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Recovery of Bacteria from Broiler Carcasses after Spray Washing with Acidified Electrolyzed Water or Sodium Hypochlorite Solutions

J. Northcutt^*,1, D. Smith, K. D. Ingram^*, A. Hinton, Jr.^* and M. Musgrove

^* USDA, Agricultural Research Service, Poultry Processing and Swine Physiology Research Unit, Athens GA 30604; USDA, Agricultural Research Service, Quality Assesment Research Unit, Athens, GA 30604; USDA, Agricultural Research Service, Egg Quality and Safety Research Unit, Athens, GA 30604

¹ Corresponding author: jnorthcutt{at}saa.ars.usda.gov

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
A study was conducted to investigate the effects of spray washing broiler carcasses with acidified electrolyzed oxidizing water (EO) or sodium hypochlorite (HOCl) solutions for 5, 10, or 15 s. Commercial broiler carcasses were contaminated with 0.1 g of broiler cecal contents inoculated with 10⁵ cells of Campylobacter and 10⁵ cells of nalidixic acid-resistant Salmonella. Numbers of bacteria recovered from unwashed control carcasses were 6.7, 5.9, 6.3, and 3.9 log₁₀ cfu/mL for total aerobic bacteria, Escherichia coli, Campylobacter, and Salmonella, respectively. Washing in either EO (50 mg/L of sodium hypochlorite, pH 2.4, oxidation reduction potential of 1,180 mV) or HOCl (50 mg/L of sodium hypochlorite, pH 8.0) significantly reduced the levels of bacteria recovered from carcasses (P < 0.05). Carcasses washed with EO had slightly lower levels of total aerobic bacteria (0.3 log₁₀ cfu/mL) and E. coli (0.2 log₁₀ cfu/mL) than HOCl-treated carcasses; however, populations of Campylobacter and Salmonella were comparable after washing in either solution. Increasing the carcass washing time from 5 to 10 s lowered the levels of total aerobic bacteria (6.1 vs. 5.8 log₁₀ cfu/mL), E. coli (4.6 vs. 4.1 log₁₀ cfu/mL), Campylobacter (5.2 vs. 4.2 log₁₀ cfu/mL), and Salmonella (2.0 vs. 1.2 log₁₀ cfu/mL), but no further microbiological reductions occurred when washing time was extended from 10 to 15 s. Data from the present study show that washing poultry carcasses with EO is slightly better (total aerobic bacteria and E. coli) or equivalent to (Campylobacter and Salmonella) washing with HOCl. Washing broiler carcasses for a period equivalent to 2 inside-outside bird washers (10 s) provided greater reductions in carcass bacterial populations than periods simulating 1 (5 s) or 3 inside-outside bird washers (15 s).

Key Words: broiler processing • carcass washing • acidified electrolyzed water • chlorine

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
During poultry processing, carcasses may become contaminated with partially digested feed (ingesta) or fecal material (Wabeck, 1972) that must be removed before the carcasses enter the chiller (USDA, 1997). To meet the zero tolerance policy on visible carcass fecal contamination and the mandated pathogen reduction performance standards (USDA, 1996), poultry processing establishments have incorporated multiple microbiological intervention strategies. These intervention strategies have included antimicrobial treatments applied in carcass washers, brushes, cabinet sprays, and dip tanks (Jackson and Curtis, 1998; Northcutt and Jones, 2004). In some establishment, a series of inside-outside bird washers (IOBW) have been installed on a single processing line to insure compliance with the zero tolerance policy for visible carcass fecal material (Jackson and Curtis, 1998; Bashor et al., 2004). Other establishments have resorted to using combinations of antimicrobial treatments (Northcutt and Jones, 2004).

The most common antimicrobial treatment used in IOBW for decontamination of poultry is chlorine (sodium hypochlorite), because it is inexpensive, safe, and easy to use (White, 1998; Northcutt and Jones, 2004). However, failure to optimize the disinfectant properties of chlorine (improper pH, concentration, or composition of incoming water) may reduce its antimicrobial efficacy and can result in offensive and harmful odors such as chlorine gas and trichloramines (Northcutt and Lacy, 2000). For this reason, there has been tremendous interest in developing acceptable alternatives to chlorine for use on poultry. Some of the antimicrobial treatments that have been used on poultry carcasses include chlorine dioxide, trisodium phosphate, cetylpyridinium chloride, ozone, hydrogen peroxide, lactic acid, acidified sodium chlorite, monochloramine, sodium metasilicate, sodium bisulfate, peroxya-cetic acid, and citric acid blended with hydrochloric and phosphoric acids (Yang and Chen, 1979; Sheldon and Brown, 1986; Mulder et al., 1987; Izat et al., 1990; Lillard, 1990, 1994; Kim et al., 1994, 1996; Hwang and Beuchat, 1995; Li et al., 1997; Xiong et al., 1998a,b; Yang et al., 1998; Kemp et al., 2000, 2001; Volk, 2004; Russell and Axtell, 2005). However, none of these treatments has been able to replace chlorine in the poultry industry. Recent studies have focused on the antimicrobial properties of a chemical derivative of chlorine known as acidified electrolyzed oxidizing water (EO; Yang et al., 1998; Venkitanarayanan et al., 1999; Park et al., 2002; Deza et al., 2003; Koseki et al., 2004; Russell, 2003; Bialka et al., 2004; Fabrizio and Cutter, 2004; Park et al., 2005). Acidified electrolyzed oxidizing water is produced by applying an electrical current to sodium chloride solutions and separating the fractions into acidic (anode) and basic (cathode) components. Acidified EO contains hypochlorous acid (active ingredient in chlorine) and small amounts of hydrochloric acid, hydrogen peroxide, ozone, and chlorine oxides (Park et al., 2002). Antimicrobial properties of acidified EO result from the synergistic effects of the low pH, high oxidation reduction potential, and high chlorine content of the water.

Research on acidified EO has shown that it reduces the level of Escherichia coli O157:H7 on the surfaces of kitchen cutting boards (Venkitanarayanan et al., 1999), lettuce (Koseki et al., 2004), and tomatoes (Deza et al., 2003). Reductions in numbers of Listeria monocytogenes, Salmonella Typhimurium, and Campylobacter coli have also been reported after applying acidified EO to fresh pork (Fabrizio and Cutter, 2004). Acidified EO has also been found to decrease levels of Salmonella Enteritidis, Salmonella Typhimurium, and L. monocytogenes recovered from shell egg surfaces after spraying or soaking (Russell, 2003; Bialka et al., 2004; Park et al., 2005). A study on chicken wings reported a 3 log cfu/mL reduction in numbers of Campylobacter jejuni after a 30-min exposure to acidified EO or chlorine (Park et al., 2002). Another study demonstrated that neutral EO (pH > 6.5) applied to chicken carcasses (17 s, 414 kPa) in a prototype IOBW caused a greater reduction (by 0.5 log) in inoculated numbers of Salmonella than chlorine (Yang et al., 1998). However, the exposure time was longer than typical commercial IOBW, which operate with a 4- to 5-s dwell time. The objective of this study was to compare the microbiological characteristics of chicken carcasses treated with acidified EO or chlorinated water for 5, 10, or 15 s.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Carcass Treatments
On each of 3 different sampling days, 30 eviscerated broiler carcasses were removed from a commercial poultry processing line after evisceration and before entering the final bird washer. Carcasses were placed individually into plastic bags, packed into coolers, and transported to the pilot processing plant for treatment (<2 h after slaughter). Ten gastrointestinal tracts were also collected from the broiler evisceration line, placed into a single bag, and transported to the pilot plant. Twenty ceca were opened, emptied into a weigh boat, and mixed with a spatula for approximately 1 min. After mixing, cecal contents (4.95 g) were inoculated with a cosuspension (0.1 mL) containing 10⁸ cells of C. jejuni and 10⁸ cells of nalidixic acid-resistant Salmonella (mixed culture of Salmonella Typhimurium, Salmonella Montevideo, Salmonella Enteritidis). The inoculated cecal material (0.1 g) was applied using a sterile spatula to each carcass, and the carcasses were held at room temperature (27°C) for 12 min before washing. Based on line speed, 12 min was selected as the holding time to simulate the longest potential contamination time in a commercial facility. Carcasses were divided into 3 treatment groups: control, acidified EO, and chlorine (HOCl). Control carcasses were subjected to a whole carcass rinse (WCR) for bacteria recovery. Carcasses assigned to the EO treatment group were washed for 5, 10, or 15 s with EO containing 50 mg/L of total chlorine. Carcasses assigned to the HOCl treatment group were washed with 50 mg/L of sodium hypochlorite (HOCl) for 5, 10, or 15 s. Immediately after washing, carcasses were drained (1 min) of excess solution and subjected to a WCR.

Fifty milligrams per liter of acidic EO (pH 2.4, oxidation reduction potential of 1,180 mV) was prepared on the same day as sampling using an EO generator (Electric Aquagenics Unlimited Inc., Lindon, UT), which was filled with a 20% (wt/vol) solution of sodium chloride. After the generator had stabilized (approximately 10 amperage), acidic EO was collected from the anode side of the generator. The 50 mg/L of HOCl solution (pH 8.0) was prepared immediately before application by mixing approximately 125 mL of 6.15% commercial bleach (Clorox Co., Oakland, CA) in 150 L of tap water. The pH of the HOCl and EO solutions was measured before spraying the carcasses using a handheld pH meter (AP5, Denver Instrument, Denver, CO). Total chlorine in the HOCl solution was measured after mixing and before carcass application using a colorimetric reaction with N, N-diethyl-p-phenylen-ediamine from the CHEMetrics 2 SAM test kit (CHEMetrics Inc., Calverton, VA). The total chlorine concentration of the EO was determined using the iodometric titration method with the Hach hypochlorite test kit (CN HRDT, Hach Co., Loveland, CO).

The spray cabinet was an individual carcass unit consisting of a pressure pump and a pressure regulator attached to a metal frame with Plexiglass sides. Cabinet dimensions were 91 x 91 x 76 cm (length x width x height). The center of the cabinet consisted of a wire cone with a spray nozzle in the center of the cone. There were 3 additional nozzles on each of 4 sides for washing the outside of the carcasses. Carcasses were placed on the wire cone in an upright position for washing. During the spray washing with EO or HOCl, each carcass received approximately 3, 6, or 9 L of solution for 5, 10, or 15 s, respectively. The IOBW was operated at a water pressure of 552 kPa.

Salmonella and Campylobacter Inoculation
The inoculum cultures were prepared according to the procedure described by Bailey et al. (1998). Three strains of nalidixic acid-resistant Salmonella (Salmonella Typhimurium, Salmonella Montevideo, and Salmonella Enteritidis) were used to inoculate carcasses. To prepare the inoculum, the cultures were streaked onto brilliant green sulfa agar (Difco Laboratories, Detroit, MI) plates containing 200 mg/L of nalidixic acid (Sigma Chemical Co., St. Louis, MO). Plates were incubated overnight at 37°C. A bacterial suspension was prepared in physiological saline solution, and the optical density (Spectronic 20D+, Thermo Electron Corporation, Waltham, MA) at 540 nm was measured to determine the concentration of the inoculum. Campylobacter jejuni cultures were streaked on Campy-Cefex agar (Stern et al., 1992) and incubated at 42°C for 24 h under microaerophilic conditions (5% O₂, 10% CO₂, and balance N₂) in a BBL GasPak jars (Becton, Dickson and Co., Sparks, MD) with an activated BBL CampyPak for 24 h. A bacterial suspension of Campylobacter was prepared in physiological saline solution, and the optical density at 540 nm was measured to determine the concentration. The 2 suspensions of Campylobacter and Salmonella were combined (1:1) to prepare the final inoculum. The final inoculum and the cecal material containing the inoculum were plated onto brilliant green sulfa agar (with nalidixic) or Campy-Cefex agar to confirm the levels added to carcasses.

Microbiological Analyses
The same plating and incubation procedures described above were used for recovery of Salmonella and Campylobacter from the carcasses rinses. Control and treated carcasses (EO and HOCl) were subjected to a low-volume WCR procedure by placing individual carcasses into a plastic bag, adding 100 mL of sterile neutralizing buffer (Difco Laboratories), and shaking the carcasses in a rotating mechanical shaker for 1 min. After shaking, carcasses were removed aseptically, and the rinse was sampled for bacteria recovery. Serial dilutions of the rinsate were made in 0.1% buffered peptone water. Total aerobic bacterial populations were enumerated on plate count agar (Becton, Dickson and Co.). A 0.1-mL sample from a serial dilution of the rinsate was plated in duplicate on the surface of the plate count agar and incubated at 35°C for 48 h before counting the resulting colony-forming units. Escherichia coli was enumerated by transferring 1 mL from the serial dilutions onto 3M petrifilm (3M Health Care, St. Paul, MN). Petrifilm plates were incubated at 35°C for 24 h. Blue colonies with entrapped gas were counted as E. coli. Campylobacter was enumerated by plating 0.1 mL from the serial dilutions onto Campy Blood agar (Blaser et al. 1979) and incubating the plates at 42°C for 36 h in a microaerophilic environment (5% O₂, 10% CO₂ and balance N₂). Colony-forming units characteristic of Campylobacter were counted. Each colony type identified as Campylobacter was confirmed for genus by examination of cellular morphology and motility on a wet mount under phase-contrast microscopy. Each colony type was confirmed as Campylobacter spp. using INDX-Campy (jcl) culture confirmation test (Integrated Diagnostics, Baltimore, MD). Nalidixic acid-resistant Salmonella counts were made by plating 0.1 mL from a serial dilution of the rinse diluent onto duplicate brilliant green sulfa plates containing 200 mg/L of nalidixic acid and 25 mg/L of novobiocin (Sigma-Aldrich, St. Louis, MO).

Statistical Analysis
Data were analyzed by the GLM procedure of the SAS/STAT program using treatment (control, EO, or HOCl), washing time (5, 10, 15 s), and replicate as main effects (SAS Institute, 2000). Analyses were performed on the data after logarithmic transformation and included analyzing the change in the counts due to washing (counts on inoculated washed carcasses minus counts on control carcasses). All first-order interactions were tested for statistical significance (P < 0.05) using the residual error MS. Because no significant replication or interaction effects were detected, the analysis was repeated after pooling the data over replicate and main effects.

	RESULTS AND DISCUSSION

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Table 1 shows the mean logarithmic microbial counts (log₁₀ cfu/mL) for total aerobic bacteria, E. coli, Campylobacter, and nalidixic acid-resistant Salmonella recovered from inoculated chicken carcasses before washing (control) or after washing with EO and HOCl. Washing in either EO or HOCl removed visible fecal material and lowered the numbers of bacteria recovered in the WCR (P < 0.05). When numbers of bacteria recovered from control and EO washed carcasses were compared, washing with EO reduced levels of total aerobic bacteria, E. coli, Campylobacter, and Salmonella by 1.0, 1.7, 1.9, and 2.7 log₁₀ cfu/mL, respectively. Similarly, populations of bacteria recovered from carcasses washed with HOCl were 0.7, 1.5, 1.6, and 2.4 log₁₀ cfu/mL lower than control carcasses for total aerobic bacteria, E. coli, Campylobacter, and Salmonella, respectively. These data are in agreement with those previously reported by Northcutt et al. (2005), who found that washing broiler carcasses with 50 mg/L of HOCl reduced numbers of total aerobic bacteria (2.3 log₁₀ cfu/mL), E. coli (2.1 log₁₀ cfu/mL), Campylobacter (2.5 log₁₀ cfu/mL), and Salmonella (0.9 log₁₀ cfu/mL).

The present study also investigated the inactivation of bacteria after different washing times (5, 10, or 15 s), because multiple IOBW in series on a single processing line has been suggested to be more effective at removing visible carcass contamination than a single IOBW (Bashor et al., 2004). This strategy has been recommended in the USDA’s Compliance Guidelines for Controlling Salmonella on Poultry (USDA, 2006). Previous research has shown that reductions in bacteria populations from poultry carcasses after washing in an IOBW were primarily due to the efficiency of the washer rather than the antimicrobial treatment (Izat et al., 1988; Bautista et al., 1997; Park et al., 2002; Northcutt et al., 2003, 2005). Northcutt et al. (2003) studied the microbiological effects of commercial IOBW in 3 different poultry establishments and reported comparable levels of coliforms and E. coli for pre- and postwashed carcasses. Inconsistencies in chlorine levels (0.5 to 33 mg/L) were cited as a possible reason for similar coliform and E. coli counts before and after washing (Northcutt et al., 2003). In another study, Northcutt et al. (2005) reported no difference in numbers of total aerobic bacteria, E. coli, and Campylobacter recovered from carcasses washed with 0 or 50 mg/L of HOCl heated to different temperatures (21.1, 43.3, or 54.4°C). It has been suggested that the limited reductions in microbial loads after carcass washing with HOCl could be due to short contact time, inactivation by organic material, changes in the chlorine concentration during application, and physical barriers (surface liquid film) prohibiting HOCl from contacting the bacteria (Baran et al., 1973; Mead et al., 1975; Teotia and Miller, 1975; Emswiler et al., 1976; Thomas and McMeekin, 1980; Bautista et al., 1997).

Research has suggested that higher volumes of water in IOBW may remove more bacteria from poultry than lower volumes, but the results were inconsistent, and antimicrobial treatments were not used (Mulder and Bolder, 1981; Geornaras and von Holy, 2000). Commercial IOBW in the United States typically have a dwell time of 4 to 5 s. To evaluate the microbiological effects of using multiple carcass washers, carcasses were sprayed for periods corresponding to 1 (5 s), 2 (10 s), or 3 (15 s) IOBW. Table 2 shows the numbers of total aerobic bacteria, E. coli, Campylobacter, and Salmonella recovered from inoculated chicken carcasses after washing in an IOBW for 5, 10, or 15 s. Statistical analyses of the data showed that there was no treatment (EO or HOCl) x time interaction effect on the dependent variables (bacterial counts); therefore, EO and HOCl data were combined across washing times. As the length of washing time was increased from 5 to 15 s, levels of total aerobic bacteria, E. coli, Campylobacter, and Salmonella were reduced by 0.3, 0.5, 1.0, and 0.8 log₁₀ cfu/mL, respectively (P < 0.05). The inoculated populations (Campylobacter and Salmonella) were more sensitive (greater reductions) to the disinfectant properties of the sprays than the other microorganisms, and this may have resulted from insufficient skin attachment. Mulder and Bolder (1981) found that spray washing with 2.5 L/carcass reduced both total aerobic bacteria and Enterobacteriaceae by 1.0 log₁₀ cfu/mL, whereas 0.4 L/carcass gave no reduction in total aerobic bacteria and a reduction of 0.11 log₁₀ cfu/mL in Enterobacteriaceae. Data from the present study seem to suggest that removal of bacteria from carcasses during washing stabilizes after 10 s. Similar results were reported by Lillard (1988, 1989) in her evaluation of multiple 60-s rinses of the same carcasses in which the numbers of bacteria in the forth rinse were only slightly different from the first rinse.

Data collected during the present study demonstrate that washing poultry carcasses with EO is comparable to HOCl for reducing numbers of bacteria. Moreover, increasing the carcass washing time from 5 to 10 s caused a greater reduction in populations of total aerobic bacteria, E. coli, Campylobacter, and Salmonella than was observed when time was increased from 10 to 15 s.

Received for publication December 18, 2006. Accepted for publication May 21, 2007.

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