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Bacterial Isolates from the Chicken Gizzard and Ceca with in Vitro Inhibitory Activity Against Salmonella Typhimurium

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Bacterial Isolates from the Chicken Gizzard and Ceca with in Vitro Inhibitory Activity Against Salmonella Typhimurium 120 Journal of Food Protection, Vol. 60, No.2, 1997, Pages 120-124 Copyright©, International Association of Milk, Food and Environmental Sanitarians Bacterial Isolates from the Chicken Gizzard and Ceca with In Vitro Inhibitory Activity against Salmonella typhimurium DOUGLAS E. COSBY,l* STEPHEN E. CRAVEN,l MARK A. HARRISON,2 and NELSON A. COXl 1United States Department of Agriculture, Agricultural Research Service, Poultry Microbiological Safety Research Unit, Richard B. Russell Research Downloaded from http://meridian.allenpress.com/jfp/article-pdf/60/2/120/1666402/0362-028x-60_2_120.pdf by guest on 27 September 2021 Center, P.O. Box 5677, Athens, Georgia 30604-5677; and 2Center for Food Safety and Quality Enhancement, Department of Food Science and Technology, University of Georgia, Athens, Georgia 30605, USA (MS# 96-60: Received 1 March 1996/Accepted 4 June 1996) ABSTRACT from colonization by the early establishment of a mature cecal microflora. Young chicks treated in this manner are Bacterial isolates (197) obtained from the gizzard and ceca of better able to resist colonization by salmonellae present in 20 broiler and 40 specific-pathogen-free chickens, 21 days to 8 the environment. Recognition of this fact has led to the months of age, were evaluated for inhibitory activity against "Nurmi concept," more commonly known as competitive Salmonella typhimurium. One-hundred forty strains were character- exclusion (CE). CE cultures can comprise undefined strains, ized as gram negative and oxidase negative, typical of the which have proven successful in several trials (5, 8, 11, 18, Enterobacteriaceae. Five of the gram-negative and oxidase- negative isolates demonstrated inhibitory activity against six 19), or defined strains, which have proven to be less strains of S. typhimurium after 10- and 20-fold concentration and successful (8, 18, 19). The main emphasis is on obtaining a ammonium sulfate precipitation of the cell-free supernatant fluid mature cecal microflora as early as possible in the young from a culture grown in M9 minimal medium. Three isolates were chicks. identified as lactobacilli, 40 other strains exhibited Gram stain, The mechanism of action by which CE flora inhibit oxidase, and catalase reactions typical of the Lactobacillus spp., salmonellae has not been well defined. The inhibition could and three known lactobacilli were included in the evaluation. stem from competition for nutrients, competition for attach- Limited inhibitory activity was exhibited by these 46 isolates when ment sites, formation of metabolic end products, or produc- tested against six S. typhimurium strains. Fourteen other strains not tion ofbacteriocins by the CE microorganisms (5, 7,12,18). characterized as presumptive enterobacteria or lactic acid bacteria The purpose of this research was twofold: (i) to compare demonstrated little or no inhibitory activity against the six test methods for detecting antagonistic microbe-microbe interac- strains. tion, and (ii) to identify bacteria isolated from the gizzard Key words: Salmonella typhimurium, Enterobacteriaceae, Lactoba- and ceca of adult chickens that will produce inhibitory cillus spp., inhibitory activity, antimicrobial agent activity against Salmonella typhimurium specifically and Salmonella spp. in general. These organisms could be used to improve the efficacy of defined CE cultures. Salmonella species continue to be one of the principal causes of human food-borne infections in many countries. MATERIALS AND METHODS Symptomless carriage of non-host-specific salmonellae in commercial poultry flocks is an important factor in the Microorganisms, maintenance, and culture conditions widespread occurrence of human salmonellosis. The non- Lactobacillus acidophilus N2, Lactobacillus delbrueckii subsp. host-specific salmonellae can be associated with infected lactis 4797, and Lactobacillus plantarum NCDO 1752 were breeder birds, contaminated feed, and presence of insects, obtained from Dr. Susan Barefoot, Clemson University, Clemson, rodents, and wild birds in the live-bird environment. Hu- SC; Salmonella typhimurium 3333/0, a spontaneous nalidixic mans can also contribute to the contamination of newly acid-resistant strain, was obtained from author Craven (7). Salmo- hatched chicks. A direct consequence is the contamination of nella typhimurium SL 1102 and SL 3019, both lipopolysaccharide a significant proportion of processed carcasses with non-host- mutant type rfaE, were obtained from the Salmonella Genetic specific salmonellae (10). Stock Center, University of Calgary, Alberta, Canada. Salmonella In 1973, Nurmi and Rantala (12) recognized that newly typhimurium SH 7915, a mutant strain demonstrating supersensitiv- ity to hydrophobic antibiotics (20) and S. typhimurium SR-ll and hatched chicks reared commercially are susceptible to SR-ll-a, a non-curliated variant, were obtained from Dr. Soila intestinal colonization by salmonellae, but can be protected Sukupolvi, Washington University, St. Louis, MO. Presumptive Enterobacteriaceae from the chicken ceca and gizzard were isolated using brilliant green sulfa, Hektoen-enteric, * Author for correspondence. Tel: 706-546-3986; Fax: 706-546-3771; violet red bile with 1.0% glucose added, and MacConkey's agar E-mail: !a03r1pms (Difco Laboratories; Detroit, MI) plates incubated at 35°C for 24 h. IN VITRO ACTIVITY OF CHICKEN BACTERIAL ISOLATES AGAINST SALMONELLA 121 All presumptive Enterobacteriaceae isolates were subcultured for MA) of the cultures. The supernatant was concentrated lO-fold by purity onto BHI agar (Difco) plates. lyophilization and resuspension in 1.5 ml of sterile distilled water. Presumptive lactic acid bacteria (LAB) strains were isolated Ammonium sulfate precipitation of the concehtrated supernatant on DeMan Rogosa and Sharpe (MRS) agar (Difco). Plates were fluid was carried out as described by Siragusa (15). The precipitates incubated at 35°C for 24 to 48 h. All presumptive LAB strains were were resuspended in 100 f.llof 0.1 M 3-[N-morpholino]propanesul- subcultured for purity onto MRS agar plates. fonic acid (MOPS) in 0.85% saline, pH 7.2. The ammonium sulfate Working cultures were maintained on MRS agar for the was not removed prior to conducting the spot-on-the-lawn assays. presumptive LABs and on BHI agar for the Enterobacteriaceae The spot-on-the-lawn assays were completed for each of the and presumptive Enterobacteriaceae. Stock cultures were main- resulting protein solutions according to the procedure of Siragusa tained in 16% glycerol, 0.85% saline at -80°C or in liquid (15). The spot-on-the-lawn assays were conducted using 10 f.llof nitrogen. the resuspended precipitates on a lawn of 105 CPU of the six Isolated strains were grouped according to Gram reaction, Salmonella test strains. Negative controls consisting of ammonium- determined by the KOH test of Graevenitz and Bucher (21) and the sulfate-precipitated, uninoculated, M9 minimal medium and sterile spot oxidase reaction (Difco). Gram-positive organisms were distilled water were included in all assays. The plates were further characterized by the catalase test. Identification of the incubated upright for 24 h at 35°C and were evaluated for Downloaded from http://meridian.allenpress.com/jfp/article-pdf/60/2/120/1666402/0362-028x-60_2_120.pdf by guest on 27 September 2021 inhibitory organisms that were gram negative and oxidase negative inhibition (cleared zones greater than or equal to 5 mm) at 6,8, 10, was conducted using Micro-ID Enteric strips (Organon-Technika, and 22 to 24 h as described above. Durham, NC). Five isolates from the above experiment showing inhibition of four or more Salmonella test strains under various growth condi- Chicken source, maintenance, screening, and sample preparation tions were chosen for further study based on the inhibition of four Twenty day-of-hatch broiler chicks from a local hatchery and or more test strains under the same growth conditions as in the 40 day-of-hatch specific-pathogen-free chicks (Select Laborato- previous step. Each isolate was grown in 100 ml of the M9 minimal ries, Gainesville, GA) were obtained and maintained in modified medium for 48 h under the appropriate growth condition. One Horsfaal units at the Poultry Disease Research Center (PDRC) at hundred milliliters of cell-free supernatant fluid (sterilized by the University of Georgia. Paper pads and transport crates were centrifugation for 10 min at 10,000 X g and by filter sterilization screened at the time of placement for the presence of indigenous with 0.2-f.lm pore size filter units (Nalge Company, Rochester, New salmonellae prior to use of the birds in experiments. Individual York)) for each isolate was lyophilized and resuspended in 5 ml of birds were sacrificed between the ages of 21 and 240 days. The sterile distilled water (20X concentration). Ammonium sulfate ceca, gizzard, and their contents were aseptically removed. The precipitations and spot-on-the-lawn assays were carried out accord- ceca and the gizzard were everted to expose the inner layer. Ten ml ing to the procedure listed above. The plates were incubated upright of sterile saline (0.85%) was added to the ceca and gizzards as a at 35°C for 24 h and were evaluated for inhibition at 6, 8, 10, and diluent. After stomaching and serial dilution, samples were plated 24h. onto selective media for isolation of bacteria. Three colonies of differing morphology were selected at random from each plate RESULTS containing isolated colonies and streaked for purity onto either BHI or MRS agar plates.
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