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Jounu:tl ofFood Protection, Vol. 45, No.6, Pages527·532 (,4pril1982) Copyright©, International Association of Milk, Food, and Environmental Sanitarians

Microbiological Characteristics of Tongues and Livers as Affected by Temperature-Abuse and Packaging Systems C. A. ROmENBERGl, B. W. BERRY2* and J. L. OBLINGER3 Science Research Laboratory, S&E, ARS, USDA, Beltsville, Maryland20705. Department ofAnimal Sciences, University ofMaryland,

College Park, Maryland, 20742, and Food Science and Human Nutrition Department, University ofFlorida, Gainesville, Florida 32611 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/6/527/1654972/0362-028x-45_6_527.pdf by guest on 29 September 2021

(Received for publication August 10,1981)

ABSTRACT livers is predominantly on the surfaces and freezing does not change the spoilage characteristics (6). Beef livers Effects of various handling, packaging, temperature-abuse were found organoleptically unacceptable after 7-10 days and storage conditions were determined on the microbiological of storage at 5°C (8,15). This was probably due to a characteristics of beef livers and tongues. These organs were souring-type spoilage and bacterial levels of 7.2-7.8 x 10 7 evaluated: (a) initially following slaughter, (b) immediately organisms/g. Variety produced with a minimum following the frozen storage period of 2-4 weeks at -29°C and (c) following a simulated shipping-temperature abuse of 24 h at of handling (12), and thus having a relatively low initial 4 2 22-28°C followed by 13 days of storage at -1 ± O.SOC. Initial number of microbes (10 organisms/cm ), can be stored counts (log/cm2) of coliforms, coagulase-positive Staphylo· 1-2 weeks longer under vacuum packaged conditions coccus aureus and Clostridium perfringens ranged from than when microbe levels were higher (105.106 organ­ 0.19-1.37. Generally, neither freezing nor temperature-abuse isms/cm2). had a significant effect on these microorganisms. Vacuum­ Additional research is necessary to determine the packaged beef tongues and livers, generally, had lower effects that standard processing, packaging and transit bacterial counts than did either naked or polyvinyl chloride procedures have on the microbiological and shelflife film-wrapped products. Generally, it was observed that abusive characteristics of variety meats. The purpose of this storage temperatures, in conjunction with the naked and study was to determine quantitative and qualitative film-wrapped packaging systems, appear to present potential changes in microorganisms on variety meats as a result of microbial spoilage problems when compared with vacuum packaging. various packaging systems and simulated temperature­ abuse conditions.

The United States currently exports approximately MATERIALS AND METHODS 190,000 tons of variety meats (worth 110 million dollars) annually to Europe. This market is a valuable outlet for Sample aquisition U.S. variety meats since their consumption is very limited Beef tongues and livers from freshly slaughtered and dressed cattle in the United States. However, there are several problems were selected and purchased at two slaughtering plants. At plants I and II (Treuth and Sons. Ellicott City, MD), sampling occurred both in (12) accompanying the export of U.S. variety meats to mid-summer (Plant I) and mid-winter (Plant II). At Plant III (Shen Europe; these include: (a) failure to adhere to product Valley Meat Packers, Timberville, VA), sampling occurred only in quality standards and specifications, (b) inappropriate mid-winter. At the plants, the variety meats were individually wrapped processing, chilling and freezing procedures, (c) un­ in plastic bags and placed in cardboard boxes immediately following controlled systems of product assembly for export by evisceration and washing. Samples were brought back to the Meat Science Research Laboratory, USDA, Beltsville, MD. Twenty seven of brokers and (d) deterioration of product and packaging the 75 beef samples and 25 of the 73 samples from during transit. both plants were analyzed by surface swabbing immediately upon Only limited information on microbial and organolep­ arrival to determine initial microbiological numbers. Samples were 6 to tic spoilage patterns of variety meats has appeared in the 8 h post-evisceration upon arrival at Beltsville, MD. Between slaughter literature. Microbiological contamination on porcine and sampling, the samples were held between 6 and l7°C. Following sampling. all of the variety meat samples were placed in a cooler at 3°C and held overnight. The following day, 36 of the samples which were 'Department of Animal Sciences (Cooperative Agreement No. 12·14· not initially sampled were divided into the various abuse treatment· 1001-238). packaging systems. The remaining samples were frozen and served as 'lvfeat Science Research Laboratory. non-temperature-abused controls at the conclusion of the temperature­ 3Food Science and Human Nutrition Departmelll. abuse.

JOURNAL OF FOOD PROTECTION, VOL. 45, APRIL 1982 528 ROTHENBERG, BERRY AND OBLINGER

Three separate packaging systems were used: (a) vacuum packaging concurrently with the microbial samples. Sample> were also removed in Cryovac B 620, polyvinylidene bags (W. R. Grace and Co., Duncan, for analysis following the temperature-abuse and control treatments. SC), with evacuation in a Multivac, (model #3696-24, type A 6500) Simulated shipping and temperature-abuse vacuum packager (b) wrapping in a single layer of polyvinyl chloride (PVC) film (Alcoa), so as to exclude as much air as possible or (c) a Boxes containing variety meats were removed from frozen storage naked (no wrapping material) product. The packaging materials had and placed on a 122 em x 102 em plastic shipping pallet in three layers. the following permeability characteristics, polyvinylidene chloride bag: Each layer consisted of six boxes. The pallet contained 18 boxes in total. Regions on the pallet not occupied by variety meat sample boxes Oxygen Transmission Rate (OTR) = 35 cc/m2 /24 h/atm, Moisture Transmission Rate (MVTR) = 7.6 g/m2 /24 h, PVC film: OTR = 15,200 were substituted with boxes containing 40-lb. ice blocks enclosed in polyethylene bags. The pallet was placed outside of the laboratory in a cc/m2/24 h/23°C; MVTR = 380 g/m2/24 h/23°C. All samples were wrapped or packaged individually. Packaged variety meats were then shaded area for 24 h where ambient temperature ranged from 22-28°C. placed into 52 em x 40 em x 15 em boxes with polyethylene liners. Beef This procedure simulated conditions variety meats might go through during assembly and loading into the cargo hold of a ship (9). During tongues were packed six per box and beef livers were packed two per winter months, pallets were assembled inside a building where the box. The boxes were then placed in a freezer at -29°C ± 2°C where they were held 2-4 weeks before the onset of the simulated shipping­ ambient temperature was artificially maintained at 22-28°C. Following temperature abuse. this simulated temperature abuse, the pallet was transferred into a cooler for 13 days where the temperature was maintained at -1.0 ±

Sampling procedure O.SOC. This procedure simulated the time-span the product would be in Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/6/527/1654972/0362-028x-45_6_527.pdf by guest on 29 September 2021 A sterile, dacron-tipped swab, moistened in 0.1% sterile peptone the cargo hold of a ship during overseas transport from ports in the (Difco) diluent was used to remove bacteria from 12.3 cm2 of the Gulf of Mexico in the United States to ports in Europe. At the end of surface, according to the procedures of Lazarus et a!. (10). Three this period, samples were reassessed for microbiological characteristics. separate 12.3 cm2 areas were swabbed with individual sterile swabs. An additional set of samples was removed from frozen storage at the The three swabs were placed into 10 ml of 0.1% peptone diluent and time of the termination of the shipping and temperature-abuse. These appropriate serial dilutions were made. samples did not receive the temperature-abuse and were used as controls to determine the effects of the frozen storage, without Salmonella detection temperature-abuse, on microbiological numbers. Beef tongues and The presence of Salmonella was assessed according to the procedures livers were held 24 hat -1.0 ± 0.5 C for thawing and then analyzed for of Poelma and Silliker (14). Other microbiological procedures are microbiological numbers. This 24-h thawing period was necessary for outlined and summarized in Table 1. minimal surface thawing required for swabbing of surfaces. Determination ofpH values Statistical analysis The pH determinations were made according to the procedures of Analysis of variance (16) was used to test the effect of temperature­ Cia and Marsh (2). These samples were taken from the product abuse, packaging treatment, variation in plant procedures and all

TABLE 1. Microbiological procedures.

Determination Medium Plating Incubation Confirmatory Technique Tests

1) Aerobic Plate Count Plate Count Agar Pour Plate 35 C for 48 hr (35 C) 2) Aerobic Plate Count Plate Count Agar Pour Plate 20 C for 5 days (20C) 3) Aerobic Plate Count Plate Count Agar Pour Plate 7 C for 10 days (7 C) 4) Coliform Count Violet Red Bile Agar Pour Plate 35 C for 24 hr Growth and gas with overlay evolution in Brilliant Green Bile Broth within 48 hr at 35 C 5) Coagulase-positive Three-tube MPN in Positive tubes 35 C for 48 hr each Coagulase test Staphylococcus au reus trypticase soy broth streaked onto with 10o/oNaCl Baird-Parker agar 6) Clostridium perfringens TSC Agar Spread Plate 35 C for42 hr Growth and gas evolution with overlay in fluid thioglycollate, nonmotility, nitrite and gelatinase test 7) KF Streptococcal count KF Streptococcus Agar Pour Plate 35 C for48 hr 8) Anaerobic Count Plate Count Agar Pour Plate 35 C for48 hr (anaerobic conditions pro­ duced by BBL Gaspak System) 9) Yeast and Mold Count Plate Count Agar with Pour Plate 20 C for 5 days 100 ppm chlortetracycline HCL and 100 ppm chlor- amphenicol 10) Total Entero­ Violet Red Bile Agar Pour Plate with 35 C for 24 hr bacteriaceae Count with 1 o/o glucose overlay

JOURNAL OF FOOD PROTECTION, VOL. 45, APRIL 1982 TABLE 2. Microbial counts on beeftongues before and after specified handling and storage conditions.

countsa/cm2 Coagulase-positive a Handling and storage ~ Staphylococcus Clostridium s:: conditions 3SC APCb 20CAPC 7CAPC au reus Coliform pet:fringens KF Streptococcal Anaerobic Yeast& Mold n""' ~ ~ INITIAL 4.20gh 3.61g 2.32h O.S4f 0.65f 0.39f 2.91f 3.65gh 1.17g t:D s;; 0 ~ ABUS£C 0 § tl Vacuum packaging 3.56h 4.08g 3.11g 0.27f 0.41f O.OOf 1.56f 3.34g 0.89g .....: 0 ;g Film wrapping. (PVC)e 4.97fg 6.03f 5.94f o.sor 0.44f O.OOf 1.78f 3.87fg 2.22f 'Tl 0 t:D Naked (no wrapping material) 5.43f 5.82f 5.81f 0.42f 0.78f o.oor 2.12f 4.46f 2.69f m ~ m (") 'Tl ~ CONTROLd 0 d Vacuum packaging 3.58gh 3.38g 1.99h 0.44f 0.16f 0.00[ l.69f 2.85g 1.24g z :<: 0 < Film wrapping. (PVC) 3.17h 3.54g 2.33h O.OOf 0.20f o.oor 1.60f 2.59g 1.06g c 0 m r Naked (no wrapping material) 3.44h 3.59g 2.53h 0.56f 0.17f o.oor 2.11f 3.15g 1.25g V> y. >z n = 25 tongues for initial, 12 for abuse and 4 for control conditions. 1:1 > 2 acounts = loglo/cm • I:: ~ b APC =Aerobic plate count. m< r :;o:l ..... CTwo-four weeks storage at -29 C. followed by a simulated shipping-temperature abuse of24 hat 22-28 C, followed by 13 days V> ~ storage at -1 0.5 C. dTwo-four weeks storage at -29 C. ~PVC =Polyvinyl chloride. fghMeans in the same column with different letters are significantly different at P<0.05.

Vl

N

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relevant interactions. When the analysis of variance revealed a well (4). Thus it is likely that these organisms grew faster significant (P

on the abused vacuum-packaged product were also Oog 1J, which was approximately one and one-half to two significantly (P

JOURNAL OF FOOD PROTECTION. VOL. 45, APRIL 1982 TABLE 3. Microbial counts on beeflivers before and after specified handling and storage conditions.

Microbiological counts a /cm2 a Coagulase-positive Handling and storage Total Staphylococcus Clostridium S!:: ~ conditions JSC APCb 20CAPC Enterobacteriaceae au reus Coliform perfringens KF Streptococcal Anaerobic Yeast& Mold n -::0 0 ~ INITIAL 3.69f 3.58g 0.30f 0.19g 0.9Sf L37f 4.00f 3.47f O.Slh t:c ~ 0 ~ 8 § ABUSF::c 0 Vacuum packaging 4.14f 3.90g 2.52f 3.76f 1.14h -< 0.4H 1.29f 0.63f O.lOg 0 ;g Film wrapping, (PVC)C 4.40f 4.54f 0.70f 1.64f 0.54f 0.06g 3.23f 4.2Sf 2.36fg 'T1 0 4.3H 3.10f t:c Naked (no wrapping material) 4.96f 4.93f 0.69f 1.79f 0.37f O.OOg 3.96f tTl t;i tTl (j 'T1 :::! ....., 0 CONTROLd 0 2.79f 3.42f 1.6Sgh z :<: Vacuum packaging 3.97f 3.64g O.OOf 1.34f 0.2Sf 0.3Sg 0 1.76f 2.76f 0.7lh c:: Film wrapping, (PVC) 3.54f 3.57g O.OOf 1.34f O.OOf O.OOg tTl ~ 2.54fg Vl r Naked (no wrapping material) 4.41f 3.83g O.OOf 1.30f 0.63f O.OOg 2.98f 3.96f z> Y'""' n 271ivers for initial, 12 for abuse and 4 control conditions. 1:1 > 2 acounts log10/ cm • c ;g < F b APC Aerobic plate count. tTl ...... ::0 CTwo-four weeks storage at -29 C, followed by a simulated shipping-temperature abuse of24 hat 22-28 C, followed 13 days storage Vl ~ "' at-1 ±O.OSC. dTwo-fourweeks storage at -29 C. epvc Polyvinyl chloride. fghMeans in the same column with different letters are significantly different at P

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TABLE 4. Aerobic plate counts at 7 C far beef livers practices. Since gram-negative organisms are susceptible according to the interaction ofplant with packaging treatment. to freezing (5), frozen storage temperatures encountered by the product could also account for the low numbers of Packaging, handling, Aerobic plate and storage conditions count at 7 ca coliforms recovered. C. perfringens was also found on fresh liver surfaces in Initial small numbers. No significant (P>0.05) differences were Plant I 2.38 seen between any of the treatments for the KF Plant II 2.70 Streptococcal and anaerobic counts. Mean KF Strepto­ Plant III 2 1.60 coccal counts (cm ) on fresh beef liver were 4.00 (log 1o). Some contamination during the evisceration process Abused (vacuum packagcd)b seems likely since enterococci generally inhabit the Plant I 2.71 intestinal contents of animals. Enterococci are relatively Plant II 3.43 resistant to freezing (J), which could probably allow large Plant III 2.05 numbers to remain after the frozen storage periods. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/45/6/527/1654972/0362-028x-45_6_527.pdf by guest on 29 September 2021 A bused (film wrapped)b Anaerobic counts did not differ between any of the Plant I 3.12 treatments. Results for yeast and mold counts on beef Plant II 4.04 livers are consistent with those observed on beef tongues. Plant III 4.06 The highest counts were found on naked product following abuse. Abused (naked)b Salmonella detection Plant I 4.32 Plant II 5.08 Salmonella was not recovered from the surfaces of any Plant III 4.49 of the beef tongues and livers sampled in this study. pH Values Control (vacuum packaged)c Plant I 3.72 The pH values for beef tongues examined ranged from Plant II 3.11 a mean value of 5.8 on fresh product to 5.9 on abused Plant III 0.57 samples. Beef tongues in the control treatment had a pH of 6.1. The pH offresh beef livers was 6.1 as opposed to Control (ftlm wrapped)c 5.9 for the abused samples and 6.0 for the controls. Plant I 3.10 These differences between packaging and handling Plant II 2.18 systems were nonsignificant (P>0.05). Plant III 2.08 In conclusion, if frozen beef tongues and livers are subjected to a temperature-abuse similar to that of this Control (naked)c study, vacuum packaging should allow for the least Plant I 3.75 microbial proliferation. Plant II 2.85 Plant III 1.45 acount logl0/cm2 bTwo-four weeks storage at -29 C. followed by a simulated ACKNOWLEDGMENTS shipping-temperature abuse of24 hat 22-28 C. followed by 13 days storage at -1 ± 0.5 C. The authors thank L. W. Douglass for his assistance with the project. CTwo-four weeks storage at -29 C. Use of a company or product name by the U.S. Department of Agriculture does not imply approval or recommendation of the product to the exclusion of others which may also be suitable.

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JOURNAL OF FOOD PROTECTION. VOL. 45, APRIL 1982