HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Gulmez, M. Articles by Vatansever, L. Search for Related Content PubMed PubMed Citation Articles by Gulmez, M. Articles by Vatansever, L.

The Effect of Water Extract of Sumac (Rhus coriaria L.) and Lactic Acid on Decontamination and Shelf Life of Raw Broiler Wings

Food Hygiene and Technology Department, Faculty of Veterinary Medicine, University of Kafkas, 36200 Kars, Turkey

¹ Corresponding author: mgulmez{at}kafkas.edu.tr

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
In an attempt to improve the bacteriological quality and refrigerated shelf life of broiler meat, 10-min surface wash treatments with sterile distilled water (DW), 8% (wt/vol) water extract of sumac (Rhus coriaria L.) fruits (WES), and 2% (vol/vol) lactic acid (LA) were compared by using a broiler wing model. The aerobic plate counts (log₁₀ cfu/g) of psychrotrophs, mesophilic aerobes, Enterobacteriaceae, coliforms and presumptive fecal coliforms on the samples were determined. Immediately after a 10-min decontaminaton, the mean count of all the bacterial groups was determined to be 3.9, 2.6, and 1.7 (log₁₀ cfu/g) for DW, WES, and LA, respectively. Because the postdecontamination population level of psychrotrophs, mesophiles, and Enterobacteriaceae were low in the LA-treated group compared to the WES group, an equity between the 2 groups in the point of view of the 3 bacterial groups existed at d 10 of cold storage (3 ± 1°C). Shelf life was 7 and 14 d for wings treated with DW and WES, respectively, whereas the LA-treated wings did not spoil after 14 d of cold storage (3 ± 1°C). Nevertheless, an undesirable pale color and an acidulous odor occurred in the LA-treated wings. In contrast, a good color appeared on the WES-treated wings, which was also superior to the color of the DW-treated wings. Such advantages of WES may be important for poultry processors and for consumers. However, the immediate decontamination and refrigerated shelf life extension potential of WES should be intensively studied in antimicrobial interventions in poultry processing plants.

Key Words: decontamination • shelf life • broiler • sumac • lactic acid

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Whereas foodborne diseases remain an important public health threat worldwide, one of the most important food safety hazards is associated with meat. Raw poultry products are perceived to be responsible for a significant amount of human illness because of the relatively high frequency of contamination of poultry with pathogens (Centers for Disease Control, 2001; Kessel et al., 2001; Zhao et al., 2001). Increased consumer awareness and concern about microbial foodborne diseases has resulted in intensified efforts to reduce contamination of raw meat, as evidenced by new meat and poultry inspection regulations being implemented in the United States. The developments have renewed and intensified interest in the development and commercial application of meat and poultry decontamination procedures (Sofos and Smith, 1998).

Controlling the cross-contamination of microorganisms to carcasses during slaughtering, processing, storage, handling, and preparation is a complex challenge (Mandrell and Wachtel, 1999). Production of a pathogen-free product is not guaranteed under current production conditions (Northcutt et al., 2003). However, the incorporation of a decontamination step during slaughter-dressing procedures can effect improvement of the microbial quality and safety of meat products. Multiple decontamination steps have been shown to be even more effective than a single-step decontamination procedure (Castillo et al., 2002).

The carcass decontamination technologies can be classified either as chemical or physical, and they include the use of ozonated or superchlorinated water, hydrogen peroxide, steam pasteurization, and a range of organic acids. The application of chemical decontaminants in poultry processing is permitted in the United States; however, their use in commercial plants in European Union countries is prohibited. Among organic acids, lactic acid (LA) has become the most commonly used organic acid in commercial practice to improve the bacterial safety and refrigerated shelf life of carcasses (Van Netten et al., 1994; Coleman et al., 2003). Nevertheless, some modifications on the lactic acid-treated chicken carcasses have been demonstrated (Deumier, 2004).

Food antimicrobials are mostly synthetic chemicals, and some are limited to use in foods, because they may cause adverse effects on public health and reluctance by consumers. Therefore, much attention in recent years has been focused on extracts from herbs and spices, which have been used for many centuries to improve the sensory characteristics and to extend the shelf life of foods. Various tanniniferous plants, including sumac (Rhus coriaria L.), have been known to contain naturally occurring compounds with antimicrobial activities (Wetherilt and Pala, 1994; Cowan, 1999; Nasar-Abbas and Halkman, 2004). Sumac grows wild in the region extending from the Canary Islands to the Mediterranean and southeastern Anatolian region of Turkey. The ground spice is used as a condiment and sprinkled over kebobs, grilled meats, soups, and some salads. In folk medicine, it is used for treatment of indigestion, anorexia, diarrhea, hemorrhages, and hyperglycemia (Wetherilt and Pala, 1994; Digrak et al., 2001; Nasar-Abbas and Halkman, 2004). The main compounds in sumac are hydrolyzable tannins and substantial amounts of flavonoids. It has been demonstrated that gallotannins in sumac leaves are decomposed by heating above 50°C (Zalacain et al., 2003). In our previous studies, heating the water extract of sumac (WES) fruits to 90°C did not influence its antibacterial property (unpublished data).

The effects of plant extracts against pathogenic bacteria in vitro are known, yet few studies have addressed the effect of these compounds against pathogens associated with muscle foods (Cutter, 2000). The bacteriostatic and bactericidal effects of WES on foodborne bacteria, including pathogens, have been demonstrated in broth and agar media (Digrak et al., 2001; Nasar-Abbas and Halkman, 2004), but we could not find a study in which sumac is used as a meat surface decontaminant. The present work was undertaken to compare the surface decontamination and shelf life activity of WES with that of LA and sterile distilled water (DW) in a broiler wing model.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Preparation of Meat Surface Decontaminants
Water Extract of Sumac.
The ripened (reddish-brown), native sumac fruit bought from a local retailer in Kars, Turkey, was added to sterile DW at the ratio of 0.8:10 (wt/vol) in a sterile bag and left at 45°C for 12 h. After this period, the bag was squeezed by hand to crush its contents. The crushed contents were then filtered through cheesecloth into a sterile Erlenmeyer flask. The contents of the flask were heated to 90°C, cooled to room temperature, and were used the same day.

Lactic Acid.
A 2% concentration of LA in sterile DW (vol/vol) was prepared from a 98% concentration (catalog no. L6402, Sigma-Aldrich, St. Louis, MO) and was used the same day.

Sterile DW.
Distilled water was autoclaved at 120°C for 15 min.

Experimental Design and Microbiological Analyses
Sample Collection and Allocation to Treatments.
The procedure described below was replicated 3 times in consecutive weeks in May 2005. In each replication, 3 1-kg samples of wings (each produced by a different company in the preceding 6 h) were bought from 3 different local retailers in Kars, Turkey, and transferred under cold storage to the lab within 20 min. To make the surface flora of the wings uniform before decontamination, each of the 1-kg samples was mixed thoroughly, then 18 wings, 6 randomly selected wings from each of the 3 bags, were transferred to another sterile bag. The bag of 18 wings was shaken vigorously by hand for 2 min, after the addition of 50 mL of physiological saline. Then, the 18 wings were regrouped randomly into 3 separate sterile bags of 6 wings. The remaining fluid was also equally dispensed to the 3 bags, and the contents of the each bag were mixed.

Surface Decontamination and Shelf Life Study.
Each of the 3 wing groups was decontaminated separately by the addition of 50 mL of one of the DW, WES, and LA (ca. 15 mL for 100 g of wing) treatments. Each bag was slowly shaken and rotated for 10 min. Then, each decontaminated wing was transferred to a separate previously weighted sterile plastic bag, weighed, and stored at 3 ± 1°C until analysis time.

Microbiological Analyses.
One randomly selected wing from each decontaminated group was analyzed immediately after 10 min of surface decontamination and at 3, 5, 7, 10, and 14 d of cold storage. For the surface rinse sampling, 25 mL of physiological saline was added onto each of the 3 wings. Each bag was shaken vigorously by hand for 2 min, then the wing was allowed to drain briefly into the bag and was discarded. The rinse fluid was transferred to a sterile Erlenmeyer flask and used for analyses. The 10-fold serial dilutions of rinse fluid were made in peptone-buffered saline, and 0.1 mL was spread plated, or 1 mL was pour plated in duplicate plates.

Plate count agar (Oxoid Ltd., Basingstoke, UK) was spread plated for psychrotrophs, and the plates were incubated at 4°C for 7 d. The same medium was also spread plated for mesophilic aerobes, and the plates were incubated at 30°C for 3 d. Violet bile glucose agar (Oxoid Ltd.) was spread plated for Enterobacteriaceae, and the plates were incubated at 30°C for 2 d. Violet bile lactose agar (Oxoid Ltd.) was pour plated for coliforms, and the plates were incubated at 37°C for 1 d. Violet bile lactose agar was also pour plated for presumptive fecal coliforms, and the plates were incubated at 44.5°C for 1 d. All of the colonies on plate count agar and colonies that were round, red to pink, 0.5 to 2 mm in diameter, and surrounded with a red to pink halo on violet bile lactose agar and violet bile glucose agar were counted. The count (cfu/mL) of each bacterial group in the rinse fluid of each wing was calculated from the mean counts of plates, multiplied by 25 to determine the count per 25 mL (cfu/25 mL) of rinse fluid, and then divided by the wing weight to determine the colony-forming units per gram for each wing sample. Then the mean of the 3 replications was calculated (log₁₀ cfu/g).

Sensory Evaluation
Sensory evaluation of wings was performed during storage by a 6-member sensory panel composed of staff from the laboratory. The same persons were used each evaluation, and all were blinded to which product was being tested. The sensory evaluation was carried out in artificial light, and the temperature of the packed product was similar to ambient temperature. Special attention was given to the color and the assessment of abnormal odors during the opening of the pack (Skandamis and Nychas, 2001). The evaluations were made in comparison with 1-d-old refrigerated broiler wings and were based on acceptability or unacceptability.

Statistical Analysis
Values from the replicate trials were used for statistical analysis. Data were analyzed using a one-way ANOVA for each type of microorganism and for each treatment group. Differences in microbial counts were determined using Tukey’s test. Analysis of variance with the GLM procedure of the SAS statistical package (SAS Institute, 1999) was used to compare treatments, total contaminants, and analysis times.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
In an attempt to improve bacteriological quality and refrigerated shelf life of broiler meat, the effect of treatments with 8% WES and 2% LA was investigated using a broiler wing model. Immediately after a 10-min surface wash treatment and at 3, 5, 7, 10, or 14 d of cold storage, psychrotrophs, mesophilic aerobes, Enterobacteriaceae, coliforms, and presumptive fecal coliforms were counted using the surface rinse sampling technique. As expected, DW had the lowest decontamination rate, whereas LA appeared to be more effective than WES at all the analysis times (Figure 1 and Figure 2, panels A through E. Whereas DW-treated wings were spoiled at 7 d, only a slight odor of spoilage was detectable in the WES-treated group at d 14 of cold storage.

View larger version (23K): [in this window] [in a new window]   Figure 1. The colony counts (mean ± SEM) of total contaminants after a 10-min decontamination. Broiler wing samples were decontaminated by using sterile distilled water (DW), water extract of sumac (WES; Rhus coriaria L, 8%, wt/vol), and L + lactic acid (LA; 2%, vol/vol) and was then stored at 3 ± 1°C. PCA 4 = plate count agar (PCA) was spread plated for psychrotrophs, and the plates were incubated at 4°C for 7 d; PCA 30 = PCA was also spread plated for mesophilic aerobes, and the plates were incubated at 30°C for 3 d; VG 30 = VG was spread plated for Enterobacteriaceae, and the plates were incubated at 30°C for 2 d; VL 37 = violet bile lactose agar (VL) was pour plated for coliforms, and the plates were incubated at 37°C for 1 d; and VL 44.5 = VL was also pour plated for presumptive fecal coliforms, and the plates were incubated at 44.5°C for 1 d.

View larger version (19K): [in this window] [in a new window]   Figure 2. The separate colony counts of some microbial populations during cold storage (3 ± 1°C). DW = sterile distilled water; WES = water extract of sumac; and LA = lactic acid.

Lactic acid is one of the most widely studied organic acids currently used in the meat industry (Ransom et al., 2003). There is good experience with surface treatment of the chilled poultry using LA, which reduces initial bacterial counts and causes a delay of the start of the logarithmic phase of their growth (Jay, 1999). In this study, LA was the most effective decontaminating agent, followed by WES and DW, respectively (Figure 1 and Figure 2, panels A through E). An undesirable pale color and acidulous odor occurred in the LA-treated wings. Such undesirable effects of LA on meat surfaces at decontamination doses have been demonstrated by many other researchers (Garcia Zepeda et al., 1994; Tosun and Tamer, 2000; Pipek et al., 2005). In contrast to this disadvantage of LA, a good color appeared on the WES-treated wings, which was also superior to the color of the DW-treated wings. Such advantages of WES may be important for poultry processors and for consumers.

The psychrotrophs, mesophilic aerobes, and Enterobacteriaceae of the DW-treated wings increased, approximately, from 5.0 to 9.0 log₁₀ cfu/g at d 7 of cold storage, when spoilage occurred (Figure 2, panels A through C). The same populations of the WES-treated wings increased, approximately, to this level at d 14 of cold storage. The counts of the same bacterial groups in LA-treated wings was found to be 0.5 to 1.0 log₁₀ cfu/g lower than that of WES-treated wings at d 14. (Figure 2, panels A through C). The population increase rates of psychrotrophs, mesophilic aerobes, and Enterobacteriaceae were in congruity during cold storage (P > 0.005). As expected, these populations increased during cold storage (Figure 2, panels A through C); in contrast, a reduction occurred in the counts of the coliforms and presumptive fecal coliforms (Figure 2, panels D and E). As in the case of the first 3 groups of microorganisms (Figure 2, panels A through C), the WES exerted an antibacterial effect against coliforms and presumptive fecal coliforms, which was, however, lower than that exhibited by LA (Figure 2, panels D and E). Lactic acid appeared to be superior than WES, both on decontamination of spoilage and pathogenic populations from poultry carcasses.

Lactic acid is generally suggested for the achievement of a 1.0 to 2.0 log units reduction in contaminating microorganisms from the surface of beef (Ransom et al., 2003). Although LA was more effective in this study, WES also yielded such achievement here (Figure 1). Immediately after decontamination, the mean values for psychrotroph were 5.2, 4.1, and 2.3 log₁₀ cfu/g for the DW-, WES-, and LA-treated groups, respectively (Figure 2, panel A). At d 7 of cold storage, the mean counts of this bacterial group reached to 9.2, 7.3, and 5.6 log₁₀ cfu/g for the DW-, WES-, and LA-treated samples, respectively (Figure 2a). At d 10, the mean counts of psychrotrophs, mesophilic aerobes, and Enterobacteriaceae in the LA-treated group increased to approximately the same level as the WES-treated group (P > 0.1; Figure 2, panels A through C). These findings confirm that the slowest growth rate of the total contaminants extends the shelf life of poultry meat.

The results of this study also suggest that WES can be used at each decontamination point whereas a surface decontaminant, such as LA, is recommended for use. Moreover, because it is natural, safe, and easy to prepare, it appears to be recommendable as a meat surface decontaminant, even in kitchens. Adopting this simple measure could decrease the cross-contamination risk in such places. However, sumac may not be unique among plants as a natural, safe, effective, abundant, and cheap antimicrobial resource. More studies should be conducted on sumac to determine the most appropriate method of preparation, treatment dose and temperature, treatment type, and duration.

Sumac is rich in water-soluble tannins, and the antimicrobial activity of tannins is well documented (Chung et al., 1998). Nasar-Abbas and Halkman (2004) have demonstrated that not only the organic acids but also other substances in WES are effective antimicrobial agents. The pH of the LA and of the WES was 2.8 and 3.6, respectively (data not shown). This demonstrates that the antibacterial activity and the pH of the treatment solutions are in congruity.

This study may also provide a basis for more detailed studies to be conducted on improving the antibacterial activity of WES and other tannin-rich plants. Other natural sources of antimicrobial plant extracts include extract of Quercus infectoria (oak) and Oreganum spp. (oregano). Tannins in oak and essential oils in oregano are antimicrobial substances (Burt and Reinders, 2003; Burt, 2004; Okoli and Iroegbu, 2004; Basri and Fan, 2005). Tannins dissolve better in water than in methanol and ethanol (Pansera et al., 2004). This property of tannins may be important for meat processors. A specially cloned line of the herb oregano, called Umass oregano has offered meat and poultry processors a consistent source of antimicrobial activity (Foodnavigator.com, 2003). The water extracts of tannin-rich plants other than sumac may also be tested to explore this potential for such alternatives.

Preservatives used in the agro-food industries may be of natural origin or obtained commercially. Because of the increasing interest of consumers in food products that contain only natural ingredients, studies on preservative molecules of natural origin, such as organic acids, peptides, and essential oils have been reported in the past several years (Burt and Reinders, 2003; Barreteau et al., 2004; Burt, 2004). This study demonstrates that WES may be a potential source of natural, safe, and cheap food decontaminant alternative to synthetic and chemical antimicrobials.

Received for publication June 28, 2005. Accepted for publication March 13, 2006.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Barreteau, H., L. Mandoukou, I. Adt, I. Gaillard, B. Courtois, and J. Courtois. 2004. A rapid method for determining the antimicrobial activity of novel natural molecules. J. Food Prot. 67:1961–1964.[ISI][Medline]

Basri, D. F., and S. H. Fan. 2005. The potential of aqueous and acetone extracts of galls of Quercus infectoria as antibacterial agents. Indian J. Pharmacol. 37:26–29.

Burt, S. 2004. Essential oils: Their antibacterial properties and potential applications in foods—a review. Int. J. Food Microbiol. 94:223–253.[ISI][Medline]

Burt, S. A., and R. D. Reinders. 2003. Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett. Appl. Microbiol. 36:162–167.[ISI][Medline]

Castillo, A., M. D. Hardin, G. R. Acuff, and J. S. Dickson. 2002. Reduction of microbial contaminants on carcasses. Page 377 in Control of Foodborne Microorganisms. V. K. Junea and J. N. Sofos, ed. Marcel Dekker Inc., New York, NY.

Centers For Disease Control. 2001. Foodborne infections: General information and technical information. http://www.cdc.gov/ncidod/dbmd/diseaseinfi/foodborneinfections_g.t.htm Accessed May 2002.

Chung, K. T., T. Y. Wong, C. I. Wei, Y. W. Huang, and Y. Lin. 1998. Tannins and human health: A review. Crit. Rev. Food Sci. Nutr. 38:421–464.[ISI][Medline]

Coleman, M. E., S. Sandberg, and S. A. Anderson. 2003. Impact of microbial ecology of meat and poultry products on predictions from exposure assessment scenarios for refrigerated storage. Risk Anal. 23:215–228.[ISI][Medline]

Cowan, M. M. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12:564–582.[Abstract/Free Full Text]

Cutter, C. N. 2000. Antimicrobial effect of herb extracts against Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella typhimurium associated with beef. J. Food Prot. 63:601–607.[ISI][Medline]

Deumier, F. 2004. Pulsed vacuum immersion of chicken meat and skin in acid solutions: Effect of mass transfers, colour and microbial quality. Int. J. Food Sci. Technol. 39:277–286.

Digrak, M., M. H. Alma, and A. Ìlcim. 2001. Antibacterial and antifungal activities of Turkish medicinal plants. Pharm. Biol. 39:346–350.

Fletcher, D. L., S. M. Russell, J. M. Walker, and J. S. Bailey. 1993. An evaluation of a rinse procedure using sodium bicarbonate and hydrogen peroxide on the recovery of bacteria from broiler carcasses. Poult. Sci. 72:2152–2156.[ISI][Medline]

Fluckey, W. M., M. X. Sanchez, S. R. McKee, D. Smith, E. Pendleton, and M. M. Brashears. 2003. Establishment of a microbiological profile for an air-chilling poultry operation in the United States. J. Food Prot. 66:272–279.[ISI][Medline]

Foodnavigator.com. 2003. Keeping meat safe-new research unveiled. http://www.foodnavigator.com/news/news-ng.asp?id=46094-keeping-meat-safe Accessed May 2005.

Garcia Zepeda, C. M., C. L. Kastner, P. B. Kenney, R. E. Campbell, and J. R. Schwenke. 1994. Aroma profile of subprimals from beef carcasses decontaminated with chlorine and lactic acid. J. Food Prot. 57:674–678.

Goksoy, E. O., S. Kirkan, and F. Kok. 2004. Microbiological quality of broiler carcasses during processing in two slaughterhouses in Turkey. Poult. Sci. 83:1427–1432.[Abstract/Free Full Text]

James, W. O., J. C. Prucha, R. L. Brewer, W. O. Williams Jr., W. A. Christensen, A. M. Thaler, and A. T. Hogue. 1992a. Effects of countercurrent scalding and postscald spray on the bacteriologic profile of raw chicken carcasses. J. Am. Vet. Med. Assoc. 201:705–708.[ISI][Medline]

James, W. O., W. O. Williams Jr., J. C. Prucha, R. Johnston, and W. Christensen. 1992b. Profile of selected bacterial counts and Salmonella prevalence on raw poultry in a poultry slaughter establishment. J. Am. Vet. Med. Assoc. 200:57–59.[ISI][Medline]

Jay, J. M. 1999. "Bacterial profile of ground beef made from carcass tissue experimentally contaminated with pathogenic and spoilage bacteria before being washed with hot water, alkaline solution, or organic acid and then stored at 4 or 12 degrees C," a comment on J. Food Prot. 61:1109–1118 (1998). J. Food Prot. 62:104–105.

Kessel, A. S., I. A. Gillespie, S. J. O’Brien, G. K. Adak, T. J. Humphrey, and L. R. Ward. 2001. General outbreaks of infectious intestinal disease linked with poultry, England and Wales, 1992–1999. Commun. Dis. Public Health 4:171–177.[Medline]

Mandrell, R. E., and M. R. Wachtel. 1999. Novel detection techniques for human pathogens that contaminate poultry. Curr. Opin. Biotechnol. 10:273–278.[ISI][Medline]

Nasar-Abbas, S. M., and A. K. Halkman. 2004. Antimicrobial effect of water extract of sumac (Rhus coriaria L.) on the growth of some food borne bacteria including pathogens. Int. J. Food Microbiol. 97:63–69.[ISI][Medline]

Northcutt, J. K., M. E. Berrang, J. A. Dickens, D. L. Fletcher, and N. A. Cox. 2004. Effect of broiler age, feed withdrawal, and transportation on levels of coliforms, Campylobacter, Escherichia coli and Salmonella on carcasses before and after immersion chilling. Poult. Sci. 82:169–173.

Okoli, A. S., and C. U. Iroegbu. 2004. Evaluation of extracts of Anthocleista djalonensis, Nauclea latifolia and Uvaria afzalii for activity against bacterial isolates from cases of non-gonococcal urethritis. J. Ethnopharmacol. 92:135–144.[ISI][Medline]

Pansera, M. R., G. A. Iob, A. C. Atti-Santos, M. Rossato, L. Atti-Serafini, and E. Cassel. 2004. Extraction of tannin by Acacia mearnsii with supercritical fluids. Braz. Arch. Biol. Technol. 47:995–998.

Pipek, P., M. ikulová, J. Jeleníková, and M. Izumimoto. 2005. Colour changes after carcasses decontamination by steam and lactic acid. Meat Sci. 69:673–680.

Ransom, J. R., K. E. Belk, J. N. Sofos, J. D. Stopforth, J. A. Scanga, and G. C. Smith. 2003. Comparison of intervention technologies for reducing Escherichia coli O157:H7 on beef cuts and trimmings. Food Prot. Trends 23:24–34.

SAS Institute. 1999. SAS/STAT User’s Guide. Release 8.0 ed. SAS Institute Inc., Cary, NC.

Skandamis, P. N., and G. J. Nychas. 2001. Effect of oregano essential oil on microbiological and physicochemical attributes of minced meat stored in air and modified atmospheres. J. Appl. Microbiol. 91:1011–1022.[Medline]

Sofos, J. N., and G. C. Smith. 1998. Nonacid meat decontamination technologies: Model studies and commercial applications. Int. J. Food Microbiol. 44:171–188.[ISI][Medline]

Tosun, H., and A. U. Tamer. 2000. A study on the effect of chilling on the microbial quality of poultry carcasses and surface decontamination with lactic acid. Turk. J. Vet. Anim. Sci. 24:517–521.

Van Netten, P., J. H. Huis in ’t Veld, and D. A. Mossel. 1994. The immediate bactericidal effect of lactic acid on meat-borne pathogens. J. Appl. Bacteriol. 77:490–496.[Medline]

Wetherilt, H., and M. Pala. 1994. Herbs and spices indigenous to turkey. Pages 285–307 in Species, Herbs and Edible Fungi: Developments in Food Science, vol. 34. G. Charalambous Elsevier, ed. Amsterdam, The Netherlands.

Zalacain, A., M. Prodanov, M. Carmona, and G. L. Alonso. 2003. Optimisation of extraction and identification of gallotannins from sumac leaves. Biosyst. Eng. 84:211–216.

Zhao, C., B. Ge, J. De Villena, R. Sudler, E. Yeh, S. Zhao, D. G. White, D. Wagner, and J. Meng. 2001. Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the greater Washington, DC, area. Appl. Environ. Microbiol. 67:5431–5436.[Abstract/Free Full Text]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Gulmez, M. Articles by Vatansever, L. Search for Related Content PubMed PubMed Citation Articles by Gulmez, M. Articles by Vatansever, L.