Document Type : Original Article

Authors

1 Department of Microbiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

2 DVM Graduate, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

3 Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

Abstract

Salmonellosis is one of the most important bacterial diseases in human and animals. Rapid diagnosis and sub sequence accurate treatment of Salmonella carriers help reduce the salmonellosis in human and livestock animals. In this study, 420 fecal samples were taken during year 2019 from buffalo in the Urmia, Khoy and Piranshahr regions in west Azerbaijan province, Iran. Samplings were carried out in different seasons. Presence of Salmonella invasion genes (FimA, Stn and InvA) were evaluated by polymerase chain reaction. The bacterial culture and biochemical tests were performed on feces samples for isolation of bacterium Salmonella; however, all samples were negative in culture method. PCR findings showed that, 50 (11.90%) fecal samples were positive to the genes. The analysis of results showed that frequency of salmonellosis outbreak in different parts of west Azerbaijan province followed a similar pattern and the incidence of salmonellosis according to forecast in the warm seasons (spring and summer) was more than in cold seasons (autumn and winter). The prevalence of Salmonella in buffalo’s feces based on warm and cold seasons were 32 (64.00%) and 18 (36.00%), respectively. The results showed significant difference between cold and warm season in the prevalence of salmonellosis. Therefore, the application of molecular technics is essential for the prevention and treatment of salmonellosis. The results also showed that specificity of PCR method was better than culture method for detection of Salmonella in feces sample.

Keywords

  1. Ahmadi M, Dalirnaghadeh B, Shirzad Aski H, et al. Comparison of polymerase chain reaction (PCR) and conventional cultivation methods for detection of carriers of Salmonella spp. in cattle and buffalo. Comp Clin Pathol 2009; 19(3): 251-255.
  2. Oloya J, Theis M, Doetkott D, et al. Evaluation of Salmonella occurrence in domestic animal and humans in North Dakota. Foodborne Pathog Dis 2007; 4(4): 551-563.
  3. Zha L, Garrett S, Sun J. Salmonella infection in chronic inflammation and gastrointestinal cancer. Diseases 2019; 7(1): 28. doi: 10.3390/diseases7010028.
  4. Lanzas C, Davies K, Erwin S, et al. On modelling environmentally transmitted pathogens. Interface Focus 2020; 10(1): 20190056. doi: 10.1098/rsfs. 2019.0056.
  5. Dong N, Li Y, Zhao J, et al. The phenotypic and molecular characteristics of antimicrobial resistance of Salmonella enterica enterica serovar Typhimurium in Henan Province, China. BMC Infect Dis 2020; 20(1): 511. doi: 10.1186/s12879-020-05203-3.
  6. Newell DG, Koopmans M, Verhoef L, et al. Food-borne diseases - the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol 2010;139 Suppl 1: S3-S15.
  7. Majowicz SE, Musto J, Scallan E, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50(6): 882-889.
  8. L Plym F, Wierup M. Salmonella contamination: a significant challenge to the global marketing of animal food products. Rev Sci Tech 2006; 25(2): 541-544.
  9. Kortman GA, Boleij A, Swinkels DW, et al. Iron availability increases the pathogenic potential of Salmonella typhimurium and other enteric pathogens at the intestinal epithelial interface. PloS One 2012; 7(1): e29968. doi: 10.1371/journal.pone.0029968.
  10. Gilchrist JJ, MacLennan CA, Hill AV. Genetic susceptibility to invasive Salmonella disease. Nat Rev Immunol 2015; 15(7): 452-463.
  11. Makendi C, Page AJ, Wren BW, et al. A phylogenetic and phenotypic analysis of Salmonella enterica serovar weltevreden, an emerging agent of diarrheal disease in tropical regions. PLoS Negl Trop Dis 2016; 10(2): e0004446. doi: 10.1371/journal.pntd.0004446.
  12. Ehuwa O, Jaiswal AK, Jaiswl S. Salmonella, food safety and food handling practices. Foods 2021; 10(5): 907. doi: 10.3390/foods10050907.
  13. Alexandre DL, Melo AMA, Furtado RF, et al. A rapid and specific biosensor for Salmonella typhimurium detection in milk. Food Bioprocess Technol 2018; 11(4): 748-756.
  14. Revolledo L, Ferreira AJ. Salmonella antibiotic-mutant strains reduce fecal shedding and organ invasion in broiler chicks. Poult Sci 2010; 89(10): 2130-2140.
  15. Liaquat S, Sarwar Y, Ali A, et al. Virulotyping of Salmonella enterica serovar Typhi isolates from Pakistan: Absence of complete SPI-10 in Vi negative isolates. PLoS Negl Trop Dis 2018; 12(11): e0006839. doi: 10.1371/journal.pntd.0006839.
  16. Borriello G, Lucibelli MG, Pesciaroli M, et al. Diversity of Salmonella spp. serovars isolated from the intestines of water buffalo calves with gastroenteritis. BMC Vet Res 2012; 8: 201. doi: 10.1186/1746-6148-8-201.
  17. Cheng RA, Eade CR, Wiedmann M. Embracing diversity: differences in virulence mechanisms, disease severity, and host adaptations contribute to the success of nontyphoidal Salmonella as a foodborne pathogen. Front Microbiol 2019; 10: 1368. doi: 10.3389/ fmicb.2019.01368.
  18. Li X, Singh N, Beshearse E, et al. Spatial epidemiology of Salmonellosis in Florida, 2009- 2018. Front Public Health 2021; 8: doi: 10.3389/fpubh. 2020.603005.
  19. Cummings KJ, Warnick LD, Alexander KA, et al. The incidence of salmonellosis among dairy herds in the northeastern United States. J Dairy Sci 2009; 92(8): 3766-3774.
  20. Quan G, Xia P, Zhao J, et al. Fimbriae and related receptors for Salmonella Enteritidis. Microb Pathog 2019; 126: 357-362.
  21. Rahman MT, Sobur MA, Islam MS, et al. Zoonotic diseases: etiology, impact, and control. Micro-organisms. 2020; 8(9): 1405. doi: 10.3390/microorganisms8091405.
  22. MacLennan CA, Martin LB, Micoli F. Vaccines against invasive Salmonella disease: current status and future directions. Hum Vaccin Immunother 2014: 10(6): 1478-1493.
  23. Humphries RM, Linscott AJ. Practical guidance for clinical microbiology laboratories: diagnosis of bacterial gastroenteritis. Clin Microbiol Rev 2015; 28(1): 3-31.
  24. Lee KM, Runyon M, Herrman TJ, et al. Review of Salmonella detection and identification methods: aspects of rapid emergency response and food safety. Food Control 2015; 47: 264-276.
  25. Park SH, Aydin M, Khatiwara A, et al. Current and emerging technologies for rapid detection and characterization of Salmonella in poultry and poultry products. Food Microbiol 2014; 38: 250-262.
  26. Aguilera-Herce J, Zarkani AA, Schikora A, et al. Dual expression of the Salmonella effector SrtJ in mammalian cells and plants. Front Microbiol 2017; 8: 2410. doi: 10.3389/fmicb.2017.02410..
  27. Zahran R., El-Behiry A. Prevalence, molecular identification and virulence attributes of Salmonella serovars isolated from feces of diarrheic cow and buffalo-calves. Int J Curr Microbiol App Sci, 2014; 3(11): 9-27.
  28. Hassanain NA. Detection of antibodies against zoonotic food borne pathogens in sera of food handlers. Glob Vet 2008; 2: 285-289.
  29. Aydin F, Umur S, Gokce G, et al. Isolation and identification of bacterial and parasitic agents from diarrheal calves in Kars region [Turkish]. Kafkas Univ Vet Med J 2001; 7(1): 7-14.
  30. Hume ME, Edrington TS, Looper ML, et al. Salmonella genotype diversity in non-lactating and lactating dairy cows. J Food Prot 2004; 67(10): 2280-2283.
  31. Mohamed ON, Farid AF, Abaza AF, et al. Fecal shedding of non-typhoidal Salmonella species in dairy cattle and their attendants in Alexandria Suburbs. J Am Sci 2011; 7(9): 623-631.
  32. Enticott G. Risking the rural: nature, morality and the consumption of unpasteurized milk. J Rural Stud 2003; 19(4): 411-424.
  33. Bell RL, Jarvis KG, Ottesen AR, et al. Recent and emerging innovations in Salmonella detection: a food and environmental perspective. Microb Biotechnol 2016; 9(3): 279-292.
  34. Rahn K, De Grandis SA, Clarke RC, et al. Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Mol Cell Probes 1992; 6(4): 271-279.
  35. Malorny B, Hoorfar J, Bunge C, et al. Multicenter validation of the analytical accuracy of Salmonella PCR: towards an international standard. Appl Environ Microbiol 2003; 69(1): 290-296.
  36. Cabral JPS. Water microbiology. Bacterial pathogens and water. Int J Environ Res Public Health 2010; 7(10): 3657-3703.
  37. Lin JS, Tsen HY. Development and use of polymerase chain reaction for the specific detection of Salmonella Typhimurium in stool and food samples. J Food Prot 1999; 62(10): 1103-1110.
  38. Salehi TZ, Badouei MA, Madadgar O, et al. Shepherd dogs as a common source for Salmonella enterica serovar Reading in Garmsar, Iran. Turk J Vet Anim Sci 2013; 37(1): 102-105.
  39. Cohen HJ, Mechanda SM, Lin W. PCR amplification of the fimA gene sequence of Salmonella typhimurium, a specific method for detection of Salmonella spp. Appl Environ Microbiol 1996; 62(12): 4303-4308.
  40. Feder I, Nietfeld JC, Galland J, et al. Comparison of cultivation and PCR-hybridization for detection of Salmonella in porcine fecal and water samples. J Clin Microbiol 2001; 39(7): 2477-2484.
  41. Chaudhary JH, Nayak JB, Brahmbhatt MN, et al. Virulence genes detection of Salmonella serovars isolated from pork and slaughterhouse environment in Ahmedabad, Gujarat. Vet World 2015; 8(1): 121-124.
  42. Kadry M, Nader SM, Dorgham SM, et al. Molecular diversity of the invA gene obtained from human and egg samples. Vet World 2019; 12(7): 1033-1038.
  43. Cohen ND, Wallis DE, Neibergs HL, et al. Detection of Salmonella enteritidis in equine feces using the polymerase chain reaction and genus-specific oligonucleotide primers. J Vet Diagn Invest 1995; 7(2): 219-222.
  44. Pusterla N, Byrne BA, Hodzic E, et al. Use of quantitative real-time PCR for the detection of Salmonella spp. in fecal samples from horses at a veterinary teaching hospital. Vet J 2010; 186(2): 252-255.
  45. Gentry-Weeks C, Hutcheson HJ, Kim LM, et al. Identification of two phylogenetically related organisms from feces by PCR for detection of Salmonella J Clin Microbiol 2002; 40(4): 1487-1492.
  46. Shanmugasamy M, Velayutham T, Rajeswar J. Inv A gene specific PCR for detection of Salmonella from broilers. Vet World 2011; 4(12): 562-564.
  47. Salehi TZ, Mahzounieh M, Saeedzadeh A. Detection of InvA gene in isolated Salmonella from broilers by PCR method. Int J Poult Sci 2005; 4(8): 557-559.
  48. Cohen ND, Martin LJ, Simpson RB, et al. Comparison of polymerase chain reaction and microbiological culture for detection of salmonellae in equine feces and environmental samples. Am J Vet Res 1996; 57(6): 780-786.
  49. Shekarforoush S, Rokni N, Karim G, et al. Study on the overview on food borne bacteria in foodstuffs with animal origin in Iran; Part two: meat and meat products [Persian]. Food Hyg 2012; 2(3): 1-14.
  50. Afshari-Nic S, Zahraei-Salehi T, Jamshidi A. Detection of Salmonella spp contamination of carcasses slaughtered in poultry abattoir in Mashhad, Iran. Arch Razi Inst 2007; 62(4): 229-233.