
  179. Zivanovic R, Oluski A, Tadic Z: Contribution to the knowledge of thermoresistance of the group D streptococci by Lancefield. Tehnologija Mesa. 1965, 6: 198-205.Google Scholar

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Acta Veterinaria Scandinavica

ISSN: 1751-0147