7.microbiology of meats

8/12/2019 7.Microbiology of Meats

1/21

7

Microbiology of Meats

DOUGLAS L. MARSHALL and M. FARID A. BALA

Mississippi State University, Mississippi State, Mississippi

I. INTRODUCTION

II. MEAT CONTAMINATION AND DECONTAMINATION

III. MEAT AS A SUBSTRATE FOR MICROBIAL PROLIFERATION

IV. MICROBIOLOGY OF FERMENTED AND CURED MEATS

V. MEAT-ASSOCIATED FUNGI

VI. MEAT-ASSOCIATED PARASITES

VII. MICROBIAL MODELING

VIII. SUMMARY

ACKNOWLEDGMENTS

REFERENCES

I. INTRODUCTION

Contamination of sterile animal muscle used as food is a direct consequence of slaughter-

ing and dressing of animal carcasses. Wide ranges of microorganisms from different

sources are introduced onto moist muscle surfaces that are rich in nutrients. It is argued that

only a small portion (10%) of these microorganisms is capable of survival and proliferation

during storage, distribution, and retail sales of meats. Additionally, an even a smaller por-

tion will eventually predominate and cause spoilage. Survival and proliferation of mi-

croorganisms deposited on meat surfaces depends on their ability to withstand processing

and storage conditions and to utilize available nutrients in the muscle through assimilation

or proteolysis of complex molecules into readily utilizable substrates.

Over the years, efforts to preserve meats have focused on retarding microbial growth

or killing selected contaminants by applying chemical, physical, or biological treatments

whose net outcome should slow or prevent the growth of spoilers or allow harmless fer-

mentative microorganisms to predominate. In either case, successful treatments extend

product shelf life and allow its delivery from farm/processor to remote consumption areas.

Copyright 2001 by Marcel Dekker, Inc. All Rights Reserved.


2/21

Microflora of meat products available to consumers at the retail level is a reflection of the

environment in which they were processed and the conditions under which they were

stored. From a numerical standpoint, using the per capita meat consumption of 88 kilo-

grams (2,109) and an average microbial load of 10,000 colony forming units (CFU) per

gram, a family of four annually brings into their home nearly 1 billion microorganisms as-

sociated with raw meat products. The nature and composition of viable microorganisms as-sociated with consumer health risks and associated economic impact on the meat industry

vary with the nature of the animal, processing, packaging, storage, and handling conditions.

Meats can acquire a large variety of pathogenic and spoilage microorganisms during pri-

mary and further processing (Table 1). Pathogens can include Clostridium perfringens,

Staphylococcus aureus, Salmonella spp., pathogenicEscherichia coli, Campylobacterspp.,

Yersinia enterocolitica, Listeria monocytogenes, andAeromonas hydrophila (44,49,112).

Meat pathogens can cause self-limiting human enteric diseases or systemic and fatal infections

of the immunocompromised, the elderly, and the young. Spoilage of meats is largely depen-

dent on initial microbiological quality and subsequent storage conditions. Pseudomonas spp.predominate in chilled airstored meats, (38) Enterobacteriaceae in temperature-abused meats,

(83) lactic acid bacteria and Micrococcaceae in meats packaged with preservatives (82,88) and

Brochothrix thermosphacta in vacuum- and modified atmospherepackaged products (118).

Gill (42) reviewed the potential sources of meat contamination during slaughter and

butchering of food animals. Animal health, hide, viscera, feces, oral microflora, and car-

cass handling are all potential sources of cross-contamination of sterile muscle during

dressing operations. Ultimately, the microbiological quality of dressed carcasses relies a

great deal on the skill level of operators during dressing operations, in particular skinning

and evisceration, more so than on physical facilities or the types of stock slaughtered (87).

Several decontamination approaches have been proposed to enhance the microbiological

quality and safety of dressed carcasses (24). Treatments with organic acids (30), hot water

(56), steam pasteurization, and steam carcass vacuuming (122) have been implemented in

some processing plants. Bacterial species vary widely in their susceptibility to decontami-

nation treatments, with 2 to 3 log population reductions possible (24,26).

Determining the microbiological quality of dressed animal carcasses requires ob-

taining samples for laboratory analysis. Classical sampling methods have included excis-

ing a meat surface portion (16,80) or swabbing a defined surface area delimited by a tem-

plate (57) to determine microbial loads per unit area. Obtained samples are either

suspended and homogenized in a diluent and bacterial counts determined directly by spread

plate, pour plates, hydrophobic grid membrane filtration (HGMF), or indirectly by ATP bi-

oluminescence or impedance measurements (51,58). According to Gill and Jones (51),

HGMF can enhance detection sensitivity to 1 CFU/100 cm2. For routine microbiological

monitoring of hygienic quality of carcasses, USDA-FSIS mandates combining samples ob-

tained from three sites of a given carcass and determiningE. coli counts (127). In any event,

carcass sampling remains a technique and its usefulness in predicting microbiological qual-

ity or microbial profiles depends on obtaining a true representative sample in high volume

operations (27,79,119). From a practical standpoint, it is impossible to monitor dressed car-

casses for all potential pathogens and spoilage microorganisms they may harbor. This con-

sideration limits meat microbiological monitoring to either total aerobic plate counts or to

E. coli counts as an indicator of fecal contamination (127). The latter approach is currently

favored in view that total aerobic plate counts bear no indication to the potential presence

of pathogens (117). However, the use ofE. coli counts, or other potential indicator organ-

isms, shows that no single indicator organism is effective for all types of foods (14).



3/21

Consumers view quality aspects of meats as being good taste, tender, juicy, fresh,

lean, healthy, and nutritious. However, cross-cultural differences exist in what is desig-

nated as fresh meat (60). The butcher in most developed countries may no longer be the

guarantor of meat freshness, quality, and safety because supermarket chains supplied from

major processors dominate the meat processing and retailing business. This chapter will ad-

dress the microbiology of meat products with emphasis placed on the roles that processing,

storage, and retailing exert on the microflora.

II. MEAT CONTAMINATION AND DECONTAMINATION

The microbiological profile of meat products presented to consumers is the sum total of

slaughtered animal health, conditions under which it was reared, quality of slaughtering,

processing, packaging, and conditions under which the meat was stored. Table 1lists the

common genera of microorganisms found on fresh, processed, and vacuum-packaged

meats. Gill (42) reviewed the potential sources of meat contamination during slaughter-

ing and butchering of food animals. Animal health, hide, viscera, feces, oral microflora,

and carcass handling are all potential sources of cross contamination of sterile muscle

during dressing operations. With cattle and sheep, the major source of initial meat con-

tamination is the animal hide or fleece (6,7,42,62). These sources are exposed to soil, fe-

ces, water, and oral microorganisms during animal rearing. It would seem logical that

cleaning the hide or fleece before dressing should reduce the number of potential con-

taminants; however, several studies have failed to confirm this point (9,10,128). On the

other hand, scalding treatments applied to pigs destroys gram-negative bacteria, leaving

predominantly gram-positive bacteria as survivors (39). Subsequent pig carcass de-

hairing reintroduces gram-negative bacteria from accumulated detritus and contaminated

recirculated water (12,44,49). Animal hides not only introduce spoilage bacteria such as

Pseudomonas, Acinetobacter, andMoraxella but also may introduce potential pathogens

such as C. perfringens, S. aureus, Salmonella spp.,E. coli, Campylobacterspp.,Y. ente-

rocolitica, L. monocytogenes, and A. hydrophila (44,49,112). Foodborne pathogens of

animal origin can cause human gastroenteritis, and in high-risk populations they can lead

to systemic and sometimes fatal infections (8). Other potential risks of meat contamina-

tion involve the potential transfer of antibiotic-resistant microorganisms to dressed meats

and their ability to subsequently transfer this resistance to other microorganisms in the

human gut (102).

Evisceration is another critical step where operator skill is required to avoid spilling

fecal matter onto skinned carcasses. It has been shown that bacteria deposited on carcasses

during eviscerating operations predominantly originate from the mouth and the anus (50).

Ultimately, the microbiological quality of dressed carcasses heavily relies on the skill level

of operators during skinning and evisceration, more so than on processing plant physical

facilities or the type of animal slaughtered (87,90). Little information exists on the impact

of misprocessing events on microbiological quality of dressed carcasses. Gill (42) advo-

cated treating common mishaps, such as spilling of gut contents onto carcasses or contam-

ination introduced by operator handling, as events that necessitate special treatment. Acci-

dentally contaminated carcasses should be flagged and detained for extra trimming and

washing to remove visible contamination. Gill and Jones (50) showed that carcass pasteur-

ization combined with a modified dressing process that prevents contamination from ani-

mal mouth and viscera can produce dressed pig carcasses with averageE. coli counts of1

per carcass and total counts of 2 CFU/cm2. Enhancing the microbiological quality of



4/21

Table 1 Genera of Microorganisms Commonly Found on Meats

Type of meat

Gram Rxn Fresh Processed Vacuum packaged

BACTERIAAchromobacter X

Acinetobacter XX X X

Aeromonas XX X X

Alcaligenes X

Alteromonas X X

Bacillus X X

Brochothrix X X XX

Campylobacter X

Carnobacterium X XX

Citrobacter XClostridium X

Corynebacterium X X X

Enterobacter X X X

Enterococcus XX X XX

Escherichia X

Flavobacterium X

Hafnia X X

Janthinobacterium X

Klebsiella X

Kluyvera X

Kocuria X X X

Kurthia X X

Lactobacillus X XX XX

Lactococcus X

Leuconostoc X X X

Listeria X X

Microbacterium X X X

Micrococcus X X X

Moraxella XX

Paenibacillus X X

Pantoea X

Pediococcus X X X

Proteus X

Providencia X X X

Pseudomonas XX X

Psychrobacter XX

Salmonella X

Serratia X X X

Shewanella XStaphylococcus X X X

Vibrio X

Weissella X X X

Yersinia X X



5/21

dressed carcasses entails recognizing microbial hazards (12,91) and designing strategies to

limit their spread to muscle foods during carcass dressing.

Following dressing, carcasses are split and knife trimmed to remove visible contam-

ination and bruised tissue (126). Studies of trimming practices have indicated that they are

purely of aesthetic value and do not contribute to enhancing microbiological quality of

dressed carcasses (42,43,57). Furthermore, trimming causes loss of meat and requires ex-

tra operator time and effort without necessarily improving microbiological quality (112).

The requirement to meet pathogen reduction performance standards has prompted a

number of studies in which antimicrobial intervention strategies have been compared.

Washes with chemicals have been most advocated. Considerable literature exists on the an-

tibacterial efficacy of dilute solutions of organic acids, hydrogen peroxide, chlorine, chlo-

rine dioxide, and organic acid salts (63,93,108,110). Overall, such interventions can result

in reduction of contaminants by 1 to 2 logs (24). In addition to benefiting meat safety, these

Table 1 Continued

Type of meat

Gram Rxn Fresh Processed Vacuum packaged

YEASTSCandida XX X

Cryptococcus X

Debaryomyces X XX

Hansenula X

Pichia X

Rhodotorula X

Saccharomyces X

Torulopsis XX

Trichosporon X X

MOLDSAcremonium X

Alternaria X X

Aspergillus X XX

Aureobasidium X

Botrytis X

Chrysosporium X

Cladosporium XX X

Fusarium X X

Geotrichum XX X

Monascus X

Monilia X X

Mucor XX X

Neurospora X

Penicillium X XX

Rhizopus XX X

Scopulariopsis X

Sporotrichum XX

Thamnidium XX X

X known to occur, XX most frequently isolated.Source: Dillon (25); Garcia-Lopez et al. (35); Jay (78).



6/21

interventions can also improve meat quality. For example, a reduction in the numbers of

psychrotrophs by 4 logs can greatly increase the refrigerated shelf life of frankfurters

(Fig. 1).

Studies that have addressed meatborne pathogens have shown varying susceptibili-

ties to such treatments. Campylobacter jejuni andY. enterocolitica are among the most sus-

ceptible pathogens to acid treatment (92,94),E. coli O157:H7 andL. monocytogenes are

more resistant (13,108,120). Smulders and Greer (123) reviewed other prospects of organic

acid decontamination and resultant adverse effects on muscle foods. Using organic acids as

a decontaminant in abattoirs has been recommended (127); however, a primary concern to

meat exporters is that European Union countries do not allow for product decontamination

treatments with anything other than potable water (123).

The use of hot water to decontaminate dressed carcasses has been studied with beef

(15,23), sheep (28), pork (56), and buffalo (113). A typical outcome of carcass washing

was the reduction of microbial loads by 2 logs with hot water treatment (80C for 10 sec)

(122). Another possible outcome of all wash operations is the uniform redistribution of

contaminants from heavily soiled areas to the whole carcass (42). Hot water washes

largely have not been adopted commercially in view that large volumes would be needed

to uniformly heat a carcass surface. Moreover, economic reasons would impose recircu-

lating hot treatment water, but sanitary concerns would not entertain such cost reductions

(42). Alternatively, steam pasteurization has been advocated as a more viable option

(19,29,97); however, to ensure adequate carcass surface heating, supra-atmospheric pres-

sures are needed, which entails the need for specialized containment chambers (19). In

commercial applications, steam is applied for 6.5 sec without appreciable sensory degra-

dation and results in 2 log and 1 log reduction in E. coli and total aerobic counts, re-

spectively (29,97,106). Steam pasteurization enriches growth of gram-positive bacteria

on meats while reducing the more thermally susceptible gram-negative enteric pathogens

(42). A less expensive alternative to steam pasteurization chambers involves the use of

hot water or steam vacuum hand-held wands. Selected carcass areas can be treated by this

method to remove visible contamination. A favorable report exists on the steam-vacuum

approach to treat artificially contaminated meats (29). Use of this method in a commer-

Figure 1 Time required for spoilage development in frankfurters held at different refrigerationtemperatures. (Data from Ref. 130.)



7/21

cial setting was advocated as an alternative to cleaning soiled carcass areas and to reduce

the need for subsequent trimming (29).

Following the dressing process, carcasses are transferred to chiller rooms. Rapid cool-

ing before the development of rigor results in toughening of the muscle and subsequent loss

of meat quality (125). On the other hand, slow cooling ensures rigor and allows for spoilage

and pathogenic bacteria to proliferate (42). Commercial chilling of dressed carcasses usechill tunnels that rely on blasts of cold air (48) or spraying of carcasses with chilled water

(55,59). It has been proposed that very fast carcass cooling can ensure muscle tenderness

and microbiological quality (81); however, major capital spending would be required to im-

plement fast cooling systems in abattoirs (42). Another consequence that accompanies air

chilling is drying of the carcass surface by the reduction of surface moisture. Typically a 0.5

log microbial count reduction is observed as a consequence of surface drying (96). Alterna-

tive techniques have desiccated the carcass surface with dry heat (18). The major objection

to carcass drying is the accompanying carcass weight loss (39). Accordingly, many abattoirs

in North America have adopted intermittent spraying with water during the first hours of

cooling to avoid weight loss (42). Gill (42) proposed an explanation for the observed re-

duction in Gram-negative andE. coli counts on spray-cooled carcasses. His twofold mech-

anism was that (a) spray cooling washed away surface bacterial loads and (b) surface freez-

ing reduces gram-negative bacteria due to their greater susceptibility to freezing.

Offal or organ meats are collected in bulk containers during carcass dressing. The ge-

ometry of their storage adversely affects subsequent chilling. Product on the periphery of

storage containers cools faster than product in the center of the bulk container (42). Even

in freezers of high cooling capacities, product at the centers of large containers will cool

more slowly (5), thus providing greater opportunity for microbial proliferation. Offal meat

pH is usually 6.0, which implies that the major hurdle in restraining microbial growth

would be temperature and potential anaerobic conditions produced at the center of bulk

containers (45,47). Enhancing the storage potential of offal can been achieved by vacuum

or CO2 packaging to noticeably extend shelf life up to several weeks (46). However, efforts

by the meat industry to ensure the microbiological quality of offal will remain proportional

to their economic value on the market.

Hot boning involves breaking down an animal carcass immediately after dressing as

boxed manufacturing meats or for further processing into comminuted, cured, or cooked

products. Boxing and stacking of hot boned meats in a cooler suffers similar limitations as

the earlier described chilling of offal (111). However, temperature control is possible using

ice or liquid carbon dioxide (42). Studies are needed to elucidate the effects of rigor devel-

opment on the proliferation of microorganisms in hot-boned meats (42).

Following chilling, carcasses are either broken down into primal cuts or transported

to other processing plants for further processing. In either event, personnel hygiene and

proper sanitation of equipment and work surfaces are prerequisites to ensure microbiolog-

ical quality and safety of processed meat products. Visible cleanliness of equipment and

work surfaces although advocated (127) may not be a true reflection of sanitary conditions

unless coupled with microbiological or bioluminescent assays to ensure efficacy (34). Im-

portant sources of microbial contamination of processed meat products include detritus ac-

cumulated in inaccessible parts of equipment that subsequently contaminate products that

come in touch with these surfaces (69,70). Under these circumstances, bacterial biofilms

flourish due to repeated applications of water and the constant availability of nutrients from

accumulated detritus. In cooled work environments, cold-tolerant (psychrotrophic)

pathogens such as L. monocytogenes, Y. enterocolitica, andA. hydrophila can flourish



8/21

(49,107). Ensuring the quality of processed meats entails making sure that biofilms do not

persist day to day on work surfaces and equipment (131).

Processed meats and primal cuts await their distribution in coolers. With raw meats,

low storage temperature and low pH (5.5) due to rigor are the only two hurdles to slow bac-

terial proliferation. At all times, meat temperatures should not exceed 7C to prevent

pathogenic mesophiles from proliferating (11). Consequently, storage and transport ofmeat at chilled temperatures lower than 7C is regarded as safe, although some pathogenic

psychrotrophs can proliferate at this temperature (42,103). Limiting psychrotroph growth

and further extending shelf life can be achieved by lowering the temperature of boxed meat

to 1.5C without obvious ice formation (54). At temperatures of 0, 2, and 5C, chilled

meat will have a storage life of 70%, 50%, and 30% of the storage life of meat stored at

1.5C (42). Alternatively, meats can be frozen for extended periods of time; however, the

microbiological concern for frozen meats requires that temperatures be maintained below

5C, the minimum growth temperature of yeast and mold fungi (42,84,85). Although

chill temperatures inhibit microbial growth, pathogens may survive for prolonged periods

in meats even though they do not multiply.

The microflora of meats available to consumers is the total sum of microorganisms

acquired during processing of animal muscle food. Animal health, dressing skills, person-

nel hygiene, abattoir cleanliness, and adequate storage and holding temperature during dis-

tribution and retail influence the constitution and number of microorganisms present

(17,72). It is unlikely that a single intervention can fully enhance quality and safety of

meats (42). Rather, consumer education (1) coupled with an integrated approach, which en-

sures better understanding and optimization of each processing step (41), are more likely

to enhance the future quality and safety of meats available to consumers.

III. MEAT AS A SUBSTRATE FOR MICROBIAL PROLIFERATION

Proliferation of microorganisms in meats is dependent on several factors, which include

microflora composition, product temperature, previous product treatments, pH, available

nutrients, oxidation-reduction potential, and the atmosphere surrounding the product.

Many of these factors are not constant throughout the shelf life of a meat product. Under-

standing the influence of these factors on microbial growth and survival and the impact on

meat spoilage has been greatly aided by the pioneering work of Ingram and Dainty

(20,21,74,75). More recently, Nychas et al. (101) reviewed the subject of chemical changes

associated with stored meats. Common defects of meats and associated bacteria are shown

in Table 2.

Microbial proliferation in meats occurs in the aqueous phase surrounding the prod-

uct. This phase is rich in substrates readily utilizable by almost all microorganisms (98).

Frozen (12C) meats prevent the growth of contaminating microorganisms but allow

for their abundant survival during storage. Spoilage of thawed meats is due to the number

and type of microbes present before freezing and the time/temperature conditions of the

product during thawing. Thawed meats are often more perishable than fresh meats because

of the abundance of drip containing readily utilizable substrates for microbial metabolism.

Although the concentrations of carbohydrates (primarily glucose and glycogen) are

low in the aqueous phase in comparison to proteins, available concentrations are sufficient

to support massive initial microbial proliferation (40,100). After glucose is depleted, mi-

croorganisms start using amino acids for energy and as a result produce volatile compounds

that are responsible for spoilage odors (31,32,124). Many bacteria, including pseudomon-

ads, produce ammonia during amino acid metabolism, which is a major cause of pH in-



9/21

crease in spoiling meat products (101). Gram-negative bacteria predominate during aero-

bic spoilage and are generally responsible for the production of putrid and sulfury odors

(35). The amino acids cystine, cysteine, and methionine are precursors for hydrogen sul-

fide, methylsulfide, and dimethylsulfide. Amino acid decarboxylation of lysine yields pu-

trescine. Increasing putrescine levels correlate with increasing pseudomonad counts in

meats. Decarboxylation of ornithine or arginine yields cadaverine. Increasing cadaverine

levels correlate with increasing Enterobacteriaceae counts (22). It has been noted that pseu-

domonads preferentially deaminate amino acids, whereas Enterobacteriaceae preferentially

decarboxylate (89). Bacteria, other than pseudomonads, responsible for malodorous

volatile compounds include Shewanella (Alteromonas) putrefaciens, Proteus, Citrobacter,

Hafnia, andSerratia (89). The expression of meat spoilage odors from the degradation of

amino acids can be delayed by the addition of glucose to meats. The presence of glucose

delays the utilization of amino acids by spoilage bacteria and their subsequent development

of sensory spoilage characteristics (4,115).

Lactate is another low molecular weight component utilized by meat microflora un-

der both aerobic and anaerobic conditions. Lactate is generally utilized after glucose is de-

pleted and can be used in similar strategies to retard spoilage (116). Indeed, according to

Gill (40), as long as readily utilizable low molecular weight substrates are available, meat

proteolysis is inhibited.

Microbial metabolism in chilled air-stored meats is primarily oxidative (101). Aero-

bic gram-negative bacteria are the common cause of spoilage of meats stored at 4C, with

Pseudomonas species predominating. For example, P. fragi, P. fluorescens, andP. lun-

densis are the dominant species on beef, lamb, and pork (35).Acinetobacter, Psychrobac-

ter, Moraxella, and psychrotrophic Enterobacteriaceae such asHafnia alvei, Serratia liq-

uefaciens, andEnterobacter agglomerans also occur but their numbers remain low relative

to the dominant pseudomonads.

Meats packaged under vacuum or modified atmospheres demonstrate a shift from a

diverse flora to one that is predominated by lactic acid bacteria andBrochothrix thermo-

Table 2 Common Defects of Meats and Causal Bacteria

Defect Meat product Bacteria

Slime Meats Pseudomonas, Lactobacillus,

Enterococcus, Weissella, Brochothrix

H2O2 greening Meats Weisella, Leuconostoc, Enterococcus,

Lactobacillus

H2S greening Vacuum-packaged meats Shewanella

H2S production Cured meats Vibrio, Enterobacteriaceae

Sulfide odor Vacuum-packaged meats Clostridium, Hafnia

Cabbage odor Bacon Providencia

Potato odor Ham Burkholderia, Pseudomonas

Putrefaction Ham Enterobacteriaceae, Proteus

Bone taint Whole meats Clostridium, Enterococcus

Bone taint Bacon Proteus, Vibrio

Pocket taint Bacon Vibrio, Alcaligenes, Proteus

Internal taint Ham Providencia

Souring Ham Lactic acid bacteria,Enterococcus,

Micrococcus, Bacillus, Clostridium

Source: Garcia-Lopez et al. (35); Gardner (37); Jay (78).



10/21

sphacta (68). The impact of this shift in microflora is shown in Fig. 2. As illustrated, the

time to develop off odors and slime is greatly extended when oxygen is removed from the

headspace of packages. Dairy/cheesy odors of meat stored in gas mixtures with carbon

dioxide are primarily due to diacetyl, acetoin, and alcohols produced byB. thermosphacta

from glucose fermentation (21). End products ofB. thermosphacta metabolism differ with

the gaseous atmosphere composition. When oxygen tension is low (2 M oxygen),

L-lactate, ethanol, and propanol are the main metabolic end products (101). Accordingly,

ethanol and propanol could be used as spoilage indicators of meat stored under vacuum of

modified atmosphere (98,101).

Future prospects of meat substrate and bacterial metabolite studies could point the

way to analytical techniques that could assess meat spoilage without resorting to time-con-

suming microbiological analysis. According to Jay (77), metabolite-based spoilage detec-

tion should ensure that (a) the spoilage indicator is not normally present in the food, (b) the

indicator concentration should increase with storage time, and (c) the concentrations of the

indicator should reflect the most predominant microorganisms and correlate with sensory

quality.

IV. MICROBIOLOGY OF FERMENTED AND CURED MEATS

Comminuted raw meats fermented into various sausages requires the aid of salt, nitrate/ni-

trite, and desirable fermentative lactic acidproducing bacteria. When properly fermented,

pathogens and spoilage bacteria will be eliminated or greatly reduced in numbers, which

yields products with superior shelf-life attributes. In addition, desirable sensory properties

are achieved. For example, cured red/pink color, robust flavor, and firm texture are unique

to this product type (68).

Growth and acid production of lactic acid-forming bacteria are promoted by pH be-

low 6.0, water activity (aw) of 0.96 due to salt (2.5 to 3.0%), 100 ppm sodium nitrite, and

0.3% glucose. When stuffed into casings, the redox potential of the sausage is reduced,

Figure 2 Hypothetical development of off-odor and slime in meat due to psychrotrophic bacterialgrowth during storage under various atmospheres at1C. (Data from Refs. 3 and 95.)



11/21

which further enhances activity of the lactic acid bacteria (68). Despite the wide variety of

fermented meats around the world and various technical differences during processing, the

bacteria that tend to dominate in naturally fermented sausages are usually Lactobacillus

sake andLactobacillus curvatus (61,73,114). Predominance of these two species is based

on their ability to grow at reduced aw (0.91) and low temperature (4C). Other psy-

chrotrophic lactics (Carnobacterium spp.,Leuconostoc spp. and Weissella spp.) are either

less halotolerant (except Weissella halotolerans) or grow poorly below 7C (Lactobacillus

pentosus, Lactobacillus plantarum, Pediococcus acidilactici, and Pediococcus pen-

tosaceus) (86).

Many traditional fermentations use nitrate as the curing agent. As such, the presence

of nitrate-reducing micrococci (Micrococcus varians, Staphylococcus carnosus, Staphylo-

coccus xylosus, orStaphylococcus piscifermentans) is necessary to form nitrite, which is

needed for proper quality (color) and safety (antibotulinal activity) (67,68,99). Because the

reliability of natural fermentations is occasionally less than desired, most industrial pro-

cessing of fermented sausages use domesticated starter culture bacteria. These starters are

either single or mixed strains of homofermentative lactic acid bacteria. When nitrate is

used, micrococci also are included (67,86). Commonly used lactics includeL. sake, L. cur-

vatus, L. plantarum, L. pentosus, and P. pentosaceus (P. cerevisiae) (33,66,86,129). Strains

are selected primarily for their ability to rapidly acidify, accelerate ripening, and improve

color intensity and stability at the fermentation temperature desired (Table 3) (64,65).

Spoilage microflora in fresh sausages generally are similar to those found in ground

meat. Type of meat, presence of preservatives, and storage temperature and atmosphere

will determine the predominant microbes (35). Like fresh meats, products in air-permeable

packaging will have pseudomonads predominating during low temperature storage and En-

terobacteriaceae during higher temperature storage. Presence of these bacteria on fully

cooked products is the result of post-heating contamination, usually during casing removal,

slicing, and subsequent handling during packaging. Because of the facultatively anaerobic

nature of most Enterobacteriaceae, they tend to predominate in vacuum-and modified at-

mospherepackaged products stored at high temperatures (10C) (35,104). However, this

group competes poorly with lactic acid bacteria under proper chill storage conditions (12).

Similarly, gram-negative bacteria usually will not spoil fermented sausages, dried meats,

and canned meats (35).

Bacteria that are resistant to salt and low aw, nitrite, and fermentation and ripening

temperatures will be selected for in fermented sausage products. Many of the same mi-

croorganisms are found on cured unfermented products such as hams and bacon. For ex-

Table 3 Lactic Acid Bacteria Used as Starter Cultures for Fermented Sausages at

Various Processing Temperatures

Bacteria type Process temperature (C) Bacterial species

Thermophiles 3038 Pediococcus acidilactici

Pediococcus cerevisiae

Mesophiles 2025 Lactobacillus pentosus

Lactobacillus plantarum

Psychrotrophs 1520 Lactobacillus sake

Lactobacillus curvatus

Source: Holzapfel (68).



12/21

ample, Micrococcaceae, lactic acid bacteria (Carnobacterium andLeuconostoc),Vibrio,

Enterobacteriaceae, and other gram-negative bacteria (Psychrobacter, Acinetobacter, and

Proteus) are the major microbial groups found on cured products (12,35,37). Among the

halophilic (salt loving) vibrios, Vibrio costicola is a common slime former (36).

V. MEAT-ASSOCIATED FUNGI

Carcasses aged at very low temperatures (5C) can have surface defects caused by molds

(Table 1).For example black, white, blue-green, and whisker spots may be evident (25).

Cladosporium cladosporioides, Cladosporium herbarum, Penicillium hirsutum, andAure-

obasidium pullulans were identified as causative agents of black spot (52,53); Chrysospo-

rium pannorum andAcremonium sp. caused white spots (85). Blue-green spots were asso-

ciated with Penicillium corylophilum and whisker spots were caused by Thamnidium

elegans andMucor racemosus (85).

In addition to bacteria, several molds have been responsible for cured meat spoilage.

Low aw and presence of oxygen selects for molds from the generaAspergillus, Alternaria,

Fusarium, Mucor, Rhizopus, Botrytis, andPenicillium (25,78). Some dry-cured products,

such as European sausages, Italian salami, and country-cured hams, can support prolific

growth of aspergilli and penicillia. There is some speculation that the characteristic flavors

of these products are due in part to the presence of these fungi (25,78,105).

Like many molds and bacteria, psychrotrophic yeasts are capable of growing on

meats during refrigerated storage (Table 1). Most yeast-associated meat spoilage occurs

when the product has been treated in such a manner to reduce the level and activity of con-

taminating bacteria. Such treatments usually include low pH by acidification or low aw by

salting, drying, or freezing (25). In fresh meats, however, yeasts generally are unable to

compete with bacteria because of their slower growth rates. As such, their numbers remain

low in proportion to bacterial counts. Candida spp. are the predominate yeast isolated from

raw meats (25,71). Spoilage caused by yeasts is typically related to slime formation on

products such as dried sausages, wieners, cured hams, and salami.Debaryomyces spp. and

Candida spp. are the predominate yeasts found in processed meats (25).

VI. MEAT-ASSOCIATED PARASITESSeveral microscopic animal parasites may be harbored in meats (Table 4).Parasitic proto-

zoa, flatworms, and roundworms associated with meat animals can be infectious to con-

sumers. Unlike bacteria and fungi, the parasites do not grow in foods but are merely trans-

ported either intramuscularly or as surface contaminates. Surface contamination can come

from contact with feces or more commonly from use of contaminated water supplies. For-

tunately, most parasites are easily killed by proper cooking (80C internal temperature)

and handling of products. Long-term freezing (10C for 30 days) or salting of meats

also has been shown to inactivate many of the parasites (78).

Among protozoa, the coccidian Toxoplasma gondii may cause toxoplasmosis in in-

dividuals consuming raw or undercooked meats from cattle, pigs, sheep, and goats

(76,121).Sarcocystis hominis andSarcocystis suihominis may be transmitted by consump-

tion of raw beef and pork (78). Cryptosporidium parvum has been linked to ingestion of

leftover beef tripe (78).

The flatworm Fasciola hepatica is infrequently found in beef livers. Most other flat-



13/21

worms are distributed in fish rather than meat animals (78). The common tapeworms Tae-

nia saginata (Taeniarhynchus saginatus) andTaenia solium can cause mild human illnessin consumers eating raw or undercooked beef and pork, respectively. Of more severity is

the illness trichinosis, caused by consumption of raw or undercooked pork containing the

roundwormTrichinella spiralis. This illness can occasionally be fatal (78).

VII. MICROBIAL MODELING

Predictive modeling of microbial growth and survival in meats has become an increasingly

important tool in studying the behavior of spoilage and pathogenic microorganisms under

different environmental conditions. Predicting the impact of intrinsic (nutrients, pH, salt,nitrite, etc.) and extrinsic (atmosphere, temperature) factors on microorganisms can help

processors and regulators determine optimum conditions needed for enhanced quality and

safety. Two computer-based modeling programs are available: Food Micromodel (Leather-

head, Surrey, UK) and Pathogen Modeling Program (USDA, Wyndmoor, PA). Example

outputs from the USDA model are illustrated in Figs. 3through5.Figure 3 shows predicted

growth potential ofE. coli O157:H7 under specified atmosphere, temperature, pH, salt, and

nitrite conditions. Figure 4demonstrates the predicted amount of time needed to achieve a

3 log or greater reduction in the numbers ofL. monocytogenes at pH 3.5, 16.9C, and 0.5%

NaCl. Figure 5 illustrates the predicted survival of S. typhimurium at 0C with increasinggamma irradiation doses.

VIII. SUMMARY

The numbers and types of microorganisms found on meats are determined by the environ-

ment under which the animals were raised and processed, and the meat packaged and

stored. With current technology it is nearly impossible to produce sterile meats without ex-

cessive thermal or irradiation processing. That said, proper animal husbandry, workplace

sanitation, and processing will produce edible meats with acceptable microbial numbers

and low or no human pathogens. However, it must be expected that raw meats will contain

potential human pathogens. In addition, with the possible exception of canned meats, most

processed meats will have a limited shelf life that is dictated by the quantity and kinds of

spoilage microorganisms on the product. Meat processors have the expectation that farm-

ers and feedlots will provide animals for slaughter that are safe for meat production. Like-

Table 4 Parasites Commonly Associated with Meats

Parasite Genus Meat

Protozoa Toxoplasma Beef, pork, sheep, goat

Sarcocystis Beef

Cryptosporidium Beef

Flatworms Fasciola Beef liver

Tapeworms Taenia Beef, pork

Roundworms Trichinella Pork

Source: Jay (78).



14/21

Figure 4 Predicted low pH inactivation time needed forListeria monocytogenes using the USDAPathogen Modeling Program.

Figure 3 Predicted aerobic growth ofEscherichia coli O157:H7 using the USDA Pathogen Mod-eling Program.



15/21

wise, consumers have the expectation that meat products available for consumption are safeand wholesome. Failure by the meat industry to meet these expectations frequently leads to

microbial problems and ultimately decreased consumer demand. Therefore, understanding

the quantity and nature of meatborne microorganisms remains a critical issue for long-term

viability of the industry.

ACKNOWLEDGMENTS

The USDA Pathogen Modeling Program ver. 5.1 was developed by R. L. Buchanan, Ph.D.,

R. C. Whiting, Ph.D., and A. R. Pickard, Ph.D., at the Microbial Food Safety Research Unitof the USDA/ARS Eastern Regional Research Center in Wyndmoor, PA.

REFERENCES

1. Altekruse, S. F., D. A. Street, S. B. Fein, and A. S. Levy. 1996. Consumer knowledge of food-

borne microbial hazards and food-handling practices. J Food Prot 59:287294.

2. Anonymous. 1997. U.S. per capita food consumption. Family Econom Nutr Rev 10:3842.

3. Ayres, J. C. 1960. The relationship of organisms of the genus Pseudomonas to the spoilage of

meat, poultry and eggs. J Appl Bacteriol 23:471486.4. Barua, M., and L. A. Shelef. 1980. Growth suppression of pseudomonads by glucose utiliza-

tion. J Food Sci 45:34951.

5. Baxter, D. C. 1962. The fusion of slabs and cylinders. J Heat Transfer 84:317320.

6. Bell, R. G. 1997. Distribution and sources of microbial contamination on beef carcasses. J

Appl Microbiol 82:292300.

7. Bell, R. G., and S. C. Hathaway. 1996. The hygienic efficiency of conventional and inverted

lamb dressing systems. J Appl Bacteriol 81:225234.

Figure 5 Predicted irradiation inactivation curve for Salmonella typhimurium using the USDAPathogen Modeling Program.



16/21

8. Bishai, W. R., and C. L. Sears. 1993. Food poisoning syndromes. Gastroenterol Clin N Am

22:579608.

9. Biss, M. E., and S. C. Hathaway. 1995. Microbiological and visible contamination of lamb car-

casses according to preslaughter presentation status: implications for HACCP. J Food Prot

58:776783.

10. Biss, M. E., and S. C. Hathaway. 1996. Effect of pre-slaughter washing of lambs on the mi-crobiological and visible contamination of the carcases. Vet Rec 138:8286.

11. Bogh-Sorensen, L., and P. Olsson. 1990. The chill chain. In: T.R. Gormley (Ed.) Chilled

Foods: The State of the Art. pp. 245267. Elsevier, London.

12. Borch, E., T. Nesbakken, and H. Christensen. 1996. Hazard identification in swine slaughter

with respect to foodborne bacteria. Int J Food Microbiol 30:925.

13. Brackett, R. E., Y. Y. Hao, and M. P. Doyle. 1994. Ineffectiveness of hot acid sprays to de-

contaminateEscherichia coli O157:H7 on beef. J Food Prot 57:198203.

14. Buchanan, R. L., F. J. Shultz, M. H. Golden, K. Bagi, and B. Marmer. 1992. Feasibility of us-

ing microbiological indicator assays to detect temperature abuse in refrigerated meat, poultry,

and seafood products. Food Microbiol 9:279301.15. Castillo, A., L. M. Lucia, K. J. Goodson, J. W. Savell, and G. R. Acuff. 1998. Use of hot wa-

ter for beef carcass decontamination. J Food Prot 61:1925.

16. Charlebois, R., R. Trudel, and S. Messier. 1991. Surface contamination of beef carcasses by

fecal coliforms. J Food Prot 54:950956.

17. Collins, J. D. 1995. Animal health and the role of the veterinary food hygienist in the control

of meat borne infections. J Food Safety 15:145156.

18. Cutter, C. N., W. J. Dorsa, and G. R. Siragusa. 1997. Rapid desiccation with heat in combina-

tion with water washing for reducing bacteria on beef carcass surfaces. Food Microbiol

14:493503.

19. Cygnarowicz-Provost, M., J. C. Craig Jr., and R. C. Whiting. 1995. Computer control of a

steam surface pasteurization process. J Food Eng 25:131139.

20. Dainty, R. H. 1982. Biochemistry of undesirable effects attributed to microbial growth on pro-

teinaceous foods stored at chill temperatures. Food Chem 9:103113.

21. Dainty, R. H., and C. M. Hibbard. 1983. Precursors of the major end products of aerobic

metabolism of Brochothrix thermosphacta meat-spoilage organisms. J Appl Bacteriol

55:127133.

22. Dainty, R. H., and B. M. Mackey. 1992. The relationship between the phenotypic properties

of bacteria from chill-stored meat and spoilage process. J Appl Bacteriol 73:Symp. Suppl.

21:103S114S.

23. Davey, K. R. 1990. A model for the hot water decontamination of sides of beef in a novel cab-

inet based on laboratory data. Int J Food Sci Technol 25:8897.

24. Dickson, J. S., and M. E. Anderson. 1992. Microbiological decontamination of food animal

carcasses by washing and sanitizing systems: a review. J Food Prot 55:133140.

25. Dillon, V. M. 1998. Yeasts and moulds associated with meat and meat products. In: A. Davies

and R. Board (Ed.) The Microbiology of Meat and Poultry. pp. 85117. Blackie Academic &

Professional, New York.

26. Dorsa, W. J. 1997. New and established carcass decontamination procedures commonly used

in the beef-processing industry. J Food Prot 60:11461151.

27. Dorsa, W. J., and G. R. Siragusa. 1998. A representative microbial sampling method for largecommercial containers of raw beef based on purge. J Food Prot 61:162165.

28. Dorsa, W. J., C. N. Cutter, and G. R. Siragusa. 1996a. Effectiveness of a steam-vacuum sani-

tizer for reducing Escherichia coli O157:H7 inoculated to beef carcass surface tissue. Lett

Appl Microbiol 23:6163.

29. Dorsa, W. J., C. N. Cutter, G. R. Siragusa, and M. Koohmaraie. 1996b. Microbial decontam-

ination of beef and sheep carcasses by steam, hot water spray washes, and a steam-vacuum

sanitizer. J Food Prot 59:127135.



17/21

30. Dorsa, W. J., C. N. Cutter, and G. R. Siragusa. 1997. Effects of acetic acid, lactic acid and

trisodium phosphate on the microflora of refrigerated beef carcass surface tissue inoculated

withEscherichia coli O157:H7,Listeria innocua, andClostridium sporogenes. J Food Prot

60:619624.

31. Edwards, R. A., and R. H. Dainty. 1987. Volatile compounds associated with the spoilage of

normal and high pH vacuum-packed pork. J Sci Food Agric 38:5766.32. Edwards, R. A., R. H. Dainty, and C. M. Hibbard. 1987. Volatile compounds produced by

meat pseudomonads and related reference strains during growth on beef stored in air at chill

temperatures. J Appl Bacteriol 62:403412.

33. Engesser, D. M., and W. P. Hammes. 1994. Non-heme catalase activity of lactic acid bacteria.

System Appl Microbiol 17:1119.

34. Farrell, B. L., A. B. Ronner, and A. C. Wong. 1998. Attachment ofEscherichia coli O157:H7

in ground beef to meat grinders and survival after sanitation with chlorine and peroxyacetic

acid. J Food Prot 61:81722.

35. Garcia-Lopez, M. L., M. Preito, and A. Otero. 1998. The physiologic attributes of Gram-neg-

ative bacteria associated with spoilage of meat and meat products. In: A. Davies and R. Board

(Ed.) The Microbiology of Meat and Poultry. pp. 134. Blackie Academic & Professional,

New York.

36. Gardner, G. A. 1981. Identification and ecology of salt-requiring Vibrio associated with cured

meats. Meat Sci 5:7181.

37. Gardner, G. A. 1983. Microbial spoilage of cured meats. In: T. A. Roberts and F. A. Skin-

ner (Ed.) Food Microbiology: Advances and Prospects. pp. 179202. Academic Press, Lon-

don.

38. Gennari, M., and F. A. Dragotto. 1992. Study of the incidence of different fluorescent Pseu-

domonas species and biovars in the microflora of fresh and spoiled meat and fish, raw milk,cheese, soil and water. J Appl Bacteriol 72:281288.

39. Gigiel, A. J., P. Collert, and S. J. James. 1989. Fast and slow beef chilling in a commercial

chiller and the effects of operational factors on weight loss. Int J Refrig 12:338349.

40. Gill, C. O. 1976. Substrate limitation of bacterial growth at meat surfaces. J Appl Bacteriol

41:401410.

41. Gill, C. O. 1995. Current and emerging approaches to assuring the hygienic condition of red

meats. Can J Anim Sci 75:113.

42. Gill, C. O. 1998. Microbiological contamination of meat during slaughter and butchering of

cattle, sheep and pigs. In: A. Davies and R. Board (Ed.) The Microbiology of Meat and Poul-

try. pp. 118157. Blackie Academic & Professional, New York.43. Gill, C. O., and L. P. Baker. 1998. Assessment of the hygienic performance of a sheep carcass

dressing process. J Food Prot 61:329333.

44. Gill, C. O., and J. Bryant. 1993. The presence ofEscherichia coli, Salmonella andCampy-

lobacterin pig carcass dehairing equipment. Food Microbiol 10:337344.

45. Gill, C. O., and K. M. Delacy. 1982. Microbial spoilage of whole sheep livers. Appl Environ

Microbiol 43:126266.

46. Gill, C. O., and L. E. Jeremiah. 1991. The storage life of non-muscle offals packaged under

vacuum or carbon dioxide. Food Microbiol 8:339353.

47. Gill, C. O., and S. D. M. Jones. 1992a. Efficiency of a commercial process for the storage and

distribution of vacuum-packaged beef. J Food Prot 55:880887.

48. Gill, C. O., and T. Jones. 1992b. Assessment of the hygienic efficiencies of two commercial

processes for cooling pig carcass. Food Microbiol 9:335343.

49. Gill, C. O., and T. Jones. 1995. The presence ofAeromonas, Listeria andYersinia in carcass

processing equipment at two pig slaughtering plants. Food Microbiol 12:135141.

50. Gill, C. O., and T. Jones. 1997. Assessment of the hygienic characteristics of a process for

dressing pasteurized pig carcasses. Food Microbiol 14:8191.



18/21

51. Gill, C. O., and T. Jones. 1998. Comparison of methods for sampling and enumeratingEs-

cherichia coli on pig carcasses. Food Microbiol 15:617623.

52. Gill, C. O., and P. D. Lowry. 1981. A note on the identities of organisms causing black spot

spoilage of meat. J Appl Bacteriol 51:183187.

53. Gill, C. O., and P. D. Lowry. 1982. Growth at sub-zero temperatures of black spot fungi from

meat. J Appl Bacteriol 52:245250.54. Gill, C. O., D. M. Phillips, and J. C. L. Harrison. 1988. Product temperature criteria for ship-

ment of chilled meats to distant markets. In: Refrigeration for Food and People. pp. 4047. Int

Inst Refrig, Paris.

55. Gill, C. O., S. D. M. Jones, and A. K. W. Tong. 1991. Application of a temperature function

integration technique to assess the hygienic adequacy of a process for spray chilling beef car-

casses. J Food Prot 54:731736.

56. Gill, C. O., D. S. McGinnis, J. Bryant, and B. Chabot. 1995. Decontamination of commercial,

polished pig carcasses with hot water. Food Microbiol 12:143149.

57. Gill, C. O., M. Badoni, and T. Jones. 1996. Hygienic effects of trimming and washing opera-

tions in a beef-carcass-dressing process. J Food Prot 59:666669.58. Greer, G. G., and B. D. Dilts. 1997. Enumeration of meatborne spoilage bacteria with hy-

drophobic grid membrane filtration. J Food Prot 60:13881390.

59. Greer, G. G., and S. D. M. Jones. 1997. Quality and bacteriological consequences of beef car-

cass spray-chilling: effects of spray duration and boxed beef storage temperature. Meat Sci

45:6173.

60. Grunert, K. G. 1997. Whats in a steak? A cross-cultural study on the quality perception of

beef. Food Qual Prefer 8:157174.

61. Gurakan, G. C., T. F. Bozoglu, and N. Weiss. 1995. Identification ofLactobacillus strains

from Turkish fermented sausages. Lebensm-Wiss u-Technol 28:139144.

62. Hadley, P. J., J. S. Holder, and M. H. Hinton 1997. Effects of fleece soiling and skinning

method on the microbiology of sheep carcases. Vet Rec 140:570574.

63. Hamby, P. L., J. W. Savell, G. R. Acuff, C. Vanderzant, and H. R. Cross. 1987. Spray-chill-

ing and carcass decontamination systems using lactic and acetic acid. Meat Sci 21:114.

64. Hammes, W. P. 1993. Zum Reifen von Rohwurst geeignete Mikroorganismen der ArtLacto-

bacillis sake. German Fed Rep Pat DE 42 01 050 C1.

65. Hammes, W. P. 1995. Zum Reifen von Rohwurst geeignete Mikroorganismen vom Stamm

Lactobacillis sake. German Fed Rep Pat EP 0 641 857 A1.

66. Hammes, W. P., A. Bantleon, and S. Min. 1990. Lactic acid bacteria in meat fermentation.

FEMS Microbiol Rev 87:165174.

67. Hammes, W. P., I. Bosch, and G. Wolf. 1995. Contribution of Staphylococcus carnosus and

Staphylococcus piscifermentans to the fermentation of protein foods. J Appl Bacteriol, Symp

Suppl 79:76S83S.

68. Holzapfel, W. H. 1998. The Gram-positive bacteria associated with meat and meat products.

In: A. Davies and R. Board (Ed.) The Microbiology of Meat and Poultry. pp. 3584. Blackie

Academic & Professional, New York.

69. Hood, S. K., and E. A. Zottola. 1997a. Adherence to stainless steel by foodborne microorgan-

isms during growth in model food systems. Int J Food Microbiol 37:145153.

70. Hood, S. K., and E. A. Zottola. 1997b. Isolation and identification of adherent gram-negative

microorganisms from four meat-processing facilities. J Food Prot 60:11351138.71. Hsieh, D. Y., and J. M. Jay. 1984. Characterization and identification of yeasts from fresh and

spoiled ground beef. Int J Food Microbiol 1:141147.

72. Hudson, W. R., G. C. Mead, and M. H. Hinton. 1996. Relevance of abattoir hygiene assess-

ment to microbial contamination of British beef carcases. Vet Rec 139:587589.

73. Hugas, M., M. Garriga, M. T. Aymerich, and J. M. Montfort. 1993. Biochemical characteri-

sation of lactobacilli from dry fermented sausages. Int J Food Microbiol 18:107113.



19/21

74. Ingram, M. 1971. Microbial changes in foodsgeneral considerations. J Appl Bacteriol

34:18.

75. Ingram, M., and R. H. Dainty. 1971. Changes caused by microbes in the spoilage of meats. J

Appl Bacteriol 34:2139.

76. Jackson, M. H., and W. M. Hutchison. 1989. The prevalence and source of Toxoplasma in-

fection in the environment. Adv Parasitol 28:55105.77. Jay, J. M. 1986. Microbial spoilage indicators and metabolites. In: M. D. Pierson and J. N.

Stern (Ed.) Foodborne Microorganisms and their Toxins: Developing Methodology. pp.

219240. Marcel Dekker, Basel.

78. Jay, J. M. 1998. Modern Food Microbiology (5th Ed.). Aspen Publishers, Gaithersburg, MD.

79. Jericho, K. W. F., J. A. Bradley, and G. C. Kozub. 1994. Bacteriological variation of groups

of beef carcasses before the wash at six Alberta abattoirs. J Appl Bacteriol 77:631634.

80. Jericho, K. W. F., J. A. Bradley, and G. C. Kozub. 1995. Microbiologic evaluation of carcasses

before and after washing in a beef slaughter plant. J Am Vet Med Assoc 206:452455.

81. Joseph, R. L. 1996. Very fast chilling of beef and tendernessa report from an EU concerted

action. Meat Sci 43:S217S227.82. Leisner, J. J., G. G. Greer, B. D. Dilts, and M. E. Stiles. 1995. Effect of growth of selected lac-

tic acid bacteria on storage life of beef stored under vacuum and in air. Int J Food Microbiol

26:231243.

83. Lindberg, A. M., A. Ljungh, S. Ahrne, S. Lofdahl, and G. Molin. 1998. Enterobacteriaceae

found in high numbers in fish, minced meat and pasteurised milk or cream and the presence of

toxin encoding genes. Int J Food Microbiol 39:1117.

84. Lowry, P. D., and C. O. Gill. 1984a. Development of a yeast microflora on frozen lamb stored

at 5C. J Food Prot 47:309311.

85. Lowry, P. D., and C. O. Gill. 1984b. Temperature and water activity minima for growth of

spoilage molds from meat. J Appl Bacteriol 56:19399.

86. Lucke, F.-K. 1996. Lactic acid bacteria involved in food fermentations and their present and

future uses in food industry. In: T. F. Bozoglu and B. Ray (Ed.) Lactic Acid Bacteria: Current

Advances in Metabolism, Genetics and Applications, Vol. 98. pp. 8199. NATO ASI Series,

Series H: l Biology, Springer Verlag, Berlin.

87. Mackey, B. M., and T. A. Roberts. 1993. Improving slaughtering hygiene using HACCP and

monitoring. Fleischwirtsch Int 2:4045.

88. Makela, P. M., H. J. Korkeala, and J. J. Laine. 1992. Ropy slime-producing lactic acid bacte-

ria contamination at meat processing plants. Int J Food Microbiol 17:2735.

89. McMeekin, T. A. 1982. Microbial spoilage of meats. In: R. Davies (Ed.) Developments in

Food Microbiology1. pp. 139. Applied Science, London.

90. Mukartini, S., C. Jehne, B. Shay, and C. M. L. Harper. 1995. Microbiological status of beef

carcass meat in Indonesia. J Food Safety 15:291303.

91. Nesbakken, T., G. Kapperud, and D. A. Caugant. 1996. Pathways ofListeria monocytogenes

contamination in the meat processing industry. Int J Food Microbiol 31:161171.

92. Netten, P. V., and J. H. Huis Int Veld. 1994. The effect of lactic acid decontamination on the

microflora on meat. J Food Safety 14:243257.

93. Netten, P. V., D. A. A. Mossel, and J. H. Huis Int Veld. 1995. Lactic acid decontamination of

fresh pork carcasses: a pilot plant study. Int. J Food Microbiol 25:19.

94. Netten, P. V., A. Valentijn, D. A. A. Mossel, and J. H. Huis Int Veld. 1997. Fate of low tem-perature and acid-adapted Yersinia enterocolitica andListeria monocytogenes that contami-

nate lactic acid decontaminated meat during chill storage. J Appl Microbiol 82:769779.

95. Newton, K. G., J. C. L. Harison, and K. M. Smith. 1977. The effect of storage in various

gaseous atmospheres on the microflora of lamb chops held at 1C. J Appl Bacteriol 43:53

96. Nottingham, P. M. 1982. Microbiology of carcass meats. In: M. H. Brown (Ed.) Meat Micro-

biology. pp. 1366. Applied Science, London.



20/21

97. Nutsch, A. L., R. K. Phebus, M. J. Riemann, D. E. Schafer, J. E. Boyer, Jr., R. C. Wilson, J.

D. Leising, and C. L. Kastner. 1997. Evaluation of a steam pasteurization process in a com-

mercial beef processing facility. J Food Prot 60:485492.

98. Nychas, G. J. E. 1994. Modified atmospheric packaging of meats. In: R. P. Singh and F. A. R.

Oliveira (Ed.) Minimal Processing of Foods and Process Optimization. pp. 417435. CRC

Press, London.99. Nychas, G. J. E., and J. S. Arkoudelos. 1990. Staphylococci: their role in fermented sausages.

J Appl Bacteriol, Symp Suppl 71:167S188S.

100. Nychas, G. J., V. M. Dillon, and R. G. Board. 1988. Glucose the key substrate in the microbi-

ological changes occurring in meat and certain meat products. Biotechnol Appl Biochem

10:203231.

101. Nychas, G.-J. E., E. H. Drosinos, and R. G. Board. 1998. Chemical changes in stored meat. In:

A. Davies and R. Board (Ed.) The Microbiology of Meat and Poultry (1st Ed.). pp. 288326.

Blackie Academic & Professional, New York.

102. Okolo, M. I. 1986. Bacterial drug resistance in meat animals: a review. Int J Zoonoses

13:14352.103. Palumbo, S. A. 1986. Is refrigeration enough to restrain food pathogens? J Food Prot

49:10031009.

104. Penney, N., C. J. Hagyard, and R. G. Bell. 1993. Extension of shelf-life of chilled sliced roast

beef by carbon dioxide packaging. Int J Food Sci Technol 28:181191.

105. Pestka, J. J. 1986. Fungi and mycotoxins in meats. In: A. M. Pearson and T. R. Dutson (Ed.)

Advances in Meat Research, Meat and Poultry Microbiology. pp. 277309. MacMillan, Bas-

ingstoke.

106. Phebus, R. K., A. L. Nutsch, D. E. Schafer, R. C. Wilson, M. J. Riemann, J. D. Leising, C. L.

Kastner, J. R. Wolf, and R. K. Prasai. 1997. Comparison of steam pasteurization and other

methods for reduction of pathogens on surfaces of freshly slaughtered beef. J Food Prot

60:476484.

107. Pociecha, J. Z., K. R. Smith, and G. J. Manderson. 1991. Incidence ofListeria monocytogenes

in meat production environments of a South Island (New Zealand) mutton slaughterhouse. Int

J Food Microbiol 13:321327.

108. Prasai, R. K., C. L. Kastner, P. B. Kenney, D. H. Kropf, D. Y. C. Fung, L. E. Mease, L. R.

Vogt, and D. E. Johnson. 1997. Microbiological quality of beef subprimals as affected by lac-

tic acid sprays applied at various points during vacuum storage. J Food Prot 60:795798.

109. Putnam, J. J., and L. A. Duewer. 1995. U.S. per capita food consumption: record-high meat

and sugars in 1994. Food Rev 18:211.

110. Reagan, J. O., G. R. Acuff, D. R. Buege, M. J. Buyck, J. S. Dickson, C. L. Kastner, J. L. Mars-

den, J. B. Morgan, R. Nickelson, II, and G. C. Smith. 1996. Trimming and washing of beef

carcasses as a method of improving the microbiological quality of meat. J Food Prot

59:751756.

111. Reichel, M. P., D. M. Phillips, R. Jones, and C. O. Gill. 1991. Assessment of the hygienic ad-

equacy of a commercial hot boning process for beef by a temperature function integration

technique. Int J Food Microbiol 14:2742.

112. Rogers, S. A., N. W. Hollywood, and G. E. Mitchell. 1992. The microbiological and techno-

logical properties of bruised beef. Meat Sci 32:43747.

113. Sachindra, N. M., P. Z. Sakhare, and D. N. Rao. 1998. Reduction in microbial load on buffalomeat by hot water dip treatment. Meat Sci 48:149157.

114. Samelis, J., F. Maurogenakis, and J. Metaxopoulos. 1994. Characterisation of lactic acid bac-

teria isolated from naturally fermented Greek dry salami. Int J Food Microbiol 23:179196.

115. Shelef, L. A. 1977. Effect of glucose on the bacterial spoilage of beef. J Food Sci

42:11721175.

116. Shelef, L. A. 1994. Antimicrobial effects of lactates: a review. J Food Prot 57:445450.



21/21

117. Sheridan, J. J. 1995. The role of indicator systems in HACCP operations. J Food Safety

15:157180.

118. Sheridan, J. J., A. M. Doherty, P. Allen, D. A. McDowell, I. S. Blair, and D. Harrington. 1997.

The effect of vacuum and modified atmosphere packaging on the shelf-life of lamb primals,

stored at different temperatures. Meat Sci 45:107117.

119. Siragusa, G. R., and C. N. Cutter. 1995. Microbial ATP bioluminescence as a means to detectcontamination on artificially contaminated beef carcass tissue. J Food Prot 58:764769.

120. Siragusa, G. R., and J. S. Dickson. 1992. Inhibition ofListeria monocytogenes on beef tissue

by application of organic acids immobilized in a calcium alginate gel. J Food Sci 57:293296.

121. Smith, J. L. 1993. Documented outbreaks of toxoplasmosis: Transmission of Toxoplasma

gondii to humans. J Food Prot 630639.

122. Smith, M. G., and K. R. Davey. 1990. Destruction ofEscherichia coli on sides of beef by a hot

water decontamination process. Food Australia 42:19598.

123. Smulders, F. J. M., and G. C. Greer. 1998. Integrating microbial decontamination with organic

acids in HACCP programs for muscle foods: prospects and controversies. Int J Food Micro-

biol 44:149169.124. Stanley, G., K. J. Shaw, and A. F. Egan. 1981. Volatile compounds associated with spoilage

of vacuum-packaged sliced luncheon meat byBrochothrix thermosphacta. Appl Environ Mi-

crobiol 41:816818.

125. Tornberg, E. 1996. Biophysical aspects of meat tenderness. Meat Sci 43:S175S191.

126. USDA. 1993. U.S. Department of Agriculture. Beef carcass trimming versus washing study:

Fiscal year 1993. Fed Regist 58:3392533932.

127. USDA. 1996. U.S. Department of Agriculture. Pathogen reduction; hazard analysis and criti-

cal control point (HACCP) system; Final rule. Fed Regist 61:3880538989.

128. Van Donkersgoed, J., G. Jewison, M. Mann, B. Cherry, B. Altwasser, R. Lower, K. Wiggins,

R. Dejonge, B. Thoriakson, and E. Moss. 1997. Canadian beef quality audit. Can Vet J38:217225.

129. Wolf, G., and W. P. Hammes. 1988. Effect of hematin on the activities of nitrite reductase and

catalase in lactobacilli. Arch Mikrobiol 149:220224.

130. Zottola, E. A. 1972. Introduction to Meat Microbiology. American Meat Institute, Chicago.

131. Zottola, E. A., and K. C. Sasahara. 1994. Microbial biofilms in food processing industry

should they be a concern? Int J Food Microbiol 23:12548.

7.microbiology of meats

Documents