The degree of Salmonella gallinarum contamination in industrial poultry farms in the northwest of Iran and the pattern of antibiotic resistance and the frequency of some virulence genes

Document Type : Original Article

Authors
Masood Khakzadihe 1
Abdolkarim Zamani Moghadam 2
Mohammadreza Mahzounieh 3
1 Department of clinical sciences, Faculty of veterinary, Shahrekord university, Shahrekord, iran
2 Professor, Department of Clinical Sciences, Faculty of Veterinary, Shahrekord University, Shahrekord, Iran
3 Professor, Department of pathobiology Faculty of Veterinary, Shahrekord University, Shahrekord, Iran
10.22034/ijvcs.2024.14571.1068
Abstract
Gallinarum disease caused by Salmonella gallinarum is one of the most challenging diseases in the poultry industry. In this study, the level of Salmonella gallinarum contamination of industrial chicken flocks in northwestern Iran, antibiotic resistance and frequency of some virulence genes (msgA, spiA, pagC) were investigated and evaluated. All the samples taken from the herds with suspected clinical symptoms of salmonellosis from the clinics of East Azarbaijan, West Azarbaijan, Ardabil and Zanjan provinces were examined and confirmed by microbial culture, chemical analysis, PCR and serological methods. After confirming the diagnosis of involvement with Salmonella gallinarum, antibiotic resistance was evaluated by disking method and the abundance of virulence genes in each isolate was checked. Of the 25 isolates of Salmonella gallinarum in this study, the highest microbial resistance was reported to tetracycline (76%), oxytetracycline (72%) and the highest sensitivity to amikacin (80%) and Fozbek (72%). 100% of the isolates were resistant to at least 6 types of antibiotics. In the study of the isolates, 8% had the msgA gene, 28% had the spiA gene, and 8% had the pagC gene, of which two isolates had all three virulence genes.
Keywords
Salmonella gallinarum
virulence gene
northwestern Iran
antibiotic resistance
industrial chicken
Subjects
1.     Bahramianfard H, Derakhshandeh A, Naziri Z, Khaltabadi Farahani R. Prevalence, virulence factor and antimicrobial resistance analysis of Salmonella Enteritidis from poultry and egg samples in Iran. BMC veterinary research. 2021;17(1):196.
2.     Barrow PA, Jones MA, Smith AL, Wigley P. The long view: Salmonella–the last forty years. Avian Pathology. 2012;41(5):413-20.
3.     Chadfield MS, Brown DJ, Aabo S, Christensen JP, Olsen JE. Comparison of intestinal invasion and macrophage response of Salmonella Gallinarum and other host-adapted Salmonella enterica serovars in the avian host. Veterinary Microbiology. 2003;92(1-2):49-64.
4.     Cosby DE, Cox NA, Harrison MA, Wilson JL, Buhr RJ, Fedorka-Cray PJ. Salmonella and antimicrobial resistance in broilers: A review. Journal of Applied Poultry Research. 2015;24(3):408-26.
5.     Crichton PB, Old DC. Salmonellae of serotypes Gallinarum and Pullorum grouped by biotyping and fimbrial-gene probing. Journal of medical microbiology. 1990;32(3):145-52.
6.     Dong H, Peng D, Jiao X, Zhang X, Geng S, Liu X. Roles of the spiA gene from Salmonella enteritidis in biofilm formation and virulence. Microbiology. 2011;157(Pt 6):1798.
7.     Groisman EA, Ochman H. How Salmonella became a pathogen. Trends in microbiology. 1997;5(9):343-9.
8.     Hosseininezhad B, Berizi E, Nader M, Mazloomi SM, Hosseinzadeh S, Ebrahimi L, Zare M. Prevalence of Salmonella contamination in consumed eggs in Iran: A systematic review and meta-analysis study on published studies from 1996 to 2018. Veterinary World. 2020;13(12):2743.
9.     Huang K, Fresno AH, Skov S, Olsen JE. Dynamics and outcome of macrophage interaction between Salmonella Gallinarum, Salmonella Typhimurium, and Salmonella Dublin and macrophages from chicken and cattle. Frontiers in cellular and infection microbiology. 2020;9:420.
10.  Jones MA, Wigley P, Page KL, Hulme SD, Barrow PA. Salmonella enterica serovar Gallinarum requires the Salmonella pathogenicity island 2 type III secretion system but not the Salmonella pathogenicity island 1 type III secretion system for virulence in chickens. Infection and immunity. 2001;69(9):5471-6.
11.  Kabir SM. Avian colibacillosis and salmonellosis: a closer look at epidemiology, pathogenesis, diagnosis, control and public health concerns. International journal of environmental research and public health. 2010;7(1):89-114.
12.  Kang MS, Kim A, Jung BY, Her M, Jeong W, Cho YM, Oh JY, Lee YJ, Kwon JH, Kwon YK. Characterization of antimicrobial resistance of recent Salmonella enterica serovar Gallinarum isolates from chickens in South Korea. Avian pathology. 2010;39(3):201-5.
13.  Kim K, Yoon S, Kim YB, Lee YJ. Virulence Variation of Salmonella Gallinarum Isolates through SpvB by CRISPR Sequence Subtyping, 2014 to 2018. Animals. 2020;10(12):2346.
14.  Kipper D, Mascitti AK, De Carli S, Carneiro AM, Streck AF, Fonseca AS, Ikuta N, Lunge VR. Emergence, Dissemination and Antimicrobial Resistance of the Main Poultry-Associated Salmonella Serovars in Brazil. Veterinary Sciences. 2022;9(8):405.
15.  Langridge GC, Fookes M, Connor TR, Feltwell T, Feasey N, Parsons BN, Seth-Smith HM, Barquist L, Stedman A, Humphrey T, Wigley P. Patterns of genome evolution that have accompanied host adaptation in Salmonella. Proceedings of the National Academy of Sciences. 2015;112(3):863-8.
16.  Lee YJ, Kim KS, Kwon YK, Tak RB. Biochemical characteristics and antimicrobials susceptibility of Salmonella gallinarum isolated in Korea. Journal of veterinary science. 2003;4(2):161-6.
17.  Lu J, Li L, Pan F, Zuo G, Yu D, Liu R, Fan H, Ma Z. PagC is involved in salmonella pullorum OMVs production and affects biofilm production. Veterinary Microbiology. 2020;247:108778.
18.  Mahdavi Z, Feizi A, Anzabi Y. Evaluating the antibiotic resistance pattern of Salmonella isolated from a number of laying poultry flocks in the northwest of the country during 2021 and investigating its relationship with the performance of the mentioned farms. Veterinary Clinical Pathology. 2023;16(64).
19.  Mølbak K, Gerner-Smidt P, Wegener HC. Increasing quinolone resistance in Salmonella enterica serotype Enteritidis. Emerging infectious diseases. 2002;8(5):514.
20.  Parvej MS, Nazir KN, Rahman MB, Jahan M, Khan MF, Rahman M. Prevalence and characterization of multi-drug resistant Salmonella Enterica serovar Gallinarum biovar Pullorum and Gallinarum from chicken. Veterinary World. 2016;9(1):65.
21.  Pattison M, McMullin P, Bradbury JM, Alexander D, editors. Poultry diseases. Elsevier Health Sciences; 2007.
22.  Prouty AM, Brodsky IE, Manos J, Belas R, Falkow S, Gunn JS. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunology & Medical Microbiology. 2004;41(2):177-85.
23.  Rakov AV, Mastriani E, Liu SL, Schifferli DM. Association of Salmonella virulence factor alleles with intestinal and invasive serovars. BMC genomics. 2019;20(1):1-4.
24.  Rotger R, Casadesús J. The virulence plasmids of Salmonella. International Microbiology. 1999;2:177-84.
25.  S Khaki P, Moradi Bidhendi S, Cheraghchi N. Study on phenotypic characteristics of Salmonella gallinarum and Sallmonella pullorum isolates based on biochemical and antimicrobial susceptibility tests in Iran. Archives of Razi Institute. 2015;70(3):171-7.
26.  Sharifi-Mood B, Metanat M, Salehi M. Salmonella gallinarum empyema-the first case from Iran. Journal of Medical Sciences (Pakistan). 2006;6:180-2.
27.  Tuhin AF, Kabir SL, Amin MM, Hossain KM. Identification and Antimicrobial Susceptibility of" Salmonella" species Isolated from Washing and Rinsed Water of Broilers in Pluck Shops. International Journal of Animal and Veterinary Advances. 2013;5(1):1-8.
28.  Wales A, Lawes J. JMM Profile: Salmonella enterica serovar Gallinarum, biovars Pullorum and Gallinarum. Journal of Medical Microbiology. 2023;72(2):001653.
29.  Zhang D, Zhuang L, Wang C, Zhang P, Zhang T, Shao H, Han X, Gong J. Virulence gene distribution of Salmonella Pullorum isolates recovered from chickens in China (1953–2015). Avian diseases. 2018;62(4):431-6.
30.  Zhou X, Kang X, Zhou K, Yue M. A global dataset for prevalence of Salmonella Gallinarum between 1945 and 2021. Scientific Data. 2022;9(1):495.