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Salmonella enterica serovars linked with poultry in India: antibiotic resistance profiles and carriage of virulence genes

  • Veterinary Microbiology - Research Paper
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Abstract

Salmonella is an important poultry pathogen with zoonotic potential. Being a foodborne pathogen, Salmonella-contaminated poultry products can act as the major source of infection in humans. In India, limited studies have addressed the diversity of Salmonella strains of poultry origin. This study represented 26 strains belonging to Salmonella serovars Typhimurium, Infantis, Virchow, Kentucky, and Agona. The strains were tested for resistance to 14 different antimicrobial agents using the Kirby-Bauer disk-diffusion assay. The presence of the invA, hilA, agfA, lpfA, sopE, and spvC virulence genes was assessed by polymerase chain reaction (PCR), and the genetic diversity was assessed by Enterobacterial Repetitive Intergenic Consensus Polymerase Chain Reaction (ERIC-PCR). The highest resistance to tetracycline (n = 17; 65.38%) followed by nalidixic acid (n = 16; 61.53%) was detected among the strains. Among the strains (n = 17) phenotypically resistant to tetracycline, 94% (n = 16) were also positive for the tetA gene. Based on the presence of virulence genes, the strains were characterized into three virulence profiles (PI, P2, and P3). Among the investigated virulence genes, invA, hilA, agfA, and lpfA were present in all strains. The sopE gene was mostly associated with serovars Virchow (n = 3; 100%) and Typhimurium (n = 8; 80%), whereas spvC gene was exclusive for two Typhimurium strains that lacked sopE gene. ERIC-PCR profiling indicated clusters correlating their serovar, geographical, and farm origins. These results demonstrate that Salmonella isolates with a wide genetic range, antibiotic resistance, and virulence characteristics can colonize poultry. The presence of such strains is crucial for both food safety and public health.

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Data availability

The data that support the findings of this study are available on request from the corresponding author.

Abbreviations

NTS:

Non-typhoidal Salmonella

ERIC-PCR:

Enterobacterial Repetitive Intergenic Consensus PCR

AMR:

Antimicrobial resistance

MDR:

Multidrug-resistant

References

  1. Jain P, Chowdhury G, Samajpati S, Basak S, Ganai A, Samanta S, Okamoto K, Mukhopadhyay AK, Dutta S (2020) Characterization of non-typhoidal Salmonella isolates from children with acute gastroenteritis, Kolkata, India, during 2000-2016. Braz J Microbiol 51(2):613–627. https://doi.org/10.1007/s42770-019-00213-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Mahindroo J, Thanh DP, Nguyen TNT, Mohan B, Thakur S, Baker S, Taneja N (2019) Endemic fluoroquinolone-resistant Salmonella enterica serovar Kentucky ST198 in northern India. Microb Genom. https://doi.org/10.1099/mgen.0.000275

  3. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J, Grimont PA, Weill FX (2010) Supplement 2003-2007 (No. 47) to the White-Kauffmann-Le Minor scheme. ResMicrobiol 161(1):26–29. https://doi.org/10.1016/j.resmic.2009.10.002

    Article  Google Scholar 

  4. Jajere SM (2019) A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. VetWorld 12(4):504–521. https://doi.org/10.14202/vetworld.2019.504-521

    Article  CAS  Google Scholar 

  5. Bhardwaj DK, Taneja NK, Taneja P, Patel P (2022) Phenotypic and genotypic characterization of multi-drug resistant, biofilm forming, human invasive strain of Salmonella Typhimurium SMC25 isolated from poultry meat in India. Microb Pathog 173(Pt A):105830. https://doi.org/10.1016/j.micpath.2022.105830

    Article  CAS  PubMed  Google Scholar 

  6. Haubert L, Maia DSV, Rauber Würfel SDF, Vaniel C, da Silva WP (2022) Virulence genes and sanitizers resistance in Salmonella isolates from eggs in southern Brazil. J Food Sci Technol 59(3). https://doi.org/10.1007/s13197-021-05113-5

  7. Li S, He Y, Mann DA et al (2021) Global spread of Salmonella Enteritidis via centralized sourcing and international trade of poultry breeding stocks. Nat Commun 12:5109. https://doi.org/10.1038/s41467-021-25319-7

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  8. Cai LL, Xie YT, Hu HJ, Xu XL, Wang HH, Zhou GH (2023) A small RNA, SaaS, promotes Salmonella pathogenicity by regulating invasion, intracellular growth, and virulence factors. Microbiology Spectrum 11(1):e02938–e02922. https://doi.org/10.1128/spectrum.02938-22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Choi J, Groisman EA (2016) Acidic pH sensing in the bacterial cytoplasm is required for Salmonella virulence. Mol Microbiol 101(6):1024–1038. https://doi.org/10.1111/mmi.13439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Masud S, van der Burg L, Storm L, Prajsnar TK, Meijer AH (2019) Rubicon-dependent Lc3 recruitment to Salmonella-containing phagosomes is a host defense mechanism triggered independently from major bacterial virulence factors. Front Cell Infect Microbiol 2(9):279. https://doi.org/10.3389/fcimb.2019.00279

    Article  CAS  Google Scholar 

  11. Siddiky NA, Sarker MS, Khan MSR, Begum R, Kabir ME, Karim MR, Rahman MT, Mahmud A, Samad MA (2021) Virulence and antimicrobial resistance profiles of Salmonella enterica serovars isolated from chicken at wet markets in Dhaka, Bangladesh. Microorganisms 9(5):952. https://doi.org/10.3390/microorganisms9050952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mohanapriya HA, Anbazhagan S, Khawaskar D, Jayakumar V, Lalrinzuala MV, Himani KM, Sophia I, Mariappan AK, Abhishek VKN, Sinha DK, Chaudhuri P, Chaturvedi VK, Singh BR, Thomas P (2023) Development and validation of multiplex PCR based molecular serotyping of Salmonella serovars associated with poultryinIndia. J Microbiol Methods 207:106710. https://doi.org/10.1016/j.mimet.2023.106710

    Article  CAS  PubMed  Google Scholar 

  13. Kumar Y, Singh V, Kumar G, Gupta NK, Tahlan AK (2019) Serovar diversity of Salmonella among poultry. Indian J Med Res 150:92–95. https://doi.org/10.4103/ijmr.ijmr_1798_17

    Article  PubMed  PubMed Central  Google Scholar 

  14. Shivaning Karabasanavar N, Benakabhat Madhavaprasad C, Agalagandi Gopalakrishna S, Hiremath J, Shivanagowda Patil G, Barbuddhe B (2020) Prevalence of Salmonella serotypes S. Enteritidis and S. Typhimurium in poultry and poultry products. J Food Saf 40:e12852. https://doi.org/10.1111/jfs.12852

    Article  CAS  Google Scholar 

  15. Singh A, Singh M, Malik MA, Padha S (2023) Is there a shift in Salmonella diversity among poultry in Northern India? Avian Dis 67(1):108–113. https://doi.org/10.1111/jfs.12852

    Article  CAS  PubMed  Google Scholar 

  16. Ramakant Sahu, Poornima Saxena  (2014) Antibiotica in Meat, Investigator Center fo Science Envairoment pollution Monitoring Laboratory, New Delhi - 110062

  17. Versalovic J, Koeuth T, Lupski R (1991a) Distribution of repetitive DNA sequences in eubacteria and application to finger printing of bacterial genomes. Nucleic Acids Res 19(24):6823–6831. https://doi.org/10.1093/nar/19.24.6823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Soares LSG, Casella T, Kawagoe EK, Benetti Filho V, Omori WP, Nogueira MCL, Wagner G, de Oliveira RR, Stahlhofer SR, Ferreira FA, Tondo EC (2023) Phenotypic and genotypic characterization of antibiotic resistance of Salmonella Heidelberg in the south of Brazil. Int J Food Microbiol 391:110151. https://doi.org/10.1016/j.ijfoodmicro.2023.110151

    Article  CAS  Google Scholar 

  19. Xu Z, Wang M, Wang C, Zhou C, Liang J, Gu G, Wang M, Wei P (2021) The emergence of extended-spectrum β-lactamase (ESBL)-producing Salmonella London isolates from human patients, retail meats and chickens in southern China and the evaluation of the potential risk factors of Salmonella London. Food Control 128:108187. https://doi.org/10.1016/j.foodcont.2021.108187

    Article  CAS  Google Scholar 

  20. Grimont PA, Weill FX, (2007) Antigenic formulae of the Salmonella serovars. WHO collaborating centre for reference and research on Salmonella, vol 9, pp. 1–166

  21. Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45(4):493–496

    Article  CAS  PubMed  Google Scholar 

  22. CLSI (2018) Performance standards for antimicrobial susceptibility testing, 28th edn. CLSI supplement M100. Clinical and Laboratory Standards Institute, Wayne

  23. Akpaka PE, Vaillant A, Wilson C, Jayaratne P (2021) Extended spectrum beta-lactamase (ESBL) produced by Gram-negative bacteria in Trinidad and Tobago. Int J Microbiol 2021. https://doi.org/10.1155/2021/5582755

  24. Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60(2):394–397. https://doi.org/10.1093/jac/dkm204

    Article  CAS  PubMed  Google Scholar 

  25. Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53(2):603–608. https://doi.org/10.1128/aac.00997-08

    Article  CAS  PubMed  Google Scholar 

  26. Ciesielczuk H, Hornsey M, Choi V, Woodford N, Wareham DW (2013) Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J Med Microbiol 62(12):1823–1827. https://doi.org/10.1099/jmm.0.064428-0

    Article  CAS  PubMed  Google Scholar 

  27. Wareham DW, Umoren I, Khanna P, Gordon NC (2010) Allele-specific polymerase chain reaction (PCR) for rapid detection of the aac (6′)-Ib-cr quinolone resistance gene. Int J Antimicrob Agents 36(5):476–477. https://doi.org/10.1016/j.ijantimicag.2010.07.012

    Article  CAS  PubMed  Google Scholar 

  28. Yamane K, Wachino JI, Suzuki S, Arakawa Y (2008) Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob Agents Chemother 52(4):1564–1566. https://doi.org/10.1128/aac.01137-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fonseca EL, Mykytczuk OL, Asensi MD, Reis EM, Ferraz LR, Paula FL, Ng LK, Rodrigues DP (2006) Clonality and antimicrobial resistance gene profiles of multidrug-resistant Salmonella enterica serovar Infantis isolates from four public hospitals in Rio de Janeiro. Brazil J Clin Microbiol 44(8):2767–2772. https://doi.org/10.1128/jcm.01916-05

    Article  CAS  PubMed  Google Scholar 

  30. Huovinen P, Sundström L, Swedberg G, Sköld OJAA (1995) Trimethoprim and sulfonamide resistance. Antimicrob Agents Chemother 39(2):279–289. https://doi.org/10.1128/aac.39.2.279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bäumler AJ, Heffron F (1995) Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella Typhimurium. J Bacteriol 177(8):2087–2097. https://doi.org/10.1128/jb.177.8.2087-2097.1995

    Article  PubMed  PubMed Central  Google Scholar 

  32. Chiu CH, Ou JT (1996) Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. J Clin Microbiol 34(10):2619–2622. https://doi.org/10.1128/jcm.34.10.2619-2622.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Guo X, Chen J, Beuchat LR, Brackett RE (2000) PCR detection of Salmonella enterica serotype Montevideo in and on raw tomatoes using primers derived from hilA. Appl Environ Microbiol 66(12):5248–5252. https://doi.org/10.1128/AEM.66.12.5248-5252.2000

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  34. Prager R, Rabsch W, Streckel W, Voigt W, Tietze E, Tschäpe H (2003) Molecular properties of Salmonella enterica serotype Paratyphi B distinguish between its systemic and its enteric pathovars. J Clin Microbiol 41(9):4270–4278. https://doi.org/10.1128/jcm.41.9.4270-4278.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Swamy SC, Barnhart HM, Lee MD, Dreesen DW (1996) Virulence determinants invA and spvC in salmonellae isolated from poultry products, wastewater, and human sources. Appl Environ Microbiol 62(10):3768–3771. https://doi.org/10.1128/aem.62.10.3768-3771.1996

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  36. Versalovic J, Koeuth T, Lupski R (1991b) Distribution of repetitive DNA sequences in eubacteria and application to fingerpriting of bacterial genomes. Nucleic Acids Res 19(24):6823–6831. https://doi.org/10.1093/nar/19.24.6823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kim JS, Lee GG, Park JS, Jung YH, Kwak HS, Kim SB, Nam YS, Kwon ST (2007) A novel multiplex PCR assay for rapid and simultaneous detection of five pathogenic bacteria: Escherichia coli O157:H7, Salmonella, Staphylococcus aureus, Listeria monocytogenes, and Vibrio parahaemolyticus. J Food Prot 70(7):1656–1662. https://doi.org/10.4315/0362-028x-70.7.1656

    Article  CAS  PubMed  Google Scholar 

  38. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM, International Collaboration on Enteric Disease “Burden of Illness” Studies (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50(6):882–889

    Article  PubMed  Google Scholar 

  39. Kumar S, Kumar Y, Kumar G, Kumar G, Tahlan AK (2022) Non-typhoidal Salmonella infections across India: emergence of a neglected group of enteric pathogens. J Taibah Univ Med Sci 17(5):747–754. https://doi.org/10.1016/j.jtumed.2019.03.003

    Article  PubMed  PubMed Central  Google Scholar 

  40. Eng S-K, Pusparajah P, Mutalib N-SA, Ser H-L, Chan K-G, Lee L-H (2015) Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci 8(3):284–293. https://doi.org/10.1080/21553769.2015.1051243

    Article  CAS  Google Scholar 

  41. Inbaraj S, Agrawal RK, Thomas P, Mohan C, Agarwal RKS, Verma MR, Chaudhuri P (2022) Antimicrobial resistance in Indian isolates of non typhoidal Salmonella of livestock, poultry and environmental origin from 1990 to 2017. Comp Immunol Microbiol Infect Dis 80:101719. https://doi.org/10.1016/j.cimid.2021.101719

    Article  CAS  PubMed  Google Scholar 

  42. Mir IA, Kashyap SK, Maherchandani S (2015) Isolation, serotype diversity and antibiogram of Salmonella enterica isolated from different species of poultry in India. Asian Pac J Trop Biomed 5(7):561–567. https://doi.org/10.1016/j.apjtb.2015.03.010

    Article  CAS  Google Scholar 

  43. Sharma J, Kumar D, Hussain S, Pathak A, Shukla M, Kumar VP, Anisha PN, Rautela R, Upadhyay AK, Singh SP (2019) Prevalence, antimicrobial resistance and virulence genes characterization of nontyphoidal Salmonella isolated from retail chicken meat shops in Northern India. Food Control 102:104–111. https://doi.org/10.1016/j.foodcont.2019.01.021

    Article  CAS  Google Scholar 

  44. Waghamare RN, Paturkar AM, Vaidya VM, Zende RJ, Dubal ZN, Dwivedi A, Gaikwad RV (2018) Phenotypic and genotypic drug resistance profile of Salmonella serovars isolated from poultry farm and processing units located in and around Mumbai city, India. Veterinary world 11(12):1682. https://doi.org/10.14202/vetworld.2018.1682-1688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zishiri OT, Mkhize N, Mukaratirwa S (2016) Prevalence of virulence and antimicrobial resistance genes in Salmonella spp. isolated from commercial chickens and human clinical isolates from South Africa and Brazil. Onderstepoort J Vet Res 83(1):1–11. https://doi.org/10.4102/ojvr.v83i1.1067

    Article  CAS  Google Scholar 

  46. Pavelquesi SLS, de Oliveira Ferreira ACA, Rodrigues ARM, de Souza Silva CM, Orsi DC, da Silva ICR (2021) Presence of tetracycline and sulfonamide resistance genes in Salmonella spp.: literature review. Antibiotics (Basel, Switzerland) 10. https://doi.org/10.3390/antibiotics10111314

  47. Dimitrov T, Udo EE, Albaksami O, Kilani AA, Shehab E-DMR (2007) Ciprofloxacin treatment failure in a case of typhoid fever caused by Salmonella enterica serotype Paratyphi A with reduced susceptibility to ciprofloxacin. J Med Microbiol 56(2):277–279. https://doi.org/10.1099/jmm.0.46773-0

    Article  CAS  PubMed  Google Scholar 

  48. Stevenson JE, Gay K, Barrett TJ, Medalla F, Chiller TM, Angulo FJ (2007) Increase in nalidixic acid resistance among non-typhi Salmonella enterica isolates in the United States from 1996 to 2003. Antimicrob Agents Chemother 51(1):195–197. https://doi.org/10.1128/aac.00222-06

    Article  CAS  PubMed  Google Scholar 

  49. Kumar SG, Adithan C, Harish BN, Sujatha S, Roy G, Malini A (2013) Antimicrobial resistance in India: a review. J Nat Sci Biol Med 4(2):286–291. https://doi.org/10.4103/0976-9668.116970

    Article  PubMed  PubMed Central  Google Scholar 

  50. Jacob JJ, Solaimalai D, Muthuirulandi Sethuvel DP, Rachel T, Jeslin P, Anandan S, Veeraraghavan B (2020) A nineteen-year report of serotype and antimicrobial susceptibility of enteric non-typhoidal Salmonella from humans in Southern India: changing facades of taxonomy and resistance trend. Gut Pathog 23(12):49. https://doi.org/10.1186/s13099-020-00388-z

    Article  CAS  Google Scholar 

  51. Bangera SR, Umakanth S, Chowdhury G, Saha RN, Mukhopadhyay AK, Ballal M (2019) Poultry: a receptacle for non-typhoidal Salmonellae and antimicrobial resistance. Iran J Microbiol 11:31–38

    PubMed  PubMed Central  Google Scholar 

  52. Brower CH, Mandal S, Hayer S, Sran M, Zehra A, Patel SJ, Kaur R, Chatterjee L, Mishra S, Das BR, Singh P, Singh R, Gill JPS, Laxminarayan R (2017) The prevalence of extended-spectrum beta-lactamase-producing multidrug-resistant Escherichia coli in poultry chickens and variation according to farming practices in Punjab. India Environ Health Perspect 125:077015

    Article  PubMed  Google Scholar 

  53. Jibril AH, Okeke IN, Dalsgaard A, Olsen JE (2021) Association between antimicrobial usage and resistance in Salmonella from poultry farms in Nigeria. BMC Vet Res 17(1):234. https://doi.org/10.1186/s12917-021-02938-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Borges KA, Furian TQ, Borsoi A, Moraes HL, Salle CT, Nascimento VP (2013) Detection of virulence-associated genes in Salmonella Enteritidis isolates from chicken in South of Brazil. Pesqui Vet Bras 33:1416–1422. https://doi.org/10.1590/S0100-736X2013001200004

    Article  Google Scholar 

  55. Wagner C, Hensel M (2011) Adhesive mechanisms of Salmonella enterica. Bacterial Adhesion: Chem, Biol Phys:17–34. https://doi.org/10.1007/978-94-007-0940-9_2

  56. Yoo AY, Yu JE, Yoo H, Lee TH, Lee WH, Oh JI, Kang HY (2013) Role of sigma factor E in regulation of Salmonella Agf expression. Biochem Biophys Res Commun 430(1):131–136. https://doi.org/10.1016/j.bbrc.2012.11.025

    Article  CAS  PubMed  Google Scholar 

  57. Mendonça EP, Melo RT, Oliveira MR, Monteiro GP, Peres PA, Fonseca BB, Giombelli A, Rossi DA (2020) Characteristics of virulence, resistance and genetic diversity of strains of Salmonella Infantis isolated from broiler chicken in Brazil. Pesqui Vet Bras 40:29–38. https://doi.org/10.1590/1678-5150-pvb-5546

    Article  Google Scholar 

  58. Zuo L, Zhou L, Wu C, Wang Y, Li Y, Huang R, Wu S (2020) Salmonella spvC gene inhibits pyroptosis and intestinal inflammation to aggravate systemic infection in mice. Front Microbiol 11:562491. https://doi.org/10.3389/fmicb.2020.562491

    Article  PubMed  PubMed Central  Google Scholar 

  59. Choudhury M, Borah P, Sarma HK, Barkalita LM, Deka NK, Hussain I, Hussain MI (2016) Multiplex-PCR assay for detection of some major virulence genes of Salmonella enterica serovars from diverse sources. Curr Sci 111(7):1252–1258. https://doi.org/10.2307/24909136

    Article  CAS  Google Scholar 

  60. Kumar N, Mohan K, Georges K, Dziva F, Adesiyun AA (2021) Occurrence of virulence and resistance genes in Salmonella in cloacae of slaughtered chickens and ducks at pluck shops in Trinidad. J Food Prot 84(1):39–46. https://doi.org/10.4315/JFP-20-203

    Article  CAS  PubMed  Google Scholar 

  61. Proroga YTR, Mancusi A, Peruzy MF et al (2019) Characterization of Salmonella Typhimurium and its monophasic variant 1,4, [5],12:i:- isolated from different sources. Folia Microbiol 64:711–718. https://doi.org/10.1007/s12223-019-00683-6

    Article  CAS  Google Scholar 

  62. de Souza AI, de Freitas Neto OC, Batista DF, Estupinan AL, de Almeida AM, Barrow PA, Berchieri A (2015) ERIC-PCR genotyping of field isolates of Salmonella enterica subsp. enterica serovar Gallinarum biovars Gallinarum and Pullorum. Avian pathol : J WVPA 44:475–479. https://doi.org/10.1080/03079457.2015.1086975

    Article  Google Scholar 

  63. Fendri I, Ben Hassena A, Grosset N, Barkallah M, Khannous L, Chuat V, Gautier M, Gdoura R (2013) Genetic diversity of food-isolated Salmonella strains through pulsed field gel electrophoresis (PFGE) and enterobacterial repetitive intergenic consensus (ERIC-PCR). PLoS One 8:e81315. https://doi.org/10.1371/journal.pone.0081315

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

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Financial support received from Director, ICAR-IVRI, Izatnagar is gratefully acknowledged.

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  1. ICAR- Indian Veterinary Research Institute, Izatnagar, Bareilly, Uttar Pradesh, 243122, India

    Dengam Geyi, Prasad Thomas, Lakshmi Prakasan, Yancy M. Issac, Sonu S. Nair, Sophia Inbaraj, Suman Kumar, Asok K. Mariappan,  Abhishek, Vinod K. Chaturvedi & Premanshu Dandapat

  2. Sher-e-Kashmir University of Agricultural Sciences and Technology of Jammu, Ranbir Singh Pura, Jammu, 181102, India

    Arvinderpal Singh

  3. Centre for One Health, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana, Punjab, 141004, India

    Maninder Singh

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  1. Dengam Geyi
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Contributions

DG and PT conceptualized and designed the study. DG, YMI, and AS carried out strain isolation and culturing. AKM carried out postmortem examination and sampling. DG, LP, SI and SN carried out AMR studies and virulence profiling. AB and PT carried out serotyping. SK generated ERIC profiles. PT and VC supervised the study. DG, LP, MS, PD, and PT wrote the manuscript. All authors contributed to manuscript revision and read and approved the submitted version.

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Correspondence to Prasad Thomas.

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Geyi, D., Thomas, P., Prakasan, L. et al. Salmonella enterica serovars linked with poultry in India: antibiotic resistance profiles and carriage of virulence genes. Braz J Microbiol 55, 969–979 (2024). https://doi.org/10.1007/s42770-024-01252-x

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