The gastrointestinal tract of newly hatched chicks is essentially sterile and highly suscep- tible to colonization/infection with pathogenic bacteria.69 One approach to prevent the colonization of pathogenic bacteria is to accelerate establishment of normal intestinal flora in chicks as early as possible, thus providing a source of competition for subsequent pathogens to which the host bird may be exposed. Competitive exclusion (CE) is the deliv- ery of a suspension of healthy adult cecal microflora, and was first described in 1973.70The benefits of competitive exclusion treatment on reducing Salmonella and Campylobacter shed- ding and environmental contamination are now well documented.71–74
The protective effect of CE has been explained by competition for attachment sites (Figure 8.1), production of volatile fatty acids, decreased oxidation-reduction potential, and competition for nutrients.70, 75CE products may consist of cultures in which the bacte- rial composition is known (defined) or unknown (undefined). Defined cultures offer some additional safety since there is decreased likelihood of introduction of unintended, poten- tially pathogenic organisms. Presently, one competitive exclusion product is licensed by the U.S. Food and Drug Administration for use in poultry for the prevention/reduction of Salmonella infections (PreemptTM, M.S. BioScience, Madison, WI) and an additional undefined culture which is presently undergoing testing (Mucosal Starter Culture, Continental Grains, Chicago, IL).
Figure 8.1 Scanning electron micrograph of cecal mucosa (mid-cecum) from broiler chicks 48 h after hatch. Bars represent 100 m. Courtesy of Dr. Robert E. Droleskey, USDA-ARS, College Station, TX. Panel A: Normal untreated chick cecal mucosa. Cecal crypts are present (arrowheads) without the large clumps of bacteria seen in similar segments following treatment with a competitive exclusion product.
In commercial field trials, both CE cultures were effective in controlling Salmonella cecal colonization in market-age broilers.27, 75 Day-of-hatch chicks provided a single dose of a defined CE culture had a significantly (p 0.05) lower incidence of Salmonella recovery (0%) compared to the non-treated controls (7%). Similarly, market-age broilers treated with an undefined CE culture in a two-step procedure (spray at hatchery and via drinking water at placement) had significantly fewer Salmonella-positive carcasses prior to chilling (6.7%) com- pared to non-treated controls (12.8%). One defined CE product has been shown to be effec- tive in protecting chicks against colonization under experimental conditions by S. enteritidis (PT13, PT 4), S. gallinarum, S. typhimurium, Clostridium perfringens, and E. coli O157:H7.74, 76–79 The use of CE products can be an effective component in an integrated control program. The efficacy of CE products is dependent on the volume and concentration of the dose as well as the delivery method. CE cultures often consist of bacterial organisms that are sensitive to antimicrobial components which, therefore, may diminish the effec- tiveness of the culture. One should consider that CE products will not eliminate the food- borne pathogens but should be included in a complete integrated control program. As effective CE programs can reduce intestinal colonization by a number of pathogens, these programs may offer alternatives to low level antimicrobial use, which should also be con- sidered with regard to cost of an integrated antemortem food-borne pathogen control program.
Vaccination
Vaccination programs are used to prevent or reduce the spread of pathogenic viruses and bacteria and generally depend on recognition of specific antigens (epitopes) by the immune system by the host. Because there are a large number of Salmonella serovars, each with individual epitopes which do not elicit cross protection against other serovars, there has been little traditional emphasis on development of generic Salmonella vaccines.
Campylobacter vaccines for poultry are not faced with the problem of large serovar diver-
sity. While one study suggested that an orally administered inactivated Campylobacter vaccine could sometimes reduce shedding in vaccinated chickens,80effective commercial vaccines have yet to be developed for commercial meat poultry use.
Figure 8.1 (continued) Panel B: Similar section of mucosa from a chick treated at hatch with a com- mercial competitive exclusion product. The majority of crypts (arrowheads) contain large clumps of bacteria (large arrows). A few crypts devoid of bacteria are also present (small arrows).
In contrast to generic Salmonella vaccination, vaccination for specific Salmonella serovar strains (e.g., S. enteritidis, S. gallinarum) has gained considerable acceptance in countries with endemic problems with these more devastating serovars, particularly in breeders and table egg production chickens (see Shivaprasad81for review). Such vaccines should be con- sidered in the event of emergence of a high level problem related to a specific Salmonella serovar.
A live-type commercial vaccine with a double gene deletion that is avirulent and immunogenic has been reported82 and other specific deletion mutants have been pro- posed.83, 84Day-of-hatch chicks vaccinated with this live-type vaccine have been shown to have serological protection to homologous and heterologous Salmonella serotypes, possibly through a mechanism similar to competitive exclusion.85, 86Furthermore, maternal anti- bodies can be demonstrated in eggs and chicks from breeders vaccinated with this vaccine. These antibodies are reported to reduce salmonellae colonization and to provide protection to laying hens up to 11 months post-inoculation.86However, susceptibility to antimicrobial agents commonly used in poultry production can reduce or eliminate the efficacy of live vaccines. While much of the published research appears encouraging, live Salmonella vac- cines have not gained widespread commercial acceptance within the U. S. for paratyphoid
Salmonella control to date.
Summary
Clearly, successful antemortem intervention programs for food-borne pathogens must be integrated and must approach multiple critical control points. To date, there is no single identified critical control point that will assure reductions of food-borne pathogens, but integration of multiple approaches, focused on known critical control points, has been par- tially effective. Present evidence indicates that a major factor for ultimate success of ante- mortem intervention will be the production and maintenance of food-borne pathogen-free breeder flocks, a problem compounded by the necessity of feed restriction during growth and stress associated with production. Emerging areas of antemortem food-borne pathogen control include the use of effective competitive exclusion products, treatment of drinking water with organic acids during the preslaughter feed withdrawal, and the treat- ment of litter with acidification or alkalinization products. The use of organic acids during feed withdrawal and the effects of environmental treatments have been recently reviewed.87 Similarly, the benefits of competitive exclusion treatment on reducing
Salmonella and Campylobacter shedding and environmental contamination are now well
documented.71–74As the future of conventional use of some antimicrobial compounds in commercial poultry production is in question, competitive exclusion may find a new role in poultry health and production, with the additional benefits of food-borne pathogen control.
References
1. United States Department of Agriculture, Food Safety Inspection Service, FSIS/CDC/FDA Sentinel Site Study: The Establishment and Implementation of an Active Surveillance System for Bacterial Foodborne Diseases in the United States, Report to Congress, February, 1997. 2. United States Department of Agriculture, Food Safety Inspection Service, Foodnet: An Active
Surveillance System Bacterial Foodborne Diseases in the United States, Report to Congress, April, 1998.
3. Tauxe, R. R. V., Salmonella: A postmodern pathogen, J. Food Prot., 54, 563, 1991.
4. Bean, N. H. and Griffin, P. M., Food-borne disease outbreaks in the United States, 1973–1987: Pathogens and trends, J. Food Prot., 53, 804, 1990.
5. Persson, U. and Jendteg, S. I., The economic impact of poultry-borne salmonellosis: how much should be spent on prophylaxis?, Int. J. Food Microbiol., 15, 207, 1992.
6. Madie, P., Salmonella and Campylobacter infections in poultry, in Proc. Solvay Chicken Health Course, Grunner U. Peterson Massey University, Palmerston North, New Zealand, 1992. 7. National Research Initiative Competitive Grants Program, Program Descriptions, Cooperative
State Research Service; United States Department of Agriculture, Washington, D.C., Section 32.0: Food Safety, 1991.
8. Barnes, H. J. and Gross, W. B., Colibacillosis, in Diseases of Poultry, 10th Ed., Calnek et al. Eds. Iowa State University Press, Ames, IA, 1997, 131.
9. Beery, J. T., Doyle, M. P., and Schoeni, J. L., Colonization of chicken cecae by Escherichia coli associated with hemorrhagic colitis, Appl. Environ. Microbiol., 49, 310, 1985.
10. Stavric, S., Buchanan, B., and Gleeson, T. M., Intestinal colonization of young chicks with Escherichia coli 0157:H7 and other verotoxin-producing serotypes, J. Appl. Bacteriol., 74, 557, 1993.
11. Doyle, M. O. and Schoeni, J. L., Isolation of Escherichia coli 0157:H7 from retail fresh meats and poultry, Appl. Environ. Microbiol., 53, 2394, 1987.
12. Griffin, P. M. and Tauxe, R. V., The epidemiology of infections caused by Escherichia coli 0157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome, Epidemiol. Rev., 13, 60, 1991.
13. Evans, J. B., Ananaba, G. A., Pate, C. A., and Bergdoll, M. S., Enterotoxin production by atypical Staphylococcus aureus from poultry, J. Appl. Bacteriol., 54, 257, 1983.
14. Gibbs, P. A., Patterson, J. T., and Harvey, J., Biochemical characteristics and enterotoxigenicity of Staphylococcus aureus strains isolated from poultry, J. Appl. Bacteriol., 44, 57, 1978.
15. Harvey, J., Patterson, J. T., and Gibbs, P. A., Enterotoxigenicity of Staphylococcus aureus strains isolated from poultry: raw poultry carcasses as a potential food-poisoning hazard, J. Appl. Bacteriol., 52, 251, 1982–258.
16. Deveriese, L. A., Devos, A. H., Beumer, J., and Moes, R., Characterization of staphylococci isolated from poultry, Poult. Sci., 51, 389, 1972.
17. Skeeles, J. K., Staphylococcosis, in Diseases of Poultry, 10th Ed., Calnek et al., Eds., Iowa State University Press, Ames, IA, 1997, 247.
18. Adams, B. W. and Mead, G. C., Incidence and properties of Staphylococcus aureus associated with turkeys during processing and further-processing operations, J. Hyg., 91, 479, 1983. 19. Notermans, S., Dufrenne, J., and van Leeuwen, W. J., Contamination of broiler chickens by
Staphylococcus aureus during processing: incidence and origin, J. Appl. Bacteriol., 52, 275, 1982. 20. Barnes, H. J., Other bacterial diseases, in Diseases of Poultry, 10th Ed., Calnek et al. Eds., Iowa
State University Press, Ames, IA, 1997, 289.
21. Marsden, J. L., Industry Perspectives on Listeria monocytogenes in foods: raw meat and poultry, dairy, Food Environ. Sanit., 14, 83, 1994.
22. Rigby, C. E. and Pettit, J. R., Changes in the Salmonella status of broiler chickens subjected to simulated shipping conditions, Can. J. Comp. Med., 44, 374, 1980.
23. Goren, E., de Jong, W. A., Doornenbal, P., Bolder, N. M., Mulder, R. W. A. W., and Jansen, A., Reduction of Salmonella infection of broilers by spray application of intestinal microflora: a longitudinal study, Vet. Q., 10, 249, 1988.
24. Jones, F., Axtell, R. C., Rives, D. V., Scheideler, S. E., Tarver, F. R., Walker, R. L., and Wineland, M. J., A survey of Campylobacter jejuni contamination in modern broiler production and processing systems, J. Food Prot., 54, 259, 1991.
25. Jones, F., Axtell, R. C., Rives, D. V., Scheideler, S. E., Tarver, F. R., Walker, R. L., and Wineland, M. J., A survey of Salmonella contamination in modern broiler production, J. Food Prot., 54, 502, 1991.
26. Stavric, S. and D’Aoust, J. Y., Undefined and defined bacterial preparations for the competitive exclusion of Salmonella in poultry—a review, J. Food Prot., 56, 173, 1993.
27. Blankenship, L. C., Bailey, J. S., Cox, N. A., Stern, N. J., Brewer, R., and Williams, O., Two-step mucosal competitive exclusion flora treatment to diminish salmonellae in commercial broiler chickens, Poult. Sci., 72, 1667, 1993.
28. Krabisch, P. and Dorn, P., The importance of living vectors for the dissemination of Salmonella in broiler flock rodents, cats and insects as vectors, Berl. Muench. Tieraerztl. Wochenschr., 93, 232, 1980.
29. Lillard, H. S., Factors affecting persistence of Salmonella during the processing of poultry, J. Food Prot., 52, 829, 1989.
30. Sarlin, L. L., Barnhart, E. T., Caldwell, D. J., Moore, R. W., Byrd, J. A., Caldwell, D. Y., Corrier, D. E., DeLoach, J. R., and Hargis, B. M., Evaluation of alternative sampling methods for Salmonella critical control point determination at broiler processing, Poult. Sci., 77, 1253, 1998. 31. Fanelli, M. J., Sadler, W. W., Franti, C. E., and Brownell., J. R., Localization of salmonellae within
the intestinal tract of chickens, Avian Dis., 15, 366, 1971.
32. Snoeyenbos, G. H., Soerjadi, A. S., and Weinack, O. M., Gastrointestinal colonization by Salmonella and pathogenic Escherichia coli in monozenic and holoxenic chicks and poults, Avian Dis., 26, 566, 1982.
33. Corrier, D. E., Hargis, B. M., Hinton, A., Lindsey, D., Caldwell, D. J., Manning, J., and DeLoach, J. R., Effect of cecal colonization resistance of layer chicks to invasive Salmonella enteritidis, Avian Dis., 35, 337, 1991.
34. Hargis, B. M., Caldwell, D. J., Brewer, R. L., Corrier, D. E., and DeLoach, J. R., Evaluation of the chicken crop as a source of Salmonella contamination for broiler carcasses, Poult. Sci., 74, 1548, 1995.
35. Corrier, D. E., Byrd, J. A., Hargis, B. M., Hume, M. E., Bailey, R. H., and Stanker, L. H., Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed withdrawal, Poult. Sci., 78, 45, 1999.
36. Byrd, J. A., Corrier, D. E., Hume, M. E., Bailey, R. H., Stanker, L. H., and Hargis, B. M., Effect of feed withdrawal on the incidence of Campylobacter in crops of preharvest broiler chickens, Avian Dis., 42, 802, 1998.
37. Lillard, H. S., Effect of surfactant or changes in ionic strength on the attachment of Salmonella typhimurium to poultry skin and muscle, J. Food Sci., 53, 727, 1988.
38. Humphrey, T. J., Baskerville, A., Whitehead, A., Rowe, B., and Henley, A., Influence of feeding patterns on the artificial infection of laying hens with Salmonella enteritidis phage type 4, Vet. Rec., 132, 407, 1993.
39. Ramirez, G. A., Sarlin, L. L., Caldwell, D. J., Yezak, C. R., Jr., Hume, M. E., Corrier, D. E., Deloach, J. R., and Hargis, B. M., Effect of feed withdrawal on the incidence of Salmonella in the crops and ceca of market age broiler chickens, Poult. Sci., 76, 654, 1997.
40. Corrier, D. E., Byrd, J. A., Hargis, B. M., Hume, M. E., Bailey, R. H., and Stanker, L. H., Survival of Salmonella in the crop contents of market-age broilers during feed withdrawal, Avian Dis., 43, 453, 1999.
41. Huff, W. E., Moore, P. A., Balog, J. M., Bayyari, G. R., and Rath, N. C., Evaluation of toxicity of alum (aluminum sulfate) in young broiler chickens, Poult. Sci., 75, 1359, 1996.
42. Moore, P. A. and Miller, D. A., Decreasing phosphorus solubility in poultry litter with aluminum, calcium and iron amendments, J. Environ. Qual., 23, 325, 1994.
43. Huff, W. E., Malone, G. W., and Chaloupka, G. W., Effect of litter treatment on broiler performance and certain litter quality parameters, Poult. Sci., 63, 2167, 1984.
44. Reece, F. N., Bate, B. J., and Lott, B. D., Ammonia control in broiler houses, Poult. Sci., 58, 754, 1979.
45. Moore, P. A., Jr., Daniel, T. C., Edwards, D. R., and Miller, D. M., Evaluation of chemical amendments to reduce ammonia volatilization from poultry litter, Poult. Sci., 75, 315, 1996. 46. Terzich, M., Quarles, C., Goodwin, M. A., and Brown, J., Effect of Poultry Litter Treatment (PLT)
on death due to ascites in broilers, Avian Dis., 42, 385, 1998.
47. Parkhurst, C. R., Hamilton, P. B., and Baughman, G. R., The use of volatile fatty acids for the control of microorganisms in pine sawdust litter, Poult. Sci., 58, 801, 1974.
48. Terzich, M., The effects of sodium bisulfate on bacteria load of poultry litter and bird
performance, in Proc. 68th Northeastern Conference on Avian Diseases, Penn State University, June 10–12, 1996.
50. Morris, G. K., McMurray, B. L., Galton, M. M., and Wells, J. G., A study of the dissemination of salmonellosis in a commercial broiler chicken operation, Am. J. Vet. Res., 30, 1413, 1969. 51. MacKenzie, M. A. and Bains, B. S., Dissemination of Salmonella serotypes from raw feed
ingredients to chicken carcasses, Poult. Sci., 55, 957, 1996.
52. Shrimpton, D. H., The Salmonella problem of Britian, Milling Flour Feed, Jan:16–17, 1989. 53. Caldwell, D. J., Hargis, B. M., Corrier, D. E., Williams, J. D., Vidal, L., and DeLoach, J. R.,
Evaluation of persistence and distribution of Salmonella serotype isolation from poultry farms using drag-swab sampling, Avian Dis., 39, 617, 1995.
54. Byrd J. A., Origin and relationship of Campylobacter and Salmonella contamination of poultry during processing, Poult. Sci., 78 (Suppl. 1), 4, 1999.
55. Stern, N. J., Clavero, M. R. S., Bailey, J. S., Cox, N. A., and Robach, M. C., Campylobacter spp. in broilers on the farm and after transport, Poult. Sci., 74, 937, 1995.
56. Hoop, R. and Ehrsam. H., Ein beitrag zur epidemiologie von Campylobacter jejuni and Campylobacter coli in der Hünnermast, Schweiz. Arch. Tierheilknd, 129, 193, 1987. 57. Mead, G. C., Hudson, W. R., and Hinton, M. H., Use of a marker organism in poultry
processing to identify sites of cross-contamination and evaluate possible control measures, Br. Poult. Sci., 35, 345, 1994.
58. Acuff, G. R., Vanderzant, C., Hanna, M. O., Ehlers, J. G., Golan, F. A., and Gardner, F. A., Prevalence of Campylobacter jejuni in turkey carcass processing and further processing of turkey products, J. Food Prot., 49, 712, 1986.
59. Wempe, J. M., Genigeorgis, C. A., Farver, T. B., and Yusufu, H. I., Prevalence of Campylobacter jejuni in two California chicken processing plants, Appl. Environ. Microbiol., 45, 355, 1983. 60. Kotula, K. L. and Pandya, Y., Bacterial contamination of broiler chickens before scalding, J. Food
Prot., 58, 1326, 1995.
61. Baker, R. C., Paredes, M. D. C. Paredes, and Qureshi, R. A., Prevalence of Campylobacter in poultry meat in New York State, Poult. Sci., 66, 1766, 1987.
62. Goodnough, M. C. and Johnson, E. A., Control of Salmonella enteritidis infections in poultry by polymyxin B and trimethoprim, Appl. Environ. Microbiol., 57, 785, 1991.
63. Muirhead, S., Feed Additive Compendium, Miller Publishing, Minneapolis, MN, 1994.
64. Manning, J. G., Hargis, B. M., Hinton, A., Corries, D. E., DeLoach, J. R., and Creger, C. R., Effect of nitrofurazone or novobiocin on Salmonella enteritidis cecal colonization and organ invasion in leghorn hens, Avian Dis., 36, 334, 1992.
65. Manning, J. G., Hargis, B. M., Hinton, A., Corrier, D. E., DeLoach, J. R., and Creger, C. R., Effect of selected antibiotics and anticoccidials on Salmonella enteritidis cecal colonization and organ invasion in Leghorn chicks, Avian Dis., 38, 256, 1994.
66. Kobland, J. D., Gale, G. O., Gutafson, R. H., and Simkins, K. L., Comparison of therapeutic versus subtherapeutic levels of chlortetracycline in the diet for selection of resistant Salmonella in experimentally challenged chickens, Poult. Sci., 66, 1129, 1987.
67. Gast, R. K. and Stephens, J. F., Effect of kanamycin administration to poultry on the proliferation of drug-resistant Salmonella, Poult. Sci., 67, 689, 1988.
68. Gast, R. K., Stephens, J. F., and Foster, D. N., Effect of kanamycin administration to poultry on the proliferation of drug-resistant Salmonella, Poult. Sci., 67, 699, 1988.
69. Jayne-Williams, and Fuller, D. J. R., The influence of intestinal microflora on nutrition, in Physiology and Biochemistry of Domestic Food, Bell, D. J. and Freeman, B. M., Eds., Academic Press, London, 1971, 74.
70. Nurmi, E. and Rantala, M., New aspects of Salmonella infection in broiler production, Nature, 241, 210, 1973.
71. Wierup M., Wahlstrom, H., and Engstrom, B., Experience of a 10-year use of competitive exclusion treatment as part of the Salmonella control programme in Sweden, Int. J. Food Microbiol., 15, 287, 1992.
72. Schoeni J. L. and Wong, C. L., Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria, Appl. Environ. Microbiol., 60(4), 1191, 1994.
73. Corrier D. E., Nisbet, D. J., Byrd, J. A., II, Hargis, B. M., Keith, N. K., Peterson, M., and DeLoach, J. R., Dosage titration of a characterized competitive exclusion culture to inhibit Salmonella colonization in broiler chickens during growout, J. Food Prot., 61, 796, 1998.
74. Nisbet, D. J., Tellez, G. I., Lowery, V. K., Anderson, R.C., Garcia, G., Nava, G., Kogut, M. H., Corrier, D. E., and Stanker, L. H., Effect of a commercial competitive exclusion culture (PREEMPT) on mortality and horizontal transmission of Salmonella gallinarium in broiler chickens, Avian Dis., 42, 651, 1998.
75. Corrier, D. E., Nisbet, D. J., Scanlan, C. M., Hollister, A. G., Caldwell, D. J., Thomas, L. A., Hargis, B. M., Tomkins, T., and DeLoach, J. R., Treatment of commercial broiler chickens with a characterized culture of cecal bacteria to reduce salmonellae colonization, Poult. Sci., 74, 1093, 1995.
76. Corrier, D. E., Hinton, A., Jr., Ziprin, R. L., Beier, R. C., and DeLoach, J. R., Effect of dietary lactose on cecal pH, bacteriostatic volatile fatty acids, and Salmonella typhimurium colonization of broiler chicks, Avian Dis., 34, 617, 1990.
77. Corrier, D. E., Nisbet, D. J., Scanlan, C. M., Tellez, G., Hargis, B. M., and DeLoach, J. R., Inhibition of Salmonella enteritidis cecal and organ colonization in leghorn chicks by a defined culture of cecal bacteria and dietary lactose, J. Food Prot., 56, 377, 1994.
78. Nisbet, D. J., Corrier, D. E., Ricke, S. C., Hume, M. E., Byrd, J. A., and DeLoach, J. R., Cecal propionic acid as a biological indicator of the early establishment of a microbial ecosystem inhibitory to Salmonella in chicks, Anaerobes, 2, 345, 1996.
79. Byrd, J. A., Nisbet, D. J., Corrier, D. E., and Stanker, L. H., Use of continuous-flow culture system to study the interaction between Clostridium perfringens and a mixed microbial competitive exclusion culture (CF3), Biosci. Microflora, 16 (Suppl.), 15, 1997.
80. Rice, B. E., Rollins, D. M., Mallinson, E. T., Carr, L. J., and Sam, W., Campylobacter jejuni in broiler chickens: Colonization and humoral immunity following oral vaccination and experimental infection, Vaccine, 15, 1922, 1997.
81. Shivaprasad, H. L., Pullorum disease and fowl typhoid, in Diseases of Poultry, 10th Ed., Calnek et al., Eds., Iowa State University Press, Ames, IA, 1997, 82.
82. Curtiss, R. S. and Kelly, M., Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic, Infect. Immun., 55, 3035, 1987. 83. Zhang-Barber, L., Turner, A. K., and Barrow, P. A., Vaccination for control of Salmonella in
poultry, Vaccine, 17, 2538, 1999.
84. Sydenham, M., Gillian, D., Bowe, F., Ahmed, S., Chatfield, S., and Dougan, G., Salmonella enterica serovar typhimurium surA mutants are attenuated and effective live oral vaccines, Infect. Immun., 68, 1109, 2000.
85. Hassan, J. O. and Curtiss, R., Development and evaluation of an experimental vaccination program using a live-avirulent Salmonella typhimurium strain to protect immunized chickens against challenge with homologous and heterologous Salmonella serotypes, Infect. Immun., 62, 5519, 1994.
83. Hassan, J. O. and Curtiss, R., Efficacy of live avirulent Salmonella typhimurium vaccine in preventing colonization and invasion of laying hens by Salmonella typhimurium and Salmonella enteritidis, Avian Dis., 41, 783, 1997.
87. Byrd J. A., Corries, D. E., Caldwell, D. J., Bailey, R. H., Brewer, R. L., Stanker, L. H., and Hargis, B. M., Effect of selected organic acids on the control of Salmonella in market-age broilers during feed withdrawal, Poult. Sci., 78 (Suppl. 1), 85, 1999.