1

4 Improvements for
5 Poultry Slaughter Inspection

7 Appendix C – Literature Review of the

8 Poultry Slaughter Process
9

10

11
12 APPENDIX C – LITERATURE REVIEW OF THE
13 POULTRY SLAUGHTER PROCESS
14 Live Receiving and Live Hanging

15 Live receiving is the initial step in the poultry slaughter process and begins when live poultry are
16 received onto the official premise. Live hanging is the process of suspending live poultry in
17 shackles after removing them from transport cages and begins when transport cages are off-
18 loaded. With chemical immobilization, live poultry may be immobilized prior to hanging.

19 Potential Risk Factors

20 Potential biological risk factors exist during live receiving and live hanging and include
21 pathogenic and non-pathogenic microorganisms on the feathers and skin, and in the crop, cecum,
22 and colon contents of live poultry. Salmonella and Campylobacter are significant pathogens;
23 psychrophilic microorganisms are significant spoilage organisms; and other microorganisms are
24 indicators of sanitation process control.

25 Large numbers of microorganisms can be found on live poultry at live receiving. Kotula and
26 Pandya (1995) found that 60.7 percent of feather samples and 41.8 percent of skin samples
27 contained 6.7 log10 and 5.9 log10 Salmonella/gram (g) respectively. Byrd et al. (1998) found
28 Campylobacter spp. in 62 percent of crops and 4 percent of ceca. Wempe et al. (1983) recovered
29 3.8 to 4.8 log10 and 5.5 to 6.8 log10 C. jejuni/g of feathers and cecal content, respectively.
30 Berrang et al., found more Campylobacter in feathers (5.4 log10) than in skin (3.8 log10, p<0.05)
31 but other enterics did not differ at the two sites. Cloaca harbored more microbes (including
32 E. coli and other coliforms) than any other site (p<0.05). Kotula and Pandya (1995) found that
33 77.5 percent of feather samples and 57.5 percent of skin samples contained 7.4 log10 and
34 6.5 log10 Campylobacter jejuni/g. respectively. Geornaras et al. (1997) found 3.8 log10
35 Pseudomonas/g of feathers. Mead et al. (1993) found 2 to 2.8 log10 Pseudomonas/g neck skin.
36 Kotula and Pandya (1995) reported that the feathers and skin contained 7.9 log10 and 6.7 log10
37 E. coli/g, respectively.

38 Microorganisms present in/or live poultry at live receiving can cross-contaminate product.
39 Bryan et al. (1968) demonstrated that Salmonella enters the establishment on incoming turkeys
40 and contaminates equipment and subsequent poultry products. Clouser et al. (1995a) found that
41 when Salmonella was present on the surface of turkeys prior to processing, the incidence of
42 Salmonella tended to increase throughout the slaughter process. Herman et al. (2003) concluded
43 that establishments cannot avoid contamination when C. jejuni-positive poultry are delivered to
44 live receiving. Furthermore, there is a statistically significant correlation (p<0.001) between
45 contamination of the carcass and presence of the microbe after processing. Berrang et
46 al. (2003b) found that >50 percent of Campylobacter-negative broilers were Campylobacter-
47 positive following exposure to feces in a commercial dump cage. Newel et al. (2001)
48 demonstrated a link between Campylobacter-positive poultry at live receiving and
49 Campylobacter-positive carcasses following immobilization, exsanguination, scalding, feather
50 removal, evisceration, and chilling. Fluckey et al. (2003) demonstrated a link between
51 Campylobacter- and Salmonella-positive cecal content in live poultry and Campylobacter- and

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52 Salmonella-positive carcasses following evisceration and chilling. By using PFGE profiles,

53 which allows identification of specific serotypes, whole carcasses were sampled at eight stages
54 of turkey processing. Prevalence data showed that contamination rates varied along the line and
55 were greatest after defeathering and after chilling. The same profiles were found to be present
56 all along the processing line, while on other occasions, additional serotypes were recovered that
57 were not detected earlier on the line, suggesting that the birds harbored more than one serotype
58 of Salmonella, or there was cross-contamination occurring during processing (Nde et al. 2006).
59 Chemical potential risk factors introduced at live receiving include violative chemical residues
60 from a pharmaceutical, feed additive, pesticide, industrial compound, and/or environmental
61 contaminate present within the edible tissue of live poultry. The U.S. Department of Agriculture
62 (USDA), Food Safety and Inspection Service (FSIS) monitors poultry products for the presence
63 of chemical residues as part of its National Residue Program. Table C-1 lists monitoring results
64 from the 2003 National Residue Program.

65 Table C-1. National Residue Program Domestic Data (USDA, FSIS, OPHS, 2003)
Chlorinated Avermectins &
Sulfonamides Arsenicals Hydrocarbons Milbemycins
N P V N P V N P V N P V
Young Chicken 385 1,087 579 476
Mature Chicken 97 1 202 5 221 1
Young Turkey 234 502 4 249 1
Mature Turkey 234 2 97 1 1 214 5
Ducks 95 336 1 248
Geese 17 13 15
Squab 20 22
Ratite 5 10 5 7
N = number of analyses, P = number of non-violative positives, V = number of violations

66 Controls. Biological and chemical potential risk factors present in or on live poultry received
67 onto the official premise cannot be prevented, eliminated, or reduced to acceptable levels during
68 live receiving or live hanging. However, they can be reduced through preharvest interventions.
69 Berrang et al. demonstrated that when the level of microorganisms on live poultry at live
70 receiving is high, the presence of microorganisms on raw product is high, and visa versa.
71 Fluckey et al. (2003) found that the incidence of Salmonella and Campylobacter on the farm
72 correlates with Salmonella and Campylobacter incidence during evisceration. Campbell et
73 al. (1982) reported a 9 percent post-evisceration incidence of Salmonella from Salmonella-free
74 turkey flocks compared to 20 percent from non-Salmonella-free flocks. Producers can eliminate
75 chemical potential risk factors through pre-harvest interventions that control pharmaceutical and
76 chemical usage.

77 The National Chicken Council (NCC) (1992) and the National Turkey Federation (NTF) (2004)
78 recommend that poultry producers implement pre-harvest sanitation and production practices
79 shown to reduce hazards in edible poultry products. They recommend microbiological standards
80 for feeds. Davies et al. (2001) and Corry et al. (2002) traced Salmonella serotypes recovered
81 from the farm and during transportation back to the feed mills.

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 Appendix C – Literature Review of the Poultry Slaughter Process

82 The NCC and NTF also recommend bio-security, maintenance, and sanitation programs for
83 facilities and equipment to reduce pathogenic and nonpathogenic microorganisms in/on live
84 poultry prior to live receiving. Davies and Wray (1996) identified rodents and faulty application
85 of disinfectants as causes for the persistence of Salmonella in growing houses. Herman et al.
86 (2003) identified employee clothing as the source of Campylobacter-positive flocks. Evans and
87 Sayers (2000) identified important factors for preventing Campylobacter infection in a flock
88 including buildings in good repair, boot dips, high standards of cleaning, and disinfecting
89 drinking water. Higgens et al. (1981) demonstrated that failure to clean and disinfect air inlets
90 and fans contributed to recontamination of facilities with Salmonella. The microbial
91 composition of the air in a high-throughput chicken slaughtering facility was examined by
92 sampling various areas. It was found that the highest counts of microorganisms were recorded in
93 the initial stages of processing, comprising the receiving-killing and defeathering areas, whereas
94 counts decreased toward the evisceration, air-chilling, packaging, and dispatch areas (Lues et
95 al. 2007). Rose et al. (2000) identified the lack of cleaning and disinfection between flocks as a
96 significant risk factor for the persistence of Salmonella. Corry et al. (2002) and Slader et
97 al. 2002) linked failure to clean and sanitize transport crates with Campylobacter- and
98 Salmonella-positive poultry being received onto the official premise during live receiving.

99 The NCC and NTF further suggest proper feed and water withdrawal to minimize fecal and
100 ingesta contamination during processing. Wabeck (1972) recommended taking broilers off feed
101 and water 8 to 10 hours prior to slaughter. Bilgili (1988) found that decreasing feed withdrawal
102 times increased the likelihood of gastrointestinal breakage during processing. Northcutt et
103 al. (2003) determined that increasing feed withdrawal to 12 hours increased Campylobacter and
104 Salmonella levels in post carcass rinses 0.4 log10 CFU/ml and 0.2 log10 colony forming unit
105 (CFU)/milliliter (ml), respectively. Bilgili and Hess (1997) found that feed withdrawal periods
106 ≥14 hours increased intestine and gallbladder fragility, which increased fecal and bile
107 contamination during evisceration. Hinton et al. (2000, 2002) found that providing broilers with
108 a 7.5 percent glucose solution or a sucrose solution during feed withdrawal decreased the crop
109 pH, increased the level of lactobacillus, and decreased the incidence of Salmonella typhimurium
110 in the crop during feed withdrawal (p<0.05). Line et al. (1997) found that feeding
111 Saccharomyces boulardii, a non-pathogenic yeast, to broilers during feed withdrawal reduced the
112 incidence of Salmonella in the cecum during to crating and transport. Acidifying the drinking
113 water at the time of feed withdrawal may help also to reduce levels of Salmonella in incoming
114 birds. Byrd et al. (2001) found that administering organic acids at the time of feed withdrawal
115 maintained a more acidic pH in the crop and provided birds with an alternative to consuming
116 potentially contaminated litter. Offering birds an organic acid in the water significantly lowered
117 post-harvest crop contamination with Salmonella (p<0.001) and Campylobacter (p<0.001). This
118 type of treatment could be a cost-effective approach that does not require radical changes in
119 current management practices. Byrd et al. (2003) suggested that sodium chlorate added to the
120 water at the time of feed withdrawal could significantly reduce levels of Salmonella in the crop
121 and ceca.

122 Feed withdrawal may, however, affect the intestinal integrity, due to depletion of intestinal
123 mucus (Thompson and Applegate 2006) as well as reduction of digestive tract mass (Nijdam et
124 al. 2006), which can increase susceptibility to infection. Recent studies suggested that special
125 diets could be a good substitute for the feed withdrawal period held before transportation to the
126 processing plant. Special diets that show favorable results include semi-synthetic feed with high

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127 carbohydrate concentration (Delezie et al. 2006) or a commercial whole wheat diet (Rathgeber et
128 al. 2007). Alternatively, a commercial whole wheat diet fed prior to feed withdrawal eliminated
129 the deleterious effects on gut weight and content (Delezie et al. 2006).

130 In addition to biosecurity measures, producers have other means of reducing Salmonella in
131 poultry flocks. Vaccinations, especially those against S. enteritidis, reduce shedding of the
132 organism in the intestine as well as in organs including the ovaries, theoretically decreasing the
133 contamination of subsequently laid eggs (Davison et al. 1999). Reducing intestinal colonization
134 and, consequently, fecal shedding of S. enteritidis could provide two-fold protection by reducing
135 both vertical and horizontal transmission (Gast et al. 1993). After infection with S. enterica
136 serovars typhimurium or enteritidis, the high titers of Salmonella-specific antibodies achieved
137 has been shown to demonstrate a high degree of cross-reactivity against other serovars (Beal and
138 Smith 2007). Furthermore, live attenuated vaccines given to very young chicks have been shown
139 to provide protection through the “colonization-inhibition effect.” Because a chick’s gut is
140 devoid of microbial flora, there is extensive multiplication by the vaccine, making it difficult for
141 pathogenic organizations to become established (Barber et al. 1999). Autogenous bacterins are
142 important interventions, and the poultry industry has petitioned the Animal Plant Inspection
143 Service (APHIS) to rewrite the regulations to allow the use of autogenous vaccines.

144 Prebiotics and probiotics are established treatment alternatives for reducing Salmonella in
145 poultry. Gibson and Roberfroid (1995) define prebiotics as “a non-digestible food ingredient
146 that beneficially affects the host by selectively stimulating the growth and/or activity of one of a
147 limited number of bacteria in the colon.” Fuller (1989) defines probiotics as “live microbial feed
148 supplements which beneficially affect the host animal by improving its intestinal balance.” It is
149 believed that prebiotics and probiotics act as dietary resources that might be instrumental in
150 stabilizing gut flora, as well as helping to prevent pathogenic organisms from colonizing the gut
151 and causing disease (Holzapfel et al. 1998). Tellez et al. (2001) found that significantly less
152 Salmonella enteritidis was isolated from the cecum and tissue organs in birds treated with an
153 Avian Pac Plus® that contained probiotics and egg-source antibodies for S. enteritidis,
154 S. typhimurium, and S. heidleberg, as compared to untreated controls. Netherwood et al. (1999)
155 found that once probiotics were discontinued, the microflora returned to levels found in untreated
156 controls, suggesting that probiotics do not become established in the gut and continued use is
157 required.

158 Other interventions that show promise are yet to be implemented. As the potential risk factor
159 over antibiotic resistance increases, there has been renewed interest in exploiting the antibacterial
160 properties of bacteriophages and bacteriocins. More effective vaccines may eventually come
161 marketed within bacterial ghosts. Richardson et al. (2003) experimented with electric space
162 charges as a means of reducing airborne transmission of bacterial pathogens. The poultry
163 industry has continued interest in using undefined competitive exclusion (CE) products. Because
164 undefined CE products make therapeutic claims, the Food and Drug Administration (FDA)
165 classifies them as drugs. Since the FDA does not recognize these products as either safe or
166 effective, it has labeled them as unapproved new drugs. The FDA did approve a defined CE
167 product, PREMPT®, which has since been removed from the market. A recent study which
168 included 118 commercial turkey hen lots, ranging from 1,542 to 30,390 hens per lot, of either
169 Nicholas or Hybrid genetic lines was conducted to look at the effect of a selected commercial
170 Lactobacillus-based probiotic (FM-B11) on turkey body weight, performance, and health. When
171 each premise was compared by level of performance as good, fair, or poor (grouping based on

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172 historical analysis of 5 previous flocks), the probiotic appeared to increase the performance of
173 the poor and fair farms (p<0.05) (Torres-Rodriguez et al. 2007).

174 Of the interventions discussed, not one alone is capable of eliminating pathogens. Interventions
175 vary in their effectiveness for both researchers and producers. Some appear to have synergistic
176 effects when used in combination. More research and application is needed to resolve these
177 issues.

178 Immobilization and Exsanguination (Bleeding)

179 Immobilization renders live poultry unconscious in preparation for exsanguination (bleeding);
180 however, death by slaughter can occur unintentionally or by design. Immobilization begins
181 when the immobilizing agent is applied and ends when the cervical vessels are severed.
182 Immobilization methods are classified as mechanical, chemical, and electrical, and should be
183 implemented in accordance with good commercial practices in a manner that will result in
184 thorough bleeding of the carcasses.

185 Mechanical immobilization is impractical in large poultry establishments. However, it is useful

186 in emergencies or to immobilize small numbers of live poultry, which makes it a practical
187 method in small and very small establishments. Decapitation, cervical dislocation, and blunt
188 trauma to the head are the most common forms of mechanical immobilization.

189 Chemical immobilization exposes live poultry to a gas, individually in boxes or tunnels, or in
190 batches. The most common gases are carbon dioxide (CO2) (Drewniak et al. 1955, Kotula et
191 al. 1961) and argon (Raj and Gregory 1990, 1994). When chemical methods are used, live
192 poultry may be immobilized prior to live hanging.

193 Electrical immobilization is the most common method in use worldwide. It is the best method of
194 achieving rapid brain failure and the cheapest and most effective method of poultry slaughter.
195 The EEC recommends electrical immobilization with a minimum of 120 milliampere (mA) to
196 instantaneous render poultry unconscious, effect ventricular fibrillation, and produce death by
197 slaughter (Fletcher 1999). A majority of U.S. poultry processors utilize low-voltage,
198 high-frequency methods (Fletcher 1999, Heath et al. 1994). The remaining U.S. processors
199 utilize high voltage with no specified waveform. Gregory and Wooton (1986) determined that
200 low-voltage immobilization with 30 to 60 volts (V), 20 to 45 mA does not result in death by
201 slaughter, while high-voltage stunning with 150 V, 100 mA induces ventricular fibrillation and
202 death by slaughter. Both systems accomplish the desired end result. Kuenzel et al. (1978)
203 determined that 50 V/60 hertz (Hz) circuits are 35 percent more cost-effective than 100 V
204 variable-frequency circuits, and 225 percent more cost-effective than direct current (DC) circuits.
205 However, Kuenzel and Walther (1978) concluded that DC currents are safer and improve
206 exsanguination time compared to alternating current (AC) circuits because blood is not shunted
207 from peripheral to central blood vessels. A recent study examined different slaughter techniques
208 to determine their effects on pH (24 hours), color (24 hours), lipid oxidation, residual
209 hemoglobin concentration (24 hours), and sensory evaluation (d 1 and 4 post mortem) in broiler
210 breast fillets, and concluded that the electrical stunning and decapitation method had the most
211 favorable results for sensory quality regardless of whether the chickens were pre-bled
212 (Alvarado et al. 2007).

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213 Exsanguination guarantees death by slaughter and ensures that poultry have stopped breathing
214 prior to scalding. Exsanguination begins when the cervical vessels are severed, and ends when
215 the carcass enters the scald process. For exsanguination to cause death by slaughter, it is
216 important that the cervical vessels be cut promptly and efficiently so that poultry do not regain
217 consciousness and/or enter the scald tank before they have stopped breathing.

218 Potential Risk Factors. Potential biological risk factors include cross-contamination with
219 pathogenic and nonpathogenic microorganisms. Immobilization (Mead et al. 1994) can void
220 feces and further contaminate the carcass exterior, scald tank water, and feather removal
221 equipment. Papa and Dickens (1989) found that 53 percent of broilers produced an average
222 excretion of 1.5 g during electrical immobilization and that the volume of the excretion increased
223 as feed withdrawal time increased. Musgrove et al. (1997) found that Campylobacter in whole
224 carcasses rinses increased 0.5 log10 CFU/ml following electrical immobilization. Mead et al.
225 (1994) found that the physical pressure of the killing knife against the carcass can void crop
226 content with similar affect.

227 Trim nonconformance is an undesirable side effect of immobilization. Raj (1994) and Raj et
228 al. (1990) identified a link between electrical and chemical immobilization and hemorrhage and
229 broken bones in turkeys and broilers. Chemical immobilization results in a lower incidence of
230 trim nonconformance compared to electrical immobilization (Raj and Nute 1995, Raj et al. 1997,
231 1998). Grossly significant hemorrhages can interfere with accurate post mortem disposition.

232 Failure to properly exsanguinate can result in poultry entering the scald tank before breathing has
233 stopped. Heath et al. (1981) speculated that red discoloration of the skin results when live
234 poultry enter the scald tank. Heath et al. (1983) later concluded that poultry entering the scald
235 tank alive develop red discoloration of the skin, that the discoloration is confined to the pterylae,
236 and that the apteria is never discolored. Griffiths (1985) demonstrated that only poultry entering
237 the scald tank alive result in red discoloration of the skin. Poultry that are dead (either by
238 slaughter or by other causes) when they enter the scald tank, do not develop in red discoloration
239 of the skin. Griffiths further demonstrated that the red discoloration is due to marked peripheral
240 vascular dilation of blood vessels in the skin and subcutis.

241 Controls. Biological and chemical potential risk factors present during immobilization and
242 exsanguination cannot be prevented, eliminated, or reduced to acceptable levels during these
243 process steps. However, they can be influenced through preharvest interventions and choice of
244 processing method.

245 Feed withdrawal time influences the incidence of feces voided during immobilization. Papa and
246 Dickens (1989) found that only 8 percent, 42 percent, 50 percent, and 58 percent of broilers
247 produced an excretion when the feed withdrawal time was 4, 8, 12, and 16 hours, respectively.
248 McNeal et al. (2003) found that exsanguination by decapitation following electrical
249 immobilization produced less wing flapping, body motion, and quivering because decapitation
250 kills poultry quicker than severance of the cervical vessels.

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251 Scalding

252 Scalding begins when the poultry carcass enters the scald system and ends when feather removal
253 commences. Scalding prepares the carcass for feather removal by breaking down the proteins
254 that hold feathers in place and opening up feather follicles.

255 Variables requiring consideration during the scald process step are mechanical, physical, and
256 chemical. Mechanical variables include counter-current flows and agitation to produce a
257 washing effect. Counter-current systems move water counter to the direction of poultry
258 carcasses at all points. Water enters the system at the point where poultry carcasses exit, and
259 water exits at the point where poultry carcasses enter, producing a dirty-to-clean gradient that
260 continually moves poultry carcasses into cleaner water. Cleaner water is a relative condition as
261 the amount of dry matter and microorganisms in the scald water increase over time. Physical
262 variables are time and temperature, which influence washing and antimicrobial effects. The
263 chemical variable is pH, which also influences the antimicrobial effect.

264 Immersion scalding is the most common scald technology in use and is best described as
265 dragging carcasses through a tank of hot water. Immersion systems come in single- and multi-
266 stage configurations, incorporating mechanical and physical variables. Single-stage systems
267 provide less washing effect than multi-stage systems.

268 U.S. Poultry processors in the United States prefer a “hard scald” combining shorter scald times
269 and higher scald temperatures. A “hard scald” facilitates removal of the epidermis, which
270 enhances the adhesion of coatings commonly used with fried foods. European poultry
271 processors prefer a “soft scald,” combining longer scald times and lower scald temperatures. A
272 “soft scald” retains much of the epidermis and natural skin color.

273 Table C-2. Common Scalding Times and Temperature for Various Classes of Poultry
Broilers (hard scald) 30-75 seconds 59-64°C
Broilers (soft scald) 90-120 seconds 51-54°C
Turkeys 50-125 seconds 59-63°C
Quail 30 seconds 53°C
Waterfowl 30-60 seconds 68-82°C
274

275 Steam-spray scalding is a less popular alternative. Klose et al. (1971), Kaufman et al. (1972),
276 and Dickens (1989) found that a mixture of steam and air at 50 to 60°C and 137.9 kPa pressure
277 applied for approximately two minutes provided a uniform scald of either dry or damp broilers,
278 facilitated feather removal, and yielded carcasses microbiologically equivalent to immersion
279 systems. Some religious dietary laws prohibit scalding and soak poultry carcasses in cold water.

280 Potential Risk Factors. Potential biological risk factors include pathogenic and non-pathogenic
281 microorganisms introduced during the scald process. These microorganisms are present on the
282 internal and external surfaces of the carcass as well as in the scald water.

283 Salmonella and Campylobacter are the most common pathogenic microorganisms identified with
284 the scalding process step. Berrang et al. (2000a) recovered 5.4 log10, 3.8 log10, 4.7 log10,
285 7.3 log10, and 7.2 log10 Campylobacter/g from feathers, skin, crop content, cecal content, and

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286 colon content, respectively, prior to scalding. Geornaras et al. (1997) isolated Salmonella from
287 100 percent, Listeria spp., from 33 percent, and Staphylococcus aureus from 20 percent of skin
288 and feather samples collected prior to scalding. Cason et al. (2000) found that 75 percent of
289 scald tank water samples were Salmonella-positive, and recovered an average of 10.9 MPN
290 Salmonella/100 ml, or about 1 Salmonella bacteria/9 ml. They found significantly lower
291 prevalence of microorganisms with increasing passes between tanks, but removal of coliforms
292 and E. coli is more effective (p<0.02) than removal of Salmonella. Wempe et al. (1983)
293 recovered an average of 1.6 log10 C. jejuni CFU/ml from a scald tank water.

294 Because scalding washes much of the dirt and feces off of the carcass exterior, more
295 microorganisms can be removed during scalding than during any other process step. Geornaras
296 et al. (1997) found a 38 percent decrease in Salmonella-positive carcasses. Acuff et al. (1986)
297 reported a 312 MPN/100 cm3 decrease in C. jejuni on turkey skin. Berrang and Dickens (2000)
298 reported a 2.9- to 4.1-log10 reduction in Campylobacter/ml in carcass rinses. Lillard (1990)
299 found a 1.1-log10 and 1.5-log10 CFU/ml decrease in aerobic bacteria and Enterobacteriaceae,
300 respectively, in carcass rinses. Geornaras et al. (1997) found a 1.0-log10 CFU/g decrease in
301 Pseudomonas spp. in skin samples. Berrang and Dickens (2000) reported 2.1-log10 and
302 2.2-log10 CFU/ml reductions in coliforms and E. coli, respectively in carcass rinses.

303 However, Berrang et al. (2003a) found that immersion scalding increased aerobic bacteria
304 0.9 log10 CFU/ml, coliforms 0.8 log10 CFU/ml, E. coli 1.5 log10 CFU/ml, and Campylobacter
305 spp., 0.8 log10 CFU/ml in lung rinses taken from broilers, indicating that microorganisms were
306 added to the respiratory tract during immersion scalding. These microorganisms carry forward
307 into subsequent processing steps. In contrast, Kaufman et al. (1972) found that the air sacs of
308 steam-scalded broilers contain 3 log10 fewer microorganisms than the air sacs of immersion-
309 scalded broilers. The number of microorganisms on poultry carcasses exiting the scald tank is
310 relative to the number of microorganisms in or on the poultry carcass entering the scald tank.
311 The scald process cannot eliminate excessively high numbers of microorganisms entering the
312 process.

313 A disadvantage of washing dirt and feces off of the exterior carcass surface is the accumulation
314 of microorganisms in the scald water, making the scald tank a source of cross-contamination for
315 subsequent carcasses. Mulder et al. (1978) recovered a marker organism introduced prior to
316 scalding from the 230th carcass exiting the scald. Cason et al. (1999) determined that the 4.2 log10
317 aerobic bacteria/ml, 2.7 log10 E. coli/ml, and 2.9 log10 Campylobacter/ml of carcass rinse present
318 on carcasses post-feather removal originated from the scald process.

319 Figure C-1 illustrates the reduction in microorganisms that occurs during the immersion
320 scalding process step. For each microorganism considered, Berrang and Dickens (2000) and
321 Berrang et al. (2003a) measured a reduction in the mean log10 CFU/ml of whole carcass rinse
322 taken from broiler carcasses pre- and post-immersion scalding (p<0.05 for all of the organisms
323 tested).

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324

9
8 Prescald
7 postscald
Log10 CFU/ml
6
5
4
3
2
1
0
Total aerobic Coliform E. coli Campylobacter

325 Figure C-1. Difference in Levels of Organisms Pre- and Post-scaling

326 Chemical potential risk factors include residues introduced during the scald process through the
327 excessive application of technical processing aids and/or antimicrobial agents. Technical
328 processing aids enhance the scalding process and include surfactants, denuding agents, and
329 emollients. Surfactants reduce surface tension, improve wetting agent function, and inhibit
330 foam. Alkaline denuding agents loosen the keratinized outer layer of the epidermis. Emollients
331 retain moisture and prevent excessive drying of the denuded dermis. Many of these chemicals
332 are generally regarded as safe (GRAS) by the FDA. Others are listed with restriction in the Code
333 of Federal Regulations, 9 CFR 424.21, “Use of Food Ingredients and Sources of Radiation.”
334 When a processing aid produces the same technical effect at lower scald water temperatures, a
335 greater number of microorganisms can survive the scald process.

336 Controls. Biological and chemical potential risk factors cannot be prevented or eliminated
337 during the scald process step; however, they can be reduced.

338 The NCC (1992) and Waldroup et al. (1992) identified counter current systems, sufficient water
339 replacement with, and a post-scald carcass rinse as good manufacturing practices for efficient
340 immersion scalding. Waldroup et al. (1993) found that counter current scalding reduced aerobic
341 bacteria, coliform, and E. coli 0.64 log10, 0.76 log10, and 0.72 log10 CFU/ml, respectively, and
342 Salmonella prevalence by 10 percent in scald water. James et al. (1993) found that counter-
343 current scalding combined with a carcass rinse reduced aerobic bacteria, Enterobacteriaceae, and
344 E. coli 0.68 log10, 0.37 log10, and 0.08 log10 CFU/carcass respectively, and the incidence of
345 Salmonella-positive carcasses by 3 percent. Multi-tank immersion systems further improve the
346 microbiological quality of the scald water. In a three-stage counter current system, Cason et al.
347 (2000) reported a reduction in coliforms from 3.4 log10 to 2.0 log10 to 1.2 log10 CFU/ml, and in
348 E. coli from 3.2 log10 to 1.5 log10 to 0.8 log10 CFU/ml in tanks 1, 2, and 3, respectively (p<0.05).
349 Cox et al. (1974) determined that 1 minute of agitation reduced aerobic bacteria on broiler skin
350 by 0.42 log10 CFU/cm2.

351 Failure to maintain a proper time/temperature combination diminishes the desired technical
352 effect of preparing feathers for removal and detracts from sanitary dressing. High scald
353 temperature can cause the carcass to become oily, which favors the retention of microorganisms
354 on the carcass surface. Cox et al. (1974) determined that immersion in hot water for 1 minute
355 reduced aerobic bacteria 0.91 log10 CFU/cm2. Yang et al. (2001) found that a 5-minute exposure

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356 at 50 to 60°C produced reductions of 3.8 log10 C. jejuni/ml and 3.0 log10 S. typhimurium/ml in
357 the scald tank water, and 1.5 log10 C. jejuni/ml and 1.3 log10 S. typhimurium/ml on chicken skins.

358 Immersion scalding produces a relatively smooth, microbiologically superior skin surface
359 compared to steam-spray and kosher methods that result in a highly wrinkled microtopography
360 that facilitates attachment of microorganisms. Kim and Doores (1993) concluded that the
361 incidence of Salmonella-positive turkey carcasses is higher with kosher processing, due to
362 trapping of Salmonella in the keratinized epithelium. Lillard (1989) concluded that
363 microorganisms become entrapped in ridges and crevices that become more pronounced in skin
364 following immersion in water and are less accessible to antimicrobial treatments. Clouser et
365 al. (1995b) recovered Salmonella from 57 percent of steam-spray and 37 percent of kosher skin
366 samples, compared to 23 percent with conventional methods.

367 Within 120 minutes of the start of operations, the dissociation of ammonium urate from poultry
368 feces to uric acid and ammonium hydroxide can reduce scald water pH from 8.4 to 6.0
369 (Humphrey 1981). The protein and minerals in the scald tank water then act as a buffer to
370 maintain this pH for the rest of the working day. S. typhimurium and S. newport are most heat
371 resistant at pH 6.1 (Okrend et al. 1986), C. jejuni at 7.0 (Humphrey and Lanning 1987),
372 Aerobacter aerogenes at pH 6.6 (Strange and Shon 1964), and Streptococcus feacalis at pH 6.6
373 (White 1963). Hydrogen ion concentration influences the rate of endogenous Ribonucleic acid
374 (RNA) degradation and a shift in pH away from optimal (while probably not the primary cause
375 of microbial death in scald water) increases RNA degradation, hinders microbial metabolism,
376 and contributes to microbial death.

377 Increasing scald water pH reduces microbial levels in the water. When scald water pH was
378 increased from 7 to 9, Humphrey and Lanning (1987) determined that the time needed to achieve
379 a 1-log10 reduction in C. jejuni was reduced from 11½ to 2 minutes, Salmonella levels were
380 reduced from 13.9 MPN/100 ml to 3 MPN/100 ml, and the incidence of Salmonella- and
381 Campylobacter-positive water samples from 100 percent to 26 percent. When scald water pH
382 was adjusted to 9 after 4 hours of production and maintained for the remainder of the day,
383 Humphrey et al. (1984) determined that aerobic bacteria and Enterobacteriaceae levels decreased
384 by 0.4 log10 CFU/ml and 0.5 log10 CFU/ml, respectively; and the death rate of Salmonella
385 typhimurium attached to the skin increased 57 percent. Lillard et al. (1987) reported that
386 reducing scald water pH to 3.6 by the addition of 0.5 percent acetic acid decreased aerobic
387 bacteria 2.2 log10 CFU/ml in scald water.

388 The same can be said for decreasing scald water pH. Okrend et al. (1986) determined that
389 reducing scald tank water pH to 4.3 by the addition of 0.1 percent acetic acid increased the death
390 rate of S. newport and S. typhimurium 91 percent. However, the same is not true for
391 microorganisms on the surface of poultry carcasses. Humphrey and Lanning (1987) reported
392 that scalding at pH 9.0 had no affect on the incidence of Salmonella and Campylobacter on
393 broiler carcasses. Lillard et al. (1987) found that reducing scald water pH to 3.6 did not reduce
394 aerobic bacteria or Enterobacteriaceae on carcass surfaces. It is important to understand that
395 these reductions take place in the scald tank water and not on the carcass surface.

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 Appendix C – Literature Review of the Poultry Slaughter Process

396 Feather Removal

397 Feather removal eliminates the feathers and stratum corneum in preparation for evisceration.
398 Feather removal begins when carcasses enter the feather removal equipment and continues until
399 the exterior surface of the poultry carcass is free of feathers and cuticle. Feather removal
400 technology is fairly uniform across the poultry industry. Carcasses pass through one or more
401 pieces of equipment that remove feathers by the mechanical action of rubber picking fingers
402 beating against the carcass. Most establishments utilize a continuous process; however, batch
403 processes are common in small, low-volume establishments. Some very small establishments
404 rely on manual methods to remove feathers. Following mechanical feather removal, goose
405 carcasses are immersed in molten wax and dipped in ice water to facilitate removal of the down
406 feathers. The hardened wax is manually removed, taking the down feathers with it.

407 Potential Risk Factors

408 Potential biological risk factors include pathogenic and nonpathogenic microorganisms
409 introduced during the feather removal process. These microorganisms are present on the internal
410 and external surfaces of the carcass, as well as on the feather removal equipment, and increase as
411 an unavoidable consequence of the process. Salmonella and Campylobacter are the most
412 common pathological microorganisms identified with the feather removal process. Acuff et al.
413 (1986) determined that regardless of the number of C. jejuni present on turkey carcasses entering
414 the establishment, on average, C. jejuni increased 150 MPN/100 cm3 during feather removal.
415 Izat et al (1988) found that feather removal increased C. jejuni on broiler carcasses
416 1.7 log10 CFU/1,000 cm3. Abu-Ruwaida et al. (1994) reported that Campylobacter and S. aureus
417 levels rose 1.6 log10 CFU/gm and 0.30 log10 CFU/gm, respectively, and the incidence of
418 Salmonella was 100 percent post-feather removal. Berrang and Dickens (2000) found that
419 Campylobacter, in whole carcass rinses increased 1.9 to 2.9 log10 CFU/ml and that Salmonella
420 (Berrang et al. 2001) on breast swabs increased 1.2 log10 CFU/cm3.

421 Clouser et al. (1995a) found a >200 percent increase in Salmonella-positive turkey carcasses
422 after feather removal, and concluded that when Salmonella is present prior to feather removal,
423 the incidence of Salmonella tends to increase throughout evisceration and chilling. Geornaras et
424 al. (1997) isolated Salmonella from 100 percent of carcasses following feather removal. The
425 feather follicle has been implicated as a harborage for microorganisms. However, Cason et al.
426 (2004) found no statistically significant difference (p>0.05) in aerobic bacteria, E. coli, and
427 Campylobacter levels between feathered and featherless birds and concluded that microbial
428 adhesion, not harborage in follicles, is the mechanism behind microorganisms present on poultry
429 skin.

430 Figure C-2 summarizes data compiled from various authors cited in this document and
431 illustrates the increase in biological potential risk factors during feather removal.

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 Improvements for Poultry Slaughter Inspection

Difference in Levels of Microorganisms between Scalding and

Feather Removal Process Steps

4.5
4
3.5
Log10 CFU

3
2.5 Post-scald
2 Post-pick
1.5
1
0.5
0
Non-pathogen Campylobacter Salmonella Total
432

433 Figure C-2. Difference in Levels of Microorganisms between Scalding and

434 Feather Removal Process Steps

435 Within the feather removal equipment, the rubber picking fingers and recycled water are sources
436 of cross-contamination. Geornaras et al. (1997) isolated Salmonella from 33 percent of the
437 picking fingers. Wempe et al. (1983) recovered an average of 3.88 log10 C. jejuni/ml from
438 94 percent of feather removal water samples. Whittemore and Lyon (1994) recovered 5.46 to
439 5.73 log10 Staphylococcus spp., 5.83 to 6.04 log10 aerobic bacteria, and 5.05-5.44 log10
440 Enterobacteriaceae from the rubber picking fingers. Mead et al. (1975) and Allen et al. (2003b)
441 found that a marker organism inoculated onto post-scalding carcasses dispersed for
442 ≤200 carcasses via feather removal. Mulder et al. (1978) found that a marker organism
443 introduced prior to feather removal could be recovered from the 580th carcass exiting the feather
444 removal equipment. Geornaras et al. (1997) attributed increases of 1.1 log10 aerobic bacteria/g,
445 0.9 log10 Enterobacteriaceae/g, and 3.1 log10 Pseudomonas spp./g in neck skin samples following
446 feather removal to the action of the rubber picking fingers.

447 Allen et al. (2003a) concluded that feces forced out of the cloaca by the action of picking fingers
448 against the carcass cross-contaminated adjacent carcasses. Berrang et al. (2001) found that the
449 incidence of Campylobacter-positive carcass rinses decreased 89 percent and Campylobacter
450 levels decreased 2.5 log10 CFU/ml when the escape of feces from the cloaca was prevented. Buhr
451 et al. (2003) confirmed the result, finding that plugging the cloaca decreased Campylobacter,
452 coliforms, E. coli, and aerobic bacteria 0.7 log10, 1.8 log10, 1.7 log10, and 0.5 log10 CFU/ml,
453 respectively, in rinse samples.

454 A clear demonstration for the role of fingers in cross contamination was shown by means of
455 molecular characterization. Salmonella subtypes found on the fingers of the picker machines
456 were similar to subtypes isolated before and after defeathering, indicating that the fingers
457 facilitate carcass cross contamination during defeathering (Nde et al. 2007). Similar conclusions
458 were made for cross contamination of Campylobacter spp., using molecular profiling (Takahashi
459 et al. 2006) in a poultry plant in Japan.

460 Airborne microorganisms have been implicated as a source of cross-contamination during

461 feather removal. Whyte et al. (2001a) recovered 12.7 log10 Campylobacter per 15 ft3 of air in

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 Appendix C – Literature Review of the Poultry Slaughter Process

462 broiler and hen establishments. Northcutt et al. (2004) recovered 1.5 log10 Enterobacteriaceae/ml
463 of air during commercial processing of Japanese quail. Lutgring et al. (1997) recovered 2.5 to
464 6 log10 psychrophilic bacteria/m3 in turkey and duck processing establishments. However,
465 Berrang et al. (2004) found that exposing Campylobacter-negative broiler carcasses to air near
466 feather removal equipment for 1 minute only increased Campylobacter 0.20 log10 CFU/ml in
467 carcass rinses, and concluded that airborne contamination does not contribute to high levels of
468 Campylobacter routinely found on broiler carcasses after feather removal (95 percent CI).

469 Controls. Biological hazards and potential risk factors cannot be prevented, eliminated, or
470 reduced to acceptable levels during feather removal.

471 The NCC (1992) and Waldroup et al. (1992) recommend preventing feather buildup, continuous
472 rinses for equipment and carcasses, and regular equipment adjustment to minimize cross-
473 contamination.

474 Changes in technique and/or equipment can affect microbial numbers on equipment and product.
475 After increasing the number of rubber feather removal fingers, decreasing chlorine levels, and
476 increasing cabinet temperature, Purdy et al. (1988) found that S. aureus, coliforms, and
477 Enterobacteriaceae on the feather removal fingers increased by 3.2 log10 CFU, 2.0 log10 CFU, and
478 4.6 log10 CFU, respectively, and S. aureus, coliforms, and Enterobacteriaceae on the poultry skin
479 samples increased by 2.8 log10 CFU, 5.0 log10 CFU, and 5.6 log10 CFU, respectively. Allen et al.
480 (2003a) determined that increasing the distance between carcasses and water curtains at the
481 entrance and/or exit of the feather removal cabinet had no effect on cross-contamination.
482 Clouser et al. (1995a) concluded that when aerobic plate counts are high at the start of feather
483 removal, they remain proportionately high throughout processing.

484 Interventions applied during feather removal have yielded mixed results. Berrang et al. (2000b)
485 concluded that rinsing carcasses with 71°C (159°F) water for 20 seconds post-feather removal
486 spraying had no significant effect on microbial contamination. Mead et al. (1975) found that a
487 10 to 20 ppm available chlorine carcass rinse did not reduce carriage of a marker organism on
488 turkey carcasses passing through the feather removal equipment and contributed the result to
489 inadequate contact time. Later, Mead et al. (1994) found that an 18 to 30 parts per million (ppm)
490 available chlorine rinse reduced carriage of a marker organism on hen carcasses passing through
491 the feather removal equipment. Dickens and Whittemore (1997) found that a 1 percent acetic
492 acid rinse post-feather removal reduced aerobic bacteria 0.6 log10 CFU/ml in whole carcass rinse
493 without altering carcass appearance; but a similar application of 0.5 percent to 1.5 percent
494 hydrogen peroxide caused bleaching and bloating of carcasses.

495 Evisceration
496 Evisceration removes the internal organs and any trim/processing defects from the carcass in
497 preparation for chilling. The technology varies widely across the poultry industry but always
498 includes the following basic process steps.

499 • Remove the crus.

500 • Remove the oil gland.
501 • Sever the attachments to the vent.
502 • Open the body cavity.

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 Improvements for Poultry Slaughter Inspection

503 • Extract the viscera.

504 • Harvest the giblets.
505 • Remove and discard the intestinal tract and air sacs.
506 • Remove and discard the trachea and crop.
507 • Remove and discard the lungs.

508 Potential Risk Factors

509 Potential chemical risk factors include antimicrobial treatments, as well as sanitizers, used to
510 prevent cross-contamination and control microbial growth on product contact surfaces.
511 Biological potential risk factors include pathogenic and nonpathogenic microorganisms on
512 carcasses and equipment surfaces.

513 The incidence of biological potential risk factors on carcasses and equipment, as well as the
514 change in absolute numbers, varies widely between poultry processing operations. Hargis et al.
515 (1995) recovered Salmonella from 15 percent of ceca and 52 percent of crops; and 8 percent of
516 crop removal devices. Byrd et al. (1998) recovered Campylobacter from 4 percent of ceca and
517 62 percent of crops. Berrang et al. (2003a) recovered 1.0 log10 Campylobacter/ml of rinse from
518 lungs. Lillard (1990) found that the incidence of Salmonella-positive carcasses increased
519 2.4 percent during evisceration. Oosterom et al. (1983) found an increase of 1.5 log10 C. jejuni/g
520 of skin and 7.0 log10 C. jejuni/g from intestinal content during evisceration. Acuff et al. (1986)
521 found that C. jejuni increased 278 MPN/100 cm3 during evisceration. Izat et al. (1988) found
522 that evisceration increased C. jejuni 0.41 log10/1,000 cm3 on skin samples. Berrang and
523 Dickens (2000) found a 0.3-log10 decrease in Campylobacter/ml in carcass rinses during
524 evisceration. Berrang et al. (2003a) found that aerobic bacteria, coliforms, E. coli, and
525 Campylobacter in carcass rinses decreased 0.5 log10, 0.3 log10, 0.67 log10, and 0.3 log10 CFU/ml,
526 repectively, during evisceration. Lillard (1990) found that evisceration decreased aerobic
527 bacteria and Enterobacteriaceae 0.61 log10 and 0.18 log10 CFU/ml, respectively. Variations in
528 the number of microorganisms recovered from carcasses and equipment are attributable to the
529 differences in the processing and sanitation practices.

530 Carcass handling during evisceration cross-contaminates product prior to opening the body
531 cavity and after extracting the viscera. Mead et al. (1975, 1994) recovered a marker organism
532 from the 50th revolution of the transfer point, the 450th carcass to pass through the vent opener,
533 and from head removal and lung extraction machines. Byrd et al. (2002) recovered a marker
534 organism placed in the crops prior to live hanging from 67 percent of carcasses at the transfer
535 station, 78 percent at viscera extraction, 92 percent pre-crop removal, 94 percent post-crop
536 removal, and 53 percent after the final carcass rinse. Berrang et al. (2003a) found that the lung
537 picks up contaminated water from the scald tank that contaminates equipment and product
538 during evisceration. Wempe et al. (1983) recovered 2.8 log10 C. jejuni/ml from recycled carcass
539 rinse water. Thayer and Walsh (1993) found that aerobic bacteria, Enterobacteriaceae, and
540 E. coli on the probe retracting viscera from chicken increased 0.10 to 0.18 log10 CFU during
541 operation. Clouser et al. (1995a) recovered L. monocytogenes from 20 percent of kosher
542 carcasses sampled post-evisceration, but found no link with L. monocytogenes preharvest and
543 concluded that the L. monocytogenes originated from the equipment.

544 The relative presence or absence of enteric microorganisms on carcasses is an indicator of

545 sanitation process control. Jimenez et al. (2003) found that, on carcasses with visible feces, a

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 Appendix C – Literature Review of the Poultry Slaughter Process

546 carcass rinse reduced Enterobacteriaceae. E. coli, and coliforms by 0.11 log10, 0.10 log10, and
547 0.02 log10 CFU/ml respectively, and on carcasses without visible feces by 0.36 log10, 0.23 log10,
548 and 0.18 log10 CFU/ml, respectively. Statistical significance was achieved only for the latter
549 case (p<0.05). However, Fluckey et al. (2003) concluded that there is no relationship between
550 the presence or absence of enteric microorganisms and the presence or absence of Salmonella or
551 Campylobacter (p>0.05). Lillard (1990) found that a carcass rinse decreased Enterobacteriaceae
552 by 0.24 log10 CFU/ml, but had no effect on the incidence of Salmonella.

553 The presence or absence of visible feces is also an indicator of sanitation process control.
554 However, there is no direct correlation between the presence or absence of visible fecal material
555 and the presence or absence of Salmonella or Campylobacter. Jimenez et al. (2002) found that
556 12 percent of broiler carcasses with visible fecal contamination were Salmonella-positive,
557 compared to 20 percent without visible fecal contamination (p>0.05) and that 37 percent of
558 carcasses with visible fecal contamination were Salmonella-positive following the carcass rinse,
559 compared to 10 percent without visible fecal contamination. Fletcher and Craig (1997) found
560 that Campylobacter levels on reprocessed carcasses with visible fecal contamination were
561 0.21 log10 CFU higher than reprocessed carcasses without visible fecal contamination, and that
562 the incidence of Campylobacter and Salmonella on reprocessed carcasses with visible fecal
563 contamination was 5 percent and 3 percent lower than on reprocessed carcasses without visible
564 fecal contamination. Blankenship et al. (1975) found no significant difference in the level of
565 aerobic bacteria, Enterobacteriacae, and presumptive Clostridium spp., in carcass rinses of
566 inspected and passed, fecal-condemned, and reprocessed fecal-condemned broiler carcasses.
567 Bilgili et al. (2002) found no correlation between the microbiological quality of broiler carcasses
568 and the presence or absence of visible contamination.

569 Evisceration systems process steps also influence the incidence of carcass contamination.
570 Russell and Walker (1997) found visible contamination on 3 percent of carcasses eviscerated
571 with the Nu-Tech® system, compared to 19 perecnt eviscerated with the streamlined inspection
572 system. Jimenez et al. (2003) found feces and/or bile on 11 percent and 5 percent of carcasses
573 post-viscera extraction. Russell and Walker (1997) found feces on 10 percent of carcasses
574 post-viscera extraction and 19 percent post-crop removal. Crop rupture and leakage is a
575 significant source of contamination during evisceration. Buhr and Dickens (2001, 2002) and
576 Buhr et al. (2000) determined that crops rupture because of greater adhesion to surrounding
577 tissues, and that fewer crops rupture when extracted toward the head compared to extracted
578 toward the thoracic inlet (p<0.05).

579 Controls. The NCC (1992) recommends proper feed and water withdrawal, maintenance and
580 adjustment of equipment, continuous rinsing and sanitizing, enforcing employee hygiene
581 standards, and a whole-carcass rinse with 20 ppm free available chlorine to control biological
582 potential risk factors during evisceration. The most common methods used to mitigate biological
583 potential risk factors are carcass rinses, off-line reprocessing, and on-line reprocessing.

584 Carcass Rinses

585 Carcass rinses are effective interventions for removing loose material from the carcass surface
586 during evisceration (Byrd et al. 2002). Waldroup et al. (1992) recommended a 20 ppm chlorine
587 carcass rinse post-evisceration as part of a strategy shown to decrease microbial contamination
588 and improve food safety. Mead et al. (1975) found that a 10 to 20 ppm free available chlorine

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 Improvements for Poultry Slaughter Inspection

589 rinse did not eliminate a marker organism; but, 18 to 30 ppm free available chlorine reduced
590 recovery of the marker organism from the 50th to the 20th revolution at the transfer point.
591 Jimenez et al. (2003) found that carcass rinses reduce visible feces and bile on post-evisceration
592 broiler carcasses by 3.4 percent and 2.9 percent, respectively. Carcass rinses can also reduce
593 biological hazards (Notermans et al. 1980). Notermans et al. (1980) found that the incidence of
594 Salmonella positive carcasses decreased 36.5 percent when carcass rinses were incorporated into
595 the evisceration process, compared to a 20.5 percent increase without carcass rinses. However,
596 carcasses rinses are not an effective intervention against attached pathogens (Kotula et al. 1967,
597 Mead et al. 1975).

598 Off-line Reprocessing

599 Off-line reprocessing is a manual process and addresses disease conditions and contamination
600 that cannot be removed by other means. When properly performed, off-line reprocessing
601 eliminates visible conditions and yields carcasses microbiologically equivalent to inspected and
602 passed carcasses (Blankenship et al. 1975); however, reductions in microorganisms are not
603 certain. Blankenship et al. (1993) found the microbiological quality of conventionally processed
604 and reprocessed carcasses to be equivalent for aerobic bacteria, Enterobacteriacea, and E. coli.
605 With respect to Salmonella prevalence, the overall difference between conventionally processed
606 and reprocessed carcasses of 5.2 percent was not statistically significant.

607 On-line Reprocessing

608 On-line reprocessing addresses incidental fecal and/or ingesta contamination during evisceration.
609 Acuff et al. (1986) and Izat et al. (1988) found that an on-line carcass wash reduced C. jejuni
610 344 MPN/100 cm3 and 0.7 log10 CFU/1,000 cm3, respectively. On-line reprocessing is
611 automated and relies on washing systems in combination with antimicrobial agents to achieve
612 desired results. Water temperature, pressure, nozzle type and arrangement, flow rate, and line
613 speed all influence the effectiveness of the washing system. Multiple washers in series are
614 generally more effective then a single large washer. Bashor et al. (2004) and Kemp et al.
615 (2001b) found that a three-stage system decreased Campylobacter by 0.45 log10 CFU/ml
616 compared to 0.31 log10 CFU/ml in a single stage system (p<0.05). Online reprocessing systems
617 installed in one plant may not perform equally well in another plant.

618 The addition of antimicrobial agents generally increases the effectiveness of an on-line
619 reprocessing system. Fletcher and Craig (1997) found that 23 ppm free available chlorine
620 reduced the incidence of Campylobacter-positive carcasses from 77 percent to 72 percent, and
621 Salmonella-positive carcasses from 5 percent to 2 percent. Bashor et al. (2004) found that TSP
622 and acidified sodium chlorite decreased Campylobacter by 1.3 log 10 CFU/ml and 1.52 log 10
623 CFU/ml, respectively (p<0.05). Yang and Slavik (1998) reduced Salmonella on carcasses
624 1.36 log10 CFU with 10 percent TSP, 1.62 log10 CFU with 5 percent cetylpyridinium chloride,
625 1.21 log10 CFU with 2 percent lactic acid, and 1.47 log10 CFU with 5 percent sodium bisulfate
626 (p<0.05). Whyte et al. (2001b) found that 10 percent TSP combined with 25 ppm free available
627 chlorine decreased Salmonella and Campylobacter by 1.44 log10 CFU/g and 1.71 log10 CFU/g,
628 respectively. On-line reprocessing is not as effective against tightly attached pathogens.
629 Reducing tightly attached microorganisms requires longer contact times then normally occurs
630 under commercial conditions (Morrison and Fleet 1985, Teotia and Miller 1975).

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631 If properly performed, on-line reprocessing of contaminated carcasses can yield better results
632 than off-line reprocessing, and improve food safety and the microbiological quality of raw
633 poultry (Kemp et al. 2001a). However, if process control is not maintained, results can be mixed
634 (Fletcher and Craig 1997) and biological potential risk factors enhanced (Blankenship et
635 al. 1993).

636 CHILLING
637 Chilling removes the natural heat from the carcass and is complete when regulatory temperature
638 requirements are met. Immersion and air chilling are the primary chilling technologies in use in
639 the world today. Immersion chilling is the more common method; however, both methods
640 acceptably decrease carcass temperature and inhibit biological potential risk factors.

641 Potential Risk Factors

642 Potential chemical risk factors are introduced during the immersion chilling process. Tsai et al.
643 (1987) found that lipids account for 84 to 98 percent of the organic matter in immersion chiller
644 water and that aldehydes, which form as these lipids auto-oxidize, react with chlorine to form
645 chlororganics, mutagenic chemicals that potentially impact the safety and wholesomeness of
646 poultry products. Marsi (1986) found that when free available chlorine levels are ≤50 ppm,
647 minimal free available chlorine reacts with aldehydes and forms chlororganics. However, when
648 free available chlorine levels ≥250 ppm, chlororganic formation rises sharply.

649 Biological potential risk factors exist during the chilling process as pathogenic and
650 nonpathogenic microorganisms on the carcass and in the chiller environment. Salmonella and
651 Campylobacter are the most common pathogenic microorganisms present on carcasses and in the
652 immersion chiller environment. Clouser et al. (1995a) recovered Salmonella from 60 percent of
653 carcasses pre-chill, and 57 percent of carcasses post-chill. Wempe et al. (1983) isolated an
654 average of 2.20 log10 C. jejuni/ml from the chiller water. Loncarevic et al. (1994) recovered
655 L. monocytogenes from 21 percent of post-chill skin samples taken from pre-chill
656 Listeria-negative carcasses and determined that L. monocytogenes was a biological potential risk
657 factor when the chlorine concentration of the chiller water was ≤10 ppm free available chlorine.
658 Clouser et al. (1995a) found a 57 percent incidence in Listeria monocytogenes-positive kosher
659 carcasses post-chilling, compared to 7 percent incidence with conventional slaughter methods,
660 found no relationship between the incidences of L. monocytogenes in the flock pre- or post-
661 chilling, and concluded that the L. monocytogenes originated from the chiller water.

662 Jimenez et al. (2003) found that immersion chilling reduced Enterobacteriaceae, E. coli, and
663 coliforms on noncontaminated carcasses by 0.36 log10, 0.89 log10, and 0.61 log10 CFU/ml in
664 carcass rinses, respectively, compared with 1.02 log10, 1.16 log10, and 1.23 log10 CFU/ml in
665 rinses from fecal contaminated carcasses. Berrang and Dickens (2000) found that immersion
666 chilling decreased APC, coliform, and E. coli in carcass rinses by 0.7 log10, 0.3 log10, and
667 0.4 log10 CFU/ml, respectively, (p<0.05). Lillard (1990) found that immersion chilling
668 decreased APC and Enterobacteriaceae by 0.92 log10 and 0.74 log10 CFU/ml.

669 Sarlin et al. (1998) found that Salmonella-negative carcasses remain negative, provided they are
670 not preceded by a Salmonella-positive flock and that the immersion chiller is a major site for
671 cross-contamination between Salmonella-negative and -positive flocks. Jimenez et al. (2003)

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 Improvements for Poultry Slaughter Inspection

672 (p>0.05) found no correlation between visible ingesta on carcasses and the presence or absence
673 of Salmonella during immersion chilling. Twelve percent of carcasses with visible fecal
674 contamination were Salmonella-positive following immersion chilling, compared to 30 percent
675 without visible fecal contamination.

676 Air chill systems come in two basic configurations: clip-bar and vent-stream. Allen et al. (2000)
677 determined that microbial counts on poultry carcasses are lower in air chilling systems,
678 compared to immersion chill systems. Sanchez et al. (2002) reported the incidence of
679 Salmonella-positive carcasses in air chillers at 18 percent, compared to 24 percent with
680 immersion chillers; and the incidence of Campylobacter-positive carcasses in air chillers at
681 39 percent, compared to 48 percent with immersion chillers (p<0.05). Conversely, they found
682 that coliforms and E. coli in whole carcass rinses were 0.25 log10 CFU/ml and 0.26 log10 CFU/ml
683 higher with air chillers than immersion chillers, respectively. The differences are not significant
684 with regard to the cooling efficiency, but do affect the degree of physical contact between
685 carcasses and the potential for cross-contamination. Mead et al. (2000) found that dispersal of a
686 marker organism was greater in a vent-stream system than in a clip-bar system. Dispersal of the
687 marker organism decreased when water sprays were turned off.

688 Controls. Chemical potential risk factors introduced during the chilling process through the
689 excessive application of antimicrobial agents can be prevented, eliminated, or reduced to
690 acceptable levels during the chilling process. Biological potential risk factors cannot be
691 prevented or eliminated during the chilling process; however, they can be reduced to acceptable
692 levels.

693 Mulder et al. (1976) found that immersion chilling decreased Salmonella-positive carcasses by 5
694 percent. Acuff et al. (1986) found that immersion chilling decreased C. jejuni 69 MPN/100 cm3.
695 Berrang and Dickens (2000) found that immersion chilling decreased Campylobacter spp., levels
696 0.8 log10 CFU/ml. Izat et al. (1988) found that immersion chilling decreased C. jejuni on
697 carcasses by 0.9 log10 CFU/1,000 cm3. Bilgili et al. (2002) found that immersion chilling
698 decreased Campylobacter by 0.86 log10 CFU/ml, and the incidence of Salmonella-positive
699 carcasses from 20.7 percent to 5.7 percent. Lillard (1990) found that, on average, immersion
700 chilling increased the incidence of Salmonella by 20.7 perecnt.

701 More reduction in biological potential risk factors can be accomplished in a properly balanced
702 immersion chiller than at any other processing step. Conversely, an improperly balanced
703 immersion chiller can increase biological potential risk factors. However, regardless of how well
704 any immersion system is operated, it cannot overcome excessive biological potential risk factors
705 entering the chilling process. The NCC (1992) recommends that processors focus on proper
706 water temperature and water quality to control biological hazards in the immersion chiller.
707 Water temperature should be maintained to ensure that product temperatures are in accordance
708 with 9 CFR 381.65. l.

709 Maintaining proper water quality requires balancing pH, maintaining a free available chlorine
710 concentration, and minimizing organic matter. Diffusion of hypochlorous acid (HOCl) in
711 solution into hydrogen (H+) and hypochlorite (OCl-) ions is influenced by pH. At pH <7.5 the
712 hypochlorite ion is favored, which increases the concentration of free available chlorine. At
713 pH >8, the hypochlorous acid moiety is favored, which decreases the concentration of free
714 available chlorine.

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 Appendix C – Literature Review of the Poultry Slaughter Process

715 Chlorine is the most common and most effective antimicrobial intervention in use in immersion
716 systems worldwide, and the effect is directly proportional to the free available chlorine
717 concentration. Thiessen et al. (1984) could not recover Salmonella from chiller water when the
718 ClO2 residual was ≥1.3 ppm. Wabeck et al. (1969) found that 20 ppm chlorine destroyed
719 3.0 log10 Salmonella/ml in solution after 4 hours, but not Salmonella, on the surface of inoculated
720 drumsticks. Villarreal et al. (1990) found that ClO2 could eliminate recoverable Salmonella from
721 carcass rinses. James et al. (1992) found that the incidence of Salmonella-positive carcasses
722 increased from 48 percent to 72 percent during immersion chilling in a nonchlorinated system
723 compared to 43 percent to 46 percent when free available chlorine at the overflow was
724 maintained at 4 to 9 ppm. Yang et al. (2001) found that 10 ppm free available chlorine
725 eliminated S. typhimurium and C. jejuni from the water in 120 and 113 minutes respectively;
726 30 ppm produced the same result in 6 and 15 minutes; and 50 ppm in 3 and 6 minutes (p<0.05).

727 Three factors determine the amount of organic matter in the immersion chiller: flow rate, flow
728 direction, and the cleanliness of the scald water. When the chiller is more like a pond than a
729 river, the water is stagnant and organic matter accumulates in the water, on the paddles, and on
730 the sides of the chiller. Thomas et al. (1979) found that when fresh water in-flow drops to
731 <½ gallon/bird, organic matter accumulates in the chiller water. Lillard (1980) found that more
732 organic matter in the chiller will result in less chlorine available to kill bacteria, as it will be
733 bound to and rendered useless by the organic matter. The recommended method for performing
734 water replacement is with a counter-current system.

735 Tsai et al. (1987, 1992) found that organic matter in an immersion chiller equilibrates after 5 to
736 6 hours of operation and requires 2 to 3 times more free available chlorine to achieve a
737 2-log10 reduction in bacteria. Lillard (1979) calculated the concentration of organic matter at
738 equilibrium to be 91 ppm. Allen et al. (2000) found that the concentration of organic matter
739 increases closer to the exit and is reflected in the concentration of free available chlorine at
740 different locations within the chiller. Filtration of recycled water reduces the level of organic
741 matter and spares free available chlorine for bactericidal activity.

742 Russell (2005) recommended a pH of 6.5 to 7.5, a water temperature 4°C (<40°F), a high flow
743 rate, and counter-current flow direction. Waldroup et al. (1992) recommended 20 to 50 ppm free
744 available chlorine in the intake water in order to reduce the total microbiological load in the
745 chiller water. The amount of chlorine added at the intake should be sufficient to achieve 1 to
746 5 ppm free available chlorine at the chiller overflow.

747 A recent study designed to examine the prevalence and number of Campylobacter on broiler
748 chicken carcasses in commercial processing plants in the United States (Berrang et al. 2007) can
749 provide an indicator for the effectiveness of reducing pathogen loads during all of the steps
750 involved in poultry processing. In the study, carcass samples were collected from each of
751 20 U.S. plants 4 times, roughly approximating the 4 seasons of 2005. At each plant on each
752 sample day, 10 carcasses were collected at rehang (prior to evisceration), and 10 carcasses from
753 the same flock were collected post-chill. A total of 800 carcasses were collected at rehang and
754 another 800 were collected post-chill. All carcasses were subjected to a whole-carcass rinse, and
755 the rinse diluent was cultured for Campylobacter. The overall mean number of Campylobacter
756 detected on carcasses at rehang was 2.66 log CFU/ml of carcass rinse. In each plant, the
757 Campylobacter numbers were significantly reduced (p<0.001) by broiler processing; the mean
758 concentration after chill was 0.43 log CFU/ml. Overall prevalence was also reduced by

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 Improvements for Poultry Slaughter Inspection

759 processing from a mean of ≥30 of 40 carcasses at rehang to ≥14 of 40 carcasses at post-chill.
760 Seven different on-line reprocessing techniques were applied in the test plants, and all techniques
761 resulted in <1 log CFU/ml after chilling. Use of a chlorinated carcass wash before evisceration
762 did not affect the post-chill Campylobacter numbers. However, use of chlorine in the chill tank
763 was related to lower numbers on post-chill carcasses (p<0.0003). Overall, U.S. commercial
764 poultry slaughter operations are successful in significantly lowering the prevalence and number
765 of Campylobacter on broiler carcasses during processing.

766 CONCLUSIONS
767 1. Physical potential risk factors are quality issues that rarely exist during poultry slaughter
768 operations, and can be eliminated or reduced to acceptable levels when good commercial
769 practices are implemented. Physical potential risk factors present a negligible risk.
770
771 2. Chemical potential risk factors are food safety and quality issues that seldom exist during
772 poultry slaughter operations and can be prevented, eliminated, or reduced to acceptable levels
773 through prerequisite programs. Violative chemical residues are a pre-harvest issue and the
774 primary chemical potential risk factor. According to the 2000 National Residue Program, the
775 incidence of violative residues was 0.11 percent for all classes of poultry. In 2000, U. S.
776 poultry processors slaughtered more than 8 billion live poultry, which means approximately
777 9.5 million poultry carcasses passed through Federally-inspected slaughter establishments
778 with violative chemical residues. Chemical potential risk factors present a minimal risk.
779
780 3. Biological potential risk factors are unavoidable food safety and quality issues that
781 continually exist during poultry slaughter operations. Biological potential risk factors are
782 present in and on all live poultry received onto official establishments and cannot be
783 prevented or eliminated; however, they can be reduced to acceptable levels through the
784 application of good manufacturing practices and process control. Biological potential risk
785 factors present a significant risk.
786
787 4. The cited data for E. coli, Enterobacteriaceae, Campylobacter, Pseudomonas, Coliform and
788 APC show that more microorganisms exist in and on poultry at live receiving than at any
789 other process step in slaughter operations. The scalding and immersion chilling steps
790 produce the greatest overall reduction by washing microorganisms from the carcass surfaces.
791 The feather removal and evisceration steps result in an increase from the previous steps in the
792 number of microorganisms. However, overall microorganisms are reduced from the number
793 present when the poultry are at live receiving to when the carcasses are exiting the chiller.
794
795 5. Numerical data are not available for Salmonella, however, Salmonella prevalence follows a
796 similar distribution pattern. No single process step, no matter how well controlled, can
797 prevent, eliminate, or reduce to acceptable levels, a biological potential risk factor.

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 Appendix C – Literature Review of the Poultry Slaughter Process

798 REFERENCES
799 Abu-Ruwaida, A. S., N. Sawaya, B. H. Dashti, M. Murad, and H.A. Al-Othman. 1994.
800 Microbiological Quality of Broilers during Processing in a modern commercial slaughterhouse in
801 Kuwait. J. Food Prot. 57:887-892.
802
803 Acuff, G. R., C. Vanderzant, M. O. Hanna, J. G. Ehlers, F. A. Golan, and F. A. Gardner. 1986.
804 Prevalence of Campylobacter jejuni in turkey carcass processing and further processing of turkey
805 products. J. Food Prot. 45:712-717.
806
807 Allen, V. M., J. E. L. Corry, C. H. Burton, R. T. Whyte, and G. C. Mead. 2000. Hygiene aspects
808 of modern poultry chilling. Inter. J. Food Micro. 58:39-48.
809
810 Allen, V. M., M. H. Hinton, D. B. Tinker, C. Gobson, G. C. Mead, and C. M. Wathes. 2003a.
811 Microbial cross-contamination by airborne dispersion and contagion during defeathering of
812 poultry. Br. Poult. Sci. 44:567-576.
813
814 Allen, V. M., D. B. Tinker, M. H. Hinton, and C. M. Wathes. 2003b. Dispersal of
815 microorganisms in commercial defeathering systems. Br. Poult. Sci. 44:53-59.
816
817 Alvarado ,C. Z., M. P. Richards, S. F. O'Keefe, and H. Wang. 2007. The effect of blood removal
818 on oxidation and shelf life of broiler breast meat. Poult. Sci. 86:156-61.
819
820 Barber, L. Z., A. K. Turner, and P. A. Barrow. 1999. Vaccination for control of Salmonella in
821 poultry. Vaccine. 17:2538-2545.
822
823 Bashor, M., P. A. Curtis, K. M. Kenner, B.W. Sheldon, S. Kathariou, and J. A. Osborne. 2004.
824 Effects of carcass washers on Campylobacter contamination in large broiler processing plants.
825 Poult. Sci. 83:1232-1239.
826
827 Beal, R. K., and A. L. Smith. 2007. Antibody response to Salmonella: its induction and role in
828 protection against avian enteric salmonellosis. Expert Rev. Anti. Infect. Ther. 5:873-81.
829
830 Berrang, M. E., and J. A. Dickens. 2000. Presence and level of Campylobacter spp. on broiler
831 carcasses throughout the processing plant. J. Appl. Poult. Res. 9:43-47.
832
833 Berrang, M. E., R. J. Buhr, and J. A. Cason. 2000a. Campylobacter recovery from external and
834 internal organs of commercial broiler carcass prior to scalding. Poult. Sci. 79:286-290.
835
836 Berrang, M. E., J. A. Dickens, and M. T. Musgrove. 2000b. Effects of hot water application after
837 defeathering on the levels of Campylobacter, coliform bacteria and Escherichia coli on broiler
838 carcasses. Poult. Sci. 79:1689-1693.
839
840 Berrang, M. E., R. J. Buhr, J. [Link], and J. A. Dickens. 2001. Broiler carcass contamination
841 with Campylobacter from feces during defeathering. J. Food Prot. 64:2063-2066.

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 Improvements for Poultry Slaughter Inspection

842 Berrang, M. E., R. J. Meinersmann, R. J. Buhr, R. W. Philips, and M. A. Harrison. 2003a.

843 Presence of Campylobacter in the respiratory tract of broiler carcasses before and after
844 commercial scalding. Poult Sci 82:1995-1999.
845
846 Berrang, M. E., J. K. Northcutt, D. L. Fletcher, and N. A. Cox. 2003b. Role of dump cage fecal
847 contamination in the transfer of Campylobacter to carcasses of previously negative broilers.
848 J. Appl. Poult. Res. 12:190-195.
849
850 Berrang, M. E., J. K. Northcutt, and J. A. Dickens. 2004. The contribution of airborne
851 contamination to Campylobacter counts on defeathered broiler carcasses. J. Appl. Poult. Res.
852 13:1-4.
853
854 Berrang, M. E., J. S. Bailey, S. F. Altekruse, B. Patel, W. K. Shaw, Jr, R. J. Meinersmann, and
855 P. J. Fedorka-Cray. 2007. Prevalence and numbers of Campylobacter on broiler carcasses
856 collected at rehang and postchill in 20 U.S. processing plants. J. Food. Prot. 70:1556-60.
857
858 Bilgili, S. F. 1988. Effect of feed and water withdrawal on shear strength of broiler
859 gastrointestinal tract. Poult. Sci. 67:845-847.
860
861 Bilgili, S. F., and J. B. Hess. 1997. Tensile strength of broiler intestines as influenced by age and
862 feed withdrawal. J Appl Poult Res 6:279-283.
863
864 Bilgili, S.F., Valdroup, A.L., Zelenka, D., and Marion, J.E. 2002. Visible Ingesta on Pre-chill
865 Carcasses Does Not Affect the Microbiological Quality of Broiler Carcasses after Immersion
866 Chilling. J. Appl. Poult. Res. 11:233-238.
867
868 Blankenship, L C., N. A. Cox, S. E. Craven, A. J. Mercuri, and R. L. Wilson. 1975. Comparison
869 of the microbiological quality of inspection-passed and fecal contamination-condemned broiler
870 carcasses. J. Food. Sci. 40:1236-1238.
871
872 Blankenship, L. C., J. S. Bailey, N. A. Cox, M. T. Musgrove, M. E. Berrang, R. L. Wilson, M. J.
873 Rose, and S. K. Dua. 1993. Broiler carcass reprocessing, a further evaluation. J. Food. Prot.
874 56:983-985.
875
876 Bryan, F. L., J. C. Ayers, and A. A. Kraft. 1968. Contributory sources of salmonellae on turkey
877 products. Am. J. Epidemiol. 87:578-597.
878
879 Buhr, R. J., and J. A. Dickens. 2001. Crop extraction load and efficiency of crop removal during
880 manual evisceration of broilers: 1. Evaluation of stunning voltage and method of bleeding.
881 J. Appl. Poult. Res. 10:71-78.
882
883 Buhr, R. J., and J. A. Dickens. 2002. Crop extraction load and efficiency of crop removal during
884 manual evisceration of broilers: 2. Influence of age, gender, and direction of extraction. J. Appl.
885 Poult. Res. 11:6-12.
886
887 Buhr, R. J., J. A. Cason, J. A. Dickens, and D. E. Marshall. 2000. Extraction load and intact crop
888 removal in modified manual evisceration of male broilers. J. Appl. Poult. Res. 9:371-374.

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 Appendix C – Literature Review of the Poultry Slaughter Process

889 Buhr, R. J., M. E. Berrang, and J. A. Cason. 2003. Bacterial recovery from breast skin of
890 genetically feathered and featherless broiler carcasses immediately following scalding and
891 picking. Poult. Sci. 82:1646-1647.
892
893 Byrd, J. A., D. E. Corrier, M. E. Hume, R. H. Bailey, L. H. Stanker, and B. M. Hargis. 1998.
894 Incidence of Campylobacter in crops of preharvest market-age broiler chickens. Poultry Sci.
895 77:1303-1305.
896
897 Byrd, J. A., B. M. Hargis, D. J. Caldwell, R. H. Bailey, K. L. Herron, J. L. McReynolds,
898 R. L. Brewer, R. C. Anderson, K. M. Bischoff, T. R. Callaway, and L. F. Kubena. 2001. Effect
899 of lactic acid administration in the drinking water during preslaughter feed withdrawal on
900 Salmonella and Campylobacter contamination of broilers. Poultry Science. 80:278-283.
901
902 Byrd, J. A., B.M. Hargis, D.E. Corrier, R. L. Brewer, D. J. Caldwell, R. H. Bailey, J. L.
903 McReynolds, K. L. Herron, and L. H. Stanker. 2002. Fluorescent marker for the detection of
904 crop and upper gastrointestinal leakage in poultry processing plants. Poult. Sci. 81:70-74.
905
906 Byrd, J. A., R. C. Anderson, T. R. Callaway, R. W. Moore, K. D. Knape, L. F. Kubena,
907 R. L. Ziprin, and D. J. Nisbet, 2003. Effect of experimental chlorate product administration in
908 the drinking water on Salmonella typhimurium contamination of broilers. Poultry
909 Science. 82:1403-1406.
910
911 Campbell, D. F., S. S. Green, C. S. Custer, and R. W. Johnson, 1982. Incidence of Salmonella in
912 fresh dressed turkeys raised under Salmonella-controlled and uncontrolled environments. Poult.
913 Sci. 61:1962-1967.
914
915 Cason, J. A., R. J. Buhr, J. A. Dickens, M. T. Musgrove, and N. J. Stern. 1999. Carcass
916 microbiological quality following intermittent scalding and defeathering. J. Appl. Poult.
917 Res. 8:368-373.
918
919 Cason, J. A., A. Hinton, and K. D. Ingram. 2000. Coliform, Escherichia coli, and salmonellae
920 concentrations in a multiple-tank, counter flow poultry scalder. J. Food Prot. 63:1184-1188.
921
922 Cason, J. A., A. Hinton, and R. J. Buhr. 2004. Impact of feathers and feather follicles on broiler
923 carcass bacteria. Poult. Sci. 83:1452-1455.
924
925 Clouser, C. S., S. Doores, M. G. Mast, and S. J. Knabel. 1995a. The Role of defeathering in the
926 contamination of turkey skin by Salmonella species and Listeria monocytogenes. Poult.
927 Sci. 74:723-731.
928
929 Clouser, C. S., J. Knabel, M. G. Mast, and S. Doores. 1995b. Effect of type of defeathering
930 system on Salmonella cross-contamination during commercial processing. Poult.
931 Sci. 74:732-741.
932
933 Corry, J. E. L., V. M. Allen, W. R. Hudson, M. F. Breslin, and R. H. Davies. 2002. Sources of
934 Salmonella on broiler carcasses during transportation and processing: modes of contamination
935 and methods of control. J. Appl. Microbiol. 92:424-432.

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 Improvements for Poultry Slaughter Inspection

936 Cox, N. A, A. J. Mercuri, J. E. Thomson, and D. W. Gregory. 1974. Quality of broiler carcasses
937 as affected by hot water treatments. Poult. Sci. 53:1566-1571.
938
939 Davies, R. H., and C. Wray. 1996. Studies of contamination of three broiler breeder houses with
940 Salmonella enteritidis before and after cleansing and disinfection. Avian Dis 40:626-633.
941
942 Davies, R. H., M. Breslin, J. E. L. Corry, W. Hudson, and V. M. Allen. 2001. Observations on
943 the distribution and control of Salmonella species in two integrated broiler companies. Vet.
944 Rec. 149:227-232.
945
946 Davison, S., C. E. Benson, D. J. Henzler, and R. J. Eckroade. 1999. Field observations with
947 Salmonella enteritidis bacterins. Avian Diseases. 43:664-669.
948
949 Delezie, E., J. Zoons, J. Buyse, and E. Decuypere, E. 2006. Influence of whole wheat inclusion
950 on optimal feed withdrawal duration. Br. Poult. Sci. 47:572-5.
951
952 Dickens, J. A. 1989. Experimental, prototype spray-scalder for poultry processing. Poult.
953 Sci. 69:409-413.
954
955 Dickens, J. A., and A. D. Whittemore. 1997. Effects of acetic acid and hydrogen peroxide
956 application during defeathering on the microbiological quality of broiler carcasses prior to
957 evisceration. Poult. Sci. 76:657-660.
958
959 Drewniak, E. E., E. R. Baush, and L. L. Davis. 1955. Carbon dioxide immobilization of turkeys
960 before slaughter. USDA. Circular 958.
961
962 Evans, S. J., and A. R. Sayers. 2000. A longitudinal study of Campylobacter infection of broiler
963 flocks in Great Britain. Prev. Vet. Med. 46:209-223.
964
965 Fletcher, D. L. 1999. Symposium: Recent advances in poultry slaughter technology. Poult.
966 Sci. 78:277-281.
967
968 Fletcher, D. L., and E. W. Craig. 1997. An evaluation of on-line reprocessing on visual
969 contamination and microbiological quality of broilers. J. Appl. Poult. Res. 6:436-442.
970
971 Fluckey, W. M., M. X. Sanchez, S. R. McKee, D. Smith, E. Pendleton, and M. M. Brashers.
972 2003. Establishment of a microbiological profile for an air-chilling poultry operation in the
973 United States. J. Food Prot. 66:272-279.
974
975 Fuller, R. 1989. Probiotics in man and animals. [Link]. Bacteriol. 66:365-378.
976
977 Gast, R. K., H. D. Stone, and P. S. Holt. 1993. Evaluation of the efficacy of oil-emulsion
978 bacterins for reducing fecal shedding of Salmonella Enteritidis by laying hens. Avian
979 Diseases. 37:1085-1091.
980

C-24
 Appendix C – Literature Review of the Poultry Slaughter Process

981 Geornaras, I., A. E. de Jesus, E. van Zyl, and A. von Holy. 1997. Bacterial populations of
982 different sample types from carcasses in the dirty area of a South African poultry abattoir. J.
983 Food Prot. 60:551-554.
984
985 Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation of the human colonic
986 microbiota:introducing the concept of probiotics. J. Nutr. 125:1401-1412.
987
988 Gregory, N. G., and S. B. Wotton. 1986. Effect of slaughter on the spontaneous and evoked
989 activity of the brain. Br. Poult. Sci. 27:195-205.
990
991 Griffiths, G. L. 1985. The occurrence of red-skin chicken carcasses. Br. Vet. J. 141:312-314.
992
993 Hargis, B. M., D. J. Caldwell, R. L. Brewer, D. E. Corrier, and J. R. Beloach. 1995. Evaluation
994 of the chicken crop as a source of Salmonella contamination of broiler carcasses. Poult.
995 Sci. 74:1548-1552.
996
997 Heath, G. B. S., D. J. Watt, P. R. Waite, and J. M. Ormond, 1981. Observations on poultry
998 slaughter. Vet. Rec. 108:97-99.
999
1000 Heath, G. B. S., D. J. Watt, P. R. Waite, and P. A. Meakins. 1983. Further observations on the
1001 slaughter of poultry. Br. Vet. J. 139:285-290.
1002
1003 Heath, G. E., A. M. Thaler, and W. O. James. 1994. A survey of stunning methods currently used
1004 during slaughter of poultry in commercial poultry plants. J. Appl. Poult. Res. 3:297-302.
1005
1006 Herman, L., M. Heyndrickx, K. Grijspeerdt, D. Vandekerchove, I. Rollier, and L. De Zutter.
1007 2003. Routes for Campylobacter contamination of poultry meat: epidemiological study from
1008 hatchery to slaughterhouse. Epidemiol. Infect. 131:1169-1180.
1009
1010 Higgins, R., R. Malo, E. René-Roberge, and R. Gauthier. 1981. Studies on the dissemination of
1011 Salmonella in nine broiler-chicken flocks. Avian. Dis. 26:26-32.
1012
1013 Hinton, A., R. J. Buhr, and K. D. Ingram. 2000. Reduction of Salmonella in the crop of broiler
1014 chickens subjected to feed withdrawal. Poult. Sci. 79:1566-1570.
1015
1016 Hinton, A., R. J. Buhr, and K. D. Ingram. 2002. Carbohydrate-based cocktails that decrease the
1017 population of Salmonella and Campylobacter in the crop of broiler chickens subjected to feed
1018 withdrawal. Poult. Sci. 81:780-784.
1019
1020 Holzapfel, W. H., P. Haberer, J. Snel, U. Schillinger, and J. H. Huis in’t Veld. 1998.
1021 International Journal of Food Microbiology. 41:85-101.
1022
1023 Humphrey, T. J. 1981. The effects of pH and levels of organic matter on the death rates of
1024 Salmonella in chicken scald tank water. J. Appl. Bact. 51:27-39.
1025

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 Improvements for Poultry Slaughter Inspection

1026 Humphrey, T. J., and D. G. Lanning. 1987. Salmonella and Campylobacter contamination of
1027 broiler chicken carcasses and scald tank water: the influence of water pH. J. Appl.
1028 Bact. 63:21-25.
1029
1030 Humphrey, T. J., D. G. Lanning, and D. Leeper. 1984. The influence of scald water pH on death
1031 rates of Salmonella typhimurium and other bacteria attached to chicken skin. J. Appl.
1032 Bact. 57:355-359.
1033
1034 Izat, A. L., F. A Gardner, J. H. Denton, and F. A. Golan. 1988. Incidence and level of
1035 Campylobacter jejuni in broiler processing. Poult. Sci. 67:1568-1572.
1036
1037 James, W. O., R. L. Brewer, J. C. Prucha, W. O. Williams, and D. R. Parham. 1992. Effects of
1038 chlorination of chill water on the bacteriologic profile of raw chicken carcasses and giblets.
1039 JAVMA. 200:60-63.
1040
1041 James, W. O., C. Prucha, and R. Brewer. 1993. Cost-effective techniques to control human
1042 enteropathogens on fresh poultry. Poult. Sci. 72:1174-1176.
1043
1044 Jimenez, S. M., M. S. Salsi, M. C. Tiburzi, and M. E. Pirovani, 2002. A comparison between
1045 broiler chicken carcasses with and without visible fecal contamination during the slaughtering
1046 process on hazard identification of Salmonella spp. J. Appl. Microbiol. 93:593-598.
1047
1048 Jimenez, S. M., M. C. Tiburzi, M. S. Salsi, M. E. Pirovani, and M. A. Moguilevsky. 2003. The
1049 role of visible fecal material as a vehicle for generic Escherichia coli, coliform, and other
1050 enterobacteria contaminating poultry carcasses during slaughtering. J. Appl.
1051 Microbiol. 95:451-456.
1052
1053 Kaufman, V. F., A. A. Klose, H. G. Bayne, M. F. Pool, and H. Lineweaver. 1972. Plant
1054 processing of sub-atmospheric steam scalded poultry. Poult. Sci. 51:1188-1194.
1055
1056 Kemp, G. K., M. L. Aldrich, M. L. Guerra, and K. R. Schneider. 2001a. Continuous online
1057 processing of fecal- and ingesta- contaminated poultry carcasses using an acidified sodium
1058 chlorite antimicrobial intervention. J. Food Prot. 64:807-812.
1059
1060 Kemp, G. K., M. L. Aldrich, and A. L. Waldroup. 2001b. Acidified sodium chlorite
1061 antimicrobial treatment of broiler carcasses. J. Food Prot. 63:1087-1092.
1062
1063 Kim, J. W., and S. Doores. 1993. Influence of three defeathering systems on microtopography of
1064 turkey skin and adhesion of Salmonella typhimurium. J. Food Prot. 56:286-291, 305.
1065
1066 Klose, A. A., U. F. Kaufman, and M. F. Pool. 1971. Scalding poultry by steam at subatmospheric
1067 pressures. Poult. Sci. 50:302-304.
1068
1069 Kotula, K. L., and Y. Pandya. 1995. Bacterial contamination of broiler chickens before scalding.
1070 J. Food Prot. 58:1326-1329.
1071

C-26
 Appendix C – Literature Review of the Poultry Slaughter Process

1072 Kotula, A. W., E. E. Drewniak, and L. L. Davis. 1961. Experimentation with in-line carbon
1073 dioxide immobilization of chickens prior to slaughter. Poult. Sci. 40:213-216.
1074
1075 Kotula, A. W., G. J. Banwar, and J. A. Kinner. 1967. Effect of post-chill washing on bacterial
1076 counts of broiler chickens. Poult. Sci. 46:1210-1216.
1077
1078 Kuenzel, W. J., and J. H. Walther. 1978. Heart beat, blood pressure, respiration and brain waves
1079 of broilers as affected by electrical stunning and bleed out. Poult. Sci. 57:655-659.
1080
1081 Kuenzel, W. J., A. L. Ingling, D. M. Denbow, J. H. Walther, and M. M. Schaefer. 1978. Variable
1082 frequency stunning and a comparison of two bleed out time intervals for maximizing blood
1083 release in processed poultry. Poult. Sci. 57:449-454.
1084
1085 Lillard, H. S. 1979. Levels of chlorine and chlorine dioxide of equivalent bactericidal effect in
1086 poultry processing water. J. Food Sci. 44:1594-1597.
1087
1088 Lillard, H. S. 1980. Effect on broiler carcasses and water of treating chiller water with chlorine
1089 or chlorine dioxide. Poult. Sci. 59:1761-1766.
1090
1091 Lillard, H. S. 1989. Factors affecting the persistence of Salmonella during the processing of
1092 poultry. J. Food Prot. 52:829-832.
1093
1094 Lillard, H. S. 1990. The impact of commercial processing procedures on the bacterial
1095 contamination and cross-contamination of broiler carcasses. J. Food Prot. 53:202-204, 207.
1096
1097 Lillard, H. S., L. C. Blankenship, J. A. Dickens, S. E. Craven, and A. D. Shackelford. 1987.
1098 Effect of acetic acid on the microbiological quality of scalded picked and unpicked broiler
1099 carcasses. J. Food Prot. 50:112-114.
1100
1101 Line, J. E., J. S. Bailey, N. E. Cox, and N. J. Stern. 1997. Yeast treatment to reduce Salmonella
1102 and Campylobacter populations associated with broiler chickens subjected to transport stress.
1103 Poult. Sci. 76:1227-1231.
1104
1105 Loncarevic, S., W. Than, and M. L. Danielsson-Tham. 1994. Occurrence of Listeria species in
1106 broilers pre- and post-chilling in chlorinated water at two slaughterhouses. Acta vet.
1107 Scand. 35:149-154.
1108
1109 Lues, J. F., M. M. Theron, P. Venter, and M. H. Rasephei. 2007. Microbial composition in
1110 bioaerosols of a high-throughput chicken- slaughtering Facility. Poult. Sci.86:142-9.
1111
1112 Lutgring, K. R., R. H. Linton, N. J. Zimmerman, M. Peugy, and A. J. Heber. 1997. Distribution
1113 and quantification of bioaerosals in poultry-slaughter plants. J. Food Prot. 60:804-810.
1114
1115 Marsi, M. 1986. Chlorinating poultry chiller water: the generation of mutagens and water re-use.
1116 Food Chem. Toxicol. 24:923-930.
1117

C-27
 Improvements for Poultry Slaughter Inspection

1118 McNeal, W. D., D. L. Fletcher, and R. J. Buhr. 2003. Effects of stunning and decapitation on
1119 broiler activity during bleeding, blood loss, carcass and breast meat quality. Poult.
1120 Sci. 82:163-168.
1121
1122 Mead, G. C., B. W. Adams, and R. T. Parry. 1975. The effectiveness of in-plant chlorination in
1123 poultry processing. Br. Poult. Sci. 16:517-526.
1124
1125 Mead, G. C., W. R. Hudson, and M. H. Hinton. 1993. Microbiological survey of five poultry
1126 processing plants in the UK. Br. Poult. Sci. 34:497-503.
1127
1128 Mead, G. C., W. R. Hudson, and M. H. Hinton. 1994. Use of a marker organism in poultry
1129 processing to identify sites of cross-contamination and evaluate possible control measures. Br.
1130 Poult. Sci 35:345-354.
1131
1132 Mead, G. C., V. M. Allen, C. H. Burton, and J. E. Corry. 2000. Microbial cross-contamination
1133 during air chilling of poultry. Br. Poult. Sci. 41:158-162.
1134
1135 Morrison, G. J., and G. H. Fleet. 1985. Reduction of Salmonella on chicken carcasses by
1136 immersion treatments. J. Food Prot. 48:939-943.
1137
1138 Mulder, R. W. A. W., W. J. Dorresteijn, G. J. P. Hofmans, and C. H. Veerkanp. 1976.
1139 Experiments with continuous immersion chilling of broiler carcasses according to the code of
1140 practice. J. Food Sci. 41:438-442.
1141
1142 Mulder, R. W. A. W., L. W. J. Dorresteijn, and J. Van der Broek. 1978. Cross-contamination
1143 during the scalding and plucking of broilers. Br. Poult. Sci. 19:61-70.
1144
1145 Musgrove, M. T., J. A. Cason, D. L. Fletcher, N. J. Stern, N. A. Cox, and J. S. Bailey. 1997.
1146 Effect of cloacal plugging on microbial recovery from partially processed broilers.
1147 Poult Sci 76:530-533.
1148
1149 NCC (National Chicken Council). 1992. Good manufacturing practices. Fresh broiler products.
1150 [Link]/p_documents/newsandinfo_160404101434.pdf.
1151
1152 NTF (National Turkey Federation). 2004. Best management practices for turkey production.
1153 [Link]/p_documents/newsandinfo_280404094832.pdf.
1154
1155 Nde, C. W., J. S. Sherwood, C. Doetkott, and C. M. Logue. 2006. Prevalence and molecular
1156 profiles of Salmonella collected at a commercial turkey processing plant. J. Food
1157 Prot. 69:1794-801.
1158
1159 Nde, C. W., J. M. McEvoy, J. S. Sherwood, and C. M. Logue. [Link] contamination of
1160 turkey carcasses by Salmonella species during defeathering. Poult. Sci. 86:162-7.
1161 Netherwood, T., H. J. Gilbert, D. S. Parker, and A. G. O’Donnell. November 1999. Probiotics
1162 shown to change bacterial community structure in the avian gastrointestinal tract. Applied and
1163 Environmental Microbiology. 5134-5138.
1164

C-28
 Appendix C – Literature Review of the Poultry Slaughter Process

1165 Newell, D. G., J. E. Shreeve, M. Toszeghy, G. Domingue, S. Bull, T. Humphrey, and G. Mead.
1166 2001. Changes in the carriage of Campylobacter strains by poultry carcasses during processing
1167 in abattoirs. Appl. Environ. Microbiol. 67:2636-2640.
1168
1169 Nijdam, E., E. Lambooij, M. J. Nabuurs, E. Decuypere, and J. A. Stegeman. 2006. Influences of
1170 feeding conventional and semisynthetic diets and transport of broilers on weight gain, digestive
1171 tract mass, and plasma hormone and metabolite concentrations. Poult. Sci. 85:1652-9.
1172
1173 Northcutt, J. K., M. E. Berrang, J.A. Dickens, D. L. Fletcher, and N. A. Cox. 2003. Effect of
1174 broiler age, feed withdrawal, and transportation on levels of coliforms, Campylobacter,
1175 Escherichia coli and Salmonella on carcasses before and after immersion chilling. Poult.
1176 Sci. 82:169-173.
1177
1178 Northcutt, J. K., D. R. Jones, and M. T. Musgrove. 2004. Airborne microorganisms during the
1179 commercial production and processing of Japanese quail. Int. J. Poult. Sci. 3:242-247.
1180
1181 Notermans, S., R. J. Terbijhe, and M. Van Schothorst. 1980. Removing fecal contamination of
1182 broilers by spray-cleaning during evisceration. Brit. Poult. Sci. 21:115-121.
1183
1184 Okrend, A. J., R. W. Jonhston, and A. B. Moran. 1986. Effect of acetic acid on the death rates at
1185 52°C of Salmonella newport, Salmonella typhimurium and Campylobacter jejuni in poultry scald
1186 water. J. Food Prot. 49:500-503.
1187
1188 Oosterom, J., S. Notermans, H. Karman, and G. B. Engels. 1983. Origin and prevalence of
1189 Campylobacter jejuni in poultry processing. J. Food Prot. 46:339-344.
1190
1191 Papa, C. M., and J. A. Dickens. 1989. Lower gut contents and defecatory responses of broiler
1192 chickens as affected by feed withdrawal and electrical treatment at slaughter. Poult.
1193 Sci. 68:1478-1484.
1194
1195 Purdy, J., C. Dodd, D. Fowler, and W. Waites. 1988. Increase in microbial contamination of
1196 defeathering machinery in a poultry processing plant after changes in the method of processing.
1197 Letters in Appl. Microbiol. 6:35-38.
1198
1199 Raj, A. B. M. 1994. An investigation into the batch killing of turkeys in their transport containers
1200 using mixtures of gases. Res. Vet. Sci. 56:325-331.
1201
1202 Raj, A. B. M., and N. G. Gregory. 1990. Investigation into the batch stunning/killing of chickens
1203 using carbon dioxide or argon-induced hypoxia. Res. Vet. Sci. 49:364-366.
1204
1205 Raj, A. B. M., and N. G. Gregory. 1994. An evaluation of humane gas stunning methods for
1206 turkeys. Vet. Rec. 135:222-223.
1207 Raj, A. B. M., and G. R. Nute. 1995. Effect of stunning method and filleting time on sensory
1208 profile of turkey breast meat. Br. Poult. Sci. 36:221-227.
1209
1210 Raj, A. B. M., T. C. Grey, A. R. Audsley, and N. G. Gregory. 1990. Effect of electrical and
1211 gaseous stunning on the carcass and meat quality of broilers. Br. Poult. Sci. 31:725-735.

C-29
 Improvements for Poultry Slaughter Inspection

1212
1213 Raj, A. B. M, L. J. Wilkins, R. I. Richardson, and S. B. Wotton. 1997. Carcass and meat quality
1214 in broilers either killed with a gas mixture or stunned with an electric current under commercial
1215 processing conditions. Br. Poult. Sci. 38:169-174.
1216
1217 Raj, A. B. M, R. I. Richardson, L. J. Wilkins, and S. B. Wotton. 1998. Carcass and meat quality
1218 in ducks killed with either gas mixtures or an electric current under commercial processing
1219 conditions. Br. Poult. Sci. 39:404-407.
1220
1221 Rathgeber, B. M., J. L. Macisaac, and M. E. MacKenzie. 2007. Feeding turkeys a highly
1222 digestible supplement during preslaughter feed withdrawal. Poult. Sci. 86:2029-33.
1223
1224 Richardson, L. J., C. L. Hofacre, B. W. Mitchell, and J. L. Wilson. 2003. Effect of electrostatic
1225 space charge on reduction of airborne transmission of Salmonella and other bacteria in broiler
1226 breeders in production and their progeny. Avian Diseases. 47(4):1352-1361.
1227
1228 Rose, N., Beaudeau, F., Drouin, P. Toux. J.Y., Rose, V., and Colin, P. 2000. Risk factors for
1229 Salmonella persistence after cleaning and disinfection in French broiler-chicken houses. Prev Vet
1230 Med 44:9-20.
1231
1232 Russell, S. M. 2005. Intervention strategies for reducing Salmonella prevalence on ready to cook
1233 chicken. University of Georgia Cooperative Extension Service.
1234 [Link]
1235
1236 Russell, S. M., and J. M. Walker. 1997. The effect of evisceration on visible contamination and
1237 the microbiological profile of fresh broiler chicken carcasses using the Nu-Tech® evisceration
1238 system or the conventional streamlined inspection system. Poult. Sci. 76:780-784.
1239
1240 Sanchez, M. X., W. M. Fluckey, M. M. Brashears, and S. R. McKee. 2002. Microbial profile and
1241 antibiotic susceptibility of Campylobacter spp. and Salmonella spp. in broilers processed in air
1242 chilled and immersion–chilled environments. J. Food Prot. 65:948-956.
1243
1244 Sarlin, L. L., E. T. Barnhart, D. J. Caldwell, R. W. Moore, J. A. Byrd, D. Y. Caldwell, D. E.
1245 Corrier, J. R. Deloach, and B. M. Hargis. 1998. Evaluation of alternative sampling methods for
1246 Salmonella critical control point determination at broiler processing. Poult. Sci. 77:1253-1257.
1247
1248 Slader, J., G. Domingue, F. Jørgensen, K. McAlpine, R. J. Owen, F. J. Bolton, and T. J.
1249 Humphrey. 2002. Impact of transport crate reuse and of catching and processing on
1250 Campylobacter and Salmonella contamination of broiler chickens. Appl. Environ.
1251 Microbiol. 68:713-719.
1252
1253 Strange, R. E., and M. Shon. 1964. Effects of thermal stress on viability and ribonucleic acid of
1254 Aerobacter aerogenes in aqueous suspensions. J. Gen. Microbiol. 34:99-114.
1255
1256 Takahashi, R., F. Shahada, T. Chuma, and K. Okamoto. 2006 Analysis of Campylobacter spp.
1257 contamination in broilers from the farm to the final meat cuts by using restriction fragment

C-30
 Appendix C – Literature Review of the Poultry Slaughter Process

1258 length polymorphism of the polymerase chain reaction products. Int. J. Food
1259 Microbiol. 110:240-5.
1260
1261 Tellez, G., V. M. Petrone, M. Escorcia, T. Y. Morishita, C.W. Cobb, and L. Villaseñor. 2001.
1262 Evaluation of avian-specific probiotic and Salmonella enteritidis, Salmonella typhimurium, and
1263 Salmonella heidleberg-specific antibodies on cecal colonization and organ invasion of
1264 Salmonella enteritidis in broilers. Journal of Food Protection. 64(3):287-291.
1265
1266 Teotia, J. S., and B. F. Miller. 1975. Destruction of Salmonella on poultry meat with lysozyme,
1267 EDTA, X-ray, microwave, and chlorine. Poul. Sci. 54:1388-1394.
1268
1269 Thayer, S., and J. L. Walsh. 1993. Evaluation of cross-contamination on automatic viscera
1270 removal equipment. Poult. Sci. 72:741-746.
1271
1272 Thiessen, G. P., W. R. Usborne, and H. L. Orr. 1984. The efficacy of chlorine dioxide in
1273 controlling Salmonella contamination and its effect on product quality of chicken broiler
1274 carcasses. Poult. Sci. 63:647-653.
1275
1276 Thomas, J. E., J. S. Bailey, N. A. Cox, D. A. Posey, and M. O. Carson. 1979. Salmonella on
1277 broiler carcasses as affected by fresh water input rate and chlorination of chiller water. J. Food
1278 Prot. 42:954-955.
1279
1280 Thompson, K. L., and T. J. Applegate. 2006. Feed withdrawal alters small-intestinal morphology
1281 and mucus of broilers. Poult. Sci. 85:1535-40.
1282
1283 Torres-Rodriguez, A., A. M. Donoghue, D. J. Donoghue, J. T. Barton, G. Tellez, and
1284 B. M. Hargis. 2007. Performance and condemnation rate analysis of commercial turkey flocks
1285 treated with a Lactobacillus spp.-based probiotic. Poult. Sci. 86:444-6.
1286
1287 Tsai, L. S., C. J. Mapes, and C. C. Huxsoll. 1987. Aldehydes in poultry chiller water. Poult.
1288 Sci. 66:983-989.
1289
1290 Tsai, L. S., J. E. Schade, and B. T. Molyneux. 1992. Chlorination of poultry chiller water:
1291 chlorine demand and disinfection efficiency. Poult. Sci. 71:188-196.
1292
1293 USDA, FSIS, OPHS. 2003 FSIS National Residue Program data. Zoonotic Diseases and
1294 Residue Surveillance Division, Washington, DC.
1295
1296 Villarreal, M. E., R. C. Baker, and J. M. Regenstein. 1990. The incidence of Salmonella on
1297 poultry carcasses following the use of slow release chlorine dioxide (Alcide). J. Food
1298 Prot. 53:465-467.
1299 Wabeck, C. J. 1972. Feed and water withdrawal time relationship to processing yield and
1300 potential fecal contamination of broilers. Poult. Sci. 51:1119-1121.
1301
1302 Wabeck, C. J., D. V. Schwall, G. M. Evancho, J. G. Heck, and A. B. Rogers. 1969. Salmonella
1303 and total count reduction in poultry treated with sodium hypochlorite solutions. Poult.
1304 Sci. 47:1090-1094.

C-31
 Improvements for Poultry Slaughter Inspection

1305
1306 Waldroup, A. L., B. M. Rathgeher, R. H. Forsythe, and L. Smoot. 1992. Effects of six
1307 modifications on the incidence and levels of spoilage and pathogenic organism on commercially
1308 processed post-chill broilers. J. Appl. Poult. Res. 1:226-234.
1309
1310 Waldroup, A., B. Rathgeber, and N. Imel. 1993. Microbiological aspects of counter current
1311 scalding. J. Appl. Poult. Res. 2:203-207.
1312
1313 Wempe, J. M., C. A. Genigeorgis, T. B. Farver, and H. I. Yusufu. 1983. Prevalence of
1314 Campylobacter jejuni in two California chicken processing plants. Appl. Environ.
1315 Microbiol. 45:355-359.
1316
1317 White, H. R. 1963. The effect of variations in pH on the heat resistance of culture of
1318 Streptococcus faecalis. J. Appl. Bact. 40:365-374.
1319
1320 Whittemore, A. D., and C. E. Lyon. 1994. Microbiological profile of rubber defeathering fingers
1321 and carcasses from processing lines with single and triple stage scalders. Poult. Sci. 73S1:24.
1322
1323 Whyte, P., J. D. Collins, K. McGill, C. Monahan, and H. O’Mahony. 2001a. Distribution and
1324 prevalence of airborne microorganisms in three commercial poultry processing plants. J. Food
1325 Prot. 64(3):388-391.
1326
1327 Whyte, P., J. D. Collins, K. McGill, C. Monahan, and H. O’Mahony. 2001b. Quantitative
1328 investigation of the effects of chemical decontamination procedures on the microbiological status
1329 of broiler carcasses during processing. J. Food Prot. 64(2):179-183.
1330
1331 Yang, Z., Y. Li, and M. F. Slavik. 1998. Use of antimicrobial spray applied with an inside-
1332 outside bird washer to reduce bacterial contamination of pre-chilled chicken carcasses. J. Food
1333 Prot. 61:829-832.
1334
1335 Yang, H., Y. Li, and M. G. Johnson. 2001. Survival and death of Salmonella typhimurium and
1336 Campylobacter jejuni in processing water and on chicken skin during poultry scalding and
1337 chilling. J. Food Prot. 64:770-776.

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