Effectiveness of Several Antimicrobials and The Effect of Contact Time in Reducing Salmonella and

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C 2019 Poultry Science Association Inc.

Effectiveness of Several Antimicrobials and the


Effect of Contact Time in Reducing Salmonella and
Campylobacter on Poultry Drumsticks
Lei Zhang,∗ Amit Morey,† Sacit F. Bilgili,† Shelly R. McKee,‡ and Laura J. Garner†,1

College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi
712100, China; † Department of Poultry Science, Auburn University, Auburn, AL 36849,
USA; and ‡ DEB EL Food Products, LLC, Newark, NJ 07206, USA

Primary Audience: researchers, plant managers

SUMMARY
Salmonella and Campylobacter are the two pathogens commonly associated with raw poul-
try meat, as poultry products are frequent vehicles of these bacteria. The objective of the
current research was to determine the optimal contact time for 6 antimicrobial treatments,
including water, 0.003% chlorine, 0.07% peracetic acid (PAA), 0.1% PAA, 0.35% cetylpyri-
dinium chloride (CPC), and 0.6% CPC. Drumsticks (n = 192) were inoculated with Salmonella
Typhimurium and Campylobacter jejuni, and allowing some bacterial attachment time, drum-
sticks were treated with the 6 antimicrobials mentioned above for 10, 20, and 30 s contact time.
The recoveries of Salmonella Typhimurium and Campylobacter jejuni were determined after
plating. The results of this study indicated the antimicrobial effect on reducing Salmonella and
Campylobacter on poultry parts, and the impact of contact time on the efficacy. This could be
a guide for industrial application of which antimicrobial to use and how to control the contact
time.

Key words: poultry, Salmonella, Campylobacter, antimicrobial, contact time


2019 J. Appl. Poult. Res. 28:1143–1149
http://dx.doi.org/10.3382/japr/pfz080

DESCRIPTION OF PROBLEM to illness [2]. The Food Safety and Inspection


Service (FSIS) issued new performance stan-
Poultry meat is the most popular meat con- dards on Salmonella and Campylobacter on
sumed in the US; the per capita consumption post-chill whole carcasses regulating a maxi-
has been steadily increasing from 20 lb (in mum of 5 Salmonella-positive samples out of
1959) to 108.5 lb (in 2017) [1]. Salmonella and 51, and a maximum of 8 Campylobacter-positive
Campylobacter, the 2 pathogens commonly as- sample out of 51 samples [3]. Additionally,
sociated with poultry meat, are among the top chicken parts are regulated to be less than 15.4%
3 food-borne pathogens in the US responsible and 7.7% for Salmonella and Campylobacter,
for the annual disease burden costs. Combined, respectively [4].
these food-borne pathogens result in approxi- There is a high possibility of cross contami-
mately $5 billion in costs every year related nation during poultry processing if the process
is not well controlled [5], for example, low water
1
Corresponding author: bauerlj@auburn.edu temperature in scalding, poor hygiene in carcass
1144 JAPR: Research Report

picking and evisceration, or inadequate antimi- control, water control, 0.003% chlorine, 0.07%
crobial contact in chilling would result in high and 0.1% PAA, as well as 0.35% and 0.6% CPC,
bacterial load on processed carcasses. A num- with 3 contact times (10, 20, and 30 s). Specific
ber of potential intervention strategies can be treatments description shown in Table 1.
applied during processing to minimize cross-
contamination. Applying chemicals as antimi- Inoculum Preparation
crobials in poultry processing is one of the most
important intervention strategies to maintain the About 1 mL of the frozen nalidixic acid-
safety of products. Chemicals can be applied resistant (0.05%) strain of Salmonella Ty-
during scalding, evisceration, inside/outside bird phimurium [7] stock solution was added to
wash, chilling, etc. Acidified sodium chlorite 10 mL sterile Trypticase Soy Broth (TSB) [13]
(ASC), chlorine dioxide, hypochlorous acid, per- with Nalidixic Acid (0.05%). The culture was
acetic acid (PAA), and cetylpyridinium chloride incubated at 37◦ C for 24 h and streaked onto
(CPC) are antimicrobials approved for carcass xylose lysine Tergitol 4 (XLT4) agar [13] with
and parts applications [6]. PAA is most fre- 0.05% nalidixic acid. One isolated black colony
quently applied to carcasses or parts post-chill was picked from the XLT4 agar plates after in-
[5], whereas CPC is applied pre-chill in drench cubating at 37◦ C for 24 h and added to 10 mL of
cabinets [7]. TSB tube. The tube was incubated at 37◦ C for
Studies have been conducted to determine the 24 h. One milliliter of Salmonella culture was
efficacy of antimicrobials applied during poultry added to 99 mL of TSB in a conical flask and
processing. PAA at a concentration of 0.2% was incubated at 37◦ C for 24 h. Cultures were cen-
demonstrated to be effective with a 30 min con- trifuged [14] at 7,168 × g for 10 min at 4◦ C. The
tact time in the chiller to reduce Salmonella and pellets were suspended in equivalent amounts of
Campylobacter on whole carcasses [8]. Nagel buffered peptone water (BPW) [13] and recen-
et al. [9] studied PAA at concentrations of 0.04% trifuged, followed by resuspension in BPW to ob-
and 0.1% with a 20 s contact time and found a 2 tain a stock culture of 108 CFU/mL Salmonella
log reduction in Salmonella on inoculated broiler Typhimurium. Spread plating was performed to
carcasses when treated in an immersion-type confirm the inoculum concentration.
post-chill system. Waldroup et al. [10] stated About 1 mL of the frozen Campylobacter je-
that CPC between 0.1% and 0.5% is the most juni (isolated from the Auburn University Poul-
efficient antimicrobial treatment on controlling try Research Unit, Auburn AL) stock solution
Campylobacter on poultry carcasses; CPC is ex- was added to 10 mL of sterile Brucella broth
pected to reduce Campylobacter by 1–2.5 log on supplemented with ferrous sulfate, sodium bio-
pre-chill carcasses. Zhang et al. [11] observed sulfite, and sodium pyruvate (FBP) Broth [13].
that CPC at 0.35% or 0.60% applied in post- The culture was incubated at 42◦ C for 48 h in an
chill decontamination tanks provided a reduc- Anaero-Jar [15] with a CampyGen sachet [15],
tion of 4 or 5 log CFU/mL on Campylobacter which generates a microaerophilic atmosphere
in poultry parts, respectively. Cook and Beers containing 5% O2 , 10% CO2 , and 85% N2 . In-
[12] demonstrated that CPC at concentrations cubated culture was streaked onto Campy-Cefex
of 0.1%, 0.2%, 0.3%, and 0.4% with a contact agar [13] and incubated in the same conditions
time of 30 s effectively reduced Campylobacter as described previously. One isolated C. jejuni
on whole carcasses. The objectives of this study colony was picked from the Campy-Cefex agar
were to determine the effect of select antimicro- plates after incubating at 42◦ C for 48 h, and
bials in reducing Salmonella and Campylobacter added to 10 mL of Brucella-FBP broth tube.
on chicken drumsticks and the impact of contact The tube was incubated at 42◦ C for 48 h in the
time on the efficacy. Anaero-Jar with 5% O2 , 10% CO2 , and 85% N2 .
About 1 mL of C. jejuni culture was added to
MATERIALS AND METHODS 99 mL of Brucella-FBP broth and incubated
for 48 h under similar conditions to achieve
A total of 8 treatments were included in the 108 cfu/mL. Cultures were centrifuged and
experiment, including positive control, negative resuspended as by the same procedures for
ZHANG ET AL.: ANTIMICROBIAL CONTACT TIME 1145

Table 1. Description of Treatments.


Chemical treatment Contact time (s) Description
Positive control NA Inoculated samples without chemical dip
Negative control NA Non-inoculated samples without chemical dip
Water 10 Inoculated samples dipped in water for 10 s
20 Inoculated samples dipped in water for 20 s
30 Inoculated samples dipped in water for 30 s
0.003% chlorine 10 Inoculated samples dipped in 0.003% chlorine for 10 s
20 Inoculated samples dipped in 0.003% chlorine for 20 s
30 Inoculated samples dipped in 0.003% chlorine for 30 s
0.07% PAA1 10 Inoculated samples dipped in 0.07% PAA for 10 s
20 Inoculated samples dipped in 0.07% PAA for 20 s
30 Inoculated samples dipped in 0.07% PAA for 30 s
0.1% PAA 10 Inoculated samples dipped in 0.1% PAA for 10 s
20 Inoculated samples dipped in 0.1% PAA for 20 s
30 Inoculated samples dipped in 0.1% PAA for 30 s
0.35% CPC2 10 Inoculated samples dipped in 0.35% CPC for 10 s
20 Inoculated samples dipped in 0.35% CPC for 20 s
30 Inoculated samples dipped in 0.35% CPC for 30 s
0.6% CPC 10 Inoculated samples dipped in 0.6% CPC for 10 s
20 Inoculated samples dipped in 0.6% CPC for 20 s
30 Inoculated samples dipped in 0.6% CPC for 30 s
1
PAA: peracetic acid.
2
CPC: cetylpyridinium chloride.

Salmonella inoculum described previously. In- [18] and 0.6% CPC) were prepared for the study.
oculum used in current research was a mixture Water used to mix the treatments was kept at 4◦ C.
of 108 cfu/mL S. Typhimurium and 108 cfu/mL Positive (non-dipped inoculated) samples were
C. jejuni. Spread plating was performed to con- applied to determine the recovery of attached
firm the inoculum concentration. Salmonella and Campylobacter on drumsticks.
Negative (non-inoculated) samples were applied
Drumsticks Preparation to determine the background of Salmonella and
Campylobacter on drumsticks. Concentrations
Drumsticks [16] (n = 192) were used for the of antimicrobials were measured before treating
experiment. In each of 2 replications, 4 non- samples. Aquachek Water Quality Test Strips
marinated drumsticks were prepared for each of [19] was used to measure the concentration of
8 treatments. Each drumstick was inoculated by chlorine. For PAA and CPC, titration drop kits
dripping 250 μL of the inoculum containing both [20] were applied to confirm the concentrations.
108 CFU/mL S. Typhimurium and 108 CFU/mL The pH of antimicrobial solutions was measured
C. jejuni. After inoculation, a sterile spreader with a pH meter [19]. The pH of 0.07% and
was used to spread the bacteria evenly on the 0.1% PAA was 3.81 ± 0.2 and 3.48 ± 0.2 and
surface of the drumstick, and a 30-min attach- for 0.35% and 0.6% CPC, it was 6.58 ± 0.2
ment period was allowed before treatments were and 6.80 ± 0.2, respectively. The pH of chlorine
applied under clean bench at room temperature treatment was adjusted by 1 N HCI to 5.92 to
(20 ± 1◦ C). Inoculated drumsticks [17] were form hypochlorous acid. About 900 mL of each
dipped in the water control and antimicrobials antimicrobial solution was held in a 1,500 mL
for various contact times (10, 20, and 30 s). beaker. Inoculated drumsticks (one at a time)
were added to the chilled water treatments and
Sample Collection agitated with a stick to mimic movement in
an online decontamination tank. Samples were
Six chilled treatments (water, 0.003% Chlo- treated for either 10, 20, or 30 s contact time
rine, 0.07% PAA [17], 0.1% PAA, 0.35% CPC in a single beaker with treatments listed. After
1146 JAPR: Research Report

Figure 1. Effectiveness of various antimicrobial treatments at different contact times in reducing Salmonella
Typhimurium. Different letters (A to F; x and y) indicate significant differences between means of treatments or
contact times (P ≤ 0.05).

removing the drumstick from the beaker, each Statistical Analysis


sample was placed into a sterile filter bag with
25 mL BPW. Briefly, each sample was shaken All microbial data was converted to log
for 1 min to rinse bacteria off of the drumstick. CFU/mL before analysis in the statistical model.
Serial dilutions were made with the rinsate using Zero cannot be statistically analyzed, so a value
BPW and plated on the appropriate media plate of 0.69 was assigned instead. Statistical Analysis
for bacteria detection. of the data was conducted using SAS 9.1 soft-
ware [21]. General Linear Model of SAS was
used to analyze the data and comparisons were
Enumeration of Salmonella and made using LSMEANS. Significant differences
Campylobacter (P < 0.05) were identified.

Salmonella Typhimurium in drumstick rinse


samples was enumerated by serially diluting
samples and spread plating (0.1 mL) on selec-
RESULTS AND DISCUSSION
tive media. Appropriate dilutions were plated on Antimicrobial Efficacy on Salmonella
XLT4 with nalidixic acid (0.05%) for the selec-
tive plating and were incubated for 24 h at 37◦ C. Figure 1 shows the recovery of 106 CFU/mL
Black colonies were counted and results were of Salmonella on the positive control samples
reported as log CFU/mL, comparing untreated inoculated with 2.5 × 106 CFU/mL Salmonella.
samples to treated samples. For the negative control samples, which were
For Campylobacter, rinsate was serially di- not inoculated, the bacterial level was under
luted and spread plated (0.1 mL) on Campy CE- the detection limit of 0.69 CFU/mL (i.e., no
FEX for selective plating. Plates were incubated background Salmonella on the drumsticks, 0.69
for 48 h at 42◦ C in AnaeroPack rectangular jars was calculated by estimating 1 colony on one
with a microaerophilic environment of 5% O2 , of the duplicate plates of the original rinsate).
10% CO2 , and 75% N2 , generated by CampyGen There were significant differences (P < 0.05)
sachets. Colonies were counted, and results were among the six antimicrobial treatments. Water
reported as log CFU/mL, comparing untreated and 0.003% chlorine treatments resulted in a
samples to treated samples. 1 log reduction compared to the positive control,
ZHANG ET AL.: ANTIMICROBIAL CONTACT TIME 1147

while both concentrations of PAA resulted in a exposure times were required, respectively, to
2 log reduction. Chen et al. [7] found that inocu- obtain a 4.5 log reduction. To inhibit bacterial
lated parts treated with a water or 0.35% chlorine attachment, 0.4% of CPC with 1, 3, and 10 min
immersion treatment (20 s contact time) reduced pre-treatment contact times resulted in 1.72,
Salmonella by approximately 0.3 log compared 1.60, and 2.63 log inhibition, respectively; for
to the positive control. Bauermeister et al. [8] 3 min pre-treatment time, inhibition was 0.90,
determined that 0.02% PAA was more effective 0.91, 1.60, and 1.90 log with CPC concentra-
than 0.0025% PAA in reducing Salmonella spp. tions of 0.1%, 0.2%, 0.4%, and 0.8%. The most
with a 30 min contact time. The results in our marked inhibition (4.9-log) inhibition of bacte-
current study did not find any differences in an- rial attachment was achieved at a CPC concen-
timicrobial efficacy against Salmonella between tration of 0.8% with 10 min pre-treatment time.
the different levels of PAA (0.07% and 0.1%) In the current study, 10, 20, and 30 s contact time
with the short contact time, which is similar to were tested, while Breen et al. [26] used extended
other studies using the higher levels of PAA and contact times of 1, 3, and 10 min. However, cur-
short contact times in an immersion treatment rent regulations state that CPC applied in an im-
[7, 9, 11]. As for the CPC, the higher concentra- mersion application should have no more than
tion (0.6%) was more effective than the 0.35% 10 s of contact time [6].
level. While, the contact times had no difference
in effectiveness for the 0.35% CPC, the 0.60% Antimicrobial Efficacy on Campylobacter
CPC did have an increased effectiveness for the
30 s contact (P > 0.05). Li et al. [22] stated that As shown in Figure 2, drumsticks inoculated
there was limited research on contact time and with 250 μL of 108 CFU/mL Campylobacter
concentration. In their research, the efficacy resulted in a 5.5 log CFU/mL recovery in the
of 30 and 90 s of spraying time using different positive control samples. For the negative con-
antimicrobials (0.85% sodium chloride (NaCl), trol, the bacterial level was under the detection
5% or 10% trisodium phosphate (TSP), 5% or limit (i.e., no background Campylobacter was
10% sodium bisulfate (SBS), 0.1% CPC, etc.) present on the drumsticks). There were signifi-
were tested on chicken carcasses, and the results cant differences (P < 0.05) among the remaining
showed that longer contact times (90 s) worked six antimicrobial treatments. Both concentra-
better than shorter (30 s). While it is hard to make tions of CPC (0.35% and 0.6%) were more ef-
a direct comparison between a spray treatment fective than the other antimicrobials, resulting in
and the dip treatments used in this study, Li et al. an approximate 4 log reduction compared to the
[22] did conclude that the longer the contact positive control. Chen et al. [7] demonstrated that
time for the 0.1% CPC spray treatment was CPC at 0.35% and 0.6% obtained approximately
more effective, which also supported the results 0.8 log reduction on Campylobacter on boneless
for the 0.6% CPC found in the current study. chicken parts that were incorporated into ground
Based on earlier studies, spraying methods are chicken when applied in a decontamination tank.
less effective than dipping methods in applying There were no significant differences between
antimicrobials [23–25]. In the current study, the two CPC concentrations. Cook and Beers
both 0.35% and 0.6% CPC were found effective [12] stated that CPC at concentrations of 0.1%,
in reducing Salmonella. The highest reduction 0.2%, 0.3% and 0.4% were effective in reducing
in Salmonella was found with the longest Campylobacter on poultry carcasses. Both con-
contact time (30 s) and highest concentration of centrations of PAA (0.07% and 0.1%) resulted
CPC (0.6%). in a 2 log reduction when compared to the pos-
Breen et al. [26] demonstrated that CPC was itive control. Zhang et al. [11] found that PAA
able to reduce bacteria attached to chicken skin (0.07% or 0.1%) applied in a decontamination
and also inhibit bacterial attachment to chicken tank reduced Campylobacter on chicken parts by
skin. The efficacy of CPC was both concentra- 1.5 logs. The mechanical action of water alone
tion and exposure time dependent. To remove resulted in a 1 log reduction of Campylobac-
attached bacteria, concentrations of CPC 0.8%, ter compared to the positive control. Chlorine
0.4%, and 0.2% with 1, 3, and 10 min CPC at 0.003% concentration was no more effective
1148 JAPR: Research Report

Figure 2. Effectiveness of various antimicrobial treatments at different contact times in reducing Campylobacter
jejuni. Different letters (A to F; x and y) indicate significant differences between means of treatments or contact
times (P ≤ 0.05).

than the mechanical action of the water treatment CONCLUSIONS AND


(P > 0.05). These results are consistent with APPLICATIONS
previous studies [7, 9, 11]. Contact times had
no effect (P > 0.05) on the effectiveness of the 1. This study indicated that CPC was the most
antimicrobials, with the exception of the 0.07% effective antimicrobial against Salmonella
PAA treatment, where the shorter contact time and Campylobacter. However, CPC can
(10 s) had the greatest reduction in this current have higher costs associated with startup
study. and use because regulations require recap-
Research conducted by Chantarapanont et al. turing before disposal. Additionally, higher
[27] tested the effectiveness of chlorine (0.004% concentrations were more effective in reduc-
or 0.01%) and PAA (0.004% or 0.01%) for 2 ing Salmonella but not Campylobacter.
and 15 min contact time. The results showed that 2. PAA was also an effective antimicrobial
40 ppm chlorine has similar efficacy when ap- tested in this study, and the concentration
plied either for 2 or 15 min. However, 0.01% of PAA had no impact on its efficacy.
chlorine had a 0.97-log CFU/mL reduction of 3. Each company would need to determine the
Campylobacter jejuni when applied for 15 min, cost-benefit associated with the selection of
while only a 0.65-log CFU/mL reduction with a each antimicrobial for a particular process.
2 min contact time. For PAA, the 15 min contact
time was more effective than the 2 min contact
time for both concentrations. This is most likely REFERENCES AND NOTES
due to the different mechanisms of action for 1. National Chicken Council. 2018. Per Capita Con-
PAA and chlorine. PAA eliminates microorgan- sumption of Poultry and Livestock, 1965 to Forecast 2019,
in Pounds. Available at: https://www.nationalchickencouncil.
isms by oxidation and subsequent disruption of org/about-the-industry/statistics/per-capita-consumption-of-
their cell membrane [28]. Whereas, chlorine di- poultry-and-livestock-1965-to-estimated-2012-in-pounds/.
rectly acts on the cellular membrane and disrupt- Accessed 16 January 2019.
ing fundamental cellular processes [29]. Thus, 2. Batz, M. B., S. Hoffmann, and J. Glenn. 2011. Rank-
ing the risks: the 10 pathogen-food combinations with the
chlorine needs longer contact times than PAA to greatest burden on public health. University of Florida,
be an effective antimicrobial. Gainesville, Florida.
ZHANG ET AL.: ANTIMICROBIAL CONTACT TIME 1149

3. USDA, The Food Safety and Inspection Service. 12. Cook, P., and K. Beers. 2015. Efficacy of cetylpyri-
2011. New performance standards for Salmonella and dinium chloride for the reduction of Campylobacter on
Campylobacter in young chicken and turkey slaugh- poultry carcasses. Presented at the International Association
ter establishments: response to comments and announce- for Food Protection, Portland, OR, 25 to 28 July 2015.
ment of implementation schedule. Fed. Regist. 76:15282– 13. Acumedia Manufactures Inc., Lansing. MI.
15290. 14. Sorvall Legent RT+ Centrifuge, Thermo Scientific,
4. USDA, The Food Safety and Inspection Service. Thermo Electron Corp., Osterode and Harz, Germany.
2016. New performance standards for Salmonella and 15. Oxoid, Ogdensburg, NY.
Campylobacter in not-ready-to-eat comminuted chicken and
turkey products and raw chicken parts and changes to re- 16. Collected from Auburn University poultry research
lated agency verification procedures: response to comments park.
and announcement of implementation schedule. Fed. Regist. 17. Spectrum; FMC, Philadelphia, PA.
81:7285–7300. 18. Cecure; Safe Food Corporation, North Little Rock,
5. McKee, S. R. 2011. Salmonella and Campylobacter AR.
control during poultry processing. Presented at the Inter- 19. Hach Company, Loveland, CO.
national Poultry Scientific Forum, Atlanta, GA, 24 to 25 20. PeroxyChem, Safe Foods Corporation.
January 2011.
21. SAS Institute, Cary, N.C.
6. U.S. Department of Agriculture, Food Safety and In-
spection Service. 2018. Safe and suitable ingredients used 22. Li, Y., M. F. Slavik, J. T. Walker, and H. Xiong. 2010.
in the production of meat, poultry, and egg products. FSIS Pre-chill spray of chicken carcasses to reduce Salmonella
Directive 7120.1. Rev. 48. U.S. Department of Agriculture, Typhimurium. J. Food Science 62:605–607.
Food Safety and Inspection Service, Washington, DC. 23. Kim, J. W., and M. F. Slavik. 1996. Cetylpyridinium
7. Chen, X., L. J. Bauermeister, G. N. Hill, M. Singh, chloride (CPC) treatment on poultry skin to reduce attached
S. F. Bilgili, and S. R. McKee. 2014. Efficacy of various Salmonella. Journal of Food Protect 59:322–326.
antimicrobials on reduction of Salmonella and Campylobac- 24. Kemp, G. K., M. L. Aldrich, and A. L. Waldroup.
ter and quality attributes of ground chicken obtained from 2000. Acidified sodium chlorite antimicrobial treatment of
poultry parts treated in a postchill decontamination tank. broiler carcasses. J. Food Protect. 63:1087–1092.
J Food Protect 77:1882–1888. 25. Wideman, N., M. Bailey, S. F Bilgili, H. Thippareddi,
8. Bauermeister, L. J., J. W. Bowers, J. C. Townsend, L. Wang, C. Bratcher, M. Sanchez-Plata, and M. Singh. 2016.
and S. R. Mckee. 2008. The microbial and quality proper- Evaluating best practices for Campylobacter and Salmonella
ties of poultry carcasses treated with peracetic acid as an reduction in poultry processing plants. Poult. Sci. 95:306–
antimicrobial treatment. Poult. Sci. 87:2390–2398. 315.
9. Nagel, G. M., L. J. Bauermeister, C. L. Bratcher, 26. Breen, P. J., H. Salari, and C. M. Compadre. 1997.
M. Singh, and S. R. McKee. 2013. Salmonella and Elimination of Salmonella contamination from poultry tis-
Campylobacter reduction and quality characteristics of sues by cetylpyridinium chloride solutions. J. Food Protect
poultry carcasses treated with various antimicrobials in a 60:1019–1021.
post-chill immersion tank. Int. J. Food Microbiol. 165: 27. Chantarapanont, W., M. E. Berrang, and J. F. Frank.
281–286. 2004. Direct microscopic observation of viability of Campy-
10. Waldroup, A. L., K. L. Beers, P. E. Cook, E. A. Dell, lobacter jejuni on chicken skin treated with selected chemical
R. Odglen, and R. A. Baker. 2010. The effects of cetylpyri- sanitizing agents. J. Food Protect. 46:1146–1152.
dinium chloride (cecure R cpc antimicrobial) on Campy- 28. Chen, J. H., Y. Ren, J. Seow, T. Liu, W. S. Bang,
lobacter spp. on raw poultry: a review. Int. J. Poult. Sci. and H. G. Yuk. 2012. Intervention technologies for ensuring
9:305–308. microbiological safety of meat: current and future trends.
11. Zhang, L., L. J. Garner, S. R. Mckee, and S. F. Compr. Rev. Food Sci. Food Safety 11:119–132.
Bilgili. 2018. Effectiveness of several antimicrobials used 29. U.S. Department of Agriculture. 2002. The use of
in a postchill decontamination tank against Salmonella and chlorine dioxide as an antimicrobial agent in poultry process-
Campylobacter on broiler carcass parts. J. Food Protect. ing in the United States. USDA-FSIS, Office of International
81:1134–1141. Affairs. Nov, 2002.

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