J. Appl. Poult. Res.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J APPL POULT RES 2009. 18:379-388. doi:10.3382/japr.2008-00140
© 2009 Poultry Science Association
This Article
Right arrow Summary Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sirsat, S. A.
Right arrow Articles by Ricke, S. C.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Sirsat, S. A.
Right arrow Articles by Ricke, S. C.

Current and Future Prospects for Natural and Organic Poultry Symposium

Antimicrobials for foodborne pathogen reduction in organic and natural poultry production1

S. A. Sirsat*, A. Muthaiyan{dagger} and S. C. Ricke*,{dagger},2

* University of Arkansas, Department of Poultry Science, Fayetteville, AR 72701; and {dagger} University of Arkansas, Center for Food Safety-IFSE and Department of Food Science, Fayetteville, AR 72704

2 Corresponding author: sricke{at}uark.edu


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 ORGANIC CHEMICAL ANTIMICROBIALS
 BIOLOGICAL METHODS
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Antimicrobials currently used in the conventional poultry industry include physical, chemical, and biological hurdles. However, there is a need for natural and organic antimicrobials to make the food safe and to retain its natural taste and texture. Potential natural or organic antimicrobials include bacteriophages, bacteriocins, antibody therapy, vaccination, and the use of natural plant compounds such as essential oils. Genomic methods applied to Salmonella responses to multiple interventions may offer opportunities to optimize combinations that are the most effective.

Key Words: biological antimicrobial • poultry • microarray • multiple hurdle


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
ORGANIC CHEMICAL ANTIMICROBIALS
 BIOLOGICAL METHODS
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Pathogenic contamination of foods is a threat to human health and has the potential to produce fatalities. Foodborne pathogens cause approximately 76 million illnesses, 325,000 hospitalizations, and 5,000 deaths in the United States each year [1]. Several antimicrobial treatments have been used in the food industry to decontaminate food, destroy disease-causing pathogens, and preserve food. These treatments can be classified as physical, chemical, or biological [2]. However, some of these agents may cause surviving pathogens to become more resistant to other treatments. Hence, strategies need to be devised to prevent any form of cross-protection that may occur because of the use of a combination of these antibacterial agents.

Additive-free, natural-tasting, microbiologically safe, and organic foods have been promoted to meet today’s consumer demand [3]. In addition, organic labels are becoming particularly attractive to the consumer because they represent natural and preservative-free forms of consumables. The USDA National Organic Program is responsible for the administration, handling, and labeling of organic agricultural products, and these products carry a USDA organic seal. The use of chemical preservatives has increased consumer concern, leading to a desire for more natural and minimally processed foods [4].

According to the USDA-Food Safety and Investigation Services regulation §205.270 titled "Organic Handling Requirements," mechanical and biological methods include, but are not limited to, the following: "cooking, baking, curing, heating, drying, mixing, grinding, churning, separating, distilling, extracting, slaughtering, cutting, fermenting, eviscerating, preserving, dehydrating, freezing, chilling, or otherwise manufacturing, and the packaging, canning, jarring, or otherwise enclosing food in a container may be used to process an organically produced agricultural product for the purpose of retarding spoilage or otherwise preparing the agricultural product for market" [5].

A list of natural and organic methods to treat food surfaces and examples of various studies are detailed in Tables 1Go and 2Go. Physical methods include exposure to heat and cold. As the temperature of a food product is reduced, so is the growth rate of the microorganisms. However, some bacteria, such as Listeria monocytogenes and Yersinia enterocolitica, can survive at 1°C. Heat has also been used in the form of pasteurization at various times and temperatures to inactivate certain microorganisms. Sterilization techniques are usually used to inactivate bacterial spores. Heat is considered one of the most efficient methods for inactivating microorganisms in foods [6].


View this table:
[in this window]
[in a new window]

  		Table 1. Antimicrobial treatment methods
 

View this table:
[in this window]
[in a new window]

  		Table 2. Physical and chemical hurdle treatments and their effect on pathogens
 

   ORGANIC CHEMICAL ANTIMICROBIALS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 ORGANIC CHEMICAL ANTIMICROBIALS
BIOLOGICAL METHODS
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Organic Acids
An organic acid is an organic compound that has acidic properties. These compounds contain the carboxylic group –C–(O)–OH and are formed by the oxidation of aldehydes. Chemical rinses using organic acids that are Generally Recognized as Safe are most commonly used in the meat industry to rinse animal carcasses. Acetic, lactic, and citric acids at concentrations of 1.5 to 2.5% are used in sprays for carcass decontamination [7]. These acids reduce the pH of the food and hence control the growth of microorganisms. In a low-pH environment, the membrane of the bacteria is saturated with hydrogen ions, which affects the permeability of the cell and eventually affects the ability of bacteria to reproduce [8]. Lactic acid is most effective when applied at higher temperatures and at a concentration of 2 to 4%. However, there have been some concerns in the food industry about potentially increasing numbers of acid-resistant bacteria because of the use of organic acids, as well as the disposal of the wastewater for environmental reasons [8–10].

Essential Oils
Unlike antibiotics, some natural antimicrobials can act on several targets at one time, making it extremely rare for resistance to develop [11]. Natural compounds such as essential oils (EO) have been studied for several years and are known for their antimicrobial properties. Based on disk diffusion assays and estimations of minimum inhibition concentrations, O’Bryan et al. [12] reported various citrus orange-based oils to be effective against 11 Salmonella strains. This study opened the possibility of using these natural compounds in the food industry after slaughter to inhibit Salmonella. Firouzi et al. [13] tested the EO from oregano and nutmeg on the survival of Y. enterocolitica and L. monocytogenes in a broth system and on barbecued chicken. In the broth system, they found that the nutmeg EO exhibited a greater effect on L. monocytogenes than the oregano EO and that the oregano EO had a greater effect on Y. enterocolitica than the nutmeg EO. However, the authors did not find a significant decrease in pathogen counts when barbecued chicken inoculated with the bacteria was treated with these EO. Burt [14] presented an extended review of EO and their uses in the food and meat industry.


   BIOLOGICAL METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 ORGANIC CHEMICAL ANTIMICROBIALS
 BIOLOGICAL METHODS
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Biological antimicrobial methods fall under the category of natural antimicrobials because they are found readily in the environment. In foods, these compounds may be present in the original food matrix or may be added as an external amendment. Biological agents include bacteriophages and bacteriocins, which possess an inherent ability to destroy specific microorganisms. Bacteriophages are ubiquitous in a variety of environments, and bacteriocins are produced by certain bacteria that act against other closely related bacteria. These biological compounds can be used in the food industry at the pre- and postslaughter processing phases to prevent bacterial contamination on the food matrix.

Bacteriophages
Bacteriophages, commonly called phages, are viruses that have the ability to infect and kill bacteria. They have been considered as possible biological alternatives to antimicrobials that are used in the food industry to decontaminate the surfaces of consumables [15]. Bacteriophages contain a protein coat that may enclose either RNA or DNA as its nucleic acid. There are 2 types of phages: virulent or lytic, and temperate or lysogenic. The life cycle of the lytic bacteriophages has been diagrammed in Figure 1Go. Virulent phages lyse bacterial cells by disrupting bacterial metabolism and leading to breakage of the cell wall, and hence cell death. The phage attaches to the cell wall of the bacteria and injects its genetic material, which eventually replicates, leading to cell lysis and release of the daughter phages in a repetitive cycle. In contrast, injection of nucleic acid of the lysogenic phage into the host bacterium leads to integration of its genetic material with that of the host.


Figure 1
View larger version (32K):
[in this window]
[in a new window]

  		Figure 1. The lytic life cycle of a bacteriophage.

 
The most intriguing feature of phages for application as antimicrobials is that they are not infective to animals and plant cells and thus could be used as antimicrobials on food because they do not cause harm to the food or consumer. These are especially advantageous compared with chemicals, which may potentially leave a residue on the food matrix. Because bacteriophages are specific to certain pathogens, the phage can be chosen depending on the food and stage in which it is being processed. For instance, a phage specific to Salmonella may be used on raw poultry, and a Listeria-specific phage may be used on ready-to-eat foods [16]. This specificity has its advantages because it may decrease the chances of acquiring and spreading resistance against different pathogens, such as is the case for broader spectrum sanitizer antimicrobials. In addition, these pathogen-specific phages could be applied to fermented meat products that contain live starter cultures because they would not destroy the beneficial bacteria. Escherichia coli phages have been isolated from a variety of food sources, such as fresh poultry, pork, beef, and vegetables, and Campylobacter phages have been isolated in high numbers from chicken [17, 18].

Several studies have been performed to test the effectiveness of phage application for foods. Phages have been used to reduce Salmonella from poultry carcasses [19, 20]. Goode et al. [21] reported that phages could control Salmonella Enteritidis inoculated on chicken skin at 1 log cfu/cm2. Phages have also been used in the preslaughter steps to reduce bacterial contamination. When Sklar and Joerger [22] inoculated young chickens with a bacteriophage capable of lysing a nalidixic acid-resistant Salmonella strain, they reported that the birds treated with the phage exhibited 0.3 to 1.3 times lower Salmonella numbers in the cecal contents compared with the control. Atterbury et al. [23] observed a significant reduction in Campylobacter in broiler chickens exposed to bacteriophages. Likewise, Wagenaar et al. [24] reported that Campylobacter-specific lytic phages reduced colonization 10-fold compared with control birds, but after an initial reduction in the bacterial numbers of the treatment group, the bacterial levels stabilized to levels of the untreated control birds. Fiorentin et al. [25] administered an oral dose of phages in broiler chickens and reported a significant reduction in Salmonella numbers in chickens that were given the dose of phages as compared with the control group.

Disadvantages of phages include a limited host range, the requirement of a certain threshold of bacteria, and possible resistance [26]. For instance, one of the several methods by which Salmonella serotypes are classified is based on the identity of the specific phage that infects the bacteria and is referred to as phage typing [27]. Hence, a single phage may not be able to target all strains of any single pathogen. This demands the use of several different phages because of their specificity to one particular pathogen. In addition, in some cases lysogenic phages may change the external membrane of the bacteria, making them more pathogenic or impervious to other phages [28]. In addition, just as pathogens become resistant to other antimicrobials, they can become resistant to phages. However, phages may also mutate and continue to infect the pathogen [29].

Bacteriocins
Bacteriocins are protein substances made by microorganisms to inhibit similar or closely related bacterial strains. One of the first bacteriocins to be characterized and studied extensively was colicin from E. coli [30]. Colicins are proteins secreted by E. coli that destroy closely related bacteria by inhibiting their cell wall synthesis or by inhibiting deoxyribonuclease or ribonuclease activity [4]. Bacteriocins such as colicin usually are high molecular weight proteins and enter the cell using specific cell-surface receptors. These protein molecules are responsible for killing bacterial cells by forming ion channels and inhibiting protein synthesis in the target cell [31]. Bacteriocins from gram-positive microorganisms, such as lactic acid bacteria, behave similarly but may have lower molecular weights.

Although lactic acid bacteria produce a variety of bacteriocins, nisin probably is the most common bacteriocin used as a food preservative because it has Generally Recognized as Safe status in the United States. When Mahadeo and Tatini [32] added nisin to the scalding water to treat any L. monocytogenes present in the water or on the surface of the turkey skin, a 1 log reduction of Listeria in the nisin-treated samples occurred and was followed by further reduction after refrigeration. Gram-negative bacteria such as Salmonella are less sensitive to nisin than are gram-positive bacteria. However, when used with EDTA or Tween 80, the activity of nisin against the pathogen can be increased. Natrajan and Sheldon [33] used nisin, EDTA, and Tween 80 on the surface of chickens that were experimentally inoculated with Salmonella and reported a reduction of 3 log10 after 72 h at 4°C. Other experiments from the same group showed an extension in the shelf life of drumsticks by 0.6 to 2.2 d when nisin-treated polyvinyl chloride overwrap was used on nisin tray pads [34].

Recently, the search for anti-Campylobacter bacteriocins has been successful. When Cole et al. [35] administered bacteriocins produced by Bacillus circulans and Paenibacillus polymyxa against Campylobacter coli, detectable Campylobacter numbers (less than 2 log Campylobacter/g of cecal contents) were eliminated when compared with control birds, which still exhibited 6 log Campylobacter/g of cecal contents. Stern et al. [36] further tested the bacteriocin secreted by P. polymyxa NRRL-B-30509 as a feed amendment and reported a significant reduction of Campylobacter jejuni numbers in the fecal matter of chickens treated with a bacteriocin as compared with the control set. When a bacteriocin from Lactobacillus salivarius NRRL B-30514 was fed to 7-d-old birds for 3 d, significant reductions (1 million-fold) of C. jejuni occurred compared with control birds when both groups were killed on d 10 [37].

Ideally, bacteriocins with a broader range of activity are needed. Liu et al. [38] isolated a Lactobacillus strain from a traditional Chinese fermented ham that produced a bacteriocin called pentocin 31-3. This bacteriocin displayed a wide range of antimicrobial activity against Listeria, Staphylococcus, Bacillus, Lactobacillus, Streptococcus, Pediococcus, and Escherichia spp. and could potentially be used as a broad-spectrum natural antimicrobial on poultry surfaces.

It is possible that target bacterial cells could develop resistance toward the bacteriocins by altering their cell surface receptors. The mechanism of action for this resistance of bacteria toward the bacteriocin is not very clear. Typically, the bacteriocins interact with the cell membrane of the bacteria; hence, resistance occurs because of changes in the cell membrane of the bacteria such that the bacteria can no longer attach and penetrate the cell [39, 40]. This issue could potentially be overcome by using bacteriocins in combination with other antimicrobial compounds, leading to synergy between the treatments and more effective elimination of the pathogen. This is especially the case when the treatments are independent in the manner in which they destroy the pathogen. For instance, Zhang and Mustapha [41] demonstrated that nisin, when used in combination with a chelator such as EDTA, could limit the growth of E. coli. In this case, EDTA disrupted the outer membrane of the pathogen and nisin entered the cell, leading to cell destruction.

Antibody Therapy and Vaccination
Addition of Salmonella-specific antibodies to feed such as corn and soybean meal to limit its colonization in poultry has been proposed [42]. This would enable a young bird or a susceptible older bird to resist colonization by foodborne pathogens preemptively because of the presence in the gut of antibodies that are specific for particular pathogens. This concept and potential implementation strategies are discussed more extensively by Berghman et al. [42].

Vaccine therapy involves the external activation of the bird’s own immune system to limit pathogen colonization. Birds are exposed to vaccines specific for certain microorganisms, leading to the development of specific antibodies to target these pathogens for an immune response. Two types of vaccines can be developed to immunize birds against the pathogen. One approach uses inactivated or killed bacterial cells and the other uses a live attenuated bacterial strain. Live vaccines have been shown to be more effective in causing immunity than killed or inactivated vaccines [43]. For instance, House et al. [44] developed live vaccines against Salmonella strains to be used in dairy cattle and swine and noted that animals treated with the vaccine exhibited decreased Salmonella shedding. Similarly, hens that were exposed to Salmonella displayed an increase in IgA, IgG, and IgM antibodies when compared with uninfected control hens [45]. Several commercially developed vaccines have already been used in production facilities [46]. In chickens, the vaccines are often enhanced by addition of an adjuvant to improve the immune response [43].

In some cases, specific proteins of pathogens may be used as vaccines. For instance, De Buck et al. [47] injected purified type I Salmonella Enteritidis fimbriae and detected IgG and IgA antibodies in the eggs and sera of the immunized chickens, along with higher Salmonella Enteritidis levels in the control hen group exposed to the fimbriae protein. Likewise, when Khoury and Meinersmann [48] produced an engineered vaccine consisting of C. jejuni flagellin fused to the β-subunit of the labile toxin of E. coli and then tested the efficacy of this hybrid protein as a chicken vaccine, they observed lower pathogen counts in vaccinated birds as compared with control birds.

Although vaccination has proved effective in commercial applications, disadvantages and drawbacks do exist. For example, Salmonella can survive in hosts that have developed an antigenic response to the bacteria. In addition, vaccines can be extremely specific to a particular bacterium and hence may not be effective against a diverse set of pathogens. For Salmonella, this could be particularly problematic, given the wide range of immunogenic serotypes.

Using Bacterial Genomics to Optimize Multiple-Hurdle Antimicrobial Technology for Natural and Organic Poultry
A hurdle is any treatment (physical, chemical, or biological) that is used to limit or eliminate the presence of pathogens on a food surface [49, 50]. These treatments pose "hurdles" to bacterial colonization and growth, hence the name. The application of more than one hurdle at a time is advantageous because this may decrease the requirement for exposures to or higher concentrations of the specific hurdle [51]. For instance, a 2% lactic acid treatment is commonly used on meat surfaces. However, if the lactic acid is combined with another intervention, a lower concentration may be used and may result in more effective elimination of pathogens. The use of these hurdles in combination is termed multiple-hurdle technology. However, in some cases, the treatments used in combination may tend to cross-protect. Cross-protection is a phenomenon in which the first treatment may render the surviving pathogens more resistant toward incoming treatments. For example, Kwon et al. [52] reported that Salmonella Typhimurium that had adapted to short-chain fatty acids at neutral pH also became more resistant to extreme conditions such as high pH, high osmolarity, and reactive oxygen.

Whole-bacterial genome microarrays can potentially be used to test the effect of these antimicrobials to identify all possible genetic responses of various pathogens. This would enable researchers to determine which genes are repressed or induced as a result of these hurdles on the bacteria. The genomic profile of the bacteria can subsequently be compared across different stress conditions. The hurdles with a maximum number of genes affected in common may potentially cross-protect against each other and hence should not be used in combination or in sequence. Combinations of treatments with fewer genes in common are preferred because this means that the 2 treatments target separate loci on the genome and hence are less likely to display cross-protection. A representation of this method has been diagrammed in Figure 2Go. The test and control sample of the bacteria are subjected to RNA extraction, followed by reverse transcription to generate cDNA labeled with fluorescent dyes. This labeled cDNA is allowed to hybridize to a microarray slide representing the entire genome of the pathogen. The slide is then scanned and the genes that are induced or repressed are analyzed using statistical methods to sort out true gene responses. As microarray analyses become more common, profiling intervention responses to differentiate optimal combinations will enhance the effective and economical application of hurdle technologies.


Figure 2
View larger version (17K):
[in this window]
[in a new window]

  		Figure 2. Flow chart representation of the use of whole-genome microarrays to test the effect on antimicrobials on the pathogen genome. Cy = cyanine.

 

   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 ORGANIC CHEMICAL ANTIMICROBIALS
 BIOLOGICAL METHODS
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 
  1. Historically, a variety of antimicrobials have been used in the poultry industry. However, recent demands for organic and natural poultry have increased the need for specific antimicrobials that fulfill the criteria for this type of production.
  2. Biological agents that have potential include bacteriophages, bacteriocins, and antibodies, which may be too specific in some cases.
  3. Combinations of biological agents to set up multiple hurdles may offer sufficient synergism to reduce the dose or exposure time for individual compounds.
  4. Optimizing multiple-hurdle approaches will require genomic screening to minimize cross-protection.


   ACKNOWLEDGMENTS
 
This review was supported by USDA National Integrated Food Safety Grant number 2008-51110-04339 and a USDA Food Safety Consortium Grant.


   FOOTNOTES
 
1 Papers from the Current and Future Prospects for Natural and Organic Poultry Symposium were presented at the Poultry Science Association’s 97th Annual Meeting in Niagara Falls, Ontario, Canada. Back


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 ORGANIC CHEMICAL ANTIMICROBIALS
 BIOLOGICAL METHODS
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

  1. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607–625.[Web of Science][Medline]
  2. Ricke, S. C., M. M. Kundinger, D. R. Miller, and J. T. Keeton. 2005. Alternatives to antibiotics: Chemical and physical antimicrobial interventions and foodborne pathogen response. Poult. Sci. 84:667–675.[Abstract/Free Full Text]
  3. Gould, G. W. 1996. Industry perspectives on the use of natural antimicrobials and inhibitors for food applications. J. Food Prot. (Suppl.):82–86.
  4. Cleveland, J., T. J. Montville, I. F. Nes, and M. L. Chikindas. 2001. Bacteriocins: Safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71:1–20.[CrossRef][Web of Science][Medline]
  5. USDA-Food Safety and Inspection Service. 2008. Agricultural Marketing Service, USDA. http://edocket.access.gpo.gov/cfr_2008/janqtr/pdf/7cfr205.270.pdf Accessed Feb. 2009.
  6. Gould, G. W. 2000. Preservation: Past, present and future. Br. Med. Bull. 56:84–96.[Abstract/Free Full Text]
  7. USDA-Food Safety and Inspection Service. 1996. The final rule on pathogen reduction and Hazard Analysis and Critical Control Point (HACCP) systems. http://www.fsis.usda.gov/oa/background/finalrul.htm#PERFORMANCE%20STANDARDS Accessed Feb. 2009.
  8. Ricke, S. C. 2003. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult. Sci. 82:632–639.[Abstract/Free Full Text]
  9. Dickens, J. A., B. G. Lyon, A. D. Whittemore, and C. E. Lyon. 1994. The effect of an acetic acid dip on carcass appearance, microbiological quality, and cooked breast meat texture and flavor. Poult. Sci. 73:576–581.[Web of Science][Medline]
  10. Dickens, J. A., and A. D. Whittemore. 1994. The effect of acetic acid and air injection on appearance, moisture pick-up, microbiological quality, and Salmonella incidence on processed poultry carcasses. Poult. Sci. 73:582–586.[Web of Science][Medline]
  11. Sahl, H.-G., and G. Bierbaum. 2008. Multiple activities in natural antimicrobials. Microbe 3:467–473.
  12. O’Bryan, C. A., P. G. Crandall, V. I. Chalova, and S. C. Ricke. 2008. Orange essential oils antimicrobial activities against Salmonella spp. J. Food Sci. 73:M264–M267.[CrossRef][Web of Science][Medline]
  13. Firouzi, R., S. S. Shekarforoush, A. H. K. Nazer, Z. Borumand, and A. R. Jooyandeh. 2007. Effects of essential oils of oregano and nutmeg on growth and survival of Yersinia enterocolitica and Listeria monocytogenes in barbecued chicken. J. Food Prot. 70:2626–2630.[Web of Science][Medline]
  14. Burt, S. 2004. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 94:223–253.[CrossRef][Web of Science][Medline]
  15. Huff, W. E., G. R. Huff, N. C. Rath, J. M. Balog, and A. M. Donoghue. 2005. Alternatives to antibiotics: Utilization of bacteriophage to treat colibacillosis and prevent foodborne pathogens. Poult. Sci. 84:655–659.[Abstract/Free Full Text]
  16. Bassett, K. D. 2007. Use of bacteriophage as an antimicrobial in food products. Master’s Thesis. Kansas State Univ., Manhattan.
  17. Atterbury, R. J., P. L. Connerton, C. E. R. Dodd, C. E. D. Rees, and I. F. Connerton. 2003. Isolation and characterization of Campylobacter bacteriophages from retail poultry. Appl. Environ. Microbiol. 69:4511–4518.[Abstract/Free Full Text]
  18. Allwood, P. B., Y. S. Malik, S. Maherchandani, K. Vought, L. A. Johnson, C. Braymen, C. W. Hedberg, and S. M. Goyal. 2004. Occurrence of Escherichia coli, noroviruses, and F-specific coliphages in fresh market-ready produce. J. Food Prot. 67:2387–2390.[Web of Science][Medline]
  19. Higgins, J. P., S. E. Higgins, K. L. Guenther, W. Huff, A. M. Donoghue, D. J. Donoghue, and B. M. Hargis. 2005. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult. Sci. 84:1141–1145.[Abstract/Free Full Text]
  20. Joerger, R. D. 2003. Alternatives to antibiotics: Bacteriocins, antimicrobial peptides and bacteriophages. Poult. Sci. 82:640–647.[Abstract/Free Full Text]
  21. Goode, D., V. M. Allen, and P. A. Barrow. 2003. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 69:5032–5036.[Abstract/Free Full Text]
  22. Sklar, I. A. N. B., and R. D. Joerger. 2001. Attempts to utilize bacteriophage to combat Salmonella enterica serovar Enteritidis infection in chickens. J. Food Saf. 21:15–29.[CrossRef]
  23. Atterbury, R. J., E. Dillon, C. Swift, P. L. Connerton, J. A. Frost, C. E. R. Dodd, C. E. D. Rees, and I. F. Connerton. 2005. Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl. Environ. Microbiol. 71:4885–4887.[Abstract/Free Full Text]
  24. Wagenaar, J. A., M. A. P. V. Bergen, M. A. Mueller, T. M. Wassenaar, and R. M. Carlton. 2005. Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet. Microbiol. 109:275–283.[CrossRef][Web of Science][Medline]
  25. Fiorentin, L., N. D. Vieira, and W. Barioni. 2005. Oral treatment with bacteriophages reduces the concentration of Salmonella Enteritidis PT4 in caecal contents of broilers. Avian Pathol. 34:258–263.[CrossRef][Web of Science][Medline]
  26. Greer, G. G. 2005. Bacteriophage control of food-borne bacteria. J. Food Prot. 68:1102–1111.[Web of Science][Medline]
  27. Ward, L. R., J. D. de Sa, and B. Rowe. 1987. A phage-typing scheme for Salmonella enteritidis. Epidemiol. Infect. 99:291–294.[Medline]
  28. Canchaya, C., C. Proux, G. Fournous, A. Bruttin, and H. Brussow. 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67:238–276.[Abstract/Free Full Text]
  29. Sulakvelidze, A., Z. Alavidze, and J. G. Morris. 2001. Bacteriophage therapy. Antimicrob. Agents Chemother. 45:649–659.[Free Full Text]
  30. Lazdunski, C. J. 1988. Pore-forming colicins: Synthesis, extracellular release, mode of action, immunity. Bio-chimie 70:1291–1296.[CrossRef][Web of Science][Medline]
  31. Bruno, M. E., and T. J. Montville. 1993. Common mechanistic action of bacteriocins from lactic acid bacteria. Appl. Environ. Microbiol. 59:3003–3010.[Abstract/Free Full Text]
  32. Mahadeo, M., and S. R. Tatini. 1994. The potential use of nisin to control Listeria monocytogenes in poultry. Lett. Appl. Microbiol. 18:323–326.[CrossRef][Web of Science]
  33. Natrajan, N., and B. W. Sheldon. 2000. Efficacy of nisin-coated polymer films to inactivate Salmonella Typhimurium on fresh broiler skin. J. Food Prot. 63:1189–1196.[Web of Science][Medline]
  34. Natrajan, N., and B. W. Sheldon. 2000. Inhibition of Salmonella on poultry skin using protein and polysaccharide-based films containing a nisin formulation. J. Food Prot. 63:1268–1272.[Web of Science][Medline]
  35. Cole, K., M. B. Farnell, A. M. Donoghue, N. J. Stern, E. A. Svetoch, B. N. Eruslanov, L. I. Volodina, Y. N. Kovalev, V. V. Perelygin, and E. V. Mitsevich. 2006. Bacteriocins reduce Campylobacter colonization and alter gut morphology in turkey poults. Poult. Sci. 85:1570–1575.[Abstract/Free Full Text]
  36. Stern, N. J., E. A. Svetoch, B. V. Eruslanov, Y. N. Kovalev, L. I. Volodina, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, and V. P. Levchuk. 2005. Research note: Paenibacillus polymyxa purified bacteriocin to control Campylobacter jejuni in chickens. J. Food Prot. 68:1450–1453.[Web of Science][Medline]
  37. Stern, N. J., E. A. Svetoch, B. V. Eruslanov, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, V. D. Pokhilenko, V. P. Levchuk, O. E. Svetoch, and B. S. Seal. 2006. Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob. Agents Chemother. 50:3111–3116.[Abstract/Free Full Text]
  38. Liu, G., Y. Lv, P. Li, K. Zhou, and J. Zhang. 2008. Pentocin 31-1, an anti-Listeria bacteriocin produced by Lactobacillus pentosus 31-1 isolated from Xuan-Wei Ham, a traditional China fermented meat product. Food Control 19:353–359.[CrossRef][Web of Science]
  39. Ming, X., and M. A. Daeschel. 1993. Nisin resistance of foodborne bacteria and the specific resistance responses of Listeria monocytogenes Scott A. J. Food Prot. 56:944–948.[Web of Science]
  40. Mazzotta, A. S., A. D. Crandall, and T. J. Montville. 1997. Nisin resistance in Clostridium botulinum spores and vegetative cells. Appl. Environ. Microbiol. 63:2654–2659.[Abstract/Free Full Text]
  41. Zhang, S., and A. Mustapha. 1999. Reduction of Listeria monocytogenes and Escherichia coli O157:H7 numbers on vacuum-packaged fresh beef treated with nisin or nisin combined with EDTA. J. Food Prot. 62:1123–1127.[Web of Science][Medline]
  42. Berghman, L. R., D. Abi-Ghanem, S. D. Waghela, and S. C. Ricke. 2005. Antibodies: An alternative for antibiotics? Poult. Sci. 84:660–666.
  43. Mastroeni, P., J. A. Chabalgoity, S. J. Dunstan, D. J. Maskell, and G. Dougan. 2001. Salmonella: Immune responses and vaccines. Vet. J. 161:132–164.[CrossRef][Web of Science][Medline]
  44. House, J. K., M. M. Ontiveros, N. M. Blackmer, E. L. Dueger, J. B. Fitchhorn, G. R. McArthur, and B. P. Smith. 2001. Evaluation of an autogenous Salmonella bacterin and a modified live Salmonella serotype Choleraesuis vaccine on a commercial dairy farm. Am. J. Vet. Res. 62:1897–1902.[CrossRef][Web of Science][Medline]
  45. Withanage, G. S. K., K. Sasai, T. Fukata, T. Miyamoto, and E. Baba. 1999. Secretion of Salmonella-specific antibodies in the oviducts of hens experimentally infected with Salmonella enteritidis. Vet. Immunol. Immunopathol. 67:185–193.[CrossRef][Web of Science][Medline]
  46. Barrow, P. A., G. C. Mead, C. Wary, and M. Duchet-Suchaux. 2003. Control of food-poisoning Salmonella in poultry—Biological options. Worlds Poult. Sci. J. 59:373–383.[CrossRef][Web of Science]
  47. De Buck, J., F. Van Immerseel, F. Haesebrouck, and R. Ducatelle. 2005. Protection of laying hens against Salmonella Enteritidis by immunization with type 1 fimbriae. Vet. Microbiol. 105:93–101.[CrossRef][Web of Science][Medline]
  48. Khoury, C. A., and R. J. Meinersmann. 1995. A genetic hybrid of the Campylobacter jejuni flaA gene with LT-B of Escherichia coli and assessment of the efficacy of the hybrid protein as an oral chicken vaccine. Avian Dis. 39:812–820.[CrossRef][Web of Science][Medline]
  49. Leistner, L. 1985. Hurdle technology applied to meat products of the shelf stable product and intermediate moisture food types. Pages 309–329 in Properties of Water in Foods. D. Simatos and J. L. Multon, ed. Nijhoff Publishers, Dordrecht, the Netherlands.
  50. Leistner, L., and L. G. M. Gorris. 1995. Food preservation by hurdle technology. Trends Food Sci. Technol. 6:41–46.[CrossRef]
  51. Leistner, L. 2000. Basic aspects of food preservation by hurdle technology. Int. J. Food Microbiol. 55:181–186.[CrossRef][Web of Science][Medline]
  52. Kwon, Y. M., S. Y. Park, S. G. Birkhold, and S. C. Ricke. 2000. Induction of resistance of Salmonella Typhimurium to environmental stresses by exposure to short-chain fatty acids. J. Food Sci. 65:1037–1040.[CrossRef][Web of Science]
  53. Whyte, P., K. McGill, and J. D. Collins. 2003. An assessment of steam pasteurization and hot water immersion treatments for the microbiological decontamination of broiler carcasses. Food Microbiol. 20:111–117.[CrossRef][Web of Science]
  54. Purnell, G., K. Mattick, and T. Humphrey. 2004. The use of ‘hot wash’ treatments to reduce the number of pathogenic and spoilage bacteria on raw retail poultry. J. Food Eng. 62:29–36.[CrossRef]
  55. Thomson, J. E., N. A. Cox, and J. S. Bailey. 1977. Control of Salmonella and extension of shelf-life of broiler carcasses with a glutaraldehyde product. J. Food Sci. 42:1353–1355.[CrossRef][Web of Science]
  56. Castillo, A., L. M. Lucia, I. Mercado, and G. R. Acuff. 2001. In-plant evaluation of a lactic acid treatment for reduction of bacteria on chilled beef carcasses. J. Food Prot. 64:738–740.[Web of Science][Medline]
  57. Yadav, A. S., N. K. Pandey, and R. P. Singh. 2004. Antimicrobial effect of turmeric extract against Aeromonas hydrophila in extending refrigerated shelf-life of minced chicken meat. Ind. J. Anim. Sci. 74:1166–1168.




This Article
Right arrow Summary Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sirsat, S. A.
Right arrow Articles by Ricke, S. C.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Sirsat, S. A.
Right arrow Articles by Ricke, S. C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS