107

Journal of Food Protection, Vol. 48, No. 2, Pages 107-111 (February 1985) Copyright" International Association of Milk, Food, and Environmental Sanitarians

Beef Jerky: Fate of Staphylococcus aureus in Marinated and Corned Beef during Jerky Manufacture and 2.5 C Storage

RICHARD A. HOLLEY

Food Research Institute, Research Branch, Agriculture Canada, Ottawa, Ontario KIA 0C6, Canada Downloaded from http://meridian.allenpress.com/jfp/article-pdf/48/2/107/1656582/0362-028x-48_2_107.pdf by guest on 23 September 2021 (Received for publication April 25, 1984)

ABSTRACT MATERIALS AND METHODS

A domestic food dehydrator was used to prepare beef jerky Jerky preparation from inside round steak and corned beef brisket slices contami­ Beef jerky was made from fresh or cured beef purchased at retail outlets. In these experiments, inside round steak and vacuum packed nated with Staphylococcus aureus. The number of added corned beef brisket weighing about 500 g each were used. Meats were staphylococci doubled within 2 h after the start of drying corned defatted and placed at -20°C for 10 min before slicing. Samples were beef slices. About 3-3.5 h were required for corned beef and cut into 6.4-mm (0.25 inch) thick slices across the muscle fibers with between 1-2.5 h for inside round slices to reach an aw of 0.86. a meat slicer (Globe Slicing Machine Co. Inc., Stamford, CT). Slices Only 15% of all staphylococci initially present survived 8 h of inside round steak were held 12 h at 4°C in a "Great Jerky" of heated-drying, and this was reduced to 5% after a week of marinade which contained salt, garlic pepper, brown sugar, garlic salt, refrigerated storage of slices. The safety of beef jerky produced soy and Worchestershire sauces (3). Slices of corned beef brisket were in the home is assured when wholesome meats used in its prep­ held at 4°C for 12 h before drying but were not marinated. Strips of aration are rapidly dried. lean meat were placed in the circular (0.38-m diameter) trays of a Har­ vest Maid Dehydrator, (model FD-101, Alternative Pioneering Systems, Inc. Minneapolis, MN), in a single layer and dried. Temperature was set at 155°F for 4 h and reduced to 140°F for an additional 4-h period. The internal temperature of the dehydrator was monitored using a Fluke Jerky can be made from either sliced raw meat or fish model 2100A digital thermometer, (J. Fluke Mfg. Co. Inc., Seattle, which has been salted, spiced and may be smoked before Wash.), equipped with a copper-constantan type T precalibrated ther­ being dried (3). Beef jerky is classifiable as a fully dry mocouple. The temperature probe was placed at 12 sites on the drying trays at each machine operating temperature. shelf-stable product (7, 8). Historically, in North America beef jerky was a very Bacterial analyses important food commodity which substituted for fresh Meat samples (11.0 g) were taken at 2-h intervals, chopped to form beef in areas where dependable refrigeration was not 6-mm cubes, added to 99 ml of phosphate-sulfate buffer (6) and treated 15 s with a Polytron tissue homogenizer, (model PT-35, Kinematica available. Today, jerky is a popular snack meat among GmbH, Lucerne, Switzerland) and analyzed for viable bacteria as indi­ campers and hikers where food stability, protein content, cated below. light weight and expense are keys to dietary choice. Staphylococcus aureus ATCC 27661 was used to contaminate meat Snack sausages are also very popular among this group slices from inside round steak and corned beef brisket. After overnight but are higher in fat. storage of 500 g of marinated steak and 500 g of corned beef slices, meat was dipped into a 24-h-old nutrient broth culture of S. aureus Smith et al. (13) inoculated a non-fermented all beef containing 2.6 x 108 cells/ml. Slices were briefly blotted with paper snack sausage with Salmonella and Staphylococcus, towels, drained in a beaker and placed in 4 trays of the food dehyd­ C which was heated for 3.5 h at 51.1-52.2 C and dried for rator. The latter was operated in a laminar flow biohazard hood, (model 4 d at 21°C and 50-55% RH. At the end of this process, B6-MM-99-T2, Canadian Cabinets Co. Ltd., Montreal, P.Q.). The fol­ the product was not pathogen-free. No viable food- lowing day 500 g of uncontaminated meat was similarly dried. poisoning organisms were found in other sausages that Total bacteria were enumerated using plate count agar (PCA) incu­ bated at 32°C for 48 h; lactobacilli by incubation of MRS agar, 32°C, had been heated at an internal temperature of 53.9-55cC 48 h, anaerobic; coliforms by overlaid violet red bile agar, VRB, 32°C, or 57.8-58.9°C for 3.5 h and dried as above. 48 h; and staphylococci (pre-poured Baird-Parker agar, BP, 37°C, 48 Little technical information was available to assist in ti). One-ml samples were split into three approximately equal portions a safety evaluation of a commercial recommendation (3) and surface-spread on BP agar. Micrococci were counted on BP plates for the use of 4-h drying at 68°C (155°F) plus 4 h at as tellurite-reducing colonies with a typical coagulase-negative reaction. A portion of homogenized sample was heated for 15 min at 80°C and 60°C (140°F) for jerky preparation in the home. This analyzed for the presence of aerobic and anaerobic spores at 32°C study was undertaken to assess the safety of jerky prepa­ (PCA, 48 h). Plates for anaerobic incubation were placed inside either ration plus to examine the effect of brief refrigerated stor­ BBL or Oxoid anaerobic jars and BBL Gaspak C02-H2 generators were age upon surviving bacterial populations. used to create anaerobic conditions. All laboratory media for bacterial

JOURNAL OF FOOD PROTECTION, VOL. 48, FEBRUARY 1985 108 HOLLEY growth were obtained from Difco Laboratories, Detroit. Procedures used from 105/g to 103/g in control samples and these or­ for enumeration of bacteria were described by Speck (14) and all sam­ ganisms increased initially in numbers but declined after ples were analyzed in duplicate. 2 h (Figs. 1A and IB). Storage On staphylococci-inoculated inside round, (Fig. 2A), To check survival of microorganisms in dried beef, freshly made the reduction in total aerobic bacteria reached 80%. The samples of jerky with or without added staphylococci, were packed in aerobic bacterial population on inoculated corned beef sterile Whirl-Pak bags (B1020, Nasco, Guelph, Ont.) and placed in a brisket slices seemed to survive better, with about only domestic refrigerator at 2.5°C. Total numbers of bacteria, staphylococci, a 7% loss in viability during 8 h of drying (Fig. 2B). micrococci and water activity (aw) were monitored at 8 and 9 d follow­ ing manufacture. This improved viability did not appear to be due to the presence of the added staphylococci since, in both the Water activity inside round and corned beef, 85% of the staphylococci Samples for aw measurement were taken in duplicate, chopped to initially present were killed during the 8-h drying period form 6-mm cubes, placed in covered sample dishes and equilibrated (Figs. 2A and 2B). to 25±0.1°C. Measurement of aw was made with a Beckman VFB hyg- roline recorder (Beckman Instruments Inc., Cedar Grove, NJ) at 25°C. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/48/2/107/1656582/0362-028x-48_2_107.pdf by guest on 23 September 2021 Saturated aqueous slurries of K2Cr207, KC1, and NaCl were used as standards to represent water activities of 0.980, 0.843 and 0.753, re­ spectively (10).

RESULTS

Drying temperatures Commercial literature (3) advised that meat strips be dried at 155°F (68.3°C) for 4 h followed by 140°F (60°C) for another 4-h period. When measured, however, tem­ peratures inside the dehydrator at 12 loci were only 52.9±0.8°C (mean ±SD) when set at 68.3°C and were 48.2±0.4°C when set at 60°C. Although actual tempera­ tures were 15.4°C and 11.8°C lower than the desired high and low temperatures, the deviation from the mean tem­ perature was small among all test locations on the four trays. It was decided during these experiments to incorpo­ rate the temperature discrepancy of the machine set- pointer to fully represent the hazard to a consumer pre­ paring beef jerky in his home who would not have access to accurate temperature measuring devices. Meat drying experiments reported here were conducted using a 4-h drying period at 52.9±0.8°C (127.2°F) followed by an additional 4 h at 48.2±0.4°C (118.8°F).

Bacterial analyses An immediate decrease in coliform number was noted from the start of drying meat slices (Figs. 1 and 2). Sporeformers on both inside round and corned beef slices generally increased within the first 2 h of drying (Figs. 1 and 2) but those on uninoculated corned beef slices increased only after the initial 4-h drying period (Fig. IB). Total numbers of bacteria recoverable on PCA agar were reduced during drying of uninoculated beef slices longer than 4 h. Almost half the organisms present in­ itially on inside round slices and greater than 75% of the total organisms present on corned beef brisket were not recoverable following 8 h of drying (Fig. 1). Small numbers of staphylococci were noted (Fig. IB) Figure 1. Changes in viable bacteria on uninoculated slices of on the uninoculated corned beef slices (<60/g) but num- inside round beef steak and corned beef brisket during heated ers present on uninoculated inside round slices (Fig. 1A) drying to prepare jerky. Inside round steak slices, (A); corned were usually below the limit of detection (<10/g). Micro­ beef slices, (B); total aerobic bacteria, (O); micrococci, (•).' cocci were detected in these control samples as tellurite- aerobic (A) and anaerobic (J^) spores; staphylococci, (9); reducing, coagulase-negative, catalase- and gram-positive coliforms, (•). Values plotted below I on ordinate are esti­ cocci on BP agar. Their numbers during drying ranged mates (

JOURNAL OF FOOD PROTECTION. VOL. 48, FEBRUARY 1985 STAPHYLOCOCCUS AUREUS IN BEEF JERKY 109

mately 0.5 h between 3 and 7 h of drying (Fig. 3).

Changes in the rate of corned beef brisket aw drop were unaffected by exposure to the bacterial inoculum (Fig. 3), although the corned beef slices dried more slowly than corresponding treatments where inside round slices were

studied. An aw of 0.86 was reached in 1 h and 2.5 h in control and inoculated inside round slices, respec­ tively, whereas in control and inoculated corned beef slices 3.5 and 3 h, respectively, were required to reach

this aw. It is generally agreed that the limiting aw for growth of staphylococci is 0.85-0.86 (5, 11).

Storage

Refrigerated storage of both inoculated and control Downloaded from http://meridian.allenpress.com/jfp/article-pdf/48/2/107/1656582/0362-028x-48_2_107.pdf by guest on 23 September 2021 corned beef jerky in Whirl-Pak bags led to a slight in­

crease in aw (Table 1). During storage for either 8 or 9 d this increase was accompanied by decreases in the total numbers of bacteria which represented a 46 and 21% loss in viability of organisms present in uninoculated and inoculated samples, respectively. A significant de­ crease (84%) also occurred in the numbers of viable staphylococci on inoculated corned beef jerky stored for 9d.

The aw of beef jerky made from inside round steaks did not change substantially during refrigerated storage (Table 2); however, a reduction in viable numbers of bac­ teria was noted in both uninoculated (29%) and inocu­ lated (67%) slices. Staphylococci in inoculated stored slices decreased 63% while micrococci in uninoculated slices decreased 61%.

HOURS Figure 2. Changes in viable bacteria present on staphylococci- inoculated slices of inside round beef steak and corned beef brisket during heated drying to prepare jerky. Inside round steak slices, (A); corned beef slices, (B); total aerobic bacteria, CO); staphylococci, (%); aerobic (A) and anaerobic CA) spores; coliforms, (M). Values plotted below 1 on ordinate are estimates (<10/g).

Much greater numbers of staphylococci in the inocu­ lated samples obscured measurement of micrococci since BP agar had been used for enumeration of both genera (Fig. 2). Bacterial numbers on MRS medium were not substan­ tially different from those obtained using PCA. Since it was found that staphylococci were also recovered on this medium in addition to lactic bacteria, the results were HOURS of limited value and are not further reported. Even though meat slices were blotted and drained fol­ Figure 3. Changes in the aK of beef slices during jerky prepara­ lowing inoculation, addition of broth inoculum to the in­ tion with or without staphylococci inoculation. Slices of inside side round beef slices initially retarded the rate of meat round steak, control CO); staphylococci-inoculated (•)• Slices drying (as measured by decreases in aw) for up to 1 h. of corned beef brisket, control CD); staphylococci-inoculated The delay due to inoculation was shortened to approxi­ (M).

JOURNAL OF FOOD PROTECTION, VOL. 48, FEBRUARY 1985 110 HOLLEY

TABLE 1. Water activity and microflora changes in corned beef jerky during refrigerated storage with or without added staphylococci. Storage conditions'1 Bacterial numbers6 Water Staphy­ Micro­ Days Temp Inocc activity*1 Total lococci cocci 0.671 4.92 1.78 3.15 2.5°C 0.712 4.65 1.48 3.04

+ 0.685 7.71 6.08 <4.0 2.5°C + 0.710 7.61 5.28 <3.0 aFrom commercially prepared, retail corned beef brisket. bDried beef strips stored in Nasco Whirl-Pak bags. cBroth inoculum contained 2.6 X 108 cells of Staphylococcus aureus/m\.

d Downloaded from http://meridian.allenpress.com/jfp/article-pdf/48/2/107/1656582/0362-028x-48_2_107.pdf by guest on 23 September 2021 aw25°C. e Log10 bacteria/g meat. TABLE 2. Water activity and microflora changes in beef jerky" during refrigerated storage with or without added staphylococci. Storage conditionsb Bacterial numbers" Waterd Staphy­ Micro­ Days Temp. Inoc' activity Total lococci cocci 0.650 5.32 <1.0 4.74 2.5°C 0.676 5.18 <1.0 4.32

+ 0.684 6.26 6.08 <4.0 2.5°C + 0.679 5.77 5.64 <3.0 "From inside round steak. bDried beef strips stored in Nasco Whirl-Pak bags. cBroth inoculum contained 2.6 X 108 cells of Staphylococcus aureuslm\. d aw 25°C. e Log]0 bacteria/g meat.

Refrigerated storage further increased the lethality of staphylococci in inoculated slices had doubled after 2 h the drying process to staphylococci. In corned beef jerky of drying. S. aureus is not particularly resistant to heat and in uncured beef jerky after a week of storage there treatment (7, 9, 11), but the enterotoxins produced by was a loss in viability of staphylococci which represented this organism are largely unaffected by the heat process 97.6 and 95.3%, respectively, of those present at the start used in jerky manufacture (12). Although in both types of drying (Tables 1 and 2). of jerky, less than 15% of staphylococci initially present were still viable after 8 h of heated drying, the initial DISCUSSION increase seen in the numbers of these organisms in inocu­ While heated drying did not eliminate the high level lated corned beef brisket was of some concern. of added staphylococci or significantly reduce levels of Increases in total viable numbers of bacteria occurred sporeformers, the process did destroy viable coliforms in the other treatments during the first 2 h of drying al­ and most naturally occurring staphylococci (Fig. 1 and though the bacterial increase in inoculated corned beef 2). was mainly due to staphylococci growth. Had these re­ High initial numbers of staphylococci were added as sults (bacteria/g) been expressed in terms of dry weight, inocula to facilitate study of their survival and growth. these increases may have been reduced or eliminated These levels were not meant to represent the situation to since drying had the effect of increasing the proportion be found in properly handled meats commercially avail­ of meat solids (including bacteria) in samples. No adjust­ able. ment in samples was made for the decreased moisture A key to the successful preparation of jerky is use of content of meat during drying. heated-drying conditions under which meat will dry rap­ The refrigerated storage of jerky for 8-9 d in moisture-

idly to an aw low enough to prevent substantial microbial permeable bags led to significant additional reductions in activity. Among the bacteria of major public health con­ both total viable numbers and inoculated staphylococci.

cern, S. aureus can grow at the lowest aw (0.86), and These changes in viability occurred without substantial

can produce thermoresistant enterotoxins above an aw of change in aw (Tables 1 and 2) and reflect the situation 0.88 (2, 4, 12, 15). The most hazardous period in the likely to be encountered in the home-use of this product. preparation of jerky is therefore the initial interval when Only 4.7 and 2.4% of staphylococci present at the start

the meat aw is above 0.86. of drying were still viable after 8-9 d of refrigerated stor­ In corned beef brisket slices where 3-3.5 h were re­ age of inoculated beef jerky and corned beef jerky, re­

quired to reach an aw of 0.86, the numbers of spectively.

JOURNAL OF FOOD PROTECTION, VOL. 48, FEBRUARY 1985 STAPHYLOCOCCUS AUREUS IN BEEF JERKY 111

Jerky manufacture rapidly yielded slices of meat incap­ 5. Marshall, B.J., D.F. Ohye, and J.M.B. Christian. 1971. Tolerance able of supporting substantial growth by most naturally of bacteria to high concentrations of NaCl and glycerol in the growth medium. Appl. Microbiol. 21:363-364. occurring microorganisms by virtue of the speed of dry­ 6. Marth, E.H. (ed.). 1978. Standard methods for the examination ing. Concern is expressed that use of commercially cured of dairy products, 14th ed. Am. Pub. Health Assoc, Washington, meats which may retain moisture longer than freshly D.C. marinated meat slices could delay the initial drying pro­ 7. Minor, T.E., and E.H. Marth. 1972. Staphylococcus aureus and cess. Since the dehydrator used in the above experiments staphylococcal food intoxications. A review, III. Staphylococci in dairy foods. J. Milk Food Technol. 35:77-82. was tested at half its specified capacity, a further increase 8. Palumbo, S.A., and J.L. Smith. 1977. Chemical and microbiologi­ in the length of time required to reach a safe aw may cal changes during sausage fermentation and ripening. Am. Chem. occur when the machine is used at full load capacity. Soc. Symp., V. Washington 47:279-294. Additional work was conducted to examine the latter in­ 9. Raccach, M., and R.C. Baker. 1979. Fermented mechanically de- fluence and test other pathogens under these conditions. boned poultry meat and survival of Staphylococcus aureus. J. Food Results are presented in a subsequent report. Prot. 42:214-217. 10. Rodel, W., K. Krispien, and L. Leistner. 1979. Measuring the

water activity (aw-value) of meat and meat products. Fleis- Downloaded from http://meridian.allenpress.com/jfp/article-pdf/48/2/107/1656582/0362-028x-48_2_107.pdf by guest on 23 September 2021 ACKNOWLEDGMENTS chwirtschaft 59:849-851. 11. Smith, J.L., R.C. Benedict, and S.A. Palumbo. 1983. Relationship The author thanks Mr. G.E. Millard for valuable technical assistance of water activity to prevention of heat injury in Staphylococcus au­ and Madeleine McAllister of Ranier Doering and Associates, Nepean, reus. Lebensm.-Wiss. Technol. 16:195-197. Ontario K2J 1V8 for providing the domestic food dehydrator. Contribu­ 12. Smith, J.L., R.L. Buchanan, and S.A. Palumbo. 1983. Effect of tion No. 593, Food Research Institute, Agriculture Canada. food environment on staphyloccocal enterotoxin synthesis. A re­ view. J. Food Prot. 46:545-555. REFERENCES 13. Smith, J.L., C.N. Huhtanen, J.C. Kissinger, and S.A. Palumbo. 1977. Destruction of Salmonella and Staphylococcus during pro­ 1. Acton, J.C., and R.L. Dick. 1976. Composition of some commer­ cessing of a non-fermented snack sausage. J. Food Prot. 40:465- cial dry sausages. J. Food Sci. 41:971-972. 467. 2. Beuchat, L.R. 1981. Microbial stability as affected by water activ­ 14. Speck, M.L. (ed.). 1976. Compendium of methods for the micro­ ity. Cereal Foods World 26:345-349. biological examination of foods. Am. Pub. Health Assoc, 3. DeLong, D. 1979. Jerky, pp. 79-82 and 151-155. In How to dry Washington, D.C. foods. H.P. Books, Tucson, AZ. 15. Tatini, S.R. 1973. Influence of food environments on growth of 4. Genigeorgis, C.A. 1976. Quality control for fermented meats. J. Staphylococcus aureus and production of various enterotoxins. J. Am. Vet. Med. Assoc. 169:1220-1228. Milk Food Technol. 36:559-563.

JOURNAL OF FOOD PROTECTION, VOL. 48, FEBRUARY 1985