The microbial safety of MAP

Modified atmospheres containing CO2 are effective in extending the shelf life of many food products. However, one major concern is the inhibition of normal aerobic spoilage bacteria and the possible growth of psychrotrophic food pathogens, which may result in the food becoming unsafe for consumption before it appears to be organoleptically unacceptable. Most of the pathogenic bacteria can be inhibited by low temperatures (<7°C). At these conditions, only psy-chrotrophic pathogens can proliferate. The effect of CO2 on the different psychrotrophic foodborne pathogens is described below.

16.5.1 Clostridium botulinum

One major concern is the suitability of MAP in the food industry. This is mainly due to the possibility that psychrotrophic, non-proteolytic strains of C. botulinum types B, E, and F are able to grow and produce toxins under MAP conditions. Little is known about the effects of modified atmosphere storage conditions on toxin production by C. botulinum. The possibility of inhibiting C. botulinum by incorporating low levels of O2 in the package does not appear to be feasible. Miller (1988, cited by Connor et al, 1989) reported that psychrotrophic strains of C. botulinum are able to produce toxins in an environment with up to 10% O2. Toxin production by C. botulinum type E, prior to spoilage, has been described in 3 types of fish, at O2 levels of 2% and 4% (O'Connor-Shaw and Reyes, 2000). Dufresne et al (2000) also proposed that additional barriers, other than headspace O2 and film, need to be considered to ensure the safety of MAP trout fillets, particularly at moderate temperature abuse conditions.

The probability of one spore of non-proteolytic C. botulinum (types B, E, and F) being toxicogenic in rock fish was outlined in a report by Ikawa and Genigeorgis (1987). The results showed that the toxigenicity was significantly affected (P < 0.005) by temperature and storage time, but not by the used modified atmosphere (vacuum, 100% CO2, or 70% CO2/30% air). In Tilapia fillets, a modified atmosphere (75% CO2/25% N2), at 8 °C, delayed toxin formation by C. botulinum type E, from 17 to 40 days, when compared to vacuum packaged fillets (Reddy et al, 1996). Similar inhibiting effects were recorded for salmon fillets and catfish fillets, at 4°C (Reddy et al, 1997a and 1997b). Toxin production from non-proteolytic C. botulinum type B spores was also retarded by a CO2 enriched atmosphere (30% CO2/70% N2) in cooked turkey at 4°C but not at 10°C nor at 15°C (Lawlor et al, 2000). Recent results in a study by Gibson et al (2000) also indicated that 100% CO2 slows the growth rate of C. botulinum, and that this inhibitory effect is further enhanced with appropriate NaCl concentrations and chilled temperatures.

16.5.2 Listeria monocytogenes

Listeria monocytogenes is considered a psychrotrophic foodborne pathogen. Growth is possible at 1 °C (Varnam and Evans, 1991) and has even been reported at temperatures as low as -1.5°C (Hudson et al, 1994). The growth of L. mono-cytogenes in food products, packaged under modified atmospheres, has been the focus of several, although in some cases contradicting, studies (Garcia de Fernando et al, 1995). In general, L. monocytogenes is not greatly inhibited by

CO2 enriched atmospheres (Zhao et al, 1992) although when combined with other factors such as low temperature, decreased water activity and the addition of Na lactate the inhibiting effect of CO2 is significant (Devlieghere et al, 2001). Listeria growth in anaerobic CO2 enriched atmospheres has been demonstrated in lamb in an atmosphere of 50:50 CO2/N2, at 5°C (Nychas, 1994); in frankfurter type sausages in atmospheres of distinct proportions of CO2/N2, at 4, 7, and 10 °C (Krämer and Baumgart, 1992) and in pork in an atmosphere of 40:60 CO2/N2, at 4 °C (Manu-Tawiah et al, 1993). However, other authors have not detected growth in chicken anaerobically packaged in 30:70 CO2/N2, at 6°C (Hart et al, 1991); in 75:25 CO2/N2 at 4 °C (Wimpfheimer et al, 1990) and at 4 °C in 100% CO2 in raw minced meat (Franco-Abuin et al, 1997) or in buffered tryptose broth (Szabo and Cahill, 1998). Several investigations demonstrated possible growth of L. monocytogenes on modified atmosphere packaged fresh-cut vegetables, although the results depended very much on the type of vegetables and the storage temperature (Berrang et al, 1989a; Beuchat and Brackett, 1990; Omary et al, 1993; Carlin et al, 1995; Carlin et al, 1996a and 1996b; Zhang and Farber, 1996; Juneja et al, 1998; Bennik et al, 1999; Jacxsens et al, 1999a; Liao and Sapers, 1999; Thomas et al, 1999; Castillejo-Rodriguez et al, 2000).

There is no agreement about the effect of incorporating O2 in the atmosphere on the antimicrobial activity of CO2 on L. monocytogenes (Garcia de Fernando et al, 1995). However, this effect could be very important in practice, as the existence of residual O2 levels after packaging, and the diffusion of O2 through the packaging film, can result in substantial O2 levels during the storage of industrially 'anaerobically' modified atmosphere packaged food products. Most publications suggest there is a decrease in the inhibitory effect of CO2 on L. monocytogenes when O2 is incorporated into the atmosphere. Experiments on raw chicken showed L. monocytogenes failed to grow at 4, 10, and 27 °C, in an anaerobic atmosphere containing 75% CO2 and 25% N2 (Wimpfheimer et al, 1990). However, an aerobic atmosphere containing 72.5% CO2, 22.5% N2, and 5% O2 did not inhibit the growth of L. monocytogenes, even at 4°C. L. monocytogenes was also only minimally inhibited on chicken legs, in an atmosphere containing 10% O2 and 90% CO2 (Zeitoun and Debevere, 1991). There was no significant difference in the inhibitory effect of CO2, between the range of 0% and 50%, when 1.5% O2, or 21% O2 was present in the atmosphere of gas packaged brain heart infusion agar plates (Bennik et al, 1995). When L. monocytogenes was cultured in buffered nutrient broth, at 7.5°C, in atmospheres containing 30% CO2, with four different O2 concentrations (0, 10, 20, and 40%), the results showed that bacterial growth increased with the increasing O2 concentrations (Hendricks and Hotchkiss, 1997).

16.5.3 Yersinia enterocolitica

Yersinia enterocolitica is generally regarded as one of the most psychrotrophic foodborne pathogens. Growth of Y. enterocolitica was reported in vacuum packaged lamb at 0°C (Doherty et al, 1995; Sheridan and Doherty, 1994; Sheridan

Table 16.3 Growth of Yersina enterocolitica in different atmospheres

Product type

(days)

Atmosphere (%O2/CO2/N2)

Increase (log cfu/g)

Reference

Beef

>6.0

-2

126

0/100/0

0

Gill and Reichel

63

vacuum

2.4

(1989)

0

98

0/100/0

0

49

vacuum

4.1

2

42

0/100/0

0

35

vacuum

5.1

5

35

0/100/0

1.9

17

vacuum

5.5

10

10

0/100/0

3.4

5

vacuum

4.0

Sliced

6.1

-1.5

112

0/100/0

0

Hudson et al

roast

56

vacuum

4.2

(1994)

beef

3

70

0/100/0

3.8

21

vacuum

4.7

Pork

5.57

30

0/100/0

0

Bodnaruk and

(normal)

4

25

vacuum

1.7

Draughon (1998)

6.21

30

0/100/0

1.7

(high)

25

vacuum

2.6

Pork

6.0

35

0/20/80

4.1

Manu-Tawiah et al

chops

4

35

0/40/60

4.0

(1993)

35

10/40/50

4.0

35

vacuum

4.1

Lamb

5.4-5.8

0

28

80/20/0

1.2

Doherty et al

28

0/50/50

3.9

(1995)

28

0/100/0

1.6

28

vacuum

5.9

5

28

80/20/0

6.8

28

0/50/50

8.5

28

0/100/0

5.6

28

vacuum

8.1

et al, 1992), beef at -2°C (Gill and Reichel, 1989), pork at 4°C (Bodnaruk and Draughon, 1998; Manu-Tawiah et al, 1993), fresh chicken breasts (Ozbas et al, 1997) and roast beef at 3 °C but not at -1.5 °C (Hudson et al, 1994).

CO2 retards the growth of Y. enterocolitica at refrigerated temperatures. The effect of CO2 on the growth of Y. enterocolitica has been described by several authors. Some of the results are shown in Table 16.3. Oxygen also seems to play an inhibiting role on the growth of Y. enterocolitica (Garcia de Fernando et al, 1995). To ensure total inhibition of Y. enterocolitica in O2 poor atmospheres and at realistic temperatures throughout the cooling chain, high CO2 concentrations in the headspace are necessary.

16.5.4 Aeromonas spp.

Aeromonas species are able to multiply in food products stored in refrigerated conditions. Growth of A. hydrophila has been detected at low temperatures in a variety of vacuum packaged fresh products, such as chicken breasts at 3 °C (Ozbas et al, 1996), lamb at 0°C under high pH conditions (Doherty et al, 1996), and at -2 °C (Gill and Reichel, 1989), and in sliced roast beef at -1.5 °C (Hudson et al, 1994). Devlieghere et al (2000a) developed a model, predicting the influence of temperature and CO2 on the growth of A. hydrophila. Proliferation of A. hydrophila is greatly affected by CO2 enriched atmospheres. Some reports regarding the effect of CO2 on the growth of A. hydrophila on meat are summarised in Table 16.4.

In a study by Berrang et al (1989b), regarding controlled atmosphere storage of broccoli, cauliflower and asparagus stored at 4°C and 15 °C, fast proliferation of A. hydrophila was observed at both temperatures, but growth was not significantly affected by gas atmosphere. Garcia-Gimeno et al (1996) published the survival of A. hydrophila on mixed vegetable salads (lettuce, red cabbage and carrots) packaged under MA (initial 10% of 02-10% CO2, after 48h 0% O2-18% CO2) and stored at 4°C while at 15 °C a fast growth was noticed (5 log units in 24h). The combination of high CO2 concentration and low temperature were revealed as responsible for the inhibition of growth. Bennik et al (1995) concluded from their solid-surface model that at MA-conditions, generally applied for minimally processed vegetables (1-5% O2 and 5-10% CO2), growth of A. hydrophila is possible. Growth was virtually the same under 1.5% and 21% O2. The behaviour of a cocktail of A. caviae (HG4) and A. bestiarum (HG2) in air or in low O2-low CO2 atmosphere was investigated in fresh-cut vegetables: no difference between both atmospheres was observed on grated carrots, a decreased growth on shredded Belgian endive and Brussels sprouts in MA but an increased growth on shredded iceberg lettuce in MA storage (Jacxsens et al, 1999a).

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