Influence of heat stress on intestinal integrity and the caecal microbiota during Enterococcus cecorum infection in broilers

. 2022 Dec 16 ; 53 (1) : 110. [epub] 20221216

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu randomizované kontrolované studie veterinární, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36527124
Odkazy

PubMed 36527124
PubMed Central PMC9756510
DOI 10.1186/s13567-022-01132-y
PII: 10.1186/s13567-022-01132-y
Knihovny.cz E-zdroje

Enterococcus cecorum (EC) is one of the most relevant bacterial pathogens in modern broiler chicken production from an economic and animal welfare perspective. Although EC pathogenesis is generally well described, predisposing factors are still unknown. This study aimed to understand the effect of heat stress on the caecal microbiota, intestinal integrity, and EC pathogenesis. A total of 373 1-day-old commercial broiler chicks were randomly assigned to four groups: (1) noninoculated, thermoneutral conditions (TN); (2) noninoculated, heat stress conditions (HS); (3) EC-inoculated, thermoneutral conditions (TN + EC); and (4) EC-inoculated, heat stress conditions (HS + EC). Birds were monitored daily for clinical signs. Necropsy of 20 broilers per group was performed at 7, 14, 21, and 42 days post-hatch (dph). A trend towards enhanced and more pronounced clinical disease was observed in the EC-inoculated, heat-stressed group. EC detection rates in extraintestinal tissues via culture were higher in the HS + EC group (~19%) than in the TN + EC group (~11%). Significantly more birds were colonized by EC at 7 dph in the HS + EC group (100%) than in the TN + EC group (65%, p < 0.05). The caecal microbiota in the two EC-inoculated groups was significantly more diverse than that in the TN group (p < 0.05) at 14 dph, which may indicate an effect of EC infection. An influence of heat stress on mRNA expression of tight junction proteins in the caecum was detected at 7 dph, where all six investigated tight junction proteins were expressed at significantly lower levels in the heat stressed groups compared to the thermoneutral groups. These observations suggest that heat stress may predispose broilers to EC-associated disease and increase the severity thereof. Furthermore, heat stress may impair intestinal integrity and promote EC translocation.

Zobrazit více v PubMed

Devriese LA, Cauwerts K, Hermans K, Wood AM. Enterococcus cecorum septicemia as a cause of bone and joint lesions resulting in lameness in broiler chickens. Vlaams Diergeneeskd Tijdschr. 2002;71:219–221.

Wood AM, MacKenzie G, McGiliveray NC, Brown L, Devriese LA, Baele M. Isolation of Enterococcus cecorum from bone lesions in broiler chickens. Vet Rec. 2002;150:27. PubMed

Herdt PD, Defoort P, Steelant JV, Swam H, Tanghe L, Goethem SV, Vanrobaeys M. Enterococcus cecorum osteomyelitis and arthritis in broiler chickens. Vlaams Diergeneeskd Tijdschr. 2009;78:44–48.

Stalker MJ, Brash ML, Weisz A, Ouckama RM, Slavic D. Arthritis and osteomyelitis associated with Enterococcus cecorum infection in broiler and broiler breeder chickens in Ontario, Canada. J Vet Diagn Invest. 2010;22:643–645. PubMed

Makrai L, Nemes C, Simon A, Ivanics E, Dudas Z, Fodor L, Glavits R. Association of Enterococcus cecorum with vertebral osteomyelitis and spondylolisthesis in broiler parent chicks. Acta Vet Hung. 2011;59:11–21. PubMed

Aitchison H, Poolman P, Coetzer M, Griffiths C, Jacobs J, Meyer M, Bisschop S. Enterococcal-related vertebral osteoarthritis in South African broiler breeders: a case report. J S Afr Vet Assoc. 2014;85:1077. PubMed

Talebi A, Taifebagherlu J, Sharifi A, Delkhosh-Kasmaie F. Spondylitis in broiler breeder farms in West-Azerbaijan province, Iran: clinical report. Vet Res Forum. 2016;7:353–355. PubMed PMC

Jung A, Rautenschlein S. Comprehensive report of an Enterococcus cecorum infection in a broiler flock in Northern Germany. BMC Vet Res. 2014;10:311. PubMed PMC

Borst LB, McLamb KA, Suyemoto MM, Chen LR, Levy MG, Sarsour AH, Cordova HA, Barnes HJ, Oviedo-Rondon EO. Coinfection with Eimeria spp. decreases bacteremia and spinal lesions caused by pathogenic Enterococcus cecorum. Anim Feed Sci Technol. 2019;250:59–68.

Schreier J, Rautenschlein S, Jung A. Different virulence levels of Enterococcus cecorum strains in experimentally infected meat-type chickens. PLoS One. 2021;16:e0259904. PubMed PMC

Borst LB, Suyemoto MM, Sarsour AH, Harris MC, Martin MP, Strickland JD, Oviedo EO, Barnes HJ. Pathogenesis of enterococcal spondylitis caused by Enterococcus cecorum in broiler chickens. Vet Pathol. 2017;54:61–73. PubMed

Wideman RF., Jr Bacterial chondronecrosis with osteomyelitis and lameness in broilers: a review. Poult Sci. 2016;95:325–344. PubMed

Remiot P, Panaget G, Chataigner E, Chevalier D (2019) Enterococcus cecorum in broilers: a survey in farm to identify risky zootechnical practices. In: 13èmes Journées de la Recherche Avicole et Palmipèdes à Foie Gras, Tours, March 2019, pp 116–120

Tsiouris V, Georgopoulou I, Batzios C, Pappaioannou N, Ducatelle R, Fortomaris P. Heat stress as a predisposing factor for necrotic enteritis in broiler chicks. Avian Pathol. 2018;47:616–624. PubMed

Quinteiro-Filho WM, Gomes AV, Pinheiro ML, Ribeiro A, Ferraz-de-Paula V, Astolfi-Ferreira CS, Ferreira AJ, Palermo-Neto J. Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella Enteritidis. Avian Pathol. 2012;41:421–427. PubMed

Tang LP, Li WH, Liu YL, Lun JC, He YM. Heat stress aggravates intestinal inflammation through TLR4-NF-kappaB signaling pathway in Ma chickens infected with Escherichia coli O157:H7. Poult Sci. 2021;100:101030. PubMed PMC

Rostagno MH. Effects of heat stress on the gut health of poultry. J Anim Sci. 2020;98:skaa090. PubMed PMC

Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW, Pallen MJ. Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS One. 2014;9:e91941. PubMed PMC

Stanley D, Geier MS, Hughes RJ, Denman SE, Moore RJ. Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One. 2013;8:e84290. PubMed PMC

Zenner C, Hitch TCA, Riedel T, Wortmann E, Tiede S, Buhl EM, Abt B, Neuhaus K, Velge P, Overmann J, Kaspers B, Clavel T. Early-life immune system maturation in chickens using a synthetic community of cultured gut bacteria. mSystems. 2021;6:01300-20. PubMed PMC

Torok VA, Hughes RJ, Mikkelsen LL, Perez-Maldonado R, Balding K, MacAlpine R, Percy NJ, Ophel-Keller K. Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Appl Environ Microbiol. 2011;77:5868–5878. PubMed PMC

Richards P, Fothergill J, Bernardeau M, Wigley P. Development of the caecal microbiota in three broiler breeds. Front Vet Sci. 2019;6:201. PubMed PMC

Torok VA, Hughes RJ, Ophel-Keller K, Ali M, Macalpine R. Influence of different litter materials on cecal microbiota colonization in broiler chickens. Poult Sci. 2009;88:2474–2481. PubMed

Seidlerova Z, Kubasova T, Faldynova M, Crhanova M, Karasova D, Babak V, Rychlik I. Environmental impact on differential composition of gut microbiota in indoor chickens in commercial production and outdoor, backyard chickens. Microorganisms. 2020;8:767. PubMed PMC

Oakley BB, Vasconcelos EJR, Diniz P, Calloway KN, Richardson E, Meinersmann RJ, Cox NA, Berrang ME. The cecal microbiome of commercial broiler chickens varies significantly by season. Poult Sci. 2018;97:3635–3644. PubMed

Song J, Xiao K, Ke YL, Jiao LF, Hu CH, Diao QY, Shi B, Zou XT. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poult Sci. 2014;93:581–588. PubMed

Shi D, Bai L, Qu Q, Zhou S, Yang M, Guo S, Li Q, Liu C. Impact of gut microbiota structure in heat-stressed broilers. Poult Sci. 2019;98:2405–2413. PubMed

Zhu L, Liao R, Wu N, Zhu G, Yang C. Heat stress mediates changes in fecal microbiome and functional pathways of laying hens. Appl Microbiol Biotechnol. 2019;103:461–472. PubMed

Varasteh S, Braber S, Akbari P, Garssen J, Fink-Gremmels J. Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PLoS One. 2015;10:e0138975. PubMed PMC

Mishra B, Jha R. Oxidative stress in the poultry gut: potential challenges and interventions. Front Vet Sci. 2019;6:60. PubMed PMC

Gu XH, Hao Y, Wang XL. Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2. Intestinal oxidative stress. Poult Sci. 2012;91:790–799. PubMed

Tellez G, Jr, Tellez-Isaias G, Dridi S. Heat stress and gut health in broilers: role of tight junction proteins. Adv Food Techn Nutr Sci. 2017;3:e1–e4.

Hu YJ, Wang YD, Tan FQ, Yang WX. Regulation of paracellular permeability: factors and mechanisms. Mol Biol Rep. 2013;40:6123–6142. PubMed

Awad WA, Hess C, Hess M. Enteric pathogens and their toxin-induced disruption of the intestinal barrier through alteration of tight junctions in chickens. Toxins (Basel) 2017;9:60. PubMed PMC

Ross 308 Broiler Management Handbook. https://en.aviagen.com/brands/ross/products/ross-308. Accessed 15 Sept 2022

Schreier J, Karasova D, Crhanova M, Rychlik I, Rautenschlein S, Jung A. Influence of lincomycin-spectinomycin treatment on the outcome of Enterococcus cecorum infection and on the cecal microbiota in broilers. Gut Pathog. 2022;14:3. PubMed PMC

Mignard S, Flandrois JP. 16S rRNA sequencing in routine bacterial identification: a 30-month experiment. J Microbiol Methods. 2006;67:574–581. PubMed

Patel JB. 16S rRNA gene sequencing for bacterial pathogen identification in the clinical laboratory. Mol Diagn. 2001;6:313–321. PubMed

Wilson KH, Blitchington RB, Greene RC. Amplification of bacterial 16S ribosomal DNA with polymerase chain reaction. J Clin Microbiol. 1990;28:1942–1946. PubMed PMC

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–857. PubMed PMC

Rzeznitzeck J, Breves G, Rychlik I, Hoerr FJ, von Altrock A, Rath A, Rautenschlein S. The effect of Campylobacter jejuni and Campylobacter coli colonization on the gut morphology, functional integrity, and microbiota composition of female turkeys. Gut Pathog. 2022;14:33. PubMed PMC

von Buchholz JS, Bilic I, Aschenbach JR, Hess M, Mitra T, Awad WA. Establishment of a novel probe-based RT-qPCR approach for detection and quantification of tight junctions reveals age-related changes in the gut barriers of broiler chickens. PLoS One. 2021;16:e0248165. PubMed PMC

Mitra T, Bilic I, Hess M, Liebhart D. The 60S ribosomal protein L13 is the most preferable reference gene to investigate gene expression in selected organs from turkeys and chickens, in context of different infection models. Vet Res. 2016;47:105. PubMed PMC

Chrzastek K, Borowska D, Kaiser P, Vervelde L. Class B CpG ODN stimulation upregulates expression of TLR21 and IFN-gamma in chicken Harderian gland cells. Vet Immunol Immunopathol. 2014;160:293–299. PubMed

Benjamini Y, Hochberg Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Statist Soc B. 1995;57:289–300.

Jung A, Petersen H, Teske L, Rautenschlein S. Colonization patterns of Enterococcus cecorum in two different broiler production cycles detected with a newly developed quantitative real-time PCR. BMC Microbiol. 2017;17:106. PubMed PMC

Calefi AS, Honda BT, Costola-de-Souza C, de Siqueira A, Namazu LB, Quinteiro-Filho WM, Fonseca JG, Aloia TP, Piantino-Ferreira AJ, Palermo-Neto J. Effects of long-term heat stress in an experimental model of avian necrotic enteritis. Poult Sci. 2014;93:1344–1353. PubMed

Norup LR, Jensen KH, Jørgensen E, Sørensen P, Juul-Madsen HR. Effect of mild heat stress and mild infection pressure on immune responses to an E. coli infection in chickens. Animal. 2008;2:265–274. PubMed

Alhenaky A, Abdelqader A, Abuajamieh M, Al-Fataftah AR. The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. J Therm Biol. 2017;70:9–14. PubMed

Bartlett J, Smith M. Effects of different levels of zinc on the performance and immunocompetence of broilers under heat stress. Poult Sci. 2003;82:1580–1588. PubMed

Johnson JS. Heat stress: impact on livestock well-being and productivity and mitigation strategies to alleviate the negative effects. Anim Prod Sci. 2018;58:1404–1413.

Deeb N, Cahaner A. Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. Poult Sci. 2002;81:293–301. PubMed

Garriga C, Hunter RR, Amat C, Planas JM, Mitchell MA, Moreto M. Heat stress increases apical glucose transport in the chicken jejunum. Am J Physiol Regul Integr Comp Physiol. 2006;290:195–201. PubMed

Quinteiro-Filho WM, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sakai M, Sa LR, Ferreira AJ, Palermo-Neto J. Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult Sci. 2010;89:1905–1914. PubMed

Tabler TW, Greene ES, Orlowski SK, Hiltz JZ, Anthony NB, Dridi S. Intestinal barrier integrity in heat-stressed modern broilers and their ancestor wild jungle fowl. Front Vet Sci. 2020;7:249. PubMed PMC

Sgavioli S, Domingues C, Santos E, de Quadros T, Borges L, Garcia R, Louzada M, Boleli I. Effect of in-ovo ascorbic acid injection on the bone development of broiler chickens submitted to heat stress during incubation and rearing. Braz J Poult Sci. 2016;18:153–162.

Chen LR, Suyemoto MM, Sarsour AH, Cordova HA, Oviedo-Rondon EO, Barnes HJ, Borst LB. Prevalence and severity of osteochondrosis of the free thoracic vertebra in three modern broiler strains and the Athens Canadian Random Bred control broiler. Avian Pathol. 2018;47:152–160. PubMed

Wideman RF, Jr, Pevzner I. Dexamethasone triggers lameness associated with necrosis of the proximal tibial head and proximal femoral head in broilers. Poult Sci. 2012;91:2464–2474. PubMed

Ekesi NS, Hasan A, Parveen A, Shwani A, Rhoads DD. Embryo lethality assay as a tool for assessing virulence of isolates from bacterial chondronecrosis with osteomyelitis in broilers. Poult Sci. 2021;100:101455. PubMed PMC

Abdelqader A, Al-Fataftah AR. Thermal acclimation of broiler birds by intermittent heat exposure. J Therm Biol. 2014;39:1–5.

Jung A, Chen LR, Suyemoto MM, Barnes HJ, Borst LB. A review of Enterococcus cecorum infection in poultry. Avian Dis. 2018;62:261–271. PubMed

Logue CM, Andreasen CB, Borst LB, Eriksson H, Hampson DJ, Sanchez S, Fulton RM. Other bacterial diseases. In: Swayne DE, Boulianne M, Logue CM, McDougald LR, Venugopal N, Suarez DL, editors. Diseases of poultry. New York: Wiley; 2020.

Suyemoto MM, Barnes HJ, Borst LB. Culture methods impact recovery of antibiotic-resistant enterococci including Enterococcus cecorum from pre- and postharvest chicken. Lett Appl Microbiol. 2017;64:210–216. PubMed

Bahrndorff S, Rangstrup-Christensen L, Nordentoft S, Hald B. Foodborne disease prevention and broiler chickens with reduced Campylobacter infection. Emerg Infect Dis. 2013;19:425–430. PubMed PMC

Hankel J, Bodmann B, Todte M, Galvez E, Strowig T, Radko D, Antakli A, Visscher C. Comparison of chicken cecal microbiota after metaphylactic treatment or following administration of feed additives in a broiler farm with enterococcal spondylitis history. Pathogens. 2021;10:1068. PubMed PMC

Mohammed AA, Jiang S, Jacobs JA, Cheng HW. Effect of a synbiotic supplement on cecal microbial ecology, antioxidant status, and immune response of broiler chickens reared under heat stress. Poult Sci. 2019;98:4408–4415. PubMed

Clarke LL. A guide to Ussing chamber studies of mouse intestine. Am J Physiol Gastrointest Liver Physiol. 2009;296:1151–1166. PubMed PMC

Tellez G (2020) Effects of a noni-supplemented diet on intestinal tight junction proteins and stress biomarkers in heat-stressed broiler chickens. Bachelor Thesis. University of Arkansas

Santos RR, Awati A, Roubos-van den Hil PJ, van Kempen T, Tersteeg-Zijderveld MHG, Koolmees PA, Smits C, Fink-Gremmels J. Effects of a feed additive blend on broilers challenged with heat stress. Avian Pathol. 2019;48:582–601. PubMed

Proszkowiec-Weglarz M, Schreier LL, Kahl S, Miska KB, Russell B, Elsasser TH. Effect of delayed feeding post-hatch on expression of tight junction- and gut barrier-related genes in the small intestine of broiler chickens during neonatal development. Poult Sci. 2020;99:4714–4729. PubMed PMC

Park I, Lee Y, Goo D, Zimmerman NP, Smith AH, Rehberger T, Lillehoj HS. The effects of dietary Bacillus subtilis supplementation, as an alternative to antibiotics, on growth performance, intestinal immunity, and epithelial barrier integrity in broiler chickens infected with Eimeria maxima. Poult Sci. 2020;99:725–733. PubMed PMC

Stefanello C, Rosa DP, Dalmoro YK, Segatto AL, Vieira MS, Moraes ML, Santin E. Protected blend of organic acids and essential oils improves growth performance, nutrient digestibility, and intestinal health of broiler chickens undergoing an intestinal challenge. Front Vet Sci. 2019;6:491. PubMed PMC

Cheng YF, Chen YP, Chen R, Su Y, Zhang RQ, He QF, Wang K, Wen C, Zhou YM. Dietary mannan oligosaccharide ameliorates cyclic heat stress-induced damages on intestinal oxidative status and barrier integrity of broilers. Poult Sci. 2019;98:4767–4776. PubMed

Macelline SP, Wickramasuriya SS, Cho HM, Kim E, Shin TK, Hong JS, Kim JC, Pluske JR, Choi HJ, Hong YG, Heo JM. Broilers fed a low protein diet supplemented with synthetic amino acids maintained growth performance and retained intestinal integrity while reducing nitrogen excretion when raised under poor sanitary conditions. Poult Sci. 2020;99:949–958. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...