Directory UMM :Data Elmu:jurnal:S:Small Ruminant Research:Vol36.Issue1.Apr2000:
Small Ruminant Research 36 (2000) 75±84
Microbial and sensory quality changes in refrigerated
minced goat meat stored under vacuum and in air
Y. Babjia,*, T.R.K. Murthyb, A.S.R. Anjaneyulub
a
Central Institute for Research on Goats, Makhdoom 281 122, Mathura, India
b
Indian Veterinary Research Institute, Izatnagar 243 122, U.P., India
Accepted 11 August 1999
Abstract
Goat mince was packed and stored at 4 18C. Mince was analysed physico-chemically and microbiologically at intervals
0, 3, 7, 10, 21 and 28 days for packs stored aerobically and 7, 14, 21, 28 and 40 days for vacuum packs. Although the initial pH
of mince was 6.5, meat pH and extract release volume declined during vacuum storage. The microbial pro®le of aerobically
stored mince was signi®cantly higher than that in vacuum packs. The mean count of total aerobes of aerobic packages was
higher than that of different groups of spoilage ¯ora in vacuum packed mince. The air packed mince comprised the climax
population (log10 cfu gÿ1) of aerobic plate counts (9.0), psychrotrophs (8.8), coliforms (6.0), enterobacteriaceae (6.0),
Pseudomonas (9.0), faecal streptococci (6.8), lactic acid bacteria (3.5), staphylococcal counts (5.5) and yeast and mould (4.0)
counts, whereas bacterial (log10 cfu gÿ1) pro®le of vacuum packed mince included total aerobic plate counts (7.0),
psychrotrophs (7.1), Pseudomonas (7.6) faecal streptococci (7.3) and lactic acid bacteria counts (3.1). The shelf-life was 28
days for vacuum packed mince whereas similar overall acceptability scores were observed at 3 days for aerobic packages.
During storage putrid odours in aerobically packed mince and sulphide odours in vacuum packs were observed. High pH of
mince and the initial heavy carcass contamination promoted the rapid multiplication of facultative anaerobes leading to
spoilage of the mince. # 2000 Published by Elsevier Science B.V. All rights reserved.
Keywords: Goat meat; Microbes; Vacuum packaging; Aerobic packaging; Spoilage; Shelf-life
1. Introduction
India possesses 1/5th of the global goat population
producing more than 0.47 million tonnes of meat.
Goat meat is the most widely consumed in this country
and the extension of its shelf-life is important in
marketing the product for internal consumption and
*
Corresponding author. Tel.: 91-0565-763280; fax: 91-0565763246.
E-mail address: [email protected] (Y. Babji).
export purposes. Vacuum packaging to extend the
shelf-life of raw meat is well established. The principal objective of vacuum packaging is the partial or
total inhibition of rapidly growing pseudomonads and
allowance of dominance by ¯ora of low spoilage
potential lactic acid bacteria. The composition of
the climax population that consequently develops
on the packaged meat will be of mixed (Gill, 1996)
type and dictates the course of spoilage which is
largely affected by relative numbers of various spoilage types in the initial ¯ora (Gill and Tan, 1979).
0921-4488/00/$ ± see front matter # 2000 Published by Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 1 - 4 4 8 8 ( 9 9 ) 0 0 1 0 6 - 6
76
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
However, dominance of lactic acid bacteria in the
climax population will depend on initial ¯ora of
lactics, pH of meat, level of initial contamination
and prevalence or absence of facultative anaerobic
biota (Grau, 1980, 1981). Initial microbial load, gas
permeability of packaging ®lm and temperature of
meat during storage play a signi®cant role in extending the shelf-life of packaged meat (Gardner et al.,
1967; Adams and Huffman, 1972; McMullen and
Stiles, 1991). High pH (>5.8) meat tissue at 08C or
below under O2 depleted CO2 atmospheres exhibited
no growth of facultative anaerobic bacteria and dominance by lactic acid bacteria (Gill and Harrison,
1989). Few studies have been conducted on vacuum
packed lamb (Shaw et al., 1980; Moore and Gill, 1987;
Sheridan et al., 1997). Compared with beef, shelf-life
of vacuum packed lamb has been reported to be short.
Gill and Jones (1994) reported a minimum shelf-life of
4 weeks for vacuum packed ground beef. The present
study described physico-chemical, microbial and sensory changes in high pH (6.5) minced goat meat stored
under vacuum in poly-ethylene pteraphthalate
(PETPE) ®lm and the aerobic storage life in low
density polyethylene (LDPE) ®lm at 4 18C.
2. Materials and methods
2.1. PETPE laminate
The PETPE ®lm was a two-layered laminate (Flex
Industries, Noida, India) with a water vapour transmission rate (WVTR) of 1.6 g cmÿ2 per 24 h at 80%
relative humidity at 378C. One layer of this laminate
was composed of PETPE with a thickness of 10m and
the other layer was polyethylene. The gas transmission
rate of the ®lm is not known. The PETPE bags were
vacuum sealed using a Roschermatic packaging
machine (Model VM 19S, Roscherwerke Gmbh, Germany) and refrigerated (4 18C).
Goat meat (obtained from non-descript animals of 2
years age) was purchased 3±4 h after slaughter from a
local meat shop. Leg portion was cut into chunks after
removing the loose fat, fascia and connective tissue.
Meat chunks from two to three animals were pooled
for each trial. Mince was prepared in the laboratory by
passing the chunks through an 8 mm plate of the
mincer (Electrolux, Sweden), and two trials were
conducted.
The minced meat was divided into 200 g portions
and placed in individual bags of LDPE for aerobic
storage or in PETPE bags for vacuum storage. The
LDPE bags were refrigerated (4 18C) without sealing the ends of pouches. The aerobically stored packs
were analysed at 0, 3, 7, 10, 21 and 28 days. The
vacuum packed samples were analysed at 0, 7, 14, 21,
28 and 40 days of storage.
2.2. Analyses of packed mince
pH of mince was determined by grinding 10 g of
mince from each storage pack with 50 ml of distilled
water with frequent blending. pH was recorded by
dipping the combined glass electrode of a digital pH
meter (Century, Model LP 901) in the mince slurry
(Trout et al., 1992). Three readings were made on each
sample and the mean recorded.
A 10 g mince from each storage pack was ground
with 200 ml of distilled water in a Warring blender and
the volume of the slurry was made up to 250 ml in a
volumetric ¯ask and ®ltered through Whatman No. 2
®lter paper. 25 ml of ®ltrate was collected to which
75 ml of distilled water was added and titrated against
0.1 N NaOH with three drops of phenolphthalein. The
amount of standardized 0.1 N NaOH required to neutralize the meat is expressed as total acidity (Konecko,
1979).
25 g mince was blended with 100 ml of distilled
water in a Warring blender for 5 min. The resultant
slurry was ®ltered through Whatman No. 2 ®lter paper
and the amount of ®ltrate released in 15 min was
expressed as extract release volume (Jay, 1964).
Minced meat was placed in sample holder of Lovibond tintometer (Model E, The Tintometer, Salisbury,
UK) and secured against the viewing aperture. The
colour of the mince was determined by adjusting the
red and yellow units while blue units were kept
constant (Froehlich et al., 1982).
2.3. Microbial analysis
Representative 10 g mince from each storage pack
was transferred to a sterile mortar and blended with
90 ml of 0.1% peptone±water for 60 s. Individual
serial decimal dilutions for mince from each storage
pack were prepared in 9 ml volume of sterile 0.1%
peptone±water up to 1 : 106 dilution of the original
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
food sample. Duplicate 0.1±0.5 ml or 1 ml inoculum
of appropriate dilutions were spread with a sterile
glass spreader on pre-poured plates or pour plated,
respectively, on the following media: for enumeration
of aerobic plate counts on spread plates of plate count
agar (PCA, Hi-Media Laboratories, M 091, Bombay)
which were incubated at 308C for 48 h; psychrotrophs
on spread plates of plate count agar (PCA, Hi-Media,
M 091) which were incubated at 4 18C for 10±14
days; Pseudomonas counts on spread plates of plate
count agar (Pseudomonas ¯uorescein agar with 1 ppm
crystal violet, Hi-Media, M 120) which were incubated at 308C for 72 h; Staphylococcal counts on
spread plates of Baird Parker agar (BPA, Hi-Media,
M 043) which were incubated at 378C for 48 h;
anaerobic plate counts on pour plates of plate count
agar (PCA, Hi-Media, M 091) which were incubated
at 358C for 24 h; Enterobacteriaceae counts on pour
plates of Violet Red Bile Glucose agar (VRBG, HiMedia, M 581) which were incubated at 378C for 24 h;
faecal streptococci on pour plates of Slanetz and
Bartley agar (SBM, Hi-Media, M 641) which were
incubated at 378C for 48 h; lactic acid bacteria counts
on pour plates of MRS agar (MRS, Hi-Media, M 641)
which were incubated at 308C for 120 h; yeast and
mould counts on pour plates of potato dextrose agar
(PDA, Hi-Media, M 096) with 2% antibiotic (Chloramphenicol and chlortetracycline, 1 : 1) and the plates
were incubated at 258C for 120 h. Colonies were
counted from each group of micro-¯ora and expressed
as log per gram. The enumeration procedures as
described by Speck (1975) were followed.
2.4. Sensory (objective) evaluation of packed mince
Goat meat mince in aerobic packages and under
vacuum was assessed 2 h after opening the packs at
each storage interval by a three member semi-trained
panel for colour, odour, discolouration and over all
acceptability traits (Gill and Jones, 1994; Gill and
McGinnis, 1995). The colour acceptability of mince
was scored on a 7-point scale with slight modi®cation
in the procedure where 7 represents bright red and 1
indicates extremely dull red. The degree of discolouration of the mince in the package was expressed in
percent on a 5 point scale (1: no discolouration, 2: 1±
10%, 3: 11±25%, 4: 25±50%, 5: 50±100%). The odour
acceptability of the mince was assessed on a 4 point
77
scale where 1 indicates no off-odour, 4 represents
strong off-odour. The type of odours developed during
storage was recorded. The overall acceptability of the
mince was assessed on a 7 point scale where 7
represents extremely acceptable and 1 indicates extremely unacceptable.
2.5. Statistical analysis
Data were analysed statistically for all the parameters according to procedures described by Snedecor
and Cochran (1967). Analysis of variance were used to
assess pH, total acidity, ERV and microbial counts
based on a linear model that included aerobic and
vacuum storage conditions and storage time within
storage condition. The difference between the means
were tested by critical difference. The sensory evaluation scores (colour, discolouration, odour and overall
acceptability) and Lovibond colour units (red, yellow
and green) of minced goat meat were tested using chisquare analysis. The hypothesis that the initial values
are not affected due to aerobic or vacuum storage was
tested for each parameter.
3. Results
The mean pH, total acidity and extract release
volume of minced goat meat under aerobic and/or
vacuum storage at 4 18C is shown in Table 1. The
initial pH of minced goat meat used in this study was
high (6.5). The extract release volume decreased and
total acidity increased during storage in both aerobic
and vacuum packages. There was no signi®cant effect
of storage period on pH of meat under both the storage
conditions (Table 1).
The microbial growth in the mince stored aerobically or under vacuum is shown in Figs. 1±9. Analysis
of variance of the data indicated a signi®cant effect of
the storage condition on the counts of all the microbial
groups except for lactic acid bacteria and yeasts and
moulds. The lactic acid bacteria and Pseudomonas
counts increased while those of enterobacteriaceae
decreased by day 7 under both the storage conditions.
There was a signi®cant drop in the lactic counts during
further storage of aerobic or vacuum stored samples up
to 28 days. The growth of Pseudomonas was
restrained while that of enterobacteriaceae increased
78
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Table 1
pH, total acidity and extract release volume (ERV) of minced goat meat under aerobic or vacuum packed (PETPE laminate) storage at
refrigeration temperaturea
Storage condition
Storage time (days)
pH
Total acidity
ERV (ml)
Initial
6.53 0.18a
0.70 0.10a
41.00 0.35a
a
b
Aerobic
3
7
10
21
28b
6.38 0.01
6.11 0.005a
6.13 0.17a
6.25 0.01a
NDd
1.00 0.00
1.00 0.00b
1.30 0.00c
1.30 0.00c
NDd
38.50 0.35a,b
36.00 1.00b
24.50 0.50c
30.25 0.25d
NDd
Vacuum
7
14
21
28
40c
6.00 0.01a
6.10 0.00a
6.07 0.01a
6.10 0.01a
6.03 0.00a
1.30 0.00b
1.20 0.00b
1.40 0.00b
1.20 0.00b
NDd
24.00 0.50b
25.50 0.50c
32.50 0.50d
24.50 0.50e
NDd
a
Means followed by the same alphabets do not differ signi®cantly (P < 0.05).
Spoiled due to putrefactive odours.
c
Spoiled due to sulphide odours.
d
ND: Not done.
b
from day 7 to 28 in the vacuum stored mince. There
was no signi®cant difference between the initial and
the day 28 counts of the vacuum stored samples for all
the microbial groups except for total aerobes, psychrotrophs and Pseudomonas.
Yeast and mould counts did not form a major part of
the prevalent micro-¯ora during storage both in aerobic (log 4.0) and vacuum (log 2.0) at day 28. Overall,
aerobically stored samples had higher microbial
counts than that of vacuum packed samples.
The vacuum packed goat meat was bright red at 7
days and moderately bright red at 14, 21 and 28 days
of storage whereas aerobically stored samples were
slightly bright red at 0, 3, 7 days and slightly dull red at
10, 21 days and dull red at 28 days (Table 2). Vacuum
packed goat meat had no discolouration up to 14 days
Fig. 1. Lactic acid bacteria counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
79
Fig. 2. Counts on Pseudomonas F-agar of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
storage and at 21 and 28 days there was a slight
discolouration 1±10% in the pack. The aerobically
stored samples showed 25±50% discolouration at 7
days and 50±100% discolouration at 21 days. The
vacuum packed samples were spoiled by sulphide
odours at 40 days while the aerobically stored packs
spoiled by putrefactive odours at 28 days. Thus, on
28th day, the vacuum packed samples were extremely
acceptable while the aerobically stored samples were
unacceptable.
Chi-square analysis of the data also indicated signi®cantly higher discolouration scores in aerobically
stored mince (Table 2), signi®cantly higher yellow
colour units for vacuum packs (Table 3) and lower
overall acceptability scores (Table 2) for aerobically
stored samples when compared with the initial values.
Fig. 3. Enterobacteriaceae counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
80
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Fig. 4. Total aerobic counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
4. Discussion
Data on microbial and sensory evaluation of minced
goat meat stored at 4 18C indicated a shelf-life of 28
days under vacuum compared with similar overall
acceptability scores at 3 days observed in aerobically
stored samples. The low storage life of aerobically
stored samples was due to loss of colour. Shaw et al.
(1980) also reported that the colour scores of refrigerated lamb loins in aerobic storage were lower than
that under vacuum for 6 weeks. Vacuum packed goat
meat mince maintained bright red colour up to 40 days
even when the meat was spoiled. Gill and Jones (1994)
observed that the master packed ground beef in anoxic
state continued to maintain its bloom up to 32 days
although its shelf-life was only 21 days. The spoilage
of vacuum packed mince by sulphide odours has also
been reported by earlier workers (Hanna et al., 1979,
1983). Greenish discolouration of the drip might be
due to oxidation of heme to greenish myoglobin or by
Fig. 5. Psychrotrophic counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
81
Fig. 6. Staphylococcal counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
formation of sulphmyoglobin between myoglobin and
hydrogen sulphide (Nicol et al., 1970; Taylor and
Shaw, 1977).
There were decreases in pH and ERV during storage
under vacuum. In normal pH meats, decrease in pH
and increase in ERV (Sutherland et al., 1975) or no
signi®cant changes in pH or ERV (Turner, 1960;
Pearson, 1968) have been reported. Total acidity
increased during storage under vacuum. Sutherland
et al. (1975) observed decrease in total alkalinity in
vacuum stored beef.
The highly variable shelf-life of vacuum packed
fresh meat has been attributed to differences in pH
(Rousset and Renerre, 1991), ®lm permeability
(Hodges et al., 1974) and initial contamination and
storage temperature (Bell and Garout, 1994). In the
present study, the initial pH of meat was very high (pH
6.5)
with
high
enterobacteriaceae
counts
Fig. 7. Yeast and mould counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
82
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Fig. 8. Coliform counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
(log 4.3 gÿ1). Meat with very high pH (>6.0) had a
very short shelf-life even in vacuum packaging (Bem
et al., 1976) as enterobacteriaceae and Brochothrix
compete better with rapid bacterial breakdown of
amino-acids producing unpleasant smelling products
such as H2S or ammonia (Newton and Gill, 1981). In
our study, the growth of lactic acid bacteria on the
vacuum packed meat in the beginning of spoilage was
very slow (log 3.1 gÿ1 at 28 days) unlike previous
studies (Egan, 1983; Dainty and Mackey, 1992). The
slow growth of lactic acid bacteria may be due to high
initial pH of meat and growth dominance by facultative anaerobic biota (enterobacteriaceae). These
results are in accordance with Grau (1980, 1981) on
high pH vacuum packed meat.
The increases in Pseudomonas counts in the ®rst
week of vacuum storage were in agreement with
Sutherland et al. (1975). There were increases in total
aerobic and psychrotrophic populations as the conditions were not completely anoxic in vacuum packa-
Fig. 9. Faecal streptococcal counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
83
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Table 2
Colour, discolouration, odour and overall acceptability scores of minced goat meat under aerobic or vacuum packed (PETPE laminate) storage
at refrigeration temperaturea
Storage
Condition
Storage time
(days)
Colour
scoresb
Discolouration
scoresc
Odour
scoresd
Overall acceptability
scorese
Initial
5.00a
1.00a
1.00a
7.00a
Aerobic
3
7
10
21
28
5.00a
5.00a
4.00a
4.00a
2.00a
1.00b
4.00b
4.00b
5.00b
5.00b
1.00a
1.00a
1.00a
1.00a
4.00a
7.00b
5.00b
4.00b
3.00b
1.00b
Vacuum
7
14
21
28
40
7.00a
6.00a
6.00a
6.00a
±
1.00a
1.00a
2.00a
2.00a
2.00a
1.00a
1.00a
1.00a
1.00a
4.00a
7.00a
7.00a
7.00a
7.00a
1.00a
a
Numbers followed by the same alphabets, placed on the basis of chi-square values, do not differ signi®cantly (P < 0.05).
7: Bright red; 4: Slightly dull; 1: Extremely dull.
c
1: No discolouration; 5: 50±100% discolouration.
d
1: No off odour; 4: Strong off odour.
e
7: Extremely acceptable; 4: Neither acceptable nor unacceptable; 1: Extremely unacceptable.
b
ging due to oxygen ingress through the plastic ®lm
(Nottingham, 1982). The low coliform and faecal
streptococcal counts in vacuum compared with the
aerobic storage were in accordance with Sutherland et
al. (1975) on vacuum packed beef. The staphylococcal
counts at 28 days of vacuum storage were lower than
in aerobic storage. However, Venugopal et al. (1993)
reported unusually high staphylococcal counts in
vacuum packed beef possibly due to high initial
contamination.
5. Conclusion
Vacuum packaging improves the colour and microbiological shelf-life of high pH minced goat meat
Table 3
Lovibond colour units of minced goat meat under aerobic or vacuum packed (PETPE laminate) storage at refrigeration temperaturea
Storage condition
Storage time (days)
Lovibond colour units
Red
Yellow
Green
Initial
5.4a
3.1a
3.0a
Aerobic
3
7
10
21
28
5.4a
5.6a
6.5a
5.4a
2.2a
4.2a
4.2a
4.5a
5.4a
3.3a
3.3a
3.2a
3.5a
4.4a
1.3a
Vacuum
7
14
21
28
40
7.4a
6.6a
6.4a
6.5a
NDb
6.5b
6.3b
5.4b
5.5b
NDb
3.2a
4.5a
4.3a
4.3a
NDb
a
b
Numbers followed by the same alphabets, placed on the basis of chi-square values, do not differ signi®cantly (P < 0.05).
ND: Not done due to greenish discolouration in the drip.
84
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
when compared with aerobic storage by maintaining
colour and restraining microbial growth with
increased acceptability scores.
References
Adams, J.R., Huffman, D.L., 1972. Effect of controlled gas
atmospheres and temperatures on quality of packaged pork. J.
Food Sci. 37, 869±872.
Bell, R.G., Garout, A.M., 1994. The effective product life of
vacuum packaged beef imported into Saudi Arabia by Sea as
assessed by chemical, microbiological and organoleptic
criteria. Meat Sci. 36, 381±396.
Bem, Z., Hechelmann, H., Leistner, L., 1976. The bacteriology of
DFD meat. Fleisch wirtschaft 56, 985±987.
Dainty, R.H., Mackey, B.M., 1992. The relationship between the
phenotypic properties of bacteria from chill-stored meat and
spoilage process. J. Appl. Bacteriol. Symp. Suppl. 73, 1035±
1145.
Egan, A.F., 1983. Lactic acid bacteria of meat and meat products.
Antonie van Leeuwenhoek. 49, 327±336.
Froehlich, D.A., Gullet, E.A., Usborne, W.R., 1982. Effect of
nitrite and salt on the colour, ¯avour and overall acceptability
of ham. J. Food Sci. 48, 152±154.
Gardner, G.A., Carson, A.W., Patton, J., 1967. Bacteriology of
prepacked pork with reference to the gas composition within
the pack. J. Appl. Bacteriol. 30, 321±332.
Gill, C.O., 1996. Extending the shelf-life of raw chilled meats.
Meat Sci. 43, S99±S107.
Gill, C.O., Harrison, J.C.L., 1989. The storage life of chilled pork
packed under carbon dioxide. Meat Sci. 26, 313±324.
Gill, C.O., Jones, T., 1994. The display life of retail-packaged beef
steaks after their storage in master packs under various
atmospheres. Meat Sci. 38, 385±396.
Gill, C.O., McGinnis, J.C., 1995. The effects of residual oxygen
concentration and temperature on the degradation of colour of
beef packaged under oxygen-depleted atmosphere. Meat Sci.
39, 387±394.
Gill, C.O., Tan, K.H., 1979. Effect of carbon dioxide on growth of
pseudomonas ¯uorescens. Appl. Environ. Microbiol. 38, 237.
Grau, F.H., 1980. Inhibition of the anaerobic growth of brochothrix
thermosphacta by lactic acid. Appl. Environ. Microbiol. 40,
443±446.
Grau, F.H., 1981. Role of pH, lactate and anaerobiosis in
controlling the growth of some fermentative gram negative
bacteria. Appl. Environ. Microbiol. 42, 1043±1050.
Hanna, M.O., Savell, J.W., Smith, G.C., Purser, D.E., Garder, F.A.,
Vanderzant, G., 1983. Effect of growth of individual meat
bacteria on pH, colour and odour of asceptically prepared
vacuum packaged round steaks. J. Food Prot. 46, 216±221.
Hanna, M.O., Smith, G.C., Hall, L.C., Vanderzant, C., 1979. Role
of Hafnia alvei and a Lactobacillus species in the spoilage of
vacuum packaged strip loin steaks. J. Food Prot. 42, 569.
Hodges, J.H., Cachill, V.R., Ockerman, H.W., 1974. Effect of vacuum
packaging on weight loss, microbial growth and palatability of
fresh beef whole sale cuts. J. Food Sci. 39, 143±146.
Jay, J.M., 1964. Release of aqueous extracts by beef homogenates
and factors affecting release volume. Food Technol. 18, 1633±
1638.
Konecko, E.W., 1979. Hand Book for Meat Chemists. Avery
Publishing Group, Wayne, USA.
McMullen, L.M., Stiles, M.E., 1991. Changes in microbial
parameters and gas composition during modi®ed atmosphere
storage of fresh pork loin chops. J. Food Prot. 54, 178±183.
Moore, V.J., Gill, C.O., 1987. The pH and display life of chilled
lamb after prolonged storage under vacuum or under CO2, NZ.
J. Agric. Res. 30, 449±452.
Newton, K.G., Gill, C.O., 1981. The microbiology of DFD fresh
meats. Meat Sci. 5, 223±232.
Nicol, D.J., Shaw, M.K., Ledward, D.A., 1970. Hydrogen sulphide
production by bacteria and sulphmyoglobin formation in
prepacked chilled beef. Appl. Microbiol. 19, 937±939.
Nottingham, P.M., 1982. Microbiology of carcass meats. In:
Brown, M.D. (Ed.), Meat Microbiology. Applied Science
Publishers, London, pp. 13±65.
Pearson, D., 1968. Assessment of meat freshness in quality control
employing chemical techniques. J. Sci. Food Agric. 19, 357±
366.
Rousset, S., Renerre, M., 1991. Effect of CO2 and vacuum
packaging on normal and high pH meat shelf-life. Int. J. Food
Sci. Tech. 26, 641±652.
Shaw, B.G., Harding, C.D., Taylor, A.A., 1980. The microbiology
and storage stability of vacuum packed lamb. J. Food. Technol.
15, 397±405.
Sheridan, J.J., Doherty, A.M., Allen, P., McDowell, D.A., Blair,
I.S., Harrington, D., 1997. Effect of vacuum and modi®ed
atmosphere packaging on the shelf-life of lamb primals, stored
at different temperatures. Meat Sci. 45, 107±117.
Snedecor, G.W., Cochran, W.G., 1967. Statistical Methods. Iowa
State University Press, Ames, IA.
Speck, M.L., 1975. Compendium of Methods for the Microbiological Examination of Foods. Am. Publ. Health Assoc.,
Washington.
Sutherland, J.P., Patterson, J.T., Murray, J.G., 1975. Some
metabolic and biochemical characteristics of representative
microbial isolates from vacuum packaged beef. J. Appl. Bact.
39, 27±237.
Taylor, A.A., Shaw, B.G., 1977. The effect of meat pH package
permeability on putrefaction and greening in vacuum packaged
beef. J. Food Technol. 12, 515±521.
Trout, E.S., Hunt, M.C., Johnson, D.E., Clons, J.R., Castner, C.L.,
Kropt, D.H., 1992. Characteristics of low fat ground beef
containing texture modifying ingredients. J. Food Sci. 57, 19±
24.
Turner, A., 1960. Assessing meat spoilage in the laboratory. Food
Mf. 35, 386.
Venugopal, R.J., Ingham, S.C., McCurdy, A.R., Jones, G.A.C.,
1993. Anaerobic microbiology of fresh beef packaged under
modi®ed atmosphere or vacuum. J. Food Sci. 58, 935±937.
Microbial and sensory quality changes in refrigerated
minced goat meat stored under vacuum and in air
Y. Babjia,*, T.R.K. Murthyb, A.S.R. Anjaneyulub
a
Central Institute for Research on Goats, Makhdoom 281 122, Mathura, India
b
Indian Veterinary Research Institute, Izatnagar 243 122, U.P., India
Accepted 11 August 1999
Abstract
Goat mince was packed and stored at 4 18C. Mince was analysed physico-chemically and microbiologically at intervals
0, 3, 7, 10, 21 and 28 days for packs stored aerobically and 7, 14, 21, 28 and 40 days for vacuum packs. Although the initial pH
of mince was 6.5, meat pH and extract release volume declined during vacuum storage. The microbial pro®le of aerobically
stored mince was signi®cantly higher than that in vacuum packs. The mean count of total aerobes of aerobic packages was
higher than that of different groups of spoilage ¯ora in vacuum packed mince. The air packed mince comprised the climax
population (log10 cfu gÿ1) of aerobic plate counts (9.0), psychrotrophs (8.8), coliforms (6.0), enterobacteriaceae (6.0),
Pseudomonas (9.0), faecal streptococci (6.8), lactic acid bacteria (3.5), staphylococcal counts (5.5) and yeast and mould (4.0)
counts, whereas bacterial (log10 cfu gÿ1) pro®le of vacuum packed mince included total aerobic plate counts (7.0),
psychrotrophs (7.1), Pseudomonas (7.6) faecal streptococci (7.3) and lactic acid bacteria counts (3.1). The shelf-life was 28
days for vacuum packed mince whereas similar overall acceptability scores were observed at 3 days for aerobic packages.
During storage putrid odours in aerobically packed mince and sulphide odours in vacuum packs were observed. High pH of
mince and the initial heavy carcass contamination promoted the rapid multiplication of facultative anaerobes leading to
spoilage of the mince. # 2000 Published by Elsevier Science B.V. All rights reserved.
Keywords: Goat meat; Microbes; Vacuum packaging; Aerobic packaging; Spoilage; Shelf-life
1. Introduction
India possesses 1/5th of the global goat population
producing more than 0.47 million tonnes of meat.
Goat meat is the most widely consumed in this country
and the extension of its shelf-life is important in
marketing the product for internal consumption and
*
Corresponding author. Tel.: 91-0565-763280; fax: 91-0565763246.
E-mail address: [email protected] (Y. Babji).
export purposes. Vacuum packaging to extend the
shelf-life of raw meat is well established. The principal objective of vacuum packaging is the partial or
total inhibition of rapidly growing pseudomonads and
allowance of dominance by ¯ora of low spoilage
potential lactic acid bacteria. The composition of
the climax population that consequently develops
on the packaged meat will be of mixed (Gill, 1996)
type and dictates the course of spoilage which is
largely affected by relative numbers of various spoilage types in the initial ¯ora (Gill and Tan, 1979).
0921-4488/00/$ ± see front matter # 2000 Published by Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 1 - 4 4 8 8 ( 9 9 ) 0 0 1 0 6 - 6
76
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
However, dominance of lactic acid bacteria in the
climax population will depend on initial ¯ora of
lactics, pH of meat, level of initial contamination
and prevalence or absence of facultative anaerobic
biota (Grau, 1980, 1981). Initial microbial load, gas
permeability of packaging ®lm and temperature of
meat during storage play a signi®cant role in extending the shelf-life of packaged meat (Gardner et al.,
1967; Adams and Huffman, 1972; McMullen and
Stiles, 1991). High pH (>5.8) meat tissue at 08C or
below under O2 depleted CO2 atmospheres exhibited
no growth of facultative anaerobic bacteria and dominance by lactic acid bacteria (Gill and Harrison,
1989). Few studies have been conducted on vacuum
packed lamb (Shaw et al., 1980; Moore and Gill, 1987;
Sheridan et al., 1997). Compared with beef, shelf-life
of vacuum packed lamb has been reported to be short.
Gill and Jones (1994) reported a minimum shelf-life of
4 weeks for vacuum packed ground beef. The present
study described physico-chemical, microbial and sensory changes in high pH (6.5) minced goat meat stored
under vacuum in poly-ethylene pteraphthalate
(PETPE) ®lm and the aerobic storage life in low
density polyethylene (LDPE) ®lm at 4 18C.
2. Materials and methods
2.1. PETPE laminate
The PETPE ®lm was a two-layered laminate (Flex
Industries, Noida, India) with a water vapour transmission rate (WVTR) of 1.6 g cmÿ2 per 24 h at 80%
relative humidity at 378C. One layer of this laminate
was composed of PETPE with a thickness of 10m and
the other layer was polyethylene. The gas transmission
rate of the ®lm is not known. The PETPE bags were
vacuum sealed using a Roschermatic packaging
machine (Model VM 19S, Roscherwerke Gmbh, Germany) and refrigerated (4 18C).
Goat meat (obtained from non-descript animals of 2
years age) was purchased 3±4 h after slaughter from a
local meat shop. Leg portion was cut into chunks after
removing the loose fat, fascia and connective tissue.
Meat chunks from two to three animals were pooled
for each trial. Mince was prepared in the laboratory by
passing the chunks through an 8 mm plate of the
mincer (Electrolux, Sweden), and two trials were
conducted.
The minced meat was divided into 200 g portions
and placed in individual bags of LDPE for aerobic
storage or in PETPE bags for vacuum storage. The
LDPE bags were refrigerated (4 18C) without sealing the ends of pouches. The aerobically stored packs
were analysed at 0, 3, 7, 10, 21 and 28 days. The
vacuum packed samples were analysed at 0, 7, 14, 21,
28 and 40 days of storage.
2.2. Analyses of packed mince
pH of mince was determined by grinding 10 g of
mince from each storage pack with 50 ml of distilled
water with frequent blending. pH was recorded by
dipping the combined glass electrode of a digital pH
meter (Century, Model LP 901) in the mince slurry
(Trout et al., 1992). Three readings were made on each
sample and the mean recorded.
A 10 g mince from each storage pack was ground
with 200 ml of distilled water in a Warring blender and
the volume of the slurry was made up to 250 ml in a
volumetric ¯ask and ®ltered through Whatman No. 2
®lter paper. 25 ml of ®ltrate was collected to which
75 ml of distilled water was added and titrated against
0.1 N NaOH with three drops of phenolphthalein. The
amount of standardized 0.1 N NaOH required to neutralize the meat is expressed as total acidity (Konecko,
1979).
25 g mince was blended with 100 ml of distilled
water in a Warring blender for 5 min. The resultant
slurry was ®ltered through Whatman No. 2 ®lter paper
and the amount of ®ltrate released in 15 min was
expressed as extract release volume (Jay, 1964).
Minced meat was placed in sample holder of Lovibond tintometer (Model E, The Tintometer, Salisbury,
UK) and secured against the viewing aperture. The
colour of the mince was determined by adjusting the
red and yellow units while blue units were kept
constant (Froehlich et al., 1982).
2.3. Microbial analysis
Representative 10 g mince from each storage pack
was transferred to a sterile mortar and blended with
90 ml of 0.1% peptone±water for 60 s. Individual
serial decimal dilutions for mince from each storage
pack were prepared in 9 ml volume of sterile 0.1%
peptone±water up to 1 : 106 dilution of the original
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
food sample. Duplicate 0.1±0.5 ml or 1 ml inoculum
of appropriate dilutions were spread with a sterile
glass spreader on pre-poured plates or pour plated,
respectively, on the following media: for enumeration
of aerobic plate counts on spread plates of plate count
agar (PCA, Hi-Media Laboratories, M 091, Bombay)
which were incubated at 308C for 48 h; psychrotrophs
on spread plates of plate count agar (PCA, Hi-Media,
M 091) which were incubated at 4 18C for 10±14
days; Pseudomonas counts on spread plates of plate
count agar (Pseudomonas ¯uorescein agar with 1 ppm
crystal violet, Hi-Media, M 120) which were incubated at 308C for 72 h; Staphylococcal counts on
spread plates of Baird Parker agar (BPA, Hi-Media,
M 043) which were incubated at 378C for 48 h;
anaerobic plate counts on pour plates of plate count
agar (PCA, Hi-Media, M 091) which were incubated
at 358C for 24 h; Enterobacteriaceae counts on pour
plates of Violet Red Bile Glucose agar (VRBG, HiMedia, M 581) which were incubated at 378C for 24 h;
faecal streptococci on pour plates of Slanetz and
Bartley agar (SBM, Hi-Media, M 641) which were
incubated at 378C for 48 h; lactic acid bacteria counts
on pour plates of MRS agar (MRS, Hi-Media, M 641)
which were incubated at 308C for 120 h; yeast and
mould counts on pour plates of potato dextrose agar
(PDA, Hi-Media, M 096) with 2% antibiotic (Chloramphenicol and chlortetracycline, 1 : 1) and the plates
were incubated at 258C for 120 h. Colonies were
counted from each group of micro-¯ora and expressed
as log per gram. The enumeration procedures as
described by Speck (1975) were followed.
2.4. Sensory (objective) evaluation of packed mince
Goat meat mince in aerobic packages and under
vacuum was assessed 2 h after opening the packs at
each storage interval by a three member semi-trained
panel for colour, odour, discolouration and over all
acceptability traits (Gill and Jones, 1994; Gill and
McGinnis, 1995). The colour acceptability of mince
was scored on a 7-point scale with slight modi®cation
in the procedure where 7 represents bright red and 1
indicates extremely dull red. The degree of discolouration of the mince in the package was expressed in
percent on a 5 point scale (1: no discolouration, 2: 1±
10%, 3: 11±25%, 4: 25±50%, 5: 50±100%). The odour
acceptability of the mince was assessed on a 4 point
77
scale where 1 indicates no off-odour, 4 represents
strong off-odour. The type of odours developed during
storage was recorded. The overall acceptability of the
mince was assessed on a 7 point scale where 7
represents extremely acceptable and 1 indicates extremely unacceptable.
2.5. Statistical analysis
Data were analysed statistically for all the parameters according to procedures described by Snedecor
and Cochran (1967). Analysis of variance were used to
assess pH, total acidity, ERV and microbial counts
based on a linear model that included aerobic and
vacuum storage conditions and storage time within
storage condition. The difference between the means
were tested by critical difference. The sensory evaluation scores (colour, discolouration, odour and overall
acceptability) and Lovibond colour units (red, yellow
and green) of minced goat meat were tested using chisquare analysis. The hypothesis that the initial values
are not affected due to aerobic or vacuum storage was
tested for each parameter.
3. Results
The mean pH, total acidity and extract release
volume of minced goat meat under aerobic and/or
vacuum storage at 4 18C is shown in Table 1. The
initial pH of minced goat meat used in this study was
high (6.5). The extract release volume decreased and
total acidity increased during storage in both aerobic
and vacuum packages. There was no signi®cant effect
of storage period on pH of meat under both the storage
conditions (Table 1).
The microbial growth in the mince stored aerobically or under vacuum is shown in Figs. 1±9. Analysis
of variance of the data indicated a signi®cant effect of
the storage condition on the counts of all the microbial
groups except for lactic acid bacteria and yeasts and
moulds. The lactic acid bacteria and Pseudomonas
counts increased while those of enterobacteriaceae
decreased by day 7 under both the storage conditions.
There was a signi®cant drop in the lactic counts during
further storage of aerobic or vacuum stored samples up
to 28 days. The growth of Pseudomonas was
restrained while that of enterobacteriaceae increased
78
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Table 1
pH, total acidity and extract release volume (ERV) of minced goat meat under aerobic or vacuum packed (PETPE laminate) storage at
refrigeration temperaturea
Storage condition
Storage time (days)
pH
Total acidity
ERV (ml)
Initial
6.53 0.18a
0.70 0.10a
41.00 0.35a
a
b
Aerobic
3
7
10
21
28b
6.38 0.01
6.11 0.005a
6.13 0.17a
6.25 0.01a
NDd
1.00 0.00
1.00 0.00b
1.30 0.00c
1.30 0.00c
NDd
38.50 0.35a,b
36.00 1.00b
24.50 0.50c
30.25 0.25d
NDd
Vacuum
7
14
21
28
40c
6.00 0.01a
6.10 0.00a
6.07 0.01a
6.10 0.01a
6.03 0.00a
1.30 0.00b
1.20 0.00b
1.40 0.00b
1.20 0.00b
NDd
24.00 0.50b
25.50 0.50c
32.50 0.50d
24.50 0.50e
NDd
a
Means followed by the same alphabets do not differ signi®cantly (P < 0.05).
Spoiled due to putrefactive odours.
c
Spoiled due to sulphide odours.
d
ND: Not done.
b
from day 7 to 28 in the vacuum stored mince. There
was no signi®cant difference between the initial and
the day 28 counts of the vacuum stored samples for all
the microbial groups except for total aerobes, psychrotrophs and Pseudomonas.
Yeast and mould counts did not form a major part of
the prevalent micro-¯ora during storage both in aerobic (log 4.0) and vacuum (log 2.0) at day 28. Overall,
aerobically stored samples had higher microbial
counts than that of vacuum packed samples.
The vacuum packed goat meat was bright red at 7
days and moderately bright red at 14, 21 and 28 days
of storage whereas aerobically stored samples were
slightly bright red at 0, 3, 7 days and slightly dull red at
10, 21 days and dull red at 28 days (Table 2). Vacuum
packed goat meat had no discolouration up to 14 days
Fig. 1. Lactic acid bacteria counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
79
Fig. 2. Counts on Pseudomonas F-agar of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
storage and at 21 and 28 days there was a slight
discolouration 1±10% in the pack. The aerobically
stored samples showed 25±50% discolouration at 7
days and 50±100% discolouration at 21 days. The
vacuum packed samples were spoiled by sulphide
odours at 40 days while the aerobically stored packs
spoiled by putrefactive odours at 28 days. Thus, on
28th day, the vacuum packed samples were extremely
acceptable while the aerobically stored samples were
unacceptable.
Chi-square analysis of the data also indicated signi®cantly higher discolouration scores in aerobically
stored mince (Table 2), signi®cantly higher yellow
colour units for vacuum packs (Table 3) and lower
overall acceptability scores (Table 2) for aerobically
stored samples when compared with the initial values.
Fig. 3. Enterobacteriaceae counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
80
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Fig. 4. Total aerobic counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
4. Discussion
Data on microbial and sensory evaluation of minced
goat meat stored at 4 18C indicated a shelf-life of 28
days under vacuum compared with similar overall
acceptability scores at 3 days observed in aerobically
stored samples. The low storage life of aerobically
stored samples was due to loss of colour. Shaw et al.
(1980) also reported that the colour scores of refrigerated lamb loins in aerobic storage were lower than
that under vacuum for 6 weeks. Vacuum packed goat
meat mince maintained bright red colour up to 40 days
even when the meat was spoiled. Gill and Jones (1994)
observed that the master packed ground beef in anoxic
state continued to maintain its bloom up to 32 days
although its shelf-life was only 21 days. The spoilage
of vacuum packed mince by sulphide odours has also
been reported by earlier workers (Hanna et al., 1979,
1983). Greenish discolouration of the drip might be
due to oxidation of heme to greenish myoglobin or by
Fig. 5. Psychrotrophic counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
81
Fig. 6. Staphylococcal counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
formation of sulphmyoglobin between myoglobin and
hydrogen sulphide (Nicol et al., 1970; Taylor and
Shaw, 1977).
There were decreases in pH and ERV during storage
under vacuum. In normal pH meats, decrease in pH
and increase in ERV (Sutherland et al., 1975) or no
signi®cant changes in pH or ERV (Turner, 1960;
Pearson, 1968) have been reported. Total acidity
increased during storage under vacuum. Sutherland
et al. (1975) observed decrease in total alkalinity in
vacuum stored beef.
The highly variable shelf-life of vacuum packed
fresh meat has been attributed to differences in pH
(Rousset and Renerre, 1991), ®lm permeability
(Hodges et al., 1974) and initial contamination and
storage temperature (Bell and Garout, 1994). In the
present study, the initial pH of meat was very high (pH
6.5)
with
high
enterobacteriaceae
counts
Fig. 7. Yeast and mould counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
82
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Fig. 8. Coliform counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
(log 4.3 gÿ1). Meat with very high pH (>6.0) had a
very short shelf-life even in vacuum packaging (Bem
et al., 1976) as enterobacteriaceae and Brochothrix
compete better with rapid bacterial breakdown of
amino-acids producing unpleasant smelling products
such as H2S or ammonia (Newton and Gill, 1981). In
our study, the growth of lactic acid bacteria on the
vacuum packed meat in the beginning of spoilage was
very slow (log 3.1 gÿ1 at 28 days) unlike previous
studies (Egan, 1983; Dainty and Mackey, 1992). The
slow growth of lactic acid bacteria may be due to high
initial pH of meat and growth dominance by facultative anaerobic biota (enterobacteriaceae). These
results are in accordance with Grau (1980, 1981) on
high pH vacuum packed meat.
The increases in Pseudomonas counts in the ®rst
week of vacuum storage were in agreement with
Sutherland et al. (1975). There were increases in total
aerobic and psychrotrophic populations as the conditions were not completely anoxic in vacuum packa-
Fig. 9. Faecal streptococcal counts of minced goat meat under aerobic or vacuum storage at refrigeration temperature.
83
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
Table 2
Colour, discolouration, odour and overall acceptability scores of minced goat meat under aerobic or vacuum packed (PETPE laminate) storage
at refrigeration temperaturea
Storage
Condition
Storage time
(days)
Colour
scoresb
Discolouration
scoresc
Odour
scoresd
Overall acceptability
scorese
Initial
5.00a
1.00a
1.00a
7.00a
Aerobic
3
7
10
21
28
5.00a
5.00a
4.00a
4.00a
2.00a
1.00b
4.00b
4.00b
5.00b
5.00b
1.00a
1.00a
1.00a
1.00a
4.00a
7.00b
5.00b
4.00b
3.00b
1.00b
Vacuum
7
14
21
28
40
7.00a
6.00a
6.00a
6.00a
±
1.00a
1.00a
2.00a
2.00a
2.00a
1.00a
1.00a
1.00a
1.00a
4.00a
7.00a
7.00a
7.00a
7.00a
1.00a
a
Numbers followed by the same alphabets, placed on the basis of chi-square values, do not differ signi®cantly (P < 0.05).
7: Bright red; 4: Slightly dull; 1: Extremely dull.
c
1: No discolouration; 5: 50±100% discolouration.
d
1: No off odour; 4: Strong off odour.
e
7: Extremely acceptable; 4: Neither acceptable nor unacceptable; 1: Extremely unacceptable.
b
ging due to oxygen ingress through the plastic ®lm
(Nottingham, 1982). The low coliform and faecal
streptococcal counts in vacuum compared with the
aerobic storage were in accordance with Sutherland et
al. (1975) on vacuum packed beef. The staphylococcal
counts at 28 days of vacuum storage were lower than
in aerobic storage. However, Venugopal et al. (1993)
reported unusually high staphylococcal counts in
vacuum packed beef possibly due to high initial
contamination.
5. Conclusion
Vacuum packaging improves the colour and microbiological shelf-life of high pH minced goat meat
Table 3
Lovibond colour units of minced goat meat under aerobic or vacuum packed (PETPE laminate) storage at refrigeration temperaturea
Storage condition
Storage time (days)
Lovibond colour units
Red
Yellow
Green
Initial
5.4a
3.1a
3.0a
Aerobic
3
7
10
21
28
5.4a
5.6a
6.5a
5.4a
2.2a
4.2a
4.2a
4.5a
5.4a
3.3a
3.3a
3.2a
3.5a
4.4a
1.3a
Vacuum
7
14
21
28
40
7.4a
6.6a
6.4a
6.5a
NDb
6.5b
6.3b
5.4b
5.5b
NDb
3.2a
4.5a
4.3a
4.3a
NDb
a
b
Numbers followed by the same alphabets, placed on the basis of chi-square values, do not differ signi®cantly (P < 0.05).
ND: Not done due to greenish discolouration in the drip.
84
Y. Babji et al. / Small Ruminant Research 36 (2000) 75±84
when compared with aerobic storage by maintaining
colour and restraining microbial growth with
increased acceptability scores.
References
Adams, J.R., Huffman, D.L., 1972. Effect of controlled gas
atmospheres and temperatures on quality of packaged pork. J.
Food Sci. 37, 869±872.
Bell, R.G., Garout, A.M., 1994. The effective product life of
vacuum packaged beef imported into Saudi Arabia by Sea as
assessed by chemical, microbiological and organoleptic
criteria. Meat Sci. 36, 381±396.
Bem, Z., Hechelmann, H., Leistner, L., 1976. The bacteriology of
DFD meat. Fleisch wirtschaft 56, 985±987.
Dainty, R.H., Mackey, B.M., 1992. The relationship between the
phenotypic properties of bacteria from chill-stored meat and
spoilage process. J. Appl. Bacteriol. Symp. Suppl. 73, 1035±
1145.
Egan, A.F., 1983. Lactic acid bacteria of meat and meat products.
Antonie van Leeuwenhoek. 49, 327±336.
Froehlich, D.A., Gullet, E.A., Usborne, W.R., 1982. Effect of
nitrite and salt on the colour, ¯avour and overall acceptability
of ham. J. Food Sci. 48, 152±154.
Gardner, G.A., Carson, A.W., Patton, J., 1967. Bacteriology of
prepacked pork with reference to the gas composition within
the pack. J. Appl. Bacteriol. 30, 321±332.
Gill, C.O., 1996. Extending the shelf-life of raw chilled meats.
Meat Sci. 43, S99±S107.
Gill, C.O., Harrison, J.C.L., 1989. The storage life of chilled pork
packed under carbon dioxide. Meat Sci. 26, 313±324.
Gill, C.O., Jones, T., 1994. The display life of retail-packaged beef
steaks after their storage in master packs under various
atmospheres. Meat Sci. 38, 385±396.
Gill, C.O., McGinnis, J.C., 1995. The effects of residual oxygen
concentration and temperature on the degradation of colour of
beef packaged under oxygen-depleted atmosphere. Meat Sci.
39, 387±394.
Gill, C.O., Tan, K.H., 1979. Effect of carbon dioxide on growth of
pseudomonas ¯uorescens. Appl. Environ. Microbiol. 38, 237.
Grau, F.H., 1980. Inhibition of the anaerobic growth of brochothrix
thermosphacta by lactic acid. Appl. Environ. Microbiol. 40,
443±446.
Grau, F.H., 1981. Role of pH, lactate and anaerobiosis in
controlling the growth of some fermentative gram negative
bacteria. Appl. Environ. Microbiol. 42, 1043±1050.
Hanna, M.O., Savell, J.W., Smith, G.C., Purser, D.E., Garder, F.A.,
Vanderzant, G., 1983. Effect of growth of individual meat
bacteria on pH, colour and odour of asceptically prepared
vacuum packaged round steaks. J. Food Prot. 46, 216±221.
Hanna, M.O., Smith, G.C., Hall, L.C., Vanderzant, C., 1979. Role
of Hafnia alvei and a Lactobacillus species in the spoilage of
vacuum packaged strip loin steaks. J. Food Prot. 42, 569.
Hodges, J.H., Cachill, V.R., Ockerman, H.W., 1974. Effect of vacuum
packaging on weight loss, microbial growth and palatability of
fresh beef whole sale cuts. J. Food Sci. 39, 143±146.
Jay, J.M., 1964. Release of aqueous extracts by beef homogenates
and factors affecting release volume. Food Technol. 18, 1633±
1638.
Konecko, E.W., 1979. Hand Book for Meat Chemists. Avery
Publishing Group, Wayne, USA.
McMullen, L.M., Stiles, M.E., 1991. Changes in microbial
parameters and gas composition during modi®ed atmosphere
storage of fresh pork loin chops. J. Food Prot. 54, 178±183.
Moore, V.J., Gill, C.O., 1987. The pH and display life of chilled
lamb after prolonged storage under vacuum or under CO2, NZ.
J. Agric. Res. 30, 449±452.
Newton, K.G., Gill, C.O., 1981. The microbiology of DFD fresh
meats. Meat Sci. 5, 223±232.
Nicol, D.J., Shaw, M.K., Ledward, D.A., 1970. Hydrogen sulphide
production by bacteria and sulphmyoglobin formation in
prepacked chilled beef. Appl. Microbiol. 19, 937±939.
Nottingham, P.M., 1982. Microbiology of carcass meats. In:
Brown, M.D. (Ed.), Meat Microbiology. Applied Science
Publishers, London, pp. 13±65.
Pearson, D., 1968. Assessment of meat freshness in quality control
employing chemical techniques. J. Sci. Food Agric. 19, 357±
366.
Rousset, S., Renerre, M., 1991. Effect of CO2 and vacuum
packaging on normal and high pH meat shelf-life. Int. J. Food
Sci. Tech. 26, 641±652.
Shaw, B.G., Harding, C.D., Taylor, A.A., 1980. The microbiology
and storage stability of vacuum packed lamb. J. Food. Technol.
15, 397±405.
Sheridan, J.J., Doherty, A.M., Allen, P., McDowell, D.A., Blair,
I.S., Harrington, D., 1997. Effect of vacuum and modi®ed
atmosphere packaging on the shelf-life of lamb primals, stored
at different temperatures. Meat Sci. 45, 107±117.
Snedecor, G.W., Cochran, W.G., 1967. Statistical Methods. Iowa
State University Press, Ames, IA.
Speck, M.L., 1975. Compendium of Methods for the Microbiological Examination of Foods. Am. Publ. Health Assoc.,
Washington.
Sutherland, J.P., Patterson, J.T., Murray, J.G., 1975. Some
metabolic and biochemical characteristics of representative
microbial isolates from vacuum packaged beef. J. Appl. Bact.
39, 27±237.
Taylor, A.A., Shaw, B.G., 1977. The effect of meat pH package
permeability on putrefaction and greening in vacuum packaged
beef. J. Food Technol. 12, 515±521.
Trout, E.S., Hunt, M.C., Johnson, D.E., Clons, J.R., Castner, C.L.,
Kropt, D.H., 1992. Characteristics of low fat ground beef
containing texture modifying ingredients. J. Food Sci. 57, 19±
24.
Turner, A., 1960. Assessing meat spoilage in the laboratory. Food
Mf. 35, 386.
Venugopal, R.J., Ingham, S.C., McCurdy, A.R., Jones, G.A.C.,
1993. Anaerobic microbiology of fresh beef packaged under
modi®ed atmosphere or vacuum. J. Food Sci. 58, 935±937.