PROCESSED MEATS
Processed meats are those meat products that are cured, smoked, or cooked. The microbiota most often associated with these products is listed in Table 5–1. The behavior of processed meats stored under vacuum or modified atmospheres is discussed in Chapter 14.
Curing
Although curing was used in ancient times as a means of meat preservation, it is employed now more for flavor and color development. The classic meat cure ingredients are NaCl, nitrite or nitrate, and sugar (sucrose or glucose), with NaCl being the major ingredient. In addition to these, some products may contain curing adjuncts such as phosphates, sodium ascorbate or ery-thorbate, potassium sorbate, monosodium glutamate, hydrolyzed vegetable proteins, lactates, or spices.
In dry curing, no water is added to the NaCl, nitrite or nitrate, and sugar mixtures. In pickle curing, these ingredients are added to water to form a brine.
Salt serves to prevent microbial growth during and after curing, and up to 2.5% may be found in finished products. Nitrite or nitrate serves to stabilize red meat color, contribute to cured meat flavor, retard rancidity, and prevent the germination of clostridial spores. The isomers sodium ascorbate and erythorbate are used to stabilize color, to speed curing, and to make the cure more uniform. Since erythorbate is more stable than its isomer, its use is preferred, and it increases the yield of nitric oxide from nitrite and nitrous acid. At a level of 550 ppm, ascorbate or erythorbate reduces nitrosamine formation. Sugar is involved in at least three curing functions: color stabilization, flavoring, and substrate for lactic fermentation. Also, it moderates the harsh flavor of NaCl. Corn syrups, molasses, or honey may be substituted for flavor.
Phosphates are used in most pumped meats (bacon, ham, roast beef, pastrami, etc.) to increase water binding. In curing brines, sodium tripolyphosphate is most commonly used, but a mixture of tripolyphosphate and sodium hexametaphosphate is used widely. See Chapter 13 for information on polyphosphates as antimicrobial agents.
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Table 5–1 Genera of Bacteria and Fungi Most Frequently Found on Processed Meats
Bacteria Fungi
Gram Relative Relative
Genus Reaction Prevalence Genus Prevalence
Acinetobacter − X Yeasts
Aeromonas − X Candida X
Alcaligenes − X Debaryomyces XX
Bacillus + X Saccharomyces X
Brochothrix + X Trichosporon X
Carnobacterium + X Yarrowia X
Corynebacterium + X Molds
Enterobacter − X Alternaria X
Enterococcus + X Aspergillus XX
Hafnia + X Botrytis X
Kocuria + X Cladosporium X
Kurthia + X Fusarium X
Lactobacillus + XX Geotrichum X
Lactococcus + X Monilia X
Leuconostoc + X Mucor X
Listeria + X Penicillium XX
Microbacterium + X Rhizopus X
Micrococcus + X Scopulariopsis X
Moraxella − X Thamnidium X
Paenibacillus + X
Pediococcus + X
Pseudomonas − XX
Serratia − X
Staphylococcus + X
Vibrio − X
Weissella + X
Yersinia − X
Carnimonas − X
Clostridium + XX
Macrococcus + X
Shewanella − X
Note: X= known to occur; XX = most frequently reported.
Sausages (L. salsus, salted or preserved) constitute one of the major groups of cured meat products and they may be classified as follows:
1. fresh (patties, links)
2. uncooked smoked (mettwurst and Polish sausage) 3. cooked smoked (bologna and wieners)
4. cooked (liver sausage) 5. dry (Genoa salami, pepperoni) 6. semidry (Lebanon bologna, cervelat)
Processed Meats and Seafoods 103
Semidry sausages have a final pH around 4.7–5.0, and refrigeration is required. The final pH of dry sausages is about the same as that for semidry but these products are shelf stable because of their lower moisture content. The relative safety of these products is discussed below.
The common cured bacon in the United States is either dry or pickle cured, with the latter being the more common. Following cure, it may be smoked. Canadian bacon is characterized by being quite lean, since it comes from the large muscle of pork loins. Wiltshire bacon is prepared from the sides of selected hogs, followed by pumping of cure ingredients and subsequent storage in pickle brines.
Most hams in commerce are of the pickle-cure variety and they are cured following injection of the pickle cure by artery pumping, single-needle stitch, or multiple-needle stitch. For dry-cured or country-cured hams, the dry curing salts are applied by rubbing followed by storage at refrigerator temperatures for 28 to 50 days, depending on size and thickness.
All curing ingredients may be expected to contain microorganisms, and care should be taken to ensure that undesirable ones are not introduced to products during ingredient application.
Smoking
This process is applied to many cured meats, and the primary purposes of smoking meat are (1) de-velopment of aroma and flavor, (2) preservation, (3) creation of new products, (4) dede-velopment of color, (5) formation of a protective skin on emulsion-type sausages, and (6) protection from oxidation.73 Smoke, whether directly from wood or in liquid form, contains phenols, alcohol, organic acids, car-bonyls, hydrocarbons, and gases. The antimicrobial properties of smoking result from the activities of some of the smoke ingredients and the heat that is associated with wood smoking. Liquid smoke contains all of the essential ingredients of wood smoke, but it is free of the carcinogen benzopyrene.
SAUSAGE, BACON, BOLOGNA, AND RELATED PRODUCTS
In addition to the meat components, sausages and frankfurters have additional sources of organisms in the seasoning and formulation ingredients that are usually added in their production. Many spices and condiments have high microbial counts. The lactic acid bacteria and yeasts in some composition products are usually contributed by milk solids. In the case of pork sausage, natural casings have been shown to contain large numbers of bacteria. In their study of salt-packaged casings, Riha and Solberg76 found counts to range from log104.48 to log107.77 cfu/g and from log10 5.26 to log107.36 cfu/g for wet-packaged casings. Over 60% of the isolates from these natural casings consisted of Bacillus spp., followed by clostridia and pseudomonads. Of the individual ingredients of fresh pork sausage, casings have been shown to contribute the largest number of bacteria.76,88
Processed meats such as bologna and salami may be expected to reflect the sum of their ingredient makeup with regard to microbial numbers and types. The biota of frankfurters has been shown to consist largely of Gram-positive organisms with micrococci, bacilli, lactobacilli, microbacteria, enterococci, and leuconostocs along with yeast.24In a study of slime from frankfurters, these investigators found that 275 of 353 isolates were bacteria, and 78 were yeast. B. thermosphacta was the most conspicuous single isolate. With regard to the incidence of C. botulinum spores in liver sausage, 3 of 276 heated (75◦C for 20 minutes) and 2 of 276 unheated commercial preparations contained type A botulinal toxin.43 The most probable number (MPN) of botulinal spores in this product was estimated to be 0.15/kg.
Wiltshire bacon has been reported to have a total count generally in the range of log10 5–6/g,53 whereas high-salt vacuum-packaged bacon has been reported to have a generally lower count—about
104 Modern Food Microbiology
log104/g. The biota of vacuum-packaged sliced bacon consists largely of catalase-positive cocci, such as micrococci and coagulase-negative staphylococci, as well as catalase-negative bacteria of the lactic acid types, such as lactobacilli, leuconostocs, pediococci, and enterococci.3,13,59The biota in cooked salami has been found to consist mostly of lactobacilli.
So-called soul foods may be expected to contain large numbers of organisms, as they consist of offal parts that are in direct contact with the intestinal-tract biota, as well as other parts, such as pig feet and pig ears, that do not receive much care during slaughtering and processing. This was confirmed in a study by Stewart86 who found a geometric mean aerobic plate count (APC) of log10 7.92/g for chitterlings (pig intestines), log107.51/g for maws, and log107.32/g for liver pudding. For S. aureus, log10 numbers of 5.18, 5.70, and 5.15/g, respectively, were found for chitterlings, maws, and liver pudding.
Jerky is a dried shelf-stable product made from lightly salted and spiced slices of meat or fish—most often beef. When drying to reduce awto or below 0.86 is carried out within 3 hours, no problems are likely to result from pathogens, but when drying is not rapid and extends over a long period of time at temperatures<60◦C, S. aureus can survive.49 In 1993, beef jerky was the vehicle food in New Mexico for 93 cases of salmonellosis caused by three serovars—S. Montevideo, Kentucky, and Typhimurium.14 The product was produced in a commercial establishment, but it is unclear how it became contaminated. To reduce awto 0.86 during jerky processing, it has been found that a period of 2.5–3.0 hours of drying at 52.9◦C is needed.50 This is not lethal to foodborne pathogens, but it would make the product stable to the growth of Staphylococcus aureus in the case of post-processing contamination. For beef jerky, a period of 10 hours of drying at 60◦C has been shown capable of reducing E. coli 0157:H7, L. monocytogenes, and Salmonella serovar Typhimurium by log105.5–6.0 units.42 In an evaluation of homestyle dehydrators, it was found that in order to achieve a log10 5 reduction of E. coli 0157:H7, the following relation needed to be observed: about 20 hours of drying at 125◦F, about 12 hours at 135◦F, about 8 hours at 145◦F, or 4 hours at 155◦F.11This organism was more sensitive in meat with 5% fat than with 20%. For example, for jerky with 5% fat, a log 5 reduction could be achieved in about 8 hours at 125◦F (51.7◦C).
From 32,800 packages of frankfurters examined by the FDA in the United States, L. monocytogenes was recovered from 532 (1.6%) and about 90% of all isolates were serotype 1/2a.96In an extensive study of luncheon meats for L. monocytogenes in the states of Maryland and California, the organism was found in 82 of 9,199 or 0.89%.38
Spoilage
Spoilage of these products is generally of three types: sliminess, souring, and greening. Slimy spoilage occurs on the outside of casings, especially of frankfurters, and may be seen in its early stages as discrete colonies, which may later coalesce to form a uniform layer of gray slime. Yeasts, lactic acid bacteria of the genera Lactobacillus, Enterococcus, Weissella, and B. thermosphacta, may be isolated from the slimy material. W. viridescens produces both sliminess and greening. Slime formation is favored by a moist surface and is usually confined to the outer casing. Removal of this material with hot or warm water leaves the product essentially unchanged.
Souring generally takes place underneath the casing of these meats and results from the growth of lactobacilli, enterococci, and related organisms. The usual sources of these organisms to processed meats are milk solids. The souring results from the utilization of lactose and other sugars by the organisms and the production of acids. Sausage usually contains a more varied biota than most other processed meats due to the different seasoning agents employed, almost all of which contribute their
Processed Meats and Seafoods 105
own biota. B. thermosphacta has been found by many investigators to be the most predominant spoilage organism for sausage.
The changes that fresh meat bacteria bring about as processed meats undergo souring are unlikely to occur in the latter since many members of the fresh meat Gram-negative biota are unable to proliferate at the lower awand pH of processed meats. Even in fresh meats, definitive spoilage changes affecting structural proteins do not occur until APC is in the 109to 1010range54.
Although mold spoilage of these meats is not common, it can and does occur under favorable conditions. When the products are moist and stored under conditions of high humidity, they tend to undergo bacterial and yeast spoilage. Mold spoilage is likely to occur only when the surfaces become dry or when the products are stored under other conditions that do not favor bacteria or yeasts.
Two types of greening occur on stored and processed red meats: one caused by H2O2 and the other by H2S. The former occurs commonly on frankfurters as well as on other cured and vacuum-packaged meats. It generally appears after an anaerobically stored meat product is exposed to air.
Upon exposure to air, H2O2 forms and reacts with nitrosohemochrome to produce a greenish oxi-dized porphyrin.73H2O2may accumulate when heating if nitrite destroys catalase, and the peroxide reacts with meat pigments to form choleglobin, which is green. Greening also occurs from growth of causative organisms in the interior core, where the low oxidation–reduction (Eh) potential allows H2O2to accumulate. Weissella viridescens is the most common organism in this type of greening, but leuconostocs, Enterococcus faecium, and Enterococcus faecalis are capable of producing greening of products. Greening can also be produced by H2O2 producers such as Lactobacillus fructivorans and Lactobacillus jensenii. W. viridescens is resistant to >200 ppm NaNO2, and it can grow in the presence of 2–4% NaCl but not in 7%.73 W. viridescens has been recovered from anaerobically spoiled frankfurters and from both smoked pork loins and frankfurter sausage stored in atmospheres of CO2 and N2.8 In spite of the discoloration, the green product is not known to be harmful if eaten.
The second type of greening occurs generally on fresh red meats that are held at 1–5◦C and stored in gas-impermeable or vacuum-packaging containers; it is caused by H2S production. H2S reacts with myoglobin to form sulphmyoglobin (Table 5–2). This type of greening does not usually occur when meat pH is below 6.0. The organism responsible in one study was thought to be Pseudomonas mephitica71but in another study of DFD meats, S. putrefaciens was the H2producer.37 In the latter, greening occurred even with glucose present, and it could be prevented by lowering pH to below 6.0.
H2S-producing lactobacilli were recovered from vacuum-packaged fresh beef and found to produce H2S in the pH range of 5.4–6.5.81Only slight greening was produced, and the H2S was from cysteine, a system that was plasmid borne. The organism reached 3× 107/cm2 after 7 days, and ultimately reached about 108/cm2at 50◦C. No offness of vacuum-packaged sliced luncheon meat was observed when another lactobacillus attained 108/cm2.
At least one strain of Lactobacillus sakei has been shown to produce H2S on vacuum-packaged beef; and the effect of pH and glucose on production is presented in Table 5–3.26The investigators found that greening by L. sakei was not as intense as that caused by S. putrefaciens and that it occurred only after about 6 weeks at 0◦C. Further, the lactobacillus produced H2S only in the absence of O2
and utilizable sugars. No greening was observed when films with an O2 transmission rate of 1 ml O2/m2or 300 ml O2/m2were used, but it did occur with films that had O2transmission rates between 25 and 200 ml/m2/24 hours.26Visible greening was seen only on samples packaged in films with O2
transmission rates of 100 and 200 ml/m2/24 hours and only after 75 days’ storage. With meat in the pH 6.4–6.6 range, H2S was detected when cell numbers reached 108/g.
A yellow discoloration of vacuum-packaged luncheon-style meat was caused apparently by Ente-rococcus casseliflavus. The discoloration appeared as small spots on products stored at 4.4◦C, and
Table5–2PigmentsFoundinFresh,Cured,orCookedMeat StateofStateofStateof PigmentModeofFormationIronHaematinNucleusGlobinColor 1.MyoglobinReductionofmetmyoglobin;deoxygenation ofoxymyoglobinFe2+IntactNativePurplishred 2.OxymyoglobinOxygenationofmyoglobinFe2+IntactNativeBrightred 3.MetmyoglobinOxidationofmyoglobin,oxymyoglobinFe3+IntactNativeBrown 4.Nitricoxide myoglobinCombinationofmyoglobinwithnitricoxideFe3+IntactNativeBrightred 5.MetmyoglobinnitriteCombinationofmetmyoglobinwithexcess nitriteFe3+IntactNativeRed 6.Globin haemochromogenEffectofheat,denaturingagentson myoglobin,oxymyoglobin;irradiationof globinhaemichromogen Fe2+IntactDenaturedDullred 7.Globin haemichromogenEffectofheat,denaturingagentson myoglobin,oxymyoglobin,metmyoglobin, haemochromogen
Fe3+IntactDenaturedBrown 8.Nitricoxide haemochromogenEffectofheat,saltsonnitricoxidemyoglobinFe2+IntactDenaturedBrightred 9.SulphmyoglobinEffectofH2SandoxygenonmyoglobinFe3+IntactbutreducedDenaturedGreen 10.CholeglobinEffectofhydrogenperoxideonmyoglobinor oxymyoglobin;effectofascorbicorother reducingagentonoxymyoglobin
Fe2+orFe3+IntactbutreducedDenaturedGreen 11.VerdohaemEffectofreagentsasin9inexcessFe3+Porphyrinring openedDenaturedGreen 12.BilepigmentsEffectsofreagentsasin9inlargeexcessFeabsentPorphyrinring destroyed;chain ofporphyrins AbsentYellowor colorless Source:ReprintedwithpermissionfromR.A.Lawrie,MeatScience,copyrightc1966,PergamonPress.
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Processed Meats and Seafoods 107
Table 5–3 Effect of Meat pH and Glucose on Hydrogen Sulfide Production by a Pure Culture of Lactobacillus sakei L13 Growing under Anaerobic Conditions at 5◦C on Beef
Hydrogen Sulfide Production
pH 6.4–6.6 with 250µg Days pH 5.6–5.7 pH 6.4–6.6 Glucose per Gram of Meat
8 −∗ − −
9 − +‡ −
11 − + −
15 − + −
18 +† + +‡
21 + + +
∗Each treatment done in triplicate.− = All three tubes negative; + = all three positive.
†One tube out of three positive.
‡Two tubes out of three positive.
Source: Egan et al.26
it was fluorescent under long-wave ultraviolet light.10 Between 3 and 4 weeks were required for the condition to develop, and the responsible organism survived 71.1◦C for 20 minutes but not 30 minutes. In addition to 4.4◦C, it occurred also at 10◦C but not at 20◦C or above. Although tentatively identified as E. casseliflavus, the causative organism did not react with Group D antisera. The other yellow-pigmented enterococcal species is E. mundtii; and both are discussed further in Chapter 20.
A summary of several spoilage conditions of processed meats is presented in Table 5–4.
Table 5–4 Summary of Some Microbial Spoilage Conditions of Processed Meats
Condition Products Affected Etiology Reference
Greening Reference vacuum-packaged bologna
C. viridans 48
Greening Vacuum-packaged beef L. sakei 26
Greening Fresh red meats P. mephitica, S. putrefaciens 41, 71
Greening DFD meats S. purefaciens 37
Greening/sliminess Wieners, bologna W. viridescens Many
Yellowing Vacuum-packaged luncheon meats
E. casseliflavus 101
Black spot Cured meats C. nigrificans 36
Souring Sausage B. thermosphacta 66
“Blown pack” Vacuum-packaged meats C. frigidicarnis, C. gasigenes 9, 10 General spoilage Vacuum-packaged meats L. algidus; L. fuchuensis 57, 79
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BACON AND CURED HAMS
The nature of these products and the procedures employed in preparing certain ones, such as smoking and brining, make them relatively insusceptible to spoilage by most bacteria. The most common form of bacon spoilage is moldiness, which may be due to Aspergillus, Alternaria, Fusarium, Mucor, Rhizopus, Botrytis, Penicillium, and other molds (Table 5–1). The high fat content and low awmake it somewhat ideal for this type of spoilage. Bacteria of the genera Enterococcus, Lactobacillus, and Micrococcus are capable of growing well on certain types of bacon such as Wiltshire, and E. faecalis is often present on several types. Vacuum-packaged bacon tends to undergo souring due primarily to micrococci and lactobacilli. Vacuum-packed, low-salt bacon stored above 20◦C may be spoiled by staphylococci.92
Cured hams undergo a type of spoilage different from that of fresh or smoked hams. This is due primarily to the fact that curing solutions pumped into the hams contain sugars that are fermented by the natural biota of the ham and also by those organisms pumped into the product in the curing solution, such as lactobacilli. The sugars are fermented to produce conditions referred to as “sours” of various types, depending on their location within the ham. A large number of genera of bacteria have been implicated as the cause of ham sours, among which are Acinetobacter, Bacillus, Pseudomonas, Lactobacillus, Proteus, Micrococcus, and Clostridium. Gassiness is not unknown to occur in cured hams where members of the genus Clostridium have been found.
In their study of vacuum-packed sliced bacon, Cavett13 and Tonge et al.92 found that when high-salt bacon was held at 20◦C for 22 days, the catalase-positive cocci dominated the biota, whereas at 30◦C the coagulase-negative staphylococci became dominant. In the case of low-salt bacon (5–7%
NaCl versus 8–12% in high-salt bacon) held at 20◦C, the micrococci as well as E. faecalis became dominant; at 30◦C the coagulase-negative staphylococci as well as E. faecalis and micrococci became dominant. In a study of Iberian dry-cured hams, over 97% of the isolates were staphylococci with the four predominant species being S. equorum, S. xylosus, S. saprophyticus, and S. cohnii.77Interestingly, one S. xylosus isolate hybridized with a DNA probe for staphylococcal enterotoxins C and D, but the investigators noted that probe-positive isolates do not always produce enterotoxins.
In a study of lean Wiltshire bacon stored aerobically at 5◦C for 35 days or 10◦C for 21 days, Gardner35found that nitrates were reduced to nitrites when the microbial load reached about 109/g.
The predominant organisms at this stage were micrococci, vibrios, and the yeast genera Candida and Torulopsis. Upon longer storage, microbial counts reached about 1010/g with the disappearance of nitrites. At this stage, Acinetobacter, Alcaligenes, and Arthrobacter-Corynebacterium spp. became more important. Micrococci were always found, whereas vibrios were found in all bacons with salt contents>4%. In a study of Italian dry fermented sausages, the most frequently isolated staphylococci were S. xylosus followed by S. saprophyticus, S. aureus, and S. sciuri.34S. xylosus appears to be the most frequently isolated from several Italian dry sausages. In Iberian dry cured hams, the two predominant organisms in the ripening process are Staphylococcus equorum and S. xylosus, and both are believed to contribute to product flavor.
Safety
Overall, fermented meat products have a long history of safety throughout the world. This is not to imply that they are never the vehicles of foodborne illness outbreaks, but when such incidents have occurred they have been sporadic. Several outbreaks of illness occurred in the United States in the 1990s involving fermented meat products as vehicles. As a consequence, the USDA mandated a log10