Correlating bacterial shedding with fecal corticosterone levels and serological responses from layer hens experimentally infected with Salmonella Typhimurium

Springer Science and Business Media LLC - Tập 48 - Trang 1-11 - 2017
Pardeep Sharma1, Vivek V. Pande1, Talia S. Moyle1, Andrea R. McWhorter1, Kapil K. Chousalkar1
1School of Animal and Veterinary Sciences, The University of Adelaide, Roseworthy, Australia

Tóm tắt

Salmonella Enteriditis and Salmonella Typhimurium are commonly isolated during egg-related outbreaks of salmonellosis and represent a significant international public health issue. In Australia, Salmonella Typhimurium is the most common serovar identified in egg product related foodborne outbreaks. While a number of studies have investigated Salmonella shedding and host responses to infection, they have been conducted over a short time period. The present study sought to characterise bacterial shedding and host responses to infection in hens infected with only Salmonella Typhimurium or co-infected with both Salmonella Typhimurium and Salmonella Mbandaka over a 16 week period. Salmonella shedding was quantified using the most probable number and qPCR methods and was highly variable over the course of the experiment. On day 1, fecal corticosterone metabolites in birds infected with Salmonella Typhimurium (674.2 ± 109.3 pg/mg) were significantly higher than control (238.0 ± 12.62 pg/mg) or co-infected (175.4 ± 8.58 pg/mg) birds. The onset of lay occurred between weeks 6–8 post-infection (pi) and Fecal corticosterone metabolite (FCM) concentrations increased in both control and co-infected birds. Antibody responses to infection were monitored in both serum and yolk samples. Salmonella Typhimurium specific antibody was lower in co-infected animals than monoinfected animals. Bacterial loads in internal organs were characterised to determine persistence. Spleen, liver and caecal tonsils were positive for bacteria in both groups, indicating that Salmonella was not cleared from the birds and internal organ colonization could serve as a reservoir for continued bacterial shedding.

Tài liệu tham khảo

Moffatt CR, Musto J, Pingault N, Miller M, Stafford R, Gregory J, Polkinghorne BG, Kirk MD (2016) Salmonella Typhimurium and outbreaks of egg-associated disease in Australia, 2001 to 2011. Foodborne Pathog Dis 13:379–385 Threlfall E, Wain J, Peters T, Lane C, De Pinna E, Little C, Wales A, Davies R (2014) Egg-borne infections of humans with salmonella: not only an S. Enteritidis problem. World Poultr Sci J 70:15–26 Chousalkar KK, Sexton M, McWhorter A, Hewson K, Martin G, Shadbolt C, Goldsmith P (2015) Salmonella Typhimurium in the Australian egg industry: multidisciplinary approach to addressing the public health challenge and future directions. Crit Rev Food Sci Nutr. doi:10.1080/10408398.2015.1113928 Williams A, Davies A, Wilson J, Marsh P, Leach S, Humphrey T (1998) Contamination of the contents of intact eggs by Salmonella Typhimurium DT104. Vet Rec 143:562–563 Okamura M, Sonobe M, Obara S, Kubo T, Nagai T, Noguchi M, Takehara K, Nakamura M (2010) Potential egg contamination by Salmonella enterica serovar Typhimurium definitive type 104 following experimental infection of pullets at the onset of lay. Poult Sci 89:1629–1634 Okamura M, Miyamoto T, Kamijima Y, Tani H, Sasai K, Baba E (2001) Differences in abilities to colonize reproductive organs and to contaminate eggs in intravaginally inoculated hens and in vitro adherences to vaginal explants between Salmonella Enteritidis and other Salmonella serovars. Avian Dis 45:962–971 Leach SA, Williams A, Davies AC, Wilson J, Marsh PD, Humphrey TJ (1999) Aerosol route enhances the contamination of intact eggs and muscle of experimentally infected laying hens by Salmonella Typhimurium DT104. FEMS Microbiol Lett 171:203–207 Borsoi A, Quinteiro-Filho WM, Calefi AS, Piantino Ferreira AJ, Astolfi-Ferreira CS, Florio JC, Palermo-Neto J (2015) Effects of cold stress and Salmonella Heidelberg infection on bacterial load and immunity of chickens. Avian Pathol 44:490–497 Quinteiro-Filho WM, Rodrigues M, Ribeiro A, Ferraz-de-Paula V, Pinheiro M, Sa L, Ferreira A, Palermo-Neto J (2012) Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute hypothalamic-pituitary-adrenal axis activation. J Anim Sci 90:1986–1994 Holt PS (1993) Effect of induced molting on the susceptibility of White Leghorn hens to a Salmonella Enteritidis infection. Avian Dis 37:412–417 Nakamura M, Nagamine N, Takahashi T, Suzuki S, Kijima M, Tamura Y, Sato S (1994) Horizontal transmission of Salmonella Enteritidis and effect of stress on shedding in laying hens. Avian Dis 38:282–288 Shini S, Kaiser P, Shini A, Bryden WL (2008) Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comp Biochem Physiol B: Biochem Mol Biol 149:324–333 Mashaly M, Hendricks G, Kalama M, Gehad A, Abbas A, Patterson P (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci 83:889–894 Quinteiro-Filho W, Gomes A, Pinheiro M, Ribeiro A, Ferraz-de-Paula V, Astolfi-Ferreira C, Ferreira A, Palermo-Neto J (2012) Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella Enteritidis. Avian Pathol 41:421–427 Gole VC, Torok V, Sexton M, Caraguel CG, Chousalkar KK (2014) Association between indoor environmental contamination by Salmonella enterica and contamination of eggs on layer farms. J Clin Microbiol 52:3250–3258 Gole VC, Caraguel CG, Sexton M, Fowler C, Chousalkar KK (2014) Shedding of Salmonella in single age caged commercial layer flock at an early stage of lay. Int J Food Microbiol 189:61–66 Pulido-Landínez M, Sanchez-Ingunza R, Guard J, Nascimento V (2013) Assignment of serotype to Salmonella enterica isolates obtained from poultry and their environment in Southern Brazil. Lett Appl Microbiol 57:288–294 Chousalkar K, Gole V, Caraguel C, Rault JL (2016) Chasing Salmonella Typhimurium in free range egg production system. Vet Microbiol 192:67–72 Glass K, Fearnley E, Hocking H, Raupach J, Veitch M, Ford L, Kirk MD (2016) Bayesian source attribution of salmonellosis in South Australia. Risk Anal 36:561–570 Doyle EM (2013) White paper on human illness caused by Salmonella from all food and non-food vectors. Update 2013 in: FRI Food Safety Reviews (Ed), Madison, pp 1-45 Guard J, Sanchez-Ingunza R, Shah DH, Rothrock MJ, Gast RK, Jones DR (2015) Recovery of Salmonella enterica serovar Enteritidis from hens initially infected with serovar Kentucky. Food Chem 189:86–92 Pulido-Landínez M, Sanchez-Ingunza R, Guard J, do Nascimento VP (2013) Presence of Salmonella Enteritidis and Salmonella Gallinarum in commercial laying hens diagnosed with fowl typhoid disease in Colombia. Avian Dis 58:165–170 Pande VV, Devon RL, Sharma P, McWhorter AR, Chousalkar KK (2016) Study of Salmonella Typhimurium infection in laying hens. Front Microbiol 7:203 USDA, U.S. Department of agriculture, food safety and inspection services (2008) most probable number procedure and tables. In: Microbiology Laboratory Guidebook. https://www.fsis.usda.gov/wps/wcm/connect/8872ec11-d6a3-4fcf-86df-4d87e57780f5/MLG-Appendix-2.pdf?MOD=AJPERES. Accessed 14 Jan 2015 Pande VV, Gole VC, McWhorter AR, Abraham S, Chousalkar KK (2015) Antimicrobial resistance of non-typhoidal Salmonella isolates from egg layer flocks and egg shells. Int J Food Microbiol 203:23–26 Akiba M, Kusumoto M, Iwata T (2011) Rapid identification of Salmonella enterica serovars, Typhimurium, Choleraesuis, Infantis, Hadar, Enteritidis, Dublin and Gallinarum, by multiplex PCR. J Microbiol Methods 85:9–15 Gole V, Chousalkar K, Roberts J (2012) Prevalence of antibodies to Mycoplasma synoviae in laying hens and possible effects on egg shell quality. Prev Vet Med 106:75–78 Greiner M, Sohr D, Gobel P (1995) A modified ROC analysis for the selection of cut-off values and the definition of intermediate results of serodiagnostic tests. J Immunol Methods 185:123–132 Dehnhard M, Schreer A, Krone O, Jewgenow K, Krause M, Grossmann R (2003) Measurement of plasma corticosterone and fecal glucocorticoid metabolites in the chicken (Gallus domesticus), the great cormorant (Phalacrocorax carbo), and the goshawk (Accipiter gentilis). Gen Comp Endocrinol 131:345–352 Rettenbacher S, Mostl E, Hackl R, Ghareeb K, Palme R (2004) Measurement of corticosterone metabolites in chicken droppings. Br Poult Sci 45:704–711 Shini S, Huff G, Shini A, Kaiser P (2010) Understanding stress-induced immunosuppression: exploration of cytokine and chemokine gene profiles in chicken peripheral leukocytes. Poult Sci 89:841–851 Gast RK, Guard-Bouldin J, Holt PS (2005) The relationship between the duration of fecal shedding and the production of contaminated eggs by laying hens infected with strains of Salmonella Enteritidis and Salmonella Heidelberg. Avian Dis 49:382–386 Chappell L, Kaiser P, Barrow P, Jones MA, Johnston C, Wigley P (2009) The immunobiology of avian systemic salmonellosis. Vet Immunol Immunopathol 128:53–59 Malorny B, Lofstrom C, Wagner M, Kramer N, Hoorfar J (2008) Enumeration of Salmonella bacteria in food and feed samples by real-time PCR for quantitative microbial risk assessment. Appl Environ Microbiol 74:1299–1304 Verbrugghe E, Dhaenens M, Leyman B, Boyen F, Shearer N, Van Parys A, Haesendonck R, Bert W, Favoreel H, Deforce D, Thompson A, Haesebrouck F, Pasmans F (2016) Host stress drives Salmonella recrudescence. Sci Rep 6:20849 Campos-Rodriguez R, Kormanovski A, Stephano AQ, Abarca-Rojano E, Berczi I, Ventura-Juarez J, Drago-Serrano ME (2012) The central nervous system modulates the immune response to Salmonella. In: Kumar Yashwant (ed) Salmonella—a diversified superbug. Intech Open Access Publisher, Croatia, pp 375–398 Rostagno M, Wesley I, Trampel D, Hurd H (2006) Salmonella prevalence in market-age turkeys on-farm and at slaughter. Poult Sci 85:1838–1842 Beal RK, Powers C, Wigley P, Barrow PA, Smith AL (2004) Temporal dynamics of the cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium. Avian Pathol 33:25–33 Gast RK, Beard CW (1990) Isolation of Salmonella enteritidis from internal organs of experimentally infected hens. Avian Dis 34:991–993 Gast RK, Beard CW (1989) Age-related changes in the persistence and pathogenicity of Salmonella Typhimurium in chicks. Poult Sci 68:1454–1460 Groves PJ, Sharpe SM, Muir WI, Pavic A, Cox JM (2016) Live and inactivated vaccine regimens against caecal Salmonella Typhimurium colonisation in laying hens. Aust Vet J 94:387–393 Gast RK (2008) Paratyphoid infections. In: Saif Y (Ed) Diseases of Poultry, 12th edn. Blackwell, Ames, pp 636–655