the aerobic psychrotrophic populations on meat and meat contact surfaces in a meat production system...

Journal of Applied Bacteriology 1990,68, 335-344 2998/0 1 j89

The aerobic psychrotrophic populations on meat and meat contact surfaces in a meat production system and on meat stored at chill temperatures

G . L . NORTJE*, L I N D A N E L , E R I K A J O R D A A N , K A R I N B A D E N H O R S T , E R N A G O E D H A R T & W . H . H o L z A P F E L t Animal and Dairy Science Research Institute, Private Bag X 2 , Irene, 1675 and ?Department of Microbiology and Plunt Pathology University of Pretoria, Pretoria, 0002, South Africa

Accepted 25 July 1989

NORTJB, G.L. , N E L , L., J O R D A A N , E . , B A D E N H O R S T , K . , COEDHART, E . & H O L Z A P F E L , W . H . 1990. The aerobic psychrotrophic populations on meat and meat contact surfaces in a meat production system and on meat stored at chill temperatures. Journal of Applied Bacteriology 68, 331-344.

At a city abattoir, a wholesaler and 10 different supermarkets, surface microbiological samples were taken of carcasses, hands and apron fronts of members of staff and equipment (mincers and saws). In addition, minced meat, packaged and displayed in chilled cabinets, was also sampled. Carcasses, personnel surfaces and equipment were monitored by a modified agar sausage technique. From each of the highest dilution psychrotrophic plate counts, five colonies were selected randomly, isolated and identified (1265 in total). Microbes developing on chilled meat were also isolated from other surfaces in the production chain. On chilled meat (51°h) and at the abattoir (36%) pseudomonads were the predominant organisms followed by the Gram-positive cocci on chilled meat and by Acinetobacter, Moraxella and Alcali- genes spp. at the abattoir. At the wholesaler Gram-positive cocci (32%) predomi- nated, followed by Alcaligenes, Moraxella and Alcaligenes spp. Pseudomonas, Alcaligenes, Neisseriaceae and related genera, Gram-positive cocci. species from the coryneform groups of bacteria and yeasts were identified from all the surfaces monitored. Identification with the API NE20 was unsatisfactory. Enterbacteriaceae, lactobacilli and endospore-forming bacteria were identified occasionally, but their significance as contaminating organisms seems low. N o Salmonella spp. were identified

Much has been published on the microbiology of carcass meats, specifically regarding the micro-organism population associated with the product and its effect on meat quality (Ayres 1955; Ingram & Roberts 1976; Gill 1982; Not- tingham 1982).

The microbiology of carcass meats is deter- mined by conditions under which animals are reared, slaughtered and processed. When meat is in close proximity to huge reservoirs of bacteria, such as the hide or fleece and the gut con- tents, there is a potential for contamination of meat surfaces (Empey & Scott 1939; Kitchell & Ingram 1967; Grau 1974). The incidence of bac-

* Corresponding author.

teria on hides varies with the ambient temperature. The numbers decline in summer and also with decreasing geographical latitude (Empey & Scott 1939; Larkin 1970). The composition of the psychrotrophic microbes also shows seasonal variation (Blake & Armstrong 1973; Jones 1973). Much of this contamination is originally of faecal origin, but it will include the normal microbes of the skin, staphylococci, micrococci, pseudomonads, yeasts and moulds as well as organisms from soil and water. Many of these organisms are psychrotrophs, able to grow at refrigeration temperatures and are potential spoilers of chilled meat (Newton et al. 1978; Patterson & Gibbs 1978). At the time of slaughter the meat portion of a normal healthy

336 G. L. Nort j i et al. animal may be regarded as essentially free from bacteria (Gill 1982). Under hygienic conditions the number of pathogens originating from sources outside the animal are usually very small (Nottingham 1982).

Many opportunities exist for contamination of the meat from the hands and clothes of the staff, from knives and other equipment and structural surfaces in boning rooms and retail premises. The specific level and nature of the contribution of these sources to contamination or the microbial numbers on surfaces, are unfortunately only mentioned by exception (Davidson et al. 1973; Newton et al. 1975; Pat- terson & Gibbs 1978; Newton et al. 1978) During the production cycle, the carcass is frequently chilled and handled, resulting in a partial lowering of the surface counts and subsequent recontamination. This practice leads to a stepwise increase in the initial counts at the different processing stages viz. abattoir, wholesaler and retailer (Nortje et al. 1989a). The opportunity for the contamination of the product therefore exists from the slaughter floor, throughout the production chain to the retailer, by contact surfaces and handling. Environ- mental factors like temperature could contribute to this phenomenon.

Much research has been done on the development of aerobic spoilage microbes on meat stored at chill temperatures (Halleck et al. 1958; Brown & Weidemann 1958; Ayres 1960; Gardner 1965; Ingram & Dainty 1971; Gill 1982; Dainty et al. 1983). Aerobically, there is no interaction between different bacterial species until the maximum cell density is approached. The composition of a spoilage population can be affected by changes in water activity and the storage atmosphere (Gill & Newton 1978). The microbial groups associated with fresh meat surfaces which are frequently described in the literature are Pseudomonas spp., Acinetobacter spp., Enterobacter spp., Brocho- thrix thermosphacta, Moraxella spp., Lacto- bacillus spp., Flauobacterium spp., Vibrio spp., Aeromonas spp. and Arthrobacter spp., with spoilage populations usually dominated by pseudomonads (Ayres 1955; Ingram & Dainty 1971; Gill 1976, 1982; Gill & Newton 1978).

A quantitative survey of the entire production chain under investigation provided psychrotrophic plate counts from all the different sites involved, which were found to be also the most

important group regarding the shelf life of the final product (Nortje et al. 1989~). Therefore, the opportunity existed to d o a qualitative survey of the same samples in the present study. A survey of this kind has not yet been reported in the literature, and information from such a trial would add to the current knowledge. The aim was to determine the detailed composition of the psychrotrophic microbial populations on carcasses and meat contact surfaces in a meat production system and on meat stored a t chill temperatures.

Materials and Methods

C O L L E C T I O N A N D T R E A T M E N T OF S A M P L E S

At a city abattoir, a wholesaler and 10 different supermarkets, surface samples were taken of carcasses, hands and apron fronts of members of staff and equipment (mincers and saws). At the wholesaler the saw used to quarter the carcasses was included as it may have contributed to contamination. The surfaces monitored at supermarket level included mincers, saws and the personnel surfaces. These surfaces were pointed out as consistent contributors to contamination (Nortje et al. 1989a). In addition, minced meat, packaged and displayed in chilled display cabinets, was also sampled, since it con- sistently gave the highest total count in a microbiological survey of different meat cuts at different supermarkets (Nortjk et al. 1989b).

Carcasses, personnel surfaces and equipment were monitored by a modified agar sausage technique (Nortje et al. 1982). An excision technique could not be used on carcasses simply because samples were taken under commercial conditions and damage to carcass surfaces had to be avoided. Five sides were monitored at the abattoir as well as the wholesaler on four occasions, two visits in the morning, before the commencement of work, and two at noon to represent an in-work situation. One sample each, was taken on the fore shank and brisket, and combined to give a total area of 12.84 cm2 per sample (Nortje et al. 1982). The areas sampled were selected as two of the most consis- tently contaminated areas on carcasses a t this specific abattoir (Nortje & Naude 1981). In addition, five samples were also taken on contact surfaces (hands, clothes and saws),

Psychrotrophs giving a total of 20 replicates for each surface. The supermarkets were visited at two occasions each, once early in the morning before the start of the working day (clean survey), and once at noon to represent an in-work situation (dirty survey). Samples were collected in sterile con- tainers using sterile equipment and techniques. The minced meat samples were taken on the day of packaging from the display cabinet. All samples were transported to the laboratory in refrigerated boxes. The samples were held at ca 4°C until microbiological examinations were carried out, within 2 h of reaching the laboratory. The remainder of the minced meat samples were kept at ca 4°C for a shelf life study. The samples were monitored after 2 and 3 d respectively.

Microbiological examination

Twenty-five ml of quarter-strength Ringer solution (Merck) was used as diluent for the agar sausage impression samples. The agar slices were homogenized with a Colworth Stomacher 400 for 2 min. The minced meat samples (20 g each) were aseptically weighed into sterile plastic bags and homogenized with 180 ml sterile quarter-strength Ringer solution, in a Stomacher for 2 min. Serial dilutions were made of each of the homogenized samples and then plated in duplicate on a series of selective and total count agar plates by the surface plate method (Nottingham et al. 1975). Standard 1 Agar (Merck) was used to isolate psychrotrophic organisms and cultures were incubated at 5°C for 7 d. From the highest dilution plates, five colonies were randomly selected and sub- cultured on Standard 1 Agar slants. These strains (1265) were subsequently purified by streaking on nutrient agar and stored on nutrient agar slants at ca 4°C for later identification.

Identification of strains

All cultures were incubated aerobically at 25°C. Plates for purification and slants for main- tenance were Standard 1 Agar incubated for 18 to 24 h. Gram-reaction, detection of catalase, oxidase, morphology and motility were deter- mined (Harrigan & McCance 1966), and reaction in 4% KOH (Gregersen 1978). Gram- negative rods were tested in the medium of

m meat surfaces 337 Hugh & Leifson (1953) for oxidative or fermentative attack on glucose. Identification of the organisms to genus level was then carried out using the keys described by Dainty et a/. (1979).

Further identiJication ofdlferent genera

Pseudomonas spp. The identification of this group was according to the keys of Dainty et al. (1979), Krieg & Holt (1984) and Stolp & Gadkari (1981).

Flavobacterium spp. were differentiated by their inability to produce acid from glucose, to use citrate as sole carbon source in Simmon’s citrate agar and to produce an alkaline reaction in this medium, as well as by their inability to reduce nitrate to nitrite (Holmes et al. 1984).

Two other genera, Agrobacterium and Borde- tella, were identified by the API NE20 system. (API Laboratory Products Ltd, Philpot House, Rayleigh, Essex). Their identification was not verified because of the small numbers identified and the high (> 90%) identification percentage obtained with the API system.

Alcaligenes. The utilization of citrate as sole source of carbon was carried out with Simmon’s citrate agar and the reduction of nitrate (Harrigan & McCance 1966).

Enterobacteriaceae. The family Enterobacte- riaceae was subdivided on basis of reactions in SIM culture medium (Merck); Triple-sugar Iron Agar (Merck) and the API 20E system.

Acinetobacter spp. The API NE20 system was used, as well as the reaction on the medium of Hugh & Leifson (1953).

Staphylococcus and Micrococcus spp. Anaero- bic growth in a glucose-containing medium, the lysostaphin test (Schleifer et al. 1981) and the production of acid from glycerol in erythro- mycin media (Schleifer & Kloos 1975), were used to differentiate staphylococci from micrococci.

Endospore forming rods and cocci. Growth on Bacillus sporulation medium (Fourie et al. 1972) were examined for presence of endospores by means of phase contrast microscopy.

Lactobacillaceae. All Gram-positive strains with a negative catalase reaction (3% (v/v) hydrogen peroxide H,O, in distilled water), were grown on MRS-agar (Merck) before further identification. To confirm the grouping

G. L. Nortjt et al. of these isolates the benzidine test was per- formed (Harrigan & McCance 1966). This was followed by phase contrast microscopy, and checked for the production of gas from glucose and for growth at 45°C and 15°C.

Corynehacterium spp. Organisms with a pro- foundly irregular shape under phase contrast microscopy were grown on Corynebacterium selective agar (Merck).

Yeasts. Yeasts were identified under phase contrast microscopy after staining by Gram’s method. No attempt was made to identify these organisms further.

Subsequent to these tests, all the strains belonging to the genera Pseudomonas, Alcali- genes and Acinetohacter were classified with API NE20. In all cases final identification was based on the keys and tests of Dainty et al. (1979), Starr et al. (1981) and Krieg & Holt (1 984).

Of 1265 strains isolated, 295 originated from three surfaces at the abattoir (carcasses, hands and clothes), 375 from four surfaces a t the wholesaler (carcasses, hands, clothes and saw) and 595 from seven additional sources at the retailers (hands, clothes, saw, mincer and from

the shelf life study, minced meat day 0, minced meat day 2 and minced meat day 3). The organisms identified and their percentage of the total number of strains isolated are given in Table 1 .

Incidence of different groups

Gram-negative aerobic rods and cocci. All strains produced acid aerobically from glucose. The families concerned were the Rhizobiaceae, the Neisseriaceae and related genera as well as the Pseudomonadaceae. Subsequently, all these isolates were further identified with the API NE20 while additional tests were carried out as described under methods.

The genera from the Rhizobiaceae, Neisseria- ceae and related bacteria comprised the second largest group of organisms identified at the abattoir, although smaller numbers were identified throughout the production chain (Table 2). Agrobacterium was identified only on one carcass at the abattoir and on the hands of workers at the abattoir and wholesaler, while Bordetella was isolated once from a carcass a t the abattoir and on clothing a t the retailer, respectively. Flauohacterium was found only at the abattoir and wholesaler. Acinetobacter, Moraxella and Alcaligenes were found through-

Table 1. Percentage composition of microbial population

Isolate classification Abattoir isolates Wholesaler isolates Retailer isolates Total isolates group Number O/o Number o/o Number % Number Yo

Pseudomonas spp. Ayrohacterium spp. Moraxella spp. Acinetohacter spp. Flavohacterium spp. Alcaliyenes spp. Bordetella spp. Enrerohacter spp. Vihrio spp. Aeromonas spp. Chromohacterium spp. Pasteurella spp. Micrococcus spp. Stuphylococrus spp. Bacillus spp. Lactobacillus spp. Coryneform group Yeasts Non Viable

Total isolates

107 36.3 3 1.0 9 3.1

21 7.1 3 1.0

13 4.4 1 0.3 6 2.0 1 0.3 1 0.3 2 0.7 1 0.3

15 5.1 26 8.8 2 0.7 2 0.7

21 7.1 29 9.8 32 10.9

295

58 15.5 1 0.3

11 2.9 18 4.8 8 2.1

10 2.7 0 0 5 1.3 1 0.3 1 0.3 1 0.3 3 0.8

51 13.6 62 16.5

3 0.8 7 1.9

51 13.6 63 16.8 21 5.6

375

~

306 51.4 0 0 4 0.7

18 3.0 0 0 9 1.5 1 0.2

13 2.2 0 0 0 0 0 0 0 0

11 1.9 75 12.6

8 1.3 10 1.7 81 13.6 19 3.2 40 6.7

595

~

47 1 4

24 57 I I 32 2

24 2 2 3 4

77 163

13 19

153 111 93

1265

37.2 0.3 1.9 4.5 0.9 2.5 0.2 1.9 0.2 0.2 0.2 0.3 6.1

12.9 1 .o I .5

12.1 8.8 7.4

Tab

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73

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87

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23

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45

30

50

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45

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Aba

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295

16

11

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6 6

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G . L. Nortjb et al. out the production system studied, with a marked decrease in frequency at the retailer (Tables 1 and 2).

Facultatively anaerobic Gram-negative rods. Enterobacteriaceae and Vibrionaceae were isolated in relatively low numbers throughout the production chain from various surfaces, carcasses, hands, clothing, saws, mincers and from retail packages of meat (Table 2). The Entero- bacteriaceae, Vibrionaceae and related genera comprised 2.8Y0 of the total strains isolated, with Enterobacter representing 52.7% of this group of organisms, originating from carcasses, personnel surfaces and meat.

Staphylococcus and Micrococcus spp. The Gram-positive cocci were identified according to the tests cited under methods and the results are given in Tables 1 and 2. At both the abattoir and the retailers the Gram-positive cocci comprised 14% of the total number isolated, while at the wholesaler the figure was 30%. O n carcasses an increase of 3% in the incidence of Gram-positive cocci occurred between the abattoir and the wholesaler, while the increase for personnel surfaces was 4% (Table 2).

Gram-positive, asporogenous catalase-negative rod shaped bacteria. Nineteen strains were identified as lactobacilli. Six of these were isolated from hands of workers, two at the abattoir and four at retail outlets. Two came from carcasses at the wholesaler, while four were isolated from the clothing of workers, three at the wholesaler and one at the retail outlets. Equipment contributed five and the final product two (Table 2).

Endospore-forming bacteria. A total of 13 strains were identified as Bacillus spp. These cultures were isolated from various surfaces throughout the production chain but never comprised a significant proportion of the population involved (Table 1 and 2).

While facultative anaerobic Gram-negative rods, lactobacilli and endospore forming bacteria were identified occasionally throughout the survey, their significance as part of the spoilage microbes seems low (Von Holy 1983).

Coryneform bacteria. Coryneforms were isolated from all the surfaces at the three different production sites (Table 1 and 2). At the abattoir coryneform bacteria constituted 7% of the strains, while a t the wholesaler and retailers they constituted 14% of them (Table 1). At the abattoir, hands were the prime source of contamination regarding this organism, while at the

wholesaler the saw and at retailers the mincers made the largest contribution. Tests on Gardner’s STAA medium (1966) showed that none of these strains was Brochothrix thermosphacta.

Yeasts. Yeasts were isolated from all surfaces examined at all three sampling sites. At the abattoir, they constituted lo%, at the wholesaler 17%i and at the retailers 3% of the strains isolated at the respective sampling sites. This is more or less the same pattern as presented by the Gram-positive cocci.

Discussion

According to Table 2 the sanitation procedures applied at the different locations had no significant selective effect on the composition of the microbial population involved. The total count is reduced, but the position of the different organisms in the population is not affected. At the abattoir a few more Pseudomonadaceae were isolated after cleaning and disinfection than during production, while the results for this group was vice versa on contact surfaces at the retailers. No particular pattern could be shown regarding this group at the wholesaler. The same was true for Gram-positive cocci at both the abattoir and retailers.

The present results endorse those of various authors cited above that Pseudomonas spp. are dominant in the microbial population associated with carcasses and meats (Table 2). It was stated by Gill & Newton (1978) that the spoilage microbes will be dominated by the organism which can grow most rapidly under the prevailing conditions unless there are interactions between competing species. They also stated that on meat stored aerobically, Pseudo- monas spp. have a marked advantage in growth rate as compared with other genera and that this advantage tends to increase with decreasing temperatures (Gill & Newton 1977).

According to the distribution encountered in this particular survey it seems that there was a shift in population regarding the dominant genus between the three sites visited. While pseudomonads dominated the microbes at the abattoir and retail outlets, it was the Gram- positive cocci (30%) that dominated at the wholesaler. The strains were all grown under psychrotrophic conditions and therefore the dominance of bacteria traditionally regarded as

Psychrotrophs on meat surfaces 34 1

mesophilic bacteria (Gram-positive cocci) at the wholesaler was remarkable. Carcasses are repeatedly handled during on- and off-loading at the abattoir and wholesaler, which could lead to cross contamination. At all three sites (abattoir, wholesaler and retailer) the staphylococci were found to be the main representatives of the Gram-positive cocci (Table 1 ) . The iso- lation of Gram-positive cocci from stored fresh meats is reported frequently (Rogers & McCles- key 1956; Ayres 1960; Gardner 1965; Newton et al. 1975; Gill 1982; Erichsen & Molin 1981). In a previous survey at this particular abattoir and wholesaler, when specific carcasses were monitored throughout the production chain, it was found that a major temperature increase occurred between the abattoir and the arrival of carcasses at the wholesaler (Fig. 3; Nortje et a / . 1983). This increase was accompanied by a related increase in total aerobic population, which was not qualified in this study, but could have been caused by an increase in Gram- positive cocci as depicted in the present study (Fig. 4; Nortje et al. 1983).

The identification of the bacteria by the API NE20 system was highly unsatisfactory and could be used only as a confirmation of the genera already identified by the keys (Dainty et al. 1979). There was no clear distinction between pseudomonads, Alcaligenes, Moraxella, Achro- mobacter, CDC group IVe and Flauobacterium by means of this system. To clarify part of this situation the key according to Tilton (1981) using the O/F reaction with glucose was applied. In the list of synonyms and mixed taxa of the API NE20 analytical profile index CDC group IVe was stated to be equivalent to Alcali- genes. CDC group IVe and Alcaligenes were thus grouped together. A possible explanation for the unsatisfactory results with the API system, is that it was originally developed for bacteria of medical origin which involves a com- pletely different habitat. Ingram & Dainty (1971) reported that strains alotted to Alcali- genes and Acinetobacter are not proteolytic, are not known to be versatile in attacking amino acids, and are also mostly indifferent towards sugars. At that time there was little evidence that they play any special part in normal spoilage, although important lipolytic properties were recognized (Ingram & Dainty 1971). For- tunately for the keeping quality of meat Acine- tobacter d o not appear to produce strong

spoilage odours (Lerke et al. 1965 cited by Gill 1982) and are inhibited by pH values below 6.0 (Gill 1982). After the completion of the present study Shaw & Latty (1988) satisfactorily resolv- ed the identification of the non-fermentative Gram-negative bacteria in foods. The incidence of these organisms in the present study (4 to 10%) supports the view that it is arguable whether they are important contributors to spoilage of proteinaceous foods in most cases where pseudomonads predominate (Table 1).

Bearing in mind the problems described in the latest edition of Bergey’s Manual (Krieg & Holt 1984) about the identification of the facultative anaerobic Gram-negative rods, the species were omitted and the strains isolated were discussed only as genera as identified with the API system. These organisms are not regarded as being very important in the shelf- life of fresh chilled meats (ca 1%) of total population), but d o play an important role in dressing hygiene and public health (Mackey & Kerridge 1988). The present results are in agree- ment with findings by Dainty et a/ . (1985). Enterobacteriaceae such as Serratia were shown to produce diamines which might be a source of putrescine and cadaverine production under spoilage conditions and contribute to off odours (Dainty et a / . 1986). Psychrotrophic Vibriona- ceae are frequently isolated from chilled meats, while certain genera from the family Enterobac- teriaceae are the most common types of organisms found on meat (Nottingham 1982; Gill 1982).

In the present study coryneforms made up ca 15% of the total population on meat at day 0 of the storage period and 14% of the total population isolated at the retailers (Tables 1 and 2). These findings differ hom previous reports in that higher percentages were recovered. Ayres (1960) found only one diphtheroid on meat while Brown & Weideman (1958), in a study on the psychrophilic bacteria isolated from chilled beef and associated sources, identified 2% of the strains as probable species of Corynebacterium. Newton et al. (1975) recovered coryneforms from sirloins and cartons used for packaging. Unfortunately, they did not express these counts as a percentage of the total population recovered. Previously, the contribution of these organisms to the contamination on meat con- tacting surfaces was never mentioned, except by Newton et al. (1975). The habitats of these

342 G. L. Nortjb et al. microbes range from soils to various vertebrates and, sometimes, plants as well as man, sheep and horses (Barksdale 1981). The recovery of these organisms from surfaces other than carcasses could therefore be due to either contamination from carriers or recontamination from carcasses. Although these organisms were detected on all surfaces in this survey it is thought, when compared with the incidence of other organisms, not to be important in spoilage of the final product. It seems, however, that these organisms are not influenced by the growth of the other genera but merely maintain a constant position as part of the population up to 3 d chilled storage of the final product. After- wards, pseudomonads may have an adverse effect on the growth of coryneforms (Table 2).

Eustace (1979) stated that although yeasts are widely distributed in nature, they are not com- monly a problem in the meat industry. Ayres (1960) stated that Pseudomonas and Micro- coccus were predominant at zero time and throughout the storage period, but at the time the meat was received, organisms including Achromobacter, Flavobacterium, spore-forming organisms, chromogenic bacteria, molds and yeasts constituted 20%) to 50% of the total population. Similarly, in the present study, this figure was approximately 27% for minced meat at day 0 of the shelf-life study, with yeast consti- tuting 5% of this population (Table 1 and 2). In a study by Rogers & McCleskey (1957), Micro- coccus, Bacillus and yeasts were found to be the most prevalent organisms at the beginning of the storage period, which is contradictory to the findings by Ayres (1955, 1960) as well as those of the present study (Table 2). Various authors reported yeast counts on fresh meats ranging from approximately 1 log,, to 5 log,, counts/g (Gardner 1965; Patterson & Gibbs 1978; Smul- ders & Woolthuis 1983; Simard et al. 1984). However, most of the workers failed to interpret their findings. Yeasts can grow at pH-values ranging from approximately 1.5 through 8.0; they are widely distributed in nature and some might be normal inhabitants of the gastro- intestinal tract of humans (Eustace 1979; Silva- Hutner & Cooper 1980). The higher incidence of these organisms at the wholesale level, as has been suggested for Gram-positive cocci, might be a cause of recontamination due to the exces- sive handling of the product a t this site. The ubiquity of yeasts in nature and their associ-

ation with humans supports this hypothesis. The inability of these organisms to feature sig- nificantly in the final spoilage population of vacuum-packaged beef samples was proposed to be the result of factors such as pH and CO, produced by bacterial and animal cells (Simard et al. 1984). Since the same effect was demon- strated under aerobic conditions in the present study, other factors like a faster growth rate of the traditional spoilage bacteria (pseudomonads), have to be considered to explain this finding (Gill & Newton 1977), although the latter still have to be proven experimentally.

The present study pointed out and supports statements that there are an interaction among surfaces involved in a meat production chain, regarding the composition of the population at different production sites (Gill & Newton, 1978). Therefore the microbial count on either the carcass or the final product will be dependant on various factors viz. the initial count on carcasses, ambient temperatures involved, personnel hygiene and the efficiency of the sanitary programme applied, changes in the water activity of the meat surface and the general manage- ment applied throughout the meat production chain.

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the aerobic psychrotrophic populations on meat and meat contact surfaces in a meat production system...

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