2542 JOURNAL OF FOOD SCIENCE—Vol. 68, Nr. 8, 2003 © 2003 Institute of Food TechnologistsFurther reproduction prohibited without permission

Food Microbiology and Safety

JFS: Food Microbiology and Safety

Growth Suppression of Inoculated Listeriamonocytogenes and Physicochemical andTextural Properties of Low-fat Sausages asAffected by Sodium Lactate and a Fat ReplacerS.H. CHOI, K.H. KIM, J.B. EUN, AND K.B. CHIN

ABSTRACT: The antilisterial effect of low-fat sausages (<2%) manufactured with a fat replacer and increasedlevel of sodium lactate (SL, 60%) solution was determined during refrigerated storage after inoculation with 103

colony-forming units/g of Listeria monocytogenes (LM) at the initial storage. The fat replacer prevented moistureloss during cooking or storage. Increased SL in combination with the fat replacer resulted in lower water activity,total plate, and LM counts. In addition, whiteness values decreased (P < 0.05), but yellowness values increased(P < 0.05) with increased SL level. During storage, low-fat sausages containing at least 3.3% SL and the fatreplacer had greater antilisterial effect than the low-fat control.

Keywords: low-fat sausages, sodium lactate, fat replacer, Listeria monocytogenes

Introduction

The need for low-fat meat products is increasing because of consumers’ health concerns. The safety of these products is closely

related to their composition. Because low-fat meat products con-tain lower fat and have a higher protein and moisture content (%)compared with their regular-fat counterparts, they have problemsrelated to shorter shelf life during storage (Keeton 1994; Muranoand Rust 1995; Bloukas and others 1997). Thus, the ingredientsthat would inhibit growth of pathogens without adversely affectingpalatability in these products should be developed to extend theshelf life during storage.

The effect of sodium lactate (SL) as a bacteriostatic agent in low-fat comminuted sausages during storage has been well document-ed. Murano and Rust (1995) reported that antimicrobial effect wasfound with the addition of SL, especially against psychrotrophicbacteria in low-fat frankfurters (5% to 7% fat). Bloukas and others(1997) observed extension of shelf life in low-fat frankfurters by theuse of protective culture and 2% SL. Sodium lactate has been re-ported to have better antimicrobial effect than potassium sorbateand trisodium phosphate in Chinese-style sausages (Lin and Lin2002). This can be attributed to various mechanisms includingfeedback inhibition, intercellular acidulation, interference withproton transfer across the cell membrane, and lowering of wateractivity of the product.

Fat replacers are defined as ingredients to contribute a minimumcalorie without affecting palatability and processing characteristics(Keeton 1994). Murano and Rust (1995) observed the effect of atexture modifier (starch-isolated soy protein, starch-ISP) alone orin combination with SL on the microbial profile of low-fat frankfurt-

er and reported that the addition of SL with the texture modifierhad increased the shelf life compared with the control or frankfurt-ers containing starch-ISP alone. Thus, the antimicrobial effect of SLin combination with fat replacers may be due to synergistic effect,compared with the use of SL alone (Chin and Choi 2002). However,the effect of fat replacer alone or in combination with varied levelsof SL has not been studied, and therefore there is need to deter-mine the best combination of a fat replacer and SL levels. Thus, theobjective of this study was to determine the minimum level of SL(0% to 5%) that could have an antimicrobial effect in combinationwith a fat replacer, and to characterize the physicochemical andmicrobial properties in very low-fat comminuted sausages (<2%fat), inoculated with Listeria monocytogenes at the level of log 103

colony-forming units (CFU)/g.

Materials and Methods

Processing of low-fat sausagesRegular-fat and low-fat control, and sausages containing a fat

replacer alone or in combination with various levels of SL solution(60%) were manufactured according to Chin and others (1998, 1999,2000) (Table 1). Pork hams purchased from a local meat marketwere trimmed to external fats, and all connective tissues were re-moved. Then the lean meats, which were cut to the size of a cubicinch, were ground through a 3- to 4-mm plate, vacuum-packaged,and frozen until analyzed. Before freezing, the proximate compo-sition of raw meat materials was measured to have a final formula-tion (Table 2). The fat replacer used for this experiments consistedof konjac flour, carrageenan (Korea Carrageenan Co. Inc, Ltd, Seoul,Korea), and soy protein isolate (SPI, EX-33, Dupont, Protein Tech-nologies Intl., St. Louis, Mo., U.S.A.) at a ratio of 1:1:3. The mixed fatreplacer was prehydrated with water (1:4, vol/vol) before use. Rawmeat materials were thawed in a refrigerator for 24 h before use andblended for 30 s in a food processor (Crypto Peerless Ltd., K55,France) for the reducing size of meat particles. The prehydrated fat

MS 20030175 Submitted 4/3/03, Revised 6/3/03, Accepted 8/8/03. Authors Choi,Kim, and Chin are with the Biotechnology Research Inst. and Dept. of Ani-mal Science, Chonnam Natl. Univ. Gwangju, Korea 500-757. Author Eun iswith the Dept. of Food Science and Technology, Chonnam Natl. Univ.,Gwangju 500-600, Korea. Direct inquiries to author Chin (E-mail:kbchin@chonnam.ac.kr).

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replacer (2.5%), salt (1.5%), sodium erythorbate (0.05%), sodiumtripolyphosphate (STPP, 0.4%), cure blend (0.25%), and a half oftotal ice water were added and finely chopped with the groundmeats for 2 to 3 min to extract salt-soluble proteins. Then fats, therest of the ice water, and other nonmeat ingredients, such as milkproteins (2%) and sausage spices (1%), were added and mixed withthe ground meats in a food processor for about 3 min as followed byChoi and Chin (2003). The meat batters were stuffed into polyvi-nylidene chloride film (PVDC, D-755R, 40-micron gauge, 46 mm,Tokyo, Japan) and sausages were cooked in a water bath that waspreheated to 75 °C until the internal temperature of the geometriccenters of sausages reached 71.7 °C. After cooking, sausages werechilled and vacuum-packaged (TAEVAC 600MX, Yoiwang-city,Kyungki, Korea) in vacuum-package film (Cryovac Sealed Air KoreaInc, T 7325B, Seoul, Korea). During storage at 4 ±1 °C, physicochem-ical, textural, and microbiological measurements were determinedat 0, 1, 2, 4, 6, and 8 wk of storage.

Inoculation of Listeria monocytogenesA Listeria monocytogenes strain (LM, ATCC, 43256) was cultured on

tryptic soy agar (TSA) and incubated at 37 °C for 48 h. Colonies inthe TSA were harvested in 5 mL tryptic soy broth and incubated in ashaking water bath at 37 °C for about 19 h. After the cellulose casingswere peeled off, the fully grown bacterial suspension (approximately109 CFU/mL) was diluted with sterilized double distilled (dd) waterto have a final concentration of 105 CFU/mL. One milliliter of bacte-rial suspension was surface inoculated and mixed with each 25 g ofsausage samples. Then sausages were vacuum-packaged (TAEVAC600MX, Yoiwang-city, Kyungki-do, Korea) into cryovac extruded film(7325B, Sealed Air Korea Inc, Seoul, Korea) at –20 mm Hg and storedat 4 °C until analyzed at 0, 1, 2, 4, 6, and 8 wk of storage.

pH, water activity, and proximate analysisMoisture and fat contents (%) were analyzed in triplicate using

the AOAC (1995). Crude protein was also determined in triplicate bythe Kjeldahl digestion, distillation, and titration units (Kjeltec dis-tillation unit, Büchi 322, Büchi laboratory-Techniques AG, flawil,Switzerland). pH values of sausage samples were measured by apH meter (Mettler-Toledo, Model 340, Schwarzenbach, Swizer-land), and water activity of sausage sample was measured usingNovasina hygrometer (EEJA-3, Switzerland).

Cooking yields and water-holding capacityCooking yields (CY) were measured by determining the differ-

ence in weights of meat batter before and after cooking from each30 g of sample in centrifuge tube. Water-holding capacity was mea-sured to the moisture amounts of free water according to the mod-ified method of Jauregui and others (1981). Approximately 1.5 g ofhomogenized sausage sample was wrapped in Whatman (nr 3, 11-cm dia) filter paper, weighed, and centrifuged at 3000 rpm for 20min. Expressible moisture (EM %) was measured as the differencebetween the total sample weight and the moisture expressed fromthe homogenized sausage during centrifugation.

Hunter color values (L, a, b)Color measurements were performed using a chromameter (CR-

200, Minolta Corp., Ramsey, N.J., U.S.A.). Hunter L, a, and b colorvalues were determined as indicators of lightness, redness, andyellowness. The color was determined on the cross-section (inter-nal) of each sausage sample.

Texture profile analysisA texture meter (TA-XT2, Stable Micro System, Hasemere, En-

gland) was used to conduct texture profile analyses (TPA) at everywk of refrigerated (4 °C) storage, as described by Bourne (1978).Ten samples (10-mm dia; height, 13 mm) per treatment were com-pressed by a 2-cycle compression test to 75% of their originalheight. Force-time deformation curves were recorded at a cross-head speed of 100 mm/min and full-scale 5 N load cell. The peakvalue from the 1st compression represents fracturability of the sam-ple, and the peak value from the 2nd compression represents hard-ness of the sausage. Springiness (cm) of the sample was measuredas the height that the sausage recovered during the time elapsedbetween the end of 1st compression and the start of the 2nd com-pression. Cohesiveness was determined the ratio of the area underthe 1st compression curve to the area under the 2nd compressioncurve. Hardness × cohesiveness equals gumminess. Chewinesswas calculated by gumminess × springiness.

Microbial determinationInoculated sausage samples (each 25 g) were mixed with 225 mL

sterilized dd water, and serial dilutions were made to plate in dupli-cate on Palcom Agar Base (Oxoid Ltd, Hampshire, England) withselective supplements for L. monocytogenes and plate count agar(PCA, Difco, Sparks, Md., U.S.A.) for total bacterial count. Then theplates were inverted and incubated at 37 °C for 48 h. After incuba-tion, the number of colonies was counted and compared with thecontrol sample. Microbial counts were expressed as log CFU/g.

Statistical analysisLow-fat and regular-fat sausages were produced with the addi-

tion of a fat replacer alone or in combination with a 0 to about 5%level of SL (60% solution, PURSAL®, Purac Inc, Gorinchem, theNetherlands). The experiment was performed in triplicate and datawere analyzed as a 4 (SL level) × 6 (storage time) factorial arrange-ment. All experiments were performed in triplicate and all param-eters except for textural analyses were measured at least in tripli-cate. Data were analyzed by 2-way analysis of variance (ANOVA)using the general linear models procedure of SAS (1989). The inter-action between SL level and storage time was tested. If interactionsbetween main effects were significant (P < 0.05), data were sepa-

Table 1—The formulations of low-fat and regular-fat sau-sages

TotalItemsa Meats NMI FR AW SL treatments

Regular-fat control 70 7.5 0 22.50 0 100Low-fat control (LFC) 54 7.5 0 38.50 0 100LFC + fat replacer (FR) 54 7.5 2.5 36.00 0 100LFC + FR + SL 1.67% 54 7.5 2.5 35.33 1.67 101LFC + FR + SL 3.33% 54 7.5 2.5 34.67 3.33 102LFC + FR + SL 5.00% 54 7.5 2.5 33.00 5.00 103a AW = added water; FR = fat replacer (konjac flour : carrageenan : soyprotein isolate = 1:1:3); NMI = nonmeat ingredients; SL = sodium lactate.

Table 2—Mean values (%) for proximate analysis of low-fatsausages

Moisture Fat ProteinTreatments Mean ± SDa Mean ± SD Mean ± SD

Regular-fat control 58.3 ± 3.23 21.5 ± 2.90 13.2 ± 1.44Low-fat contro1 (LFC) 75.5 ± 1.58 1.45 ± 0.98 15.2 ± 0.50Fat treatments (pooled) 73.8 ± 1.37 1.67 ± 0.48 14.6 ± 0.61aMeans of triplicates; SD = standard deviation.

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Antilisterial effects in low-fat sausages . . .

rated by SL and storage time. Duncan’s multiple range tests wereperformed for each treatment, if interactions were not observed be-tween the 2 factors.

Results and Discussion

Because there were no interactions between SL level and storagetime, data were pooled by SL level or storage time as separated

parameters.

The effects of a fat replacer and SL level effectThe overall mean values of moisture, fat, and protein contents,

and pH values of lean meats were 75.9 ± 1.62, 3.07 ± 0.65,20.4 ± 0.93%, and 5.76 ± 0.23, respectively, whereas those of fatmeats were 10.2 ± 0.78, 83.6 ± 1.03, 6.10 ± 0.10%, and 6.54 ± 0.43, re-spectively. Mean values for moisture, fat, and protein content (%)of low-fat and regular-fat sausages using these raw lean and fatmeats are shown in Table 2. The developed low-fat (<2%) sausag-es in our study reduced the fat content by more than 90%, and in-creased protein and moisture contents were observed, comparedwith the regular-fat (approximately 20%) control. Results indicat-ed that our low-fat products were not similar in fat levels to thosemade previously (Bloukas and others 1997; Lin and Lin 2002) dueto extremely low fat content (<2%).

Table 3 shows the physicochemical, textural, and microbiologicalproperties of low-fat and regular-fat sausages as affected by the fatreplacer and various SL levels. Low-fat sausages containing 5% SLsolution and the fat replacer had higher pH values (P < 0.05) com-pared with the low-fat control. This result was supported by thework of Childers and others (1982), who reported that sodium ionsmay increase the pH. However, Bloukas and others (1997) report-ed that the SL level in the range of 0% to 3% had no effect on pH inlow-fat frankfurters (9% fat). The addition of the fat replacer did notchange the water activity values. However, increased SL levelslightly reduced (P < 0.05) the water activity values in low-fat sau-sages. This result was in accordance with the previous observations(Hammer and Wirth 1985; Debevere 1989). The lowering water ac-tivity by the addition of SL may retard microbial growth in low-fatsausages (Troller 1983). The addition of the fat replacer improvedthe vacuum purge and water-holding capacity in low-fat sausages,even though no differences in these parameters were observedamong varied SL levels evaluated. This result was in agreement

with that of the previous study by Murano and Rust (1995), whoreported a decrease in percent purge of low-fat sausage when thecombination of starch and isolate soy protein was incorporated intothe low-fat frankfurter. Results also indicted that the addition ofthe fat replacer could extend the shelf life by preventing moistureloss from the products during storage. Therefore, to retain morewater during storage use of the fat replacer could be essential dur-ing the manufacture of low-fat meat products. The addition of 3.3%or more SL solution clearly reduced the bacterial counts for L.monocytogenes (P < 0.05), which was inoculated in the 3 log CFU/gat the initial storage. Thus, SL solution at the level of lower than3.3% was not effective in retarding the inoculated LM in these prod-ucts. This result confirmed that of Murano and Rust (1995), whoreported that SL was not listeriostatic at concentrations lower than4%. However, a combination of 2% to 3% SL and 2% sodium chloridehad an antilisteric effect in low-fat frankfurters. In addition, thepotential of 3% SL as an antibacterial agent was investigated forChinese-style sausages by Lin and Lin (2002). No differences inredness values were observed among the treatments and controls.However, addition of fat replacer reduced the whiteness slightlyand the increased level of SL solution tended to increase yellow-ness. The addition of a fat replacer alone reduced the cohesiveness,and reduced springiness and gumminess values were observed inthe sausages containing 5% SL solution, as compared with low-fatcontrol. These results also indicated that 5% SL solution had a det-rimental effect for texture, even though it had a strong antibacterialeffect. Therefore, the minimum level for the antibacterial effectwithout deterioration of product quality could be 3.33% SL solutionin combination with the fat replacer in low-fat sausages.

Storage time effectStorage time affects pH, water activity, expressible moisture (%),

inoculated bacterial counts, and color values (Table 4). pH valuestended to increase, and water activity values were reduced slightlywith increased storage time. Differences in pH and water activitywith respect to the storage time (wk) were observed between the4th and 6th wk. Lin and Lin (2002) observed the relatively stable pHvalues of Chinese-style sausage during storage time, which wascaused by its buffering capacity. However, the product pH was af-fected by the storage time as also suggested by Bloukas and others(1997). This discrepancy in pH results may be attributed in part to

Table 3—Mean values for physicochemical, microbiological, and textural properties of low-fat and regular-fat sau-sages as affected by a fat replacer (FR) and various sodium lactate during storagea

ParametersTreatmentsb Sodium lactate (%)

(n = 18) CTL LFC LF + FR 1.67 3.33 5.00

pH 6.12ab 6.08b 6.10ab 6.15ab 6.13ab 6.20aWater activity 0.936ab 0.937a 0.936ab 0.934bc 0.932cd 0.930dVacuum purge 3.36b 6.32a 3.47b 3.36b 3.75b 3.92bExpressible moisture (%) 29.8b 37.6a 30.1b 29.1b 29.6b 30.0bHunter color valuesL 71.6a 68.8b 68.0c 67.6cd 67.0d 67.4cda 11.8a 12.6a 11.8a 12.5a 12.4a 12.4ab 7.77ab 6.36c 7.06bc 7.86ab 7.95abc 8.71a

Textural propertiesHardness 3859b 5593a 5412a 5036a 5383a 5205aCohesiveness 0.16c 0.21a 0.19b 0.18b 0.19b 0.19bChewiness 166a 260a 243a 524a 366a 242aSpringiness 0.17c 0.26a 0.26a 0.25ab 0.26ab 0.24bGumminess 634c 1168a 1024ab 967b 1023ab 984b

aMean with same row having same letters are not different. Data were pooled over the storage time.bTreatments: CTL = regular fat control; LFC = low-fat control; LF + FR = low-fat control with a fat replacer SL % 1.67, 3.33, and 5.00, low-fat control with a fatreplacer and sodium lactate solution (60%) 1.67, 3.33, and 5.00%, respectively.

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factors such as ingredient formulation and initial pH values beingtested. The pH values of Bloukas and others (1997) were higherthat those of Lin and Lin (2002) because of the addition of beef anddifferences in the composition of the ingredients in the formula-tion. In our study, the magnitude of pH difference during refriger-ated storage was not significant enough to have a practical differ-ence due to differences being small, even though it was statisticallydifferent. Lin and Lin (2002) has reported that water activity of sau-sages products tended to decrease during storage time. Expressiblemoisture (%) to determine water-holding capacity increased fromthe 4th wk of storage in our study. Microbial counts of the 6th wkwere different from those the 8th wk, which indicated that the prod-ucts started to spoil from the 6th wk. Hunter a values (redness)decreased, and b values increased with increased storage time.Results from color values indicated that the 4th through 6th wkcould be the upper limit of storage time for the deterioration ofcolor. However, textural profile analysis values of low-fat and regu-

lar-fat sausages were not significantly different during 8 wk of re-frigerated storage.

The microbial growth as affected by a fat replacer andSL during storage time

Because the inoculated Listeria monocytogenes (103 CFU/g) wasthe predominant flora in the products during or at the end of stor-age, the total bacterial counts had similar trends to those of L. mono-cytogenes (Figure 1). The numbers of L. monocytogenes detected onsausages showed differences between controls and treatmentsfrom the second wk. Significant inhibitory effect was apparent forthe addition of SL solution up to the 6th wk, when the bacterialnumber of L. monocytogenes was significantly lower (P < 0.05) thancontrols. At 8 wk of storage, low-fat sausages containing 1.67% SLsolution started to spoil, whereas those containing 3.33% and 5% SLsolution had still less than 105 CFU/g, which did not have any symp-toms of spoilage. These results indicated no significant inhibitionfrom the addition of 1.67% SL solution. However, sausages contain-ing 3.33% and 5% SL solution apparently retarded microbial growthduring storage, resulting in the delay of the lag phase at least 2 to4 wk compared with controls (Figure 1). In addition, the detectedlevels of LM were significantly lower in low-fat sausages with 3.33%and 5% SL compared with others. Miller and Acuff (1994) reportedthat roasts treated with 4% SL contained significantly lower levelsof LM on day 14, 21, and 28 compared with all other treatments, asthe bacterial numbers did not increase during storage. Chen andShelef (1992) found more than 55% suppression of LM in a meatmodel system containing 4% SL. Bloukas and others (1997) report-ed that 2% SL extended shelf life up to 6 wk compared with 3 and 4wk of shelf life for low-fat and high-fat control frankfurters, respec-tively. Our results are in agreement with these studies, in that atleast 3.33% or more levels of SL solution was required to reduce sig-nificantly the growth of LM. Furthermore, it is apparent that bacte-rial counts of LM decreased (P < 0.05) with increasing SL level dur-ing storage time. Further studies are planned to reduce the SL levelin combination with other natural ingredients to have the similarantimicrobial effect of low-fat sausages.

Conclusions

A fat replacer, the combination of konjac flour, carrageenan, andsoy protein isolate at the ratio of 1:1:3, improved the vacuum

purge and water holding capacity in low-fat sausages. Increased SL

Table 4—Mean values for physicochemical, microbiological, and textural properties of pooled low-fat and regular-fatsausages as affected by storage timea

Storage time (wk)

Parameter (n = 12) 0 1 2 4 6 8

pH 6.10ab 6.11ab 6.08b 6.08b 6.19a 6.21aWater activity 0.936a 0.937a 0.937a 0.934ab 0.931bc 0.930cVacuum purge (%) – 3.97 3.66 4.07 4.22 4.26Expressible moisture (%) 30.7ab 30.5ab 28.6b 32.7a 32.4a 31.3aHunter color valuesL 68.4a 68.5a 68.7a 68.5a 67.9a 68.4aa 13.4a 12.7ab 12.1ab 11.7b 12.0b 11.6bb 6.71b 7.20ab 7.75ab 7.90ab 8.09a 8.05a

Texture profile analysisHardness 4809a 5120a 4840a 5176a 5108a 5435aCohesiveness 0.18a 0.18a 0.19a 0.19a 0.19a 0.19aChewiness 218a 231a 241a 268a 273a 571aSpringiness 0.22b 0.24ab 0.24a 0.24a 0.24a 0.24aGumminess 855b 946ab 886ab 996ab 1037ab 1057a

aMean with same row having same superscripts are not different. Data were pooled over treatments.

Figure 1—Changes of bacterial counts for Listeria mono-cytogenes of regular-fat and low-fat sausages as affectedby a fat replacer and increased level of sodium lactateduring storage. 1 = regular-fat control; 2 = low-fat control;3 = low-fat with a fat replacer; 4,5,6 = low-fat with a fatreplacer and 1.67%, 3.33%, and 5.0% sodium lactate.

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(>3.3% of 60% SL solution) in combination with the fat replacer in-creased pH and shelf life, however, increased SL level resulted inlower water activity values. In addition, lower total bacterial andinoculated LM counts were observed when low-fat sausages con-tained at least 3.3% of SL solution with a fat replacer, as comparedwith low-fat control. pH, water activity, expressible moisture (%),inoculated bacterial counts and color values were also affected bystorage time, regardless of the SL levels. This result indicated thatthe optimum SL level that retarded the contaminated pathogenssuch as LM was 3.3%, and the fat replacer played an important rolein preventing moisture loss during storage.

AcknowledgmentsThis study was supported by a grant of the Korea Health 21 R&D

project, Ministry of Health & Welfare, Republic of Korea (01-PJ1-PG3-22000-0062).

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