Inhibition of Listeria monocytogenes and Salmonella enteritidis on chicken wings using scallop-shell powder A. Cagri-Mehmetoglu1 Department of Food Engineering, Sakarya University, Turkey 54187 ABSTRACT The present study was designed to determine the inhibitory effect of scallop-shell powder (SSP) on Listeria monocytogenes and Salmonella enteritidis on chicken wings. Chicken wings artificially inoculated with L. monocytogenes (8.3 log10 cfu/g) or S. enteritidis (8.8 log10 cfu/g) were immersed in distilled water (0.10 or 0.50% wt/vol) of SSP slurries for 10 or 30 min, respectively. The amount of L. monocytogenes, S. enteritidis, mesophilic aerobic bacteria (MAB), and yeast
or mold was determined for the chicken wings at d 0 or 7 of storage at 4°C. Results indicated that 0.5% SSP decreased the amount of L. monocytogenes and S. enteritidis on chicken wings by 3.7 and 5.0 log10 cfu/g, respectively. The growth of L. monocytogenes, S. enteritidis, MAB, and yeast or mold was inhibited by SSP during the 7-d refrigerated storage. Color and odor of chicken wings were not significantly changed by SSP treatment (P > 0.05).
Key words: scallop-shell powder, Listeria monocytogenes, Salmonella enteritidis, chicken wing 2011 Poultry Science 90:2600–2605 doi:10.3382/ps.2011-01540
INTRODUCTION Chicken is a significant food source in most countries around the world. In the United States, the estimated consumption of poultry increased by approximately 25% per capita from 1997 to 2007 (FRW, 2009). This increased consumption of poultry may contribute to an increase in poultry-associated food-borne disease, particularly salmonellosis and listeriosis (Flake and Paterson, 1999). Salmonella and Listeria monocytogenes are the significant food-borne pathogens present in raw meat products and in their processing environment (Arnold, 1998; Jay, 2000; Bailey et al., 2002; Berrang et al., 2002; CDC, 2002a,b; Mikołajczyk and Radkowski, 2002). A variety of disinfectants, including chlorine, organic acids, bacteriocins, hydrogen peroxide, ozone, ultrahigh pressure, irradiation, and UV light have been tested for decreasing the levels of pathogens on poultry carcasses, with a primary focus on disinfectants that are practical and effective (Izat et al., 1989; Dickson and Anderson, 1992; Rose et al., 2002). However, few of these disinfectant treatments have been accepted by the poultry industry. Aspects limiting their extensive
©2011 Poultry Science Association Inc. Received April 13, 2011. Accepted July 7, 2011. 1 Corresponding author:
[email protected]
use have included carcass quality decline, instability of product, possible health risk and consumer conflict, and cost implications (Waldroup, 1993; Conner and Bilgili, 1994; Dickens and Whittemore, 1997; Conner et al., 2001; Capita et al., 2002). Scallop-shell powder (SSP) may offer another possible intervention strategy for eliminating Salmonella or L. monocytogenes that are attached to chicken wings. Scallop shells are regarded as waste products in the scallop harvesting districts of Korea and Japan (Ozdemir and Pamuk, 2006). Calcium carbonate (the main component of scallop shells) can be heated and converted into calcium oxide (CaO), which is known to possess antibacterial properties against several food-borne pathogens, including Escherichia coli O157:H7, L. monocytogenes, Salmonella Typhimurium, and Staphylococcus aureus (Sawai et al., 1995, 1996a,b, 1997, 2001b, 2003; Conner et al., 2001; Bae et al., 2006). Moreover, these studies reported that shell powder also enhanced the shelf life and quality of kimchi, shredded cabbage, tofu, and frankfurters (Sawai et al., 2001a; Choi et al., 2006; Kim et al., 2007; Bodur et al., 2010). The results of these previous studies showed that the application of SSP on L. monocytogenes and E. coli O157:H7 significantly decreased the populations of those bacteria on frankfurters (Bodur et al., 2010). Hence, the goals of this study were to (a) assess the effectiveness of SSP on inhibiting L. monocytogenes and S. enteritidis associated with chicken wings, (b) assess the effect of SSP on growth of mesophilic aerobic bacteria (MAB), and
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yeast or mold associated with chicken wings along with the effect on pH of chicken wings, and (c) assess the sensory attributes of chicken wings treated with SSP.
MATERIALS AND METHODS Bacterial Inocula Listeria monocytogenes ATCC 7644 and Salmonella enteritidis were obtained from the Turkish Public Health Agency (Ankara, Turkey). These 2 strains were maintained at −18°C in trypticase soy broth (TSB) containing 10% (vol/vol) glycerol and were subcultured twice at 35°C for 18 to 24 h in TSB containing 0.6% (wt/vol) yeast extract (Difco Laboratories, Detroit, MI).
Inoculation and Application Chicken wings were obtained immediately after evisceration from a poultry processing plant and transported to the laboratory in an ice chest. At the laboratory, the chicken wings were stored at 4°C for no longer than 2 h before use. Chicken wings were immersed for 5 min in a suspension of L. monocytogenes or S. enteritidis at a concentration of 8 log10 cfu/g at room temperature. Inoculated samples were dried for 30 min at room temperature to allow the bacteria to attach to the wings. The inoculated chicken wings were randomly divided into 4 groups, each containing 10 wings. Samples in group 1 were immersed in sterile distilled water for 10 or 30 min. Samples in groups 2 and 3 were immersed in 0.10 or 0.50% (wt/vol) SSP (Hacettepe Pharmaceutical LTD, Turkey) and stirred for either 10 or 30 min., respectively. Group 4 was untreated in order to serve as a control. After the treatments, the chicken wings were drained for 15 min at room temperature. Each wing was placed in a sterile Stomacher bag (17.7 × 30.5 cm2; LDPE; Seward Laboratory System Inc., NY), heat sealed, and stored at 4°C. All samples were examined for levels of the inoculum, MAB, and yeast or mold immediately after treatment and again after 7 d of refrigerated storage at 4°C.
Microbiological Analysis Chicken wings (25 g each) were added to 225 mL of sterile 0.10% (wt/vol) peptone water (PW; Difco Laboratories) and homogenized for 3 min in a Stomacher 400 (Tekmar Co., ). Appropriate dilutions in PW were surface plated on modified Oxford agar, XLT4 agar, plate count agar, and oxytetracycline glucose yeast extract agar (Difco Laboratories) to quantify L. monocytogenes, S. enteritidis, MAB, and yeast or mold, respectively.
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pH Test Chicken wing samples were homogenized in 100 mL of distilled water for 1 min. The pH values of the solutions were determined using a pH meter equipped with a standard combination electrode (Fisher Scientific, Hanover Park, IL).
Sensory Analysis Sensory characteristics of the chicken wing samples were determined by dipping the chicken wings in distilled water, 0.10% (wt/vol) SSP slurry, or 0.50% (wt/ vol) SSP slurry for 10 or 30 min. Sensory evaluation for both the control and the treated samples was conducted by 7 trained panelists. The panelists had 10 training sessions before initiating the experiment in order to be familiarized with the product. Sliminess, color, and offodors of the chicken-wing samples were assessed. The sensory attributes were evaluated by a scoring test using a 5-point hedonic scale with scores from 1 to 5. A score of 1 indicated no slime on the external surface, whereas a score of 5 in this category indicated slime of high viscosity. A 1 in the color category indicated an unacceptable color (lost natural color), whereas a 5 indicated a very natural color. For the off-odor category, a 1 indicated an unacceptable odor (odor atypical of the product), whereas a 5 indicated a natural odor of the raw chicken. The control and treated samples were removed from the storage conditions and allowed to stand before evaluation at room temperature until the temperature equilibrated.
Statistical Analysis All the assays were repeated 3 times with different batches of wing samples. The values represent mean ± SD of 3 replicated samples. The one-way ANOVA test was used to analyze the data from the experimental and control groups, with P values of < 0.05 considered to be significant.
RESULTS AND DISCUSSION Microbiologic Analysis L. monocytogenes. Table 1 summarizes the inhibitory effect of SSP on L. monocytogenes. The populations of L. monocytogenes on chicken wings was decreased from 8.1 to 5 log10 cfu/g and from 8.1 to 4.4 log10 cfu/g in 10 min posttreatment with 0.10 or 0.50% SSP, respectively. Additionally, the L. monocytogenes populations were also decreased by 4.1 or 4.7 log10 cfu/g after dipping the chicken wings in a 0.10 or 0.50% SSP slurry for 30 min, respectively. The decreasing effect of 0.50% SSP on Listeria populations was found to be significantly greater than the effect of 0.10% SSP (P < 0.05). Moreover, a 30-min treatment was signifi-
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Cagri-Mehmetoglu Table 1. Scallop-shell powder (SSP) treatment on Listeria monocytogenes or Salmonella enteriditis on the surface of chicken wing samples1 Days of storage (at 4°C) L. monocytogenes (log10 cfu/g) Time and treatment Control (untreated) 10-min treatment Distilled water 0.10% SSP (wt/vol) 0.50% SSP (wt/vol) 30-min treatment Distilled water 0.10% SSP (wt/vol) 0.50% SSP (wt/vol)
0 8.1 ±
S. enteritidis (log10 cfu/g) 7
0.2a
8.6 ±
0 0.2a
8.8 ±
7 0.1a
9.2 ± 0.2a
5.1 ± 0.1c 5.0 ± 0.3c 4.4 ± 0.4d
5.1 ± 0.1c 4.7 ± 0.3c 4.8 ± 0.4c
6.9 ± 0.2b 5.3 ± 0.1c 3.8 ± 0.2d
6.8 ± 0.1b 5.4 ± 0.1c 3.8 ± 0.2d
5.6 ± 0.1b 4.3 ± 0.3d 3.7 ± 0.4e
5.5 ± 0.1b 4.4 ± 0.3c 3.7 ± 0.4d
7.0 ± 0.4b 5.7 ± 0.3c 2.9 ± 0.2e
7.0 ± 0.1b 5.8 ± 0.4c 2.8 ± 0.3e
a–eMeans 1Mean
in same column with different superscripts are significantly different (P < 0.05). ± SD (n = 3).
cantly more effective than a 10-min treatment (P < 0.05). Dipping the chicken wings in distilled water also reduced Listeria populations by approximately 2 to 3 log10 cfu/g. In agreement with the present study, Bodur et al. (2010) and Bae et al. (2006) also indicated that SSP had an inhibitory effect on L. monocytogenes. In our previous study, dipping frankfurters in 0.10% SSP for 10 min killed 3.6 log10 of Listeria populations on the surface (Bodur et al., 2010). Similarly, Bae et al. (2006) also reported that the populations of L. monocytogenes were decreased by 45, 40, and 30 to 50% after treatment in a 0.05% CaO solution for 10 min, 0.10% CaO solution for 5 min, and 0.15% CaO solution for 2 to 3 min, respectively. The results also indicated that during the 7-d refrigerated storage, the samples from group 2 showed inhibited growth of L. monocytogenes by 0.3 to 0.5 log10 cfu/g compared with control samples. However, no significant decrease in the number of Listeria populations was observed during storage. Given that L. monocytogenes is a psychotropic microorganism, populations in control samples and the samples dipped in distilled water were expected to significantly increase during the 7-d storage period. On the contrary, only 0.5 log10 growth on control samples was recorded in this study. The reason for this phenomenon can be explained by the fact that the growth rates of Brochothricx thermosphacta and other gram-positive bacteria in chicken wings is greater than that of L. monocytogenes at refrigeration temperatures, and spoilage occurs before any marked increase in levels of pathogenic microorganisms (del Rio et al., 2006). On the other hand, a similar study found that the number of L. monocytogenes increased by approximately 1.2 log10 on chicken wing control samples during a 5-d refrigerated storage period (Capita et al., 2002). It is likely that the amount of competitive background flora in their samples was lower than that in the samples used in our present study. Scallop-shell powder residue remaining on chicken wings may continue to inhibit bacterial growth during storage, with the high alkalinity of the SSP slurry (pH
12.5) most likely being responsible for the observed antimicrobial activity. However, according to Sawai et al. (1999), the bactericidal action of SSP is greater than that of NaOH solution at an identical pH. Additionally, in a similar study, like shell powder, 2 other alkali decontaminants (trisodium phosphate (TSP) and NaOH at a pH of 12.5) were tested as disinfectants against Listeria on chicken wings. The results showed that TSP (12%) or NaOH (0.22%) killed only 3.24 or 3.28 log10 cfu/g of Listeria cells, respectively (Capita et al., 2002). Therefore, SSP (0.50%) at the same pH could be more effective against Listeria than TSP or NaOH. Hydroxyl ions released from SSP were suggested as the primary mechanism by which antibacterial activity occurred (Bae et al., 2006). Hydroxyl ions are highly oxidizing free radicals that show extreme reactivity, reacting with several biomolecules (Freeman and Crapo, 1982; Siqueira and Lopes, 1999). Their lethal effects on bacterial cells likely result from damage to the bacterial cytoplasmic membrane, and by DNA and protein denaturation. S. enteritidis. Salmonella enteritidis on the surface of the chicken wing samples (8.8 log10 cfu/g) was significantly decreased by 3.4 or 5.0 log10 cfu/g by treating them with a 0.1 or 0.5% SSP slurry for 10 min, respectively (Table 1; P < 0.05). Similarly, 0.1 or 0.5% SSP treatment for 30 min significantly decreased S. enteritidis populations from 8.7 log10 cfu/g to 5.7 or 3.0 log10 cfu/g, respectively. The effects of 0.1 and 0.5% SSP treatment or the effects of 10-min and 30-min treatment times on the amount of S. enteritidis on the samples were found to be significantly different (P < 0.05). Distilled-water dipping alone decreased S. enteritidis populations on wing samples by 1.8 to 2.0 log10 cfu/g. Similarly, Takama et al. (1999) found that SSP showed a strong bacteriostatic effect and completely inhibited cell growth of S. enteritidis (104 cfu/mL) at concentrations greater than 0.4%. The growth of S. enteritidis on our samples was inhibited by approximately 0.4 log10 cfu/g owing to the application of 0.5% SSP slurry for 10 or 30 min com-
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pared with the control samples during the 7-d refrigerated storage period (Table 1). However, the SSP treatments did not significantly decrease the populations of Salmonella on the sample surface during the same storage period (P > 0.05). MAB. The initial amount of MAB on the chicken wings was determined to be 3.6 log10 cfu/g. Application of either 0.10 or 0.50% SSP for 30 min killed 0.2 or 0.8 log10 cfu/g of MAB on the surface of the chicken wing samples, respectively (Table 2). However, the 10min treatment time for both concentrations of SSP did not decrease the populations of MAB. The growth of MAB during the 7-d refrigerated storage period was suppressed by approximately 0.4 or 0.7 log10 cfu/g by the application of 0.50% SSP for 10 or 30 min, respectively, compared with the control samples. However, SSP did not significantly decrease the populations of MAB during the 7-d refrigerated storage period (P > 0.05). These findings also agree with the results of our previous study, where application of 0.10% SSP for 10 or 30 min decreased MAB populations on frankfurters by 0.7 to 1.2 log10 cfu/g, respectively. Growth of MAB on frankfurters during a 7-d storage period at 4°C was also inhibited by approximately 0.5 log10 cfu/g using SSP compared with the control (Bodur et al., 2010). Also, according to Sawai et al. (2001a), treatment of shredded cabbage with 0.10% SSP killed approximately 1 log of viable bacterial cells. However, Kim et al. (2007) and Choi et al. (2006) demonstrated that either 0.05 or 0.1% CaO treatment of tofu or kimchi did not affect bacterial growth during a 12-d storage period at 10°C. Given that the natural flora found in kimchi, tofu, and cabbage are different from that of chicken wings, comparing or interpreting results from these 3 studies may not be exactly appropriate. Yeast and Mold. The amount of yeast on the chicken wing samples decreased by approximately 1 log10 cfu/g owing to the treatment of 0.5% SSP for 30 min (Table 2). However, the amount of yeast on the samples did
not decrease by 10-min treatments with either 0.10 or 0.50% SSP. During the 7-d refrigerated storage period, yeast growth was suppressed by approximately 0.8 or 1.4 log10 cfu/g owing to the treatment of 0.50% SSP for 10 or 30 min, respectively, compared with the untreated control samples. No mold was detected on treated or nontreated samples on d 0. During the storage period, 0.50% SSP treatment for 30 min decreased the growth of mold by 0.6 log10 cfu/g compared with the control samples. Application of 0.10% SSP for 10 min or 30 min did not change the growth of mold on chicken wing samples. Similarly, in our previous study on frankfurters, yeast populations on the surface samples decreased by 0.4 to 1.0 log10 cfu/g after treatment with 0.10% SSP, and no mold growth was observed.
Sensory Analysis Sensory characteristics of the samples were determined by dipping the chicken wings into different SSP concentrations for 10 or 30 min and then rating the samples using a hedonic scale (1 to 5). The sliminess of the chicken wing samples treated with distilled water, 0.1% SSP for 10 min, or 0.5% SSP for 10 min were scored as 3.9, 3.7, and 3.5, respectively. The scores were not statistically different (P > 0.05; Table 3). Moreover, the panelists gave higher scores for sliminess to the samples dipped in distilled water than to the samples treated for 30 min with either 0.1 or 0.5% SSP. Again, no statistical difference was found (P > 0.05). However, wings in the 30-min treatment compared with the 10min treatment were rated as significantly less slimy (P < 0.05). Similarly, in our previous study, panelists gave higher scores for sliminess of frankfurter sample surface to the control than to the treated samples owing to an increase in surface pH because SSP tends to remove fat from the surface. The scores of 4.3 or 4.0 given for off-odor to samples immersed in distilled water only or 0.1% SSP slurry
Table 2. Scallop-shell powder (SSP) treatment on mesophilic aerobic bacteria (MAB), yeast, and mold on the surface of chicken wing samples1 Days of storage (at 4°C) MAB (log10 cfu/g) Time and treatment Control (untreated) 10-min treatment Distilled water 0.10% SSP (wt/vol) 0.50% SSP (wt/vol) 30-min treatment Distilled water 0.10% SSP (wt/vol) 0.50% SSP (wt/vol) a–cMeans
0
Mold (log10 cfu/g) 7
0 ND2
1.9 ±
3.6 ± 0.1a 3.6 ± 0.3a 3.6 ± 0.4a
7.6 ± 0.1a 7.4 ± 0.3a 7.3 ± 0.4a
ND ND ND
3.6 ± 0.8a 3.4 ± 0.3a 2.7 ± 0.1b
7.8 ± 0.2a 7.5 ± 0.1a 6.1 ± 0.9b
ND ND ND
7.7 ±
in same row with different superscripts are significantly different (P < 0.05). ± SD (n = 3). 2ND = not detected. 1Mean
7
0.2a
3.6 ±
0.2a
Yeast (log10 cfu/g) 0
0.4a
7 0.2a
6.4 ± 0.4a
2.0 ± 0.1a 2.1 ± 0.1a 2.0 ± 0.3a
4.3 ± 0.1a 4.3 ± 0.3a 4.2 ± 0.1a
6.3 ± 0.1a 6.1 ± 0.7a 5.5 ± 0.3b
2.1 ± 0.2a 2.0 ± 0.3a 1.4 ± 0.1b
4.4 ± 0.2a 4.3 ± 0.1a 3.3 ± 0.3b
6.4 ± 0.5a 6.2 ± 0.8a 3.9 ± 0.1c
4.3 ±
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Cagri-Mehmetoglu Table 3. Scallop-shell powder (SSP) treatment on sensory properties of chicken wing samples1 Time and treatment Control (untreated) 10-min treatment Distilled water 0.10% SSP (wt/vol) 0.50% SSP (wt/vol) 30-min treatment Distilled water 0.10% SSP (wt/vol) 0.50% SSP (wt/vol)
Sliminess
Off-odor
0.4a
0.2a
4.0 ±
4.1 ±
Color 4.0 ± 0.5a
3.9 ± 0.3a 3.7 ± 0.5a 3.6 ± 0.7a
4.3 ± 0.3a 4.0 ± 0.8a 3.1 ± 0.6ab
3.9 ± 0.9a 3.6 ± 0.4a 3.0 ± 0.2ab
3.3 ± 0.4ab 3.2 ± 0.7ab 3.1 ± 0.3ab
3.3 ± 0.4ab 3.3 ± 0.5ab 2.7 ± 0.2b
3.6 ± 0.7a 3.6 ± 0.6a 2.9 ± 0.8ab
a,bMeans 1Mean
in same column with different superscripts are significantly different (P < 0.05). ± SD (n = 3).
for 10 min, respectively, were not significantly different from the control samples (P > 0.05). Also, off-odor ratings of the control samples were significantly higher than those treated with distilled water, 0.1 % SSP for 30 min, or 0.5% SSP for 30 min (P < 0.05). The chicken wing samples evaluated by the panelists were described as having a chemical odor. The color of the chicken wings was not significantly changed owing to the application of distilled water or 0.1% SSP for 10 or 30 min (P > 0.05). The results were similar in previous studies by Choi et al. (2006) and Bodur et al. (2010) where the addition of 0.05 or 0.1% SSP did not significantly affect overall acceptability of kimchi or frankfurters, respectively.
pH Analysis The treatment of SSP at 0.1 or 0.5% for 10 min increased the pH of the samples from 6.32 to 7.1 or 8.63, respectively. Treatment with 0.1 or 0.5% for 30 min significantly increased the pH of the samples from 6.32 to 7.1 or 9.01, respectively (P < 0.05; Figure 1). However, distilled water alone did not significantly change the pH of the samples (P > 0.05). The SSP slurry has an alkaline pH of 12.5, and these results demonstrate
Figure 1. The effect of scallop-shell powder (SSP) treatment at concentrations of 0.0, 0.10, or 0.50% for 10 min or 30 min on the pH of chicken wing samples. a–cpH values with different letters are significantly different.
that the pH of the treated samples was significantly increased by SSP application (P < 0.05).
Conclusion The results of this study show that L. monocytogenes or S. enteritidis present on the surface of chicken wings could be decreased significantly by immersion of the wings in SSP. Additionally, growth inhibition after a 7-d refrigerated storage period of L. monocytogenes, S. enteritidis, or natural flora by SSP was also shown. Given that the application of 0.1% SSP did not negatively affect the chicken-wing sensory properties, it is suggested that it be used in the meat industry for the purpose of disinfection and shelf life extension.
ACKNOWLEDGMENTS We thank Hacettepe Pharmaceutical Ltd. for providing the scallop-shell powder for this study (Ankara, Turkey).
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