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Journal o.fFood Protection, VoL 44, No.5, Pages 341-346 (May 1981) Copyright ©, International Association of Milk, Food, and Environmental Sanitarians

Effects of Nitrite and Sorbate on Bacterial Populations in Frankfurters and Thuringer Cervelat CATHERINE M. HALLERBACH and NORMAN N. POTTER" Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 Department ofFood Science, Cornell University, Ithaca, New York 14853

(Received for publication July 21, 1980)

ABSTRACT Quality Service ofthe USDA proposed to reduce the level Four batches of frankfurter emulsion were prepared with no of nitrite in to 40 ppm of sodium nitrite used with additives, 0.26o/o potassium sorbate, 140 ppm of sodium nitrite plus 550 ppm of sodium isoascorbate, and 40 ppm sodium 0.26 o/o of potassium sorbate (J). The anti-botulinal nitrite plus 0.26% potassium sorbate plus 550 ppm sodium activity of potassium sorbate used with lowered levels of isoascorbate, and processed. Five batches of thuringer cervelat nitrite has since been substantiated in a study conducted emulsion were prepared with no additives, 0.26% potassium by the FSQS (2). Bacon has received special attention sorbate, 156 ppm of sodium nitrite, 78 ppm of sodium nitrite because nitrosamines may be formed in small amounts plus 0.26% potassium sorbate, and 78 ppm of sodium nitrite when it is cooked to the crisp state; however, plus 156 ppm of sodium nitrate, and processed. The finished nitrosamines also have been found in other nitrite-cured products were stored aerobically and bacterial growth patterns meat products (6,12). were monitored. At 20 C, presence of sodium nitrite and Use of decreased levels of nitrite in cured meat potassium sorbate, separateiy or together, in the frankfurters products other than bacon has attracted interest, and were without appreciable effect on total aerobic, total nitrite-free products that depend upon refrigera­ anaerobic, gram-positive, and laetobacillus-pediococcus counts, although at 7 to 9 C these additives moderately lowered tion or freezing for microbiological safety are commer­ bacterial counts. Bacterial counts of the thuringer cervelat were cially available. Further, Skjelkvale and Tjaberg (27) not affected by sodium nitrite, potassium sorbate or sodium observed the microflora of made with and without nitrate at either temperature. Staphylococcus aureus and nitrite to be similar, and other workers have observed the Clostridium per.fringens were inoculated into all emulsions microflora of frankfurters, including selected pathogens, before further processing to determine if the modified cures, or to be little affected by the level or presence of nitrite possible changes in normal microflora, influenced these (4,20,26). With respect to sorbate, antibotulinal activity pathogens. S. aureus was reduced to below detectable levels in uncured, cooked and then inoculated sausage has after heat-processing in all systems. C. per.fringens survived been reported by Tompkin et al. (31) while inoculated processing and then underwent equally slow death in all stored Clostridium peifringens decreased rapidly with or frankfurter emulsions, and stabilization of counts in thuringer without sorbate. In the same study, surface-applied cervelat emulsions. Results indicate that the modified cures did not appreciably alter the natural microflora of these products, salmonellae were inhibited by sorbate while Staphylo· nor survival of added pathogens. coccus aureus was not. Sorbate is effective against a variety of molds, yeasts and bacteria but is said to only mildly inhibit growth of lactic acid bacteria (21). Yet lvey et a!. (16) demonstrated significant inhibition by Nitrite use in cured meat products has been under 0.26% potassium sorb ate of the lactobacillus population federal and public scrutiny since the 1950s, and the of bacon after 2 weeks of aerobic storage. Little is to be economic, health-related and political areas of contro­ found in the literature on effects of decreased levels of versy have been detailed in several recent reviews nitrite used with sorbate on the microflora of cured meat (6.14,25,29.32). products other than bacon. Potassium sorbate has received much attention as a The present study was undertaken to determine the potential nitrite substitute with anti-botulinal activity effects of nitrite levels and sorb ate on growth patterns of (16,31). Further, formation ofnitrosamines in meats such the normal microflora of frankfurters and fermented as bacon is diminished by the substitution of sorbate semi-dry thuringer cervelat. Since changes in normal (2.22). Therefore, in May of 1978, the Food Safety and microflora can influence contaminants of public health

JOURNAL OF FOOD PROTECTION, VOL. 44, MAY 1981 342 HALLERBACH AND POTTER

TABLE 1. Frankfurter and thuringer cervelat formulations.

Frankfurtera cervelatb Ingredient Weight (g) Lean 2270 Beef 2724 .S0/50 trim 2270 Pork trim 1616 Ice 1089.6 Salt 127.1 Water 726.4 Dextrose 90.8 Salt 145.4 Cane sugar 90.8 Corn syrup solids 107.6 Whole peppercorns 17.0 White pepper 18.2 Ground coriander 5.68 Ground coriander 10.9 Mustard seed 2.84 Ground nutmeg 7.3 Ground nutmeg 1.42 Liquid smoke 20 Ground allspice 1.42 a To this were added different levels of sodium nitrite, sodium isoascorbate and potassium sorb ate. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 bTo this were added Lactacel MC starter culture and different levels of sodium nitrite, sodium nitrate and potassium sorbate. concern, observations also were made on S. aureus and TABLE 2. Frankfurter and thuringer cervelat smokehouse C. peifringens added to the sausage emulsions before schedule. processing. Time at Dry bulb Wet bulb MATERIALS AND METHOllS temperature temperature temperature (C) (C) Formulation and processing ofmeat products 30min 60 43 The formulations of the frankfurters and thuringer cervelat are Frankfurter presented in Table l. Four separate batches of frankfurter emulsion 60min 82 63 were prepared (Treatment I, no additives; Treatment II. 0.26% Thuringer 20 ha 39 36 potassium sorbate; Treatment III, 140 ppm of sodium nitrite, 550 ppm cervelat 1.2h 71 49 of sodium isoascorbate; Treatment IV, 40 ppm of sodium nitrite. 0.26"7o potassium sorbate, 550 ppm of sodium isoascorbate). Five aA 1-h smoke treatment was applied after the 4th hour of separate batches ofthuringer cervelat were prepared (freatment I, no processing. additives; Treatment II, 0.26% potassium sorbate; Treatment III, 156 ppm of sodium nitrite; Treatment IV, 78 ppm of sodium nitrite. distilled water at low speed for 1 min in a laboratory Waring blender 0.26% potassium sorbate; Treatment V, 78 ppm of sodium nitrite, and pH was read on a Corning research pH meter. 156 ppm of sodium nitrate). The meat was coarsely ground from freshly Microbiological tests slaughtered animals. Sample storage. Each frankfurter link was individually wrapped in a To prepare the frankfurter emulsion, the beef. ice, half of the water and pre-mixed salt. corn syrup solids. spices and appropriate additives Glad plastic sandwich bag. For the thuringer cervelat, the ends of the were placed in a small silent chopper (Hobart Model 8181D) and sausage were removed and the remainder was cut into one inch slices. chopped for 4 min. The pork, remaining water and inocula of C. Each slice was stored in a Glad plastic sandwich bag. petj'ringens and S. aureus, to be described below, were added to the Normal microjlora studies. Total aerobic. total anaerobic, gram­ chopper and the chop was continued until a temperature of 14 C was positive, and lactobacillus-pediococcus counts were monitored at both reached. The emulsion was stuffed with a Buffalo stuffer into 22- to 7 to 9 C and 20 C. An 11-g sample of meat was blended with 99 ml of 25-mm colored cellulosic casings. The frankfurters were linked (Linker 0.1% peptone water diluent at low speed for 2 min in a laboratory Machines. Inc., Model 122 ACL #4937). hung on racks and placed in Waring blender. For the frankfurter. the meat was removed equitably the smokehouse. The smokehouse schedule is presented in Table 2. from the ends and the center of the link. For the thuringer cervelat. an When the frankfurters reached an internal temperature of 6 7 to 70 C, 11-g cross-section of meat. the length of the diameter of the slice, was removed. Samples of raw emulsion also were analyzed. The 1:10 they were hosed down with cold water for approximately S min. To prepare the thuringer cervelat. the beef. pork. preblended spices and dilutions were further serially diluted and plated in duplicate. Total additives were chopped for 40 sec in the silent chopper. Then the C. aerobic and total anaerobic plates were enumerated on APT agar petj'ringens and S. au reus inocula (described below) and 23.7 ml of a (Difco) (I 7). For the 7- to 9-C storage study, total aerobic and anaerobic diluted Lactacel MC starter culture (Lactobacillus plantarum and plates were incubated at 20 C for 4 days. For the 20-C storage study. Pediococcus cerevisiae) (Microlife Technics, Sarasota, Fla.) were added plates were incubated at 35 C for 48 h. Anaerobic conditions were to the mixture in the chopper and the chop was continued for 2 min. generated through the use of the Gas Pak Anaerobic System (5). The emulsion was stuffed into presoaked 64-mm diameter fibrous Gram-positive bacteria were estimated on Phenylethyl Alcohol Agar casings with the Buffalo stuffer. The were hung from racks (5). Phenylethyl Alcohol Agar plates were incubated at 30 C for 3 davs. and placed in the smokehouse. The smokehouse schedule followed is Meat lactobacilli and pediococci were estimated on LBS agar (8,J6,ifi). presented in Table 2. At the end of the smokehouse treatment, the LBS agar plates were incubated at 30 C for 4 days. thuringer cervelat had reached an internal temperature of 53 to 56 C. Observations on pathogens. Ten ml of an active sporulating culture They immediately received a cold shower for 5 min and then were of C. petj'ringens NCTC 8239. obtained by following the procedure of allowed to stand in open air until they reached room temperature Duncan and Strong (9). and 10 ml of a culture of S. aureus FRI 100 (approximately 4 h). at which time they were stored at 4 C overnight. (Food Research Institute. Univ. of Wisconsin) propagated in Brain Heart Infusion (Difco) for 24 hat 37 C were incorporated in the sausage Analytical tests emulsions as indicated above. C. perfringens populations were The AOAC procedures for fat and moisture were followed G). For monitored at 7 to 9 C and 20 C with enumeration on SFP agar base salt. the AOAC procedures for solution preparation and standardiza­ (Difco) made up and supplemented with cycloserine (11). Plates were tion were used with the method outlined by Kramlich et al. (19) for the poured and incubated anaerobically for 24 h at 35 C (11). Black salt titration. For meat pH, a lO-g sample was blended with 90 ml of colonies were recognized as C. petj'ringens. Attempts to monitor S.

JOURNAL OF FOOD PROTECTiON. VOL. 44. MAY 1981 NITRITE AND SORBATE IN SAUSAGES 343 aureus were with Baird-Parker Medium {11), using Baird-Parker Agar At 20 C, presence of sodium nitrite and potassium Base {Difco) and Egg Yolk Telluritc Enrichment (3). By this method, S. sorbate in the cure was without appreciable effect on the aureus colonies are recognized as black, shiny, convex and surrounded normal microflora, as seen in Fig. 5 and 6 for the aerobic by an opaque zone, then a clear zone {5,11). and anaerobic counts. The counts on the Phenylethyl RESULTS AND DISCUSSION Moisture, fat and salt levels Alcohol and Lactobacillus Selection Agars were very similar to the counts on the APT agars and are not Average values for all frankfurters (duplicate samples presented. of each treatment) were as follows: moisture, 58.13o/o The bacteriostatic action of nitrite and potassium (range: 57.19-59.12%); fat, 25.84% (range: 25.28- sorbate is pH-dependent. Sorbates are optimally effective 26.41 %); salt, 2.1% (range: 2.1-2.2%). Those for below pH 6.0 but will function up to pH 6.5 (21). The thuringer cervelat were: moisture, 55.22% (range: bacteriostatic action of nitrite increases in an acid 52.70-56.28%); fat, 17.20% (range: 16.40-18.28%); salt, environment (7). As seen in Table 4, the pH of the 2.6% (range: 2.6-2.7%). The compositions of the meat frankfurters was not highly acidic; therefore, the limited products are consistent with the reported compositions of similar type products (19). Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 Normal flora studies Frankfurters. Bacterial counts of the raw frankfurter emulsions are presented in Table 3. The microflora of the raw emulsions consisted largely of gram-positive microorganisms, as reflected by similar counts on the total aerobic, total anaerobic and Phenylethyl Alcohol Agar Plates. Gram-negative bacteria, common contami­ nants of raw meats (13), most likely comprised much of the remaining flora (23). The bacterial counts of the frankfurters stored at 7 to z rr: 9 C are presented in Fig. 1-4. The survivors of the heat L'] process were largely gram-positive organisms as again nc 0 reflected by the comparable counts on the total aerobic and anaerobic plates with the count on Phenylethyl l.'l 0 Alcohol Agar. The less heat-resistant gram-negative rods _j were killed since they do not survive the heat of properly processed frankfurters. Counts on the LBS agar were less than 10 1 (lower limit of detection) for all treatments except Treatment I (no additives), at 5 days of storage. By 10 days of storage, these counts had increased. The bacterial counts of the frankfurters processed with 0.26% potassium sorbate were moderately lower than those processed without 0.26% potassium sorbate. The IS: frankfurters prepared with 140 ppm of sodium nitrite TIME had moderately lower counts than those prepared with Figure 1. Total aerobic plate counts offrankfurters stored at no additives. Further, the frankfurters processed with 7 to 9 C (no additives Jt,._; 0.26% potassium sorbate Jt.---; 0.26% potassium sorbate and 40 ppm of sodium nitrite 140 ppm sodiuM nitrite, 550 ppm of sodium isoascorbate generally developed slightly lower counts than those •-: 40 ppm of sodium nitrite, 0.26% potassium sorbate, processed with only0.26o/opotassium sorbate. 550 ppm o_fsodium isoascorbate •---). TABLE 3. Bacterial counts offrankfurter and thuringer cervelat raw emulsions.

Plate Total Total Phenylethyl Meat Treatrnenta aerobic anaerobic alcohol selection agar

5 2 Frankfurter I 7.0 X 105 2.7 X 10 3.0 x to• 4.0 X 10 6 Frankfurter II 2.3 X 106 2.0 X 10 1.1 x to• 5.5 X 1()4 Frankfurter III 4.0 X 106 3.9 X 106 1.1 x to• 3.5 X 10~ Frankfurter IV 2.5 x to• 2.9 X 106 2.2 X 106 3.2 X 10~ 7 7 6 Thuringer cervelat I 5.5 X 107 6.7 X 10 2.9 X 10 7.6 X 10 7 Thuringer cervelat II 5.5 X 107 4.7 X 1Q7 2.2 X 10 1.4 X 1Q7 7 7 7 Thuringer cervelat III 5.1 X 107 5.2 X 10 1.4 X 10 1.7 X 10 7 7 7 Thuringer cervelat IV 5.9 X 107 4.6 X 10 1.2 X 10 1.4 X 10 7 7 7 v 4.9 X 107 5.5 X 10 2.0 X 10 1.2 X 10 asee MATERIALS AND METHODS. Formulation and processing of meat products.

JOURNAL OF FOOD PROTECTION. VOL. 44, MAY 1981 344 HALLERBACH AND POTTER

numbers between treatments was observed and the 91 populations remained in a stabilized state throughout the lengths of the storage study. The fermentation was 8+ not inhibited by the sodium nitrite, sodium nitrate or potassium sorbate, as seen from the pH data in Table 4. 7 These results agree with those of Skjelkvale and Tjaberg (27) and Zaika et al. (33). They found the microflora of l!l 5 produced with or without sodium U1 nitrite to be similar. ";;:: L~ The pH values of the stored thuringer cervelat in 2 5' Table 4 hardly changed with time, paralleling the a: insignificant change in bacterial numbers. While the a::I..:.J 0 '11 bacteriostatic action of nitrite increases in an acid

environment, the relatively tolerant nature of Pedio­ Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 I..:.J coccus sp. and Lactobacillus sp. to nitrite explains the 0 ...J 3 similar population curves in sausage prepared with and without nitrite. Further, the pH of the sausage is not the 2 • optimum for the effectiveness of potassium sorbate, which only mildly inhibits lactic acid bacteria. Noticeable changes in odor and general appearance occurred in all samples after 71 h at 20 Cor 18 days at 7 to 9 C. Changes included the development of an off-odor 0t~----~----~----~-----~----~ and slime formation on the surface of the thuringer 0 10 cervelat slices. In the samples prepared without TIME

JOURNAL OF FOOD PROTECTION. VOL.44. MAY 1981 NITRITE AND SORBATE IN SAUSAGES 345

which were not differently affected by the various nitrite-sorbate systems.

tt ACKNOWLEDGMENT The authors thank Dr. Donald H. Beermann, Department of Animal 7j Science, for his consultation and help in the preparation of the meat products. !.:J 5~ A~ REFERENCES "L11 2.: 1. Anon. 1978. News notes Washington. Food Techno!. 32(10):99. Ll1 2. Anon. 1979. News of the week. Chern. Engr. News 57(32):7. :z s a:: I \.II 3. A.O.A.C. 1975. Otlicial methods of analysis, 12th ed. Association ;_ .-" L~ // - ofOfticial Analytical Chemists, Inc., Washington, D.C. [t: -- -~- 0 lj 4. Bayne, H. G., and H. D. Michener. 1975. Growth of staphy­ lococcus and salmonella on frankfurters with and without sodium Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 L'l nitrite. Appl. Microbiol. 30:844-849. 0 5. BBL. 1968. BBL Manual, 5th ed. BBL Division of Becton, _J 3 Dickinson and Co., Maryland. 6. CAST. 1978. Nitrite in meat curing: Risks and benefits. Rept. No. 74, Iowa State Univ., Ames, Iowa. I 7. Castellani, A. G., and C. F. Niven, Jr. 1955. Factors affecting the bacteriostatic action of sodium nitrite. Appl. Microbio). 3:154-159. 8. Deibel, R. H., C. F. Niven, and G. D. Wilson. 1961. Microbiology of meat curing. III. Some microbiological and related technological aspects in the manufacture of fermented sausages. Appl. Microbiol. 9:156-161. 10 2S 9. Duncan, C. L. 1976. Clostridium perfringens. pp. 170-197. In M. P. Defigueiredo and D. F. Splittstoesser (eds.) Food micro· TIME

:1 /..'X:: .. "\ Observations on pathogens /,/ ..... " -1 ...... The S. aureus counts of the raw frankfurter and 7' ...../ 4 1"; thuringer cervelat emulsions ranged from 2.9 x 10 to 5.8 1_.)(. x 104 and were reduced in all systems to below detectable 1.!1 f 5 /1 1.11 levels by the heat, or the fermentation plus heat, of the ' I I ~ sausage-making processes. This concurs with observa­ 1.11 IJA tions on frankfurters by Palumbo et al. (24). Nor was 2 s I I a: I I there any evidence of subsequent recovery and growth of l'J 1!: I S. aureus in any system on storage. 0 y I The C. perjringens counts of all raw emulsions ranged I 3 4 l'J I from 5.6 x 10 to 4.3 x 10 and were not reduced by 0 I processing. At both 7 to 9 C and 20 C for periods up to 20 ..J 3 days and 74 h, respectively, slow death occurred in all frankfurter emulsions as evidenced by a gradual 1- to 2 2-log reduction in C. peifringens counts. Similar results were obtained by Hall and Angelotti (15), although Solberg and Elkind (30) demonstrated rapid growth of C. peifringens in frankfurters inoculated before the heat process and held after processing at abusive tempera­ 0+---t---1---+--t----+----t---r---1 tures. Upon storage at 7 to 9 C and 20 C for periods up to 0 !0 20 30 Yt1 S0 60 70 80 23 days and 96 h, respectively, stabilization of C. TIME

JOURNAL OF FOOD PROTECTION. VOL. 44, MAY 1981 346 HALLERBACH AND POTTER

TABLE 4. pH values of frankfurter and thuringer cervelat raw emulsions and stored products. Treatments a (£ Frankfurter system II III IV ./:_/ ...... "" Raw emulsion 6.0 5.9 6.0 6.1 // . / Stored frankfurters ;4 / 0 h 6.1 6.1 6.2 6.2 ~ I 20C 20.5 h 6.1 6.1 6.2 6.2 "U1 /I ~ f! 20C 36 h 5.9 6.0 6.0 6.0 U1 20 c 46 h 6.0 6.2 6.1 6.0 z I;/' 20C 60 h 5.9 5.9 5.9 6.1 [[ I I l'J 20C 74 h 5.8 5.9 6.1 6.0 n: I I 0 'I I 7-9C 5 days 6.0 6.0 6.2 6.2 I 7-9C 10 days 6.3 6.2 6.1 6.1 A I Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 ~ 7-9 c 15 days 6.2 6.1 6.2 6.2 0 I ...J 3 7-9 c 20 days 5.5 5.6 5.9 5.9 I • Thuringer cervelat Treatments a 2 System I II III IV v Raw emulsion 6.0 5.9 6.0 6.0 5.8 Stored thur. cerve. 0 h 4.5 4.5 4.6 4.5 4.4 20C 23 h 4.4 4.4 4.5 4.6 4.6 20C 47 h 4.3 4.4 4.6 4.6 4.5 0+---~---+----r---+-~~~--+ 20C 71h 4.3 4.5 4.4 4.5 4.5 0 10 30 50 70 83 20C 96 h 4.3 4.4 4.4 4.4 4.4 TIME < . ) 7-9 c 5 days 4.2 4.4 4.5 4.6 4.4 Figure 6. Total anaerobic plate counts offrankfurters stored 7-9 c 11 days 4.2 4.4 4.4 4.6 4.3 at 20 C (no additives &_; 0.26% potassium sorbate &·--; 7-9 c 18 days 4.3 4.4 4.3 4.4 4.3 140 ppm of sodium nitrite. 550 ppm of sodium isoascorbate 7-9 c 23 4.2 4.4 4.3 4.4 4.3 ._; 40 ppm of sodium nitrite, 0.26% potassium sorbate, a see MATERIALS AND METHODS - Formulation and 550 ppm ofsodium isoascorbate •---). processing of meat products.

11. FDA. 1976. Bacteriological analytical manual for food, 4th ed. :r -., Association of Official Analytical Chemists, Washington, D.C., !}:::.~L~~·-·...... a~p:...--·-<'"··~~ - .. '. pp. A-5, XI-2-XI-3. XV -3-XV-4. -~=------12. Fiddler, W., E. G. Piotrowski, J. W. Pensabene, R. C. Doerr, and I:J r-- .•. ,...... _ A. E. Wasserman. 1972. Effect of sodium nitrite concentration on Lil ~ ~ :L" N-nitrosodimethylamine formation in frankfurters. J. Food Sci. l!l 37:668-6 70. z 13. Frazier. W. C., and D. C. Westhoff. 1978. Food microbiology. [[ McGraw-Hill Book Co., New York, N.Y. L'J 'j fL 14. Gray. J. I., and C. J. Randall. 1979. The nitrite/n-nitrosamine CJ problem in meats: An update. J. Food Prot. 42:168-179. 15. Hall, H. E., and R. Angelotti. 1965. Clostridium perfringens in L'J 0 meat and meat products. Appl. Microbiol. 13:352-357. ..J 8 16. Ivey, F. J., K. J. Shaver, L. N. Christiansen, and R. B. Tompkin . 1978. Effect of potassium sorbate in toxigenesis of Clostridium botulinum in bacon. J. Food Prot. 41:621-625. 17. Johnston, R. W., and R. P. Elliott. 1976. Meat and poultry products. pp. 540-548. In M. L. Speck (ed.) Compendium of methods for the microbiological examination of foods. Amer. Public Health Assoc .. Washington. D.C. 18. Kantor. M. A., and N. N. Potter. 1975, Persistence of echovirus and poliovirus in fermented sausages. Effects of sodium nitrite and processing variables. J. Food Sci. 40:968-972. 19. Kramlich. W. E .. A. M. Pearson, and F. W. Tauber. 1973. TIME

12. Genigeorgis, C. 1978. Fermented sausage. Recent experiences. pp. enterotoxin production by staphylococci in . J. Food 21-35. In A. W. Brant (ed). Proc. Meat Processing Conference. Prot. 40:325-329. Department of Food Science and Technology, University of 22. Medwid, R. D., and D. W. Grant. 1980. Inactivation of staphy­ California, Davis. California. lococcal thermonuclease by an enzyme-like factor produced by 13. Genigeorgis, C., and J. K. Kuo. 1976. Recovery of staphylococcal Streptococcus faecalis subsp. liquefaciens. J. Food Prot. 43: enterotoxin from foods by affinity chromatography. Appl. 201-202. Microbiol. 31:274-279. 23. Minor, T. E., and E. H. Marth. 1976. Staphylococci and their 14. Genigeorgis, C., and H. Riemann. 1979. Food processing and significance in foods. Elsevier Pub!. Co., New York. hygiene. pp. 613-713. In H. Riemann and F. L Bryan, (eds). 24. Niskanen, A., and E. Nurmi. 1976. Effect of starter culture on Food-borne infections and intoxications, 2nd ed. Academic Press, staphylococcal enterotoxin and thermonuclease production in dry Inc., New York. sausage. Appl. Microbial. 31:11-20. 15. Genigeorgis, C., A. Nychas, and C. Loullis. 1977. Interaction of 25. Raccach, M., and R. C. Baker. 1979. Fermented mechanically Salmonella with food environments. Proc. 7th Inter. Symp. World deboned poultry meat and survival of Staphylococcus aureus. J. Assoc. Vet. Food Hygienists. 1:269-275. Food Prot. 42:214-217. 16. Haines. W. C., and L. G. Harmon. 1973. Effect of variations in 26. Raccach, M., R. C. Baker, J. M. Regenstein, and E. J. Mulnix. conditions of incubation upon inhibition of Staphylococcus aureus 1979. Potential application of microbial antagonism to extended

by Pediococcus cerevisiae and Streptococcus lactis. Appl. storage stability of a flesh type food. J. Food Sci. 44:43-46. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/44/5/341/1650311/0362-028x-44_5_341.pdf by guest on 02 October 2021 Microbiol. 25:169-172. 27. Silverman, S. J., A. R. Knort, and M. Howard. 1968. Rapid, 17. Haines, W. C., and L. G. Harmon. 1973. Effect of selected lactic sensitive assay for staphylococcal enterotoxin and comparison of acid bacteria on growth of Staphylococcus aureus and production serological methods. Appl. Microbiol. 16:1019-1023. of enterotoxin. Appl. Micro bioi. 25:436-441. 28. Tatini. S. R., B. R. Cords, and J. Gramoli. 1976. Screening for 18. Horwitz, W. (ed.) 1975. Official methods of analysis, 12th ed. staphylococcal enterotoxins in food. Food Techno!. 30(4):64-74. Association of Official Analytical Chemists, Washington, D.C. 29. Tatini, S. R., R. Y. Lee, W. A. McCall, and W. M. Hill. 1976. 19. Lachica, R. V. F., P .D. Hoeprich, and C. Genigeorgis. 1972. Meta­ Growth of Staphylococcus aureus and production of enterotoxins chromatic agar-diffusion microslide technique for detecting in . J. Food Sci. 41:223-225. staphylococcal nuclease in foods. Appl. Microbial. 23:168-169. 30. Yip, B., and C. Genigeorgis. 1980. Interactions of Clostridium 20. Lachica, R. V. F., P.O. Hoeprich, and H. P. Riemann. 1972. perfringens and certain curing factors in laboratory media. World Tolerance of staphylococcal thermonuclease to stress. Appl. Congress of Food-borne Infection and Intoxications. Berlin. p. 171. Microbiol. 23:994-997. (Abstr.) 21. Lee, I. C., L. G. Harmon, and J. F. Price. 1977. Growth and

Hallerbach and Potter, con't.fromp. 346

23. Palumbo. S. A., C. N. Huhtanen, and J. L. Smith. 1974. Micro­ Proceedings, SOS/70, Third international congress, food science biology of the frankfurter process: Salmonella and natural aerobic and technology. Inst. Food Techno!., Chicago, lJI. flora. Appl. Microbiol. 27:724-732. 29. Sofos, J. N .. F. F. Busta, and C. E. Allen. 1979. Botulism control 24. Palumbo, S. A., J. L. Smith. and J. C. Kissinger. 1977. by nitrite and sorbate in cured meats: A review. J. Food Prot. Destruction of Staphylococcus aureus during frankfurter process­ 42:739-770. ing. Appl. Environ. Microbiol. 34:740-744. 30. Solberg. M., and B. Elkind. 1970. Effect of processing and storage 25. Sebranek. J. G. 1979. Advances in technology of nitrite use and conditions on the microflora of Clostridium pelfringens-inoculated consideration of alternatives. Food Techno!. 33(7):58-62. frankfurters. J. Food Sci. 35:126-129. 26. Simon. S .. D. E. Ellis, B. B. MacDonald, D. G. Miller. R. C. 3!. Tompkin, R. B .. L. N. Christiansen. A. B. Shaparis, and H. Bolin. Waldman, and D. 0. Westerberg. 1973. Influence of nitrite and 1974. Effect of potassium sorbate on Salmonella, Staphylococcus nitrate curing ingredients on quality of packaged frankfurters. aureus. Clostridium perfringens and Clostridium botulinum in J. Food Sci. 38:919-923. cooked, uncured sausage. Appl. Microbiol. 28:262-264. 27. Skjelkvale, R .• and T. B. Tjaberg. 1974. Comparison of salami 32. Wasserman, A. E. 1978. The nitrite-nitrosamine situation: A sausage produced with and without sodium nitrite and sodium review. Food Engr. 50(9): 110-116. nitrate. J. Food Sci. 39:520-524. 33. Zaika. L. L., T. E. Zell, J. L. Smith, S. A. Palumbo. and J. C. 28. Smith. L. D. S. 1971. Factors affecting the growth of Clostridium Kissinger. 1976. The role of nitrite and nitrate in , perfringens. pp. 661-664. In G. F. Stewart and C. L. Willey (eds.) a fermented sausage. J. Food Sci. 41:1457-1460.

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