Evaluation of Disinfectants Used in Pre-Chilling water Tanks of Poultry Processing Plants

ABSTRACT

In poultry processing plants, disinfectants are often added to pre-chilling water tanks to reduce microbial contamination. The present study aimed at evaluating the effect of five disinfectants (acidified sodium chlorite, alkyl dimethyl benzyl ammonium chloride, chlorine dioxide, peracetic acid, and sodium hypochlorite) on the populations of food quality indicator microorganisms and on Salmonella Enteritidis (SE) in the presence and absence of organic matter. The results showed that chlorine dioxide and sodium hypochlorite did not reduce microbial carcass counts. On the other hand, acidified sodium chlorite, alkyl dimethyl benzyl ammonium chloride and peracetic acid reduced total and fecal coliform counts. Peracetic acid reduced the number of psychrotrophic microorganisms. All products were effective in reducing SE counts only in the absence of organic matter. Acidified sodium chlorite, alkyl dimethyl benzyl ammonium chloride and peracetic acid could be candidates for the replacement of sodium hypochlorite (commonly used in Brazil) in pre-chilling tanks.

Keywords:
Broiler carcasses; disinfectant; indicator microorganisms; pre-chilling tank; Salmonella Enteritidis

INTRODUCTION

During broiler carcass processing, evisceration, carcass wash, pre-chilling and cooling steps can favor the dissemination of microorganisms and carcass contamination (USDA, 2002). One infected broiler arriving at the processing plant may be the source of contamination of many other carcasses (Lillard, 1989; Rasschaert et al., 2008). Some microorganisms present in the broiler intestine, such as Salmonella spp., Campylobacter spp., and thermotolerant coliforms, represent a threat to public health (Scallan et al., 2011). Carcasses can be also contaminated with spoilage microorganisms that reduce the shelf life of meat products (Silva et al., 2006).

Outbreaks of foodborne diseases in Brazil remain largely uninvestigated, and consequently, few data are available. For instance, from 1999 to 2012, the Brazilian Health Surveillance Division reported 1,525 outbreaks of human foodborne salmonellosis, most of them related to food of poultry origin (Brazil, 2013). Other causes of foodborne diseases (e.g. campylobacteriosis) are rarely diagnosed in Brazil. In 2013, campylobacteriosis represented about 6.5% of all cases of human foodborne diseases in the United States of America (Crim et al., 2014) and contaminated poultry meat was the main source of this pathogen. The Brazilian legislation establishes that Salmonella spp. must be absent in broiler carcasses after processing (Brazil, 2001), but no requirements are established for the presence Campylobacter spp.

Disinfectant compounds are added to the pre-chilling and chilling water tanks with the purpose of minimizing carcass microbial contamination, particularly of pathogens and spoilage bacteria (Brazil, 1998; HACCP, 1995). According to the Brazilian legislation, only chlorine compounds, at a maximum level of 5 ppm, can be added to the pre-chiller water in poultry processing plants (Brazil, 1998). However, other countries allow the use of other substances, such as sodium methyl sulfate and peracetic acid (peroxyacetic acid) (USA, 1977). Recently, alkyl dimethyl benzyl ammonium chloride was also recommended for pre-chilling tanks (Busch et al., 2013).

The present study aimed at evaluating alternative compounds that could replace the current chlorine-based compounds commonly used in Brazil. The effect of five disinfectant compounds (acidified sodium chlorite, alkyl dimethyl benzyl ammonium chloride, chlorine dioxide, peracetic acid and sodium hypochlorite) on the counts of food quality indicator microorganisms and Salmonella enterica subsp. enterica serovar Enteritidis (Salmonella Enteritidis) were evaluated in the presence and absence of organic matter.

MATERIAL AND METHODS

Two separate experiments were performed to evaluate the effect of selected of disinfectants on chicken carcass microbial counts: one with meat quality indicator microorganisms, and the second with Salmonella Enteritidis. All assays were performed at 25°C.

1. Experiment 1

1.1. Sampling

Seven samplings were performed. In each sampling, 18 broiler carcasses were purchased from processing plants located in the state of São Paulo, Brazil state. Carcasses were taken in isothermal containers to the Avian Pathology laboratory of the Department of Veterinary Pathology, School of Agriculture and Veterinary Sciences (FCAV/UNESP), São Paulo, Brazil.

1.2. Treatment of broilers carcasses

Six plastic buckets were filled with 30 L of cold water (14-16°C). Acidified sodium chlorite, alkyl dimethyl benzyl ammonium chloride, chlorine dioxide, peracetic acid, and sodium hypochloriteat the concentrations of50, 175, 5, 50and 5 ppm, respectively, were added to one bucket each. The sixth bucket contained only water (negative control). Three carcasses were immersed in each bucket for 25 minutes in order to simulate the pre-chilling processing step.

1.3. Microbiological analyses

Upon removal of the buckets, carcasses were placed in sterile plastic bags containing 400 mL of 0.1% Buffered Peptone Water (BPW) (Difco^(tm), Detroit, Michigan, USA) and 400 mL of a mixture of neutralizers, consisting of 64.5 g of Tween 80, 20% sodium bisulfite, 7.84 g of sodium thiosulfate pentahydrate, 5 g of sodium thioglycolate, and 1.5 g of L-cysteine, all diluted in 1,000 mL of tryptone-salt solution (pH 7.2) (Espigares et al., 2003). The neutralized BPW was further processed in order to obtain the most probable number (MPN) of total and fecal coliforms and counts of viable strict and facultative aerobic mesophylls, both according to the methodology described by Downes & Ito (2001). Additionally, the presence of aerobic psychrotrophic microorganisms was determined according to Downes & Ito (2001).

1.3.1. Determination of the Most Probable Number (MPN)

The neutralized BPW resulting from carcass washing was serially diluted, and 1 mL of each dilution inoculated into three inverted Durham culture tubes containing10 mL of Lauryl Tryptose Broth (LTB) (Difco^(tm), Detroit, Michigan, US). The tubes were incubated at 37°C for 48h. Cultured tubes presenting turbidity and gas production or effervescence by subtle shaking, were considered presumptively positive.

In order to determine the MPN of total coliforms/mL, a sterile bacterial loop was plunged into the presumptively LTB-positive culture tubes followed by inoculation in 10 mL Brilliant Green Bile 2% (BGB) (Difco^(tm), Detroit, Michigan, USA) also contained an inverted Durham tube, and incubation at 37°C for 48h. When gas production was observed on upper section of the inverted tube, the sample was considered positive.

The MPN of fecal coliforms/mL was surveyed similarly to the total coliforms, although Escherichia coli (EC) medium (Difco^(tm), Detroit, Michigan, US) in an inverted Durham tube instead of BGB was used. The tubes were incubated in water bath at 45.5 ± 0.2°C for 48h and the positive samples were identified as described above, according to the methodology of Silva et al. (2007). Finally, the MPN/mL was determined based on Hoskins' table (Hoskins, 1934).

1.3.2. Standard count of viable strict and facultative aerobic mesophylls

This bacterial count was carried out using the pour-plate technique. Neutralized BPW obtained from carcass washing was decimally diluted in a new sterile 0.1% BPW up to 10^-6. Then, 1 mL of each dilution was poured on disposable sterile bacteriological Petri dishes (90 x 15 mm) containing 15 mL of Plate Count Agar (PCA) (Difco^(tm), Detroit, Michigan, USA) at approximately 45°C. Cultures were mixed and after agar solidification, Petri dishes were incubated at 37°C for 48h. Thereafter, colony-forming units per milliliter (CFU/mL) were enumerated.

1.3.3. Standard count of aerobic psychrotrophic microorganisms

A volume of 0.1 mL from the neutralized BPW and its decimal dilutions were inoculated onto PCA medium (Difco^(tm), Detroit, Michigan, USA). Colonies were counted according to Downes & Ito (2001) after 10 days of incubation at 7°C.

2. Experiment

2.1.In-vitro assessment of disinfectant activity on Salmonella Enteritidis

A spontaneous mutant of Salmonella Enteritidis resistant to nalidixic acid and to spectinomycin (SE Nal^rSpc^r), stored in the bacterial culture collection of the Avian Pathology laboratory of the Department of Veterinary Pathology of FCAV/UNESP, was used in this trial. This strain was inoculated into 10 mL of Lysogeny broth (LB) (Difco^(tm), Detroit, Michigan, US) and incubated at 37°C for16h under constant shaking (150 rpm). After that, the culture was centrifuged at 4,000 rpm for 20 min at 4°C and suspended in 10 mL phosphate buffered saline (PBS, pH 7.2). This wash step was repeated three times. Bacterial counts were performed in bacteriological Petri dishes (90 x 15 mm) containing Lysogeny agar (Difco^(tm), Detroit, Michigan, US) with nalidixic acid (100 µg/mL) and spectinomicyn (100 µg/mL) after incubation at 37°C for 24h (Hoskins, 1934). A volume of 0.1 mL SE Nal^rSpc^r inoculum, containing about 4 x 10⁸colony-forming units (CFU), was added to each disinfectant solution at 14 to 16°C with or without organic matter (carcass wash solution). Each disinfectant was tested in the presence and in the absence of organic matter (carcass wash solution), as described in Table 1. Bacterial colonies were counted 5 and 25 minutes after disinfectant neutralization with 10 mL of the neutralizing solution described above. Colony-forming units (CFU) were converted to log₁₀ for statistical analyses.

Table 1
Experimental design of experiment 2.

Disinfectants	Treatments performed 5 and 25 minutes afterincubation*
**A, B, C, D and E	(T1) 9.9 mL of PBS + 0.1 mL of SE NalrSpcr (T2) 9.9 mL (PBS + disinfectant) + 0.1 mL of
	SE NalrSpcr (after each time point, 10 mL of neutralizer were added followed by bacterial counting) (T3) 9.9 mL of organic matter + 0.1 mL of SE
	NalrSpcr (T4) 9.9 mL (disinfectant + organic matter) + 0.1 mL of SE NalrSpcr(after each time point, 10 mL of neutralizer were added followed by bacterial counting)

• * T1: suspension containing the test microorganism and control PBS, with no organic matter (control or carcass wash solution); T2: suspension containing the test microorganism and the evaluated disinfectant, with no organic matter; T3: suspension containing the test microorganism andorganic matter; T4: suspension containing the test microorganism, the evaluated disinfectant solution, and organic matter.
• ** A - acidified sodium chlorite (50 ppm); B - alkyl dimethyl benzyl ammonium chloride (175 ppm); C -chlorine dioxide (5 ppm); D - peracetic acid (50 ppm); E - sodium hypochlorite (5 ppm).The final volume of each disinfectant solution in the test was 10 mL.

Statistical analyses

Bacterial count results (CFU and MPN) were transformed in log₁₀ and means compared by Tukey's test at 5% (p<0.05) significance level. Analyses were performed using Statistical Analysis System (SAS) software version 9.1. In the second experiment, disinfectant substances were considered efficient when the SE Nal^rSpc^r counts decreased at least to 10⁵ CFU/mL, according to the recommendations of the European Committee for Standardization (CEN, 2009).

RESULTS

The results of the effects of the tested disinfectants on the counts of meat quality indicator microorganisms in broiler carcasses are shown in Table 2. None of the disinfectant tested reduced mesophyll counts (p>0.05). Peracetic acid reduced the psychrotrophic population (4.01 CFU/mL) compared with the control solution (4.73 CFU/mL) (p<0.05). The other evaluated disinfectants did not demonstrate any activity on psychrotrophic microorganisms (p<0.05). According to the statistical analysis, acidified sodium chlorite, alkyl dimethyl benzyl ammonium chloride and peracetic acid reduced total coliform counts from 2.47 (untreated control) to 1.67 MPN/mL, 1.74 MPN/mL, 1.75 MPN/mL and (p<0.05), respectively. These products also reduced the contamination of carcasses with thermotolerant coliforms from 2.32 MPN/mL (control) to 1.49 MPN/mL, 1.53 MPN/mL and 1.61 MPN/mL (p<0.05), respectively.

Table 2
Average counts (log₁₀)of meat quality indicator microorganisms in broiler carcasses washed with different disinfectant compounds.

Disinfectant substances	Microbial group (log10)
	Mesophylls (CFU/mL)	Psycrotrophic bacteria (CFU/mL)	Total coliforms (MPN/mL)	Thermotolerant coliforms (MPN/mL)
Acidified sodium chlorite (50 ppm)	4.15a	4.43ab	1.67b	1.49b
Alkyl dimethyl benzyl ammonium chloride (175 ppm)	4.00a	4.20ab	1.75b	1.61b
Chlorine dioxide (5 ppm)	4.34a	4.55ab	2.08ab	2.02ab
Peracetic acid (50 ppm)	4.01a	4.01b	1.74b	1.53b
Sodium hypochlorite (5 ppm)	4.39a*	4.45ab	2.24ab	2.05ab
Group control	4.53a	4.73a	2.47a	2.32a

• * Means followed by the same letter in the same column do not differ by Turkey's test at significance level of 5% (p<0.05).

Peracetic acid showed the best results in reducing meat quality indicator microorganisms, whereas sodium hypochlorite and chlorine dioxide did not affect these populations when applied at the concentration allowed by Brazilian legislation (5 ppm).

The in-vitro assessment of the action of the tested compounds on SE Nal^rSpc^r is presented in Table 3. When compared with the PBS control group (T1),all tested disinfectants were efficient to reduce SE Nal^rSpc^r counts in the absence of organic matter(T2) (p<0.05), according to the European Committee for Standardization (CEN, 2009). Under the conditions of the present experiment, no SE Nal^rSpc^r was detected 5 and 25 minutes after disinfectant addition.

Table 3
Average Salmonella Enteritidis (SE Nal^rSpc^r) counts in the presence and absence of organic matter 5 and 25 minute after disinfectant addition.

Treatment*	Time
	5 minutes	25 minutes
Acidified sodium chlorite (50 ppm)
T1	7.08a	7.09a
T2	≤ 1.00b	≤ 1.00b
T3	7.11a	7.15a
T4	7.11a	6.98a
Alkyl dimethyl benzyl ammonium chloride (175 ppm)
T1	7.08a	7.10a
T2	≤ 1.00b	≤ 1.00b
T3	7.11a	7.14a
T4	6.98a	7.13a
Chlorine dioxide (5 ppm)
T1	7.22a	7.25a
T2	≤ 1.00b	≤ 1.00b
T3	7.18a	7.23a
T4	7.15a	7.21a
Peracetic acid (50 ppm)
T1	7.00a,**	7.03a
T2	≤ 1.00b	≤ 1.00b
T3	7.07a	7.42a
T4	7.14a	7.02a
Sodium hypochlorite (5 ppm)
T1	7.15a	7.18a
T2	≤ 1.00b	≤ 1.00b
T3	7.18a	7.20a
T4	7.16a	7.28a

• SE Nal^rSpc^r= Salmonella Enteritidis resistant to nalidixic acid and to spectinomycin; *Treatments are detailed in Table 1;**For each disinfectant solution, means followed by the same latter in the same column or row are not different by Turkey's test at 5% (p<0.05) significance level.

DISCUSSION

Microorganisms are considered good indicators of the hygienic conditions present during food manufacturing process (Hoffmann et al. 2004). For example, high coliform counts indicate post-processing contamination and/or unsuitable sanitization (Kottwitz et al. 2010). Salmonella spp., Escherichia coli and Staphylococcus aureus are examples of food-contaminating microorganisms that cause foodborne diseases in human beings. These bacteria are frequently found in contaminated chicken meat (Jakobsen et al. 2012; Kottwitz et al. 2010; Silva et al. 2010), and therefore, should be eliminated or, at least, reduced in broiler carcasses.

The addition of disinfectants in pre-chilling tanks is an important tool to minimize the presence of microorganisms in chicken carcasses during processing. The addition of peracetic acid and many other chemical compounds in pre-chilling tanks is allowed in the United States of America (USA, 1977). On the other hand, the Brazilian legislation only allows the use of chlorine-based compounds at a maximum concentration of 5 ppm (Brazil, 1998). Therefore, studies assessing the efficacy of other disinfectants added in pre-chilling tanks may encourage Brazilian public health authorities to review the current legislation. According to Voidarou et al. (2007), the pre-chilling step itself without any disinfectant has little effect on reducing microorganisms in broiler carcasses.

In the present study, sodium hypochlorite and chlorine dioxide did not show any effect on the evaluated meat quality indicator microorganisms. These results are consistent with the findings of Lopes et al. (2007), who did not observe any effect of those compounds in broiler carcass bacterial counts when added to pre-chilling tanks in processing plants. On the other hand, another study reported 1.5% and 70% reduction of coliform and Campylobacter spp. populations, respectively, using sodium hypochlorite and chlorine dioxide (Kameyama et al., 2012). However, in this study, sodium hypochlorite was added at 10 ppm and chlorine dioxide at 50 ppm (USA, 1977), which are higher than the 5 ppm currently allowed in the Brazilian legislation. Bashor et al. (2004) also reported that addition of chlorine at 25 to 35 ppm reduced Campylobacter spp. populations in broiler carcasses in 0.5 log CFU/mL of washing solution. Therefore, it is clear that the current Brazilian legislation regarding the use of sodium hypochlorite in pre-chilling tanks needs to be reviewed.

Russell & Axtell (2005) reported that utilization of sodium hypochlorite at 50 ppm in pre-chilling tanks reduced carcass contamination by Salmonella spp. and Pseudomonas fluorencens, but it was not successful in reducing Escherichia coli. In an trial carried out by Mergonsi et al. (2007), the addition of chlorine to a pre-chilling tank, where organic matter was present, did not reduce the number of carcasses contaminated with Salmonella spp. Consistent results were obtained in the present experiment, where no effect of the evaluated disinfectants on Salmonella Enteritidis counts in the presence of organic matter was detected.

The results of the present study showed that peracetic acid at 50 ppm, acidified sodium chlorite at 50 ppm and alkyl dimethyl benzyl ammonium chloride at 175 ppm decreased thermotolerant coliform counts. However, Mead et al. (2000) reported that the addition of chlorine at 50 ppm during the pre-chilling stage did not prevent cross-contamination of carcasses by Escherichia coli. Buhr et al. (2005) also showed that the addition of chlorine at 20 ppm in pre-chilling tanks reduced the counts of coliforms, total aerobes, Escherichia coli and Campylobacter spp. in broiler carcasses, but did the number of carcasses positive for Salmonella spp was not decreased.

In the present study, acidified sodium chlorite decreased the population of coliforms. Oyarzabal et al. (2004) and Sexton et al. (2007), using that disinfectant in pre-chilling tanks also reported a reduction in Escherichia coli and Salmonella spp. counts in broiler carcasses. In contrast, in our study, this compound did not reduce Salmonella Enteritidis counts in the presence of organic matter. It should be noted, however, that Oyarzabal et al. (2004) and Sexton et al. (2007) applied different methods to assess disinfectant action, which could explain the divergent results.

Li et al. (2002) evaluated the action of a chorine solution (50 ppm) spray on broiler carcasses and reported positive results in terms of bacterial count reduction. In the present study, acidified sodium chlorite showed better bacterial effect than other tested chlorine-based compounds (sodium hypochlorite and chlorine dioxide). The lower pH and the higher concentration (50 ppm) of sodium chlorite applied may have contributed for this result.

In agreement with the report of Bauermeister et al. (2008), in the present study, peracetic acid was more effective in reducing microbial counts than chlorine-based compounds. The weaker microbicidal effect of chlorine may be explained by the fact that it is easily neutralized by organic compounds (Northcutt & Lacy, 2000).

Kich et al. (2004) observed that sodium hypochlorite (1,000 ppm), quaternary ammonium (400 ppm), and peracetic acid (53.33 ppm) were all able to reduce Salmonella Typhimurium in the absence of organic matter. These authors also reported that, in the presence of organic matter, only peracetic acid reduced the counts of this pathogen. In the present study, none of the disinfectant tested, including peracetic acid, reduced Salmonella Enteritidis counts in the presence organic matter. Differences in amounts of organic matter and disinfectant concentrations could explain the differences between our results and those described by Kich et al. (2004).

According to Sidhu et al. (2002), the inefficiency of quaternary ammonium solutions against mesophyll and psychrotrophic present in products of animal origin could be a result of resistance induced by the wide utilization of such substance as disinfectant in animal production facilities. For instance, all Pseudomonas aeruginosa strains isolated of food of animal origin were resistant to that compound (Langsrud & Sundhein, 1997). In the present study, the ineffectiveness of alkyl dimethyl benzyl ammonium chloride in reducing mesophyll and psychrotrophic microorganisms could be also a result of neutralization by organic matter.

Taking into account the antagonist effect of organic matter on disinfectant activity, as demonstrated here and previously by other authors (Kich et al. 2004; Lopes et al. 2007), it is clear that the cleaning of pre-chilling tanks is essential to enhance disinfectant efficiency against contaminating bacteria. Chlorine-based compounds, when applied at the concentration permitted by the Brazilian legislation, did not reduce the counts of meat quality indicator microorganisms nor of Salmonella Enteritidis. In the present study, acidified sodium chlorine, alkyl dimethyl benzyl ammonium chloride, and peracetic acid at 175, 50 and 50 ppm, respectively, were able to reduce total and thermotolerant coliform counts. In terms of microbial control, those three compounds presented better results than sodium hypochloriteat 5 ppm typically applied in Brazilian poultry processing plants.

ACKNOWLEDGMENTS

We are grateful to biologist Bruna da Silva Moura for dedicated laboratorial assistance and to the entire group of the laboratory of Food Microbiology placed at the Preventive Veterinary Medicine department from FCAV/UNESP under responsibility of Prof. Dr. Oswaldo Durival Rossi Jr. We also thank to the Coordination of Improvement of Higher Education Personnel (CAPES) and The National Program of Academic Cooperation (PROCAD/CNPq, number: 88881.068412/2014-01) for the scholarships granted to perform this study.

REFERENCES

• Bashor MP, Curtis PA, Keener KM, Sheldon BW, Kathariou S, Osborne JA. Effects of carcass washers on Campylobacter contamination in large broiler processing plants. Poultry Science 2004;83(7):1232-1239.
• Bauermeister LJ, Bowers JWJ, Townsend JC, McKee SR. Validating the efficacy of peracetic acid mixture as an antimicrobial in poultry chillers. Journal of Food Protection 2008;71(6):1119-1122.
• Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Portaria n° 210, de 10 de novembro de 1998. Aprova o Regulamento técnico da inspeção tecnológica e higiênico-sanitária de carne de aves. Diário Oficial [da] República Federativa do Brasil. Brasília, DF, 26 nov. 1998. Seção 1, p. 226.
• Brasil. Ministério da Saúde. Agência Nacional de Vigilância Sanitária. Resolução RDC n.12, de 2 de janeiro de 2001. Regulamento técnico sobre os padrões microbiológicos para alimentos. 2001. [cited 2014 Dec 23]. Available from: http://e-legis.anvisa.gov.br/leisref/public/showAct.php?id=144
  » http://e-legis.anvisa.gov.br/leisref/public/showAct.php?id=144
• Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Análise epidemiológica dos surtos de doenças transmitidas por alimentos no Brasil. 2013 [cited 2014 Oct 21]. Available from: http://foodsafetybrazil.com/surtos-alimentares-no-brasil-dados-atualizados-em-2013/
  » http://foodsafetybrazil.com/surtos-alimentares-no-brasil-dados-atualizados-em-2013/
• Buhr RJ, Bourassa DV, Northcutt JK, Hinton Junior, A, Ingram KD, Cason JA. Bacteria recovery from genetically feathered and featherless broiler carcasses after immersion chilling. Poultry Science 2005;84(9):1499-1504.
• Busch F, Burwell SR, O'Reilly M. Antimicrobial compositions and methods of use thereof. United States Patent Application Publication US 2013/0137732 A1. 2013 May 30.
• CEN - European Committee for Standardization. Chemical disinfectants and antiseptics - Quantitative suspension test for the evaluation of bactericidal activity of chemical disinfectants and antiseptics used in food, industrial, domestic, and institutional areas - tests methods and requirements (phase 2/ step 1) (EN 1276). London: British Standard Publications; 2009.
• Crim SM, Iwamoto M, Huang JY, Griffin PM, Gilliss D, Cronquist AB, et al. Incidence and trends of infection with pathogens transmitted commonly through food - foodborne diseases active surveillance network, 10 U.S. Sites, 2006-2013. Morbidity and Mortality Weekly Report 2014;63 (15):328-332.
• Downes FP, Ito K. Compendium of methods for the microbiological examination of foods. Washington: American Public Health Association; 2001.
• Espigares E, Bueno A, Fernández-Crehuet M, Espigares M. Efficacy of some neutralizers in suspension tests determining the activity of disinfectants. The Journal of Hospital Infection 2003;55(2):137-140.
• HACCP. HACCP in microbiological safety and quality, microorganisms in foods. Oxford: Blackwell Scientific; 1995.
• Hoffmann FL, Gonçalves TMV, Coelho AR, Hirooka EY, Hoffmann P. Qualidade microbiologia de queijos ralados de diversas marcas comerciais, obtidos do comércio varejista do município de São José do Rio Preto, SP. Higiene Alimentar 2004;(122):62-66.
• Hoskins JK. Most probable numbers for evaluation of coli aerogenes test by fermentation tube method. Public Health Reports 1934;49(12):393-405.
• Jakobsen L, Garneau P, Bruant G, Harel J, Olsen SS, Porsbo LJ, et al. Is Escherichia coli urinary tract infection a zoonosis? Proof of direct link with production animals and meat. European Journal of Clinical Microbiology & Infectious Diseases 2012;31(6):1121-1129.
• Kameyama M, Chuma T, Nishimoto T, Oniki H, Yanagitani Y, Kanetou R, et al. Effect of cooled and chlorinated chiller water on Campylobacter and coliform counts on broiler carcasses during chilling at a middle-size poultry processing plant. The Journal of Veterinary Medical Science 2012;74(1):129-133.
• Kich JD, Borowsky LM, Silva VS, Ramenzoni M, Trinques N, Kooler FL, et al. Avaliação da atividade antimicrobiana de seis desinfetantes comerciais frente a amostras de Salmonella Typhimurium isoladas de suínos. Acta Scientiae Veterinariae 2004;32(1):33-39.
• Kottwitz LBM, Oliveira TCRM, Alcocer I, Farah SMSS, Abrahão WSM, Rodrigues DP. Avaliação epidemiológica de salmonelose ocorridos no período de 1999 a 2008 no estado do Paraná, Brasil. Acta Scientiarum Health Sciences 2010;32(1):9-15.
• Langsrud S, Sundheim G. Factors contributing to the survival of poultry associated Pseudomonas spp. exposed to a quaternary ammonium compound. Journal of Applied Microbiology 1997;82(6):705-712.
• Li Y, Yang H, Swem BL. Effect of high-temperature inside-outside spray on survival of Campylobacter jejuni attached to prechill chicken carcasses. Poultry Science 2002;81(9):1371-1377.
• Lillard HS. Factors affecting the persistence of Salmonella during the processing of poultry. Journal of Food Protection 1989;52:829-832.
• Lopes M, Galhardo JA, Oliveira JT, Tamanini R, Sanches SF, Muller EE. Pesquisa de Salmonella spp. e microrganismos indicadores em carcaças de frango e água de tanques de pré-resfriamento em abatedouro de aves. Semina: Ciências Agrárias 2007;28(3):465-476.
• Mead GC, Allen VM, Burton CH, Corry JE. Microbial cross-contamination during air chilling of poultry. British Poultry Science 2000;41(2):158-162.
• Mergonsi C, Bergonsi C, Bastos JRH, Moraes, HLS, Rocha SLS, Giotto DB. Eficácia do resfriamento na redução de enterobactérias, coliformes e Salmonellasp. em carcaças de frango resfriadas. Anais do 19º Salão de Iniciação Científica; 2007; Porto Alegre, Rio Grande do Sul. Brasil. p. 130.
• Northcutt JK, Lacy MP. Odor problems associated with chlorineus age in poultry processing plants [abstr.]. Poultry Science 2000;78(Suppl. 1):47.
• Oyarzabal OA, Hawk C, Bilgili SF, Warf CC, Kemp GK. Effects of postchill application of acidified sodium chlorite to control Campylobacter spp. and Escherichia coli on commercial broiler carcasses. Journal of Food Protection 2004;67(10):2288-2291.
• Rasschaert G, Houf K, Godard C, Wildemauwe C, Pastuszczak-Frak M, De Zutter L. Contamination of carcasses with Salmonella during poultry slaughter. Journal of Food Protection 2008;71(1):146-152.
• Russell SM, Axtell SP. Monochloramine versus sodium hypochlorite as antimicrobial agents for reducing populations of bacteria on broiler chicken carcasses. Journal of Food Protection 2005;68(4):758-763.
• Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States - major pathogens. Emerging Infectious Diseases 2011;17(1):7-15.
• Sexton M, Raven G, Holds G, Pointon A, Kiermeier, A, Sumner J. Effect of acidified sodium chlorite treatment on chicken carcasses processed in South Australia. International Journal of Food Microbiology 2007;115(2):252-255.
• Sidhu MS, Sorum H, Holck A. Resistence to quaternary ammonium compounds in food-related bacteria. Microbial Drug Resistance 2002;8(4):393-398.
• Silva EP, Bergamini AMM, Oliveira MA. Alimentos e agentes etiológicos envolvidos em toxinfecções na região de Ribeirão Preto, SP, Brasil - 2005 a 2008. Boletim Epidemiológico Paulista 2010;7(77):4-10.
• Silva MP, Cavalli DR, Oliveira TCRM. Avaliação do padrão de coliformes a 45 ºC e comparação da eficiência das técnicas dos tubos múltiplos e Petrifilm EC na detecção de coliformes totais e Escherichiacoli em alimentos. Ciência e Tecnologia de Alimentos 2006;26(2):352-359.
• Silva N, Junqueira VCA, Silveira NFA, Taniwaki MH, Santos RFS, Gomes RAR. Manual de métodos de análise microbiológica de alimentos. 3ª ed. São Paulo: Livraria Varela; 2007.
• USA. USDHHS - United States Department of Health and Human Service. Code of Federal Regulations n°173. Secondary direct food additives permitted in food for human consumption - specific usage additives (Subpart D). 1997 [cited 2014 Jan 11]. Available from: http://www.accessdata.fda.gov/SCRIPTs/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=173
  » http://www.accessdata.fda.gov/SCRIPTs/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=173
• USDA. Food safety and Inspetion Service .Prevalence of Salmonella on young chicken carcasses in the U.S.: 1999-2000. 2002 [cited 2014 Dec 9]. Available from: http://www.fsis.usda.gov/OA/speeches/2002/IAFP_poster/iafp.pdf
  » http://www.fsis.usda.gov/OA/speeches/2002/IAFP_poster/iafp.pdf
• Voidarou C, Vassos D, Kegos T, Koutsotoli A, Tsiotsias A, Skoufos J, et al. Aerobic and anaerobic microbiology of the immersion chilling procedure during poultry processing. Poultry Science 2007;86(6):1218-1222.

Publication Dates

• Publication in this collection
  Apr-Jun 2016

History

• Received
  June 2015
• Accepted
  Oct 2015