Frequency and antibiotic resistance pattern of Salmonella spp. isolated from traditional dairies and raw milks collected in Yazd province, Iran
Abstract
Background and Objectives: Salmonellosis is among the most common food-born infections, caused by Salmonella spp. bacteria. Present study has investigated the frequency and antibiotic resistance pattern of Salmonella spp. isolated from traditional dairy products and raw milk supplied in Yazd, Iran.
Materials and Methods: In a cross-sectional study, 350 samples of raw milk and traditional dairy products were randomly collected from July to September 2018. Following culturing the samples, isolates went through biochemical tests for phenotypic identification. Results were confirmed through PCR technique by targeting invA gene. Antimicrobial susceptibility test was conducted by means of disk diffusion method.
Results: The rate of contamination with Salmonella bacteria was 6.57% in all samples. The PCR assay of all isolates showed that 23 isolates (100%) carried the invA gene. No significant association between the frequency of salmonella spp. and types of dairy and their origin was reported (P>0.05). The highest antibiotic resistance rate among the isolates belonged to tetracycline (34.8%) and the highest sensitivity was seen to imipenem, cefepime, and cefotaxime (each 91.3%).
Conclusion: According to our results there has been a rise in multiple drug resistance and contamination rate in traditional dairy products in Yazd province.
2. Garbaj AM, Gawella TBB, Sherif JA, Naas HT, Eshamah HL, Azwai SM, et al. Occurrence and antibiogram of multidrug-resistant Salmonella enterica isolated from dairy products in Libya. Vet World 2022; 15: 1185-1190.
3. Grace D, Wu F, Havelaar AH. MILK Symposium review: Foodborne diseases from milk and milk products in developing countries-Review of causes and health and economic implications. J Dairy Sci 2020; 103: 9715-9729.
4. Gebeyehu A, Taye M, Abebe R. Isolation, molecular detection and antimicrobial susceptibility profile of Salmonella from raw cow milk collected from dairy farms and households in southern Ethiopia. BMC Microbiol 2022; 22: 84.
5. Huo Y, Li H, Wang J, Gu B, Zhou L, Liu G, et al. Risk-based detection as a cost-effective strategy to reduce foodborne illness due to salmonella. Heliyon 2023; 9(11): e22392.
6. Jajere SM. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet World 2019; 12: 504-521.
7. Ikhimiukor OO, Oaikhena AO, Afolayan AO, Fadeyi A, Kehinde A, Ogunleye VO, et al. Genomic characterization of invasive typhoidal and non-typhoidal Salmonella in southwestern Nigeria. PLoS Negl Trop Dis 2022; 16(8): e0010716.
8. Cobo-Simón M, Hart R, Ochman H. Gene flow and species boundaries of the genus Salmonella. mSystems 2023; 8(4): e0029223.
9. Amajoud N, Bouchrif B, El Maadoudi M, Skalli Senhaji N, Karraouan B, El Harsal A, et al. Prevalence, serotype distribution, and antimicrobial resistance of Salmonella isolated from food products in Morocco. J Infect Dev Ctries 2017; 11: 136-142.
10. Ayuti SR, Khairullah AR, Al-Arif MA, Lamid M, Warsito SH, Moses IB, et al. Tackling salmonellosis: A comprehensive exploration of risks factors, impacts, and solutions. Open Vet J 2024; 14: 1313-1329.
11. García-Díez J, Moura D, Grispoldi L, Cenci-Goga B, Saraiva S, Silva F, et al. Salmonella spp. in domestic ruminants, evaluation of antimicrobial resistance based on the one health Approach-A systematic review and Meta-Analysis. Vet Sci 2024; 11: 315.
12. Farid N, Waheed A, Motwani S. Synthetic and natural antimicrobials as a control against food borne pathogens: A review. Heliyon 2023; 9(6): e17021.
13. Foley SL, Lynne AM. Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci 2008; 86(14 Suppl): E173-E187.
14. Chen H-M, Wang Y, Su L-H, Chiu C-H. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol 2013; 54: 147-152.
15. Ehuwa O, Jaiswal AK, Jaiswal S. Salmonella, food safety and food handling practices. Foods 2021; 10: 907.
16. Fagbamila IO, Ramon E, Lettini AA, Muhammad M, Longo A, Antonello K, et al. Assessing the mechanisms of multi-drug resistant non-typhoidal Salmonella (NTS) serovars isolated from layer chicken farms in Nigeria. PLoS One 2023; 18(9): e0290754.
17. Khan MAS, Rahman SR. Use of phages to treat antimicrobial-resistant Salmonella infections in poultry. Vet Sci 2022; 9: 438.
18. Zhao S, Chen J, Fei P, Feng H, Wang Y, Ali MA, et al. Prevalence, molecular characterization, and antibiotic susceptibility of Bacillus cereus isolated from dairy products in China. J Dairy Sci 2020; 103: 3994-4001.
19. Liu Y, Jiang J, Ed-Dra A, Li X, Peng X, Xia L, et al. Prevalence and genomic investigation of Salmonella isolates recovered from animal food-chain in Xinjiang, China. Food Res Int 2021; 142: 110198.
20. Castro-Vargas RE, Herrera-Sanchez MP, Rodriguez-Hernandez R, Rondon-Barragan IS. Antibiotic resistance in Salmonella spp. isolated from poultry: A global overview. Vet World 2020; 13: 2070-2084.
21. ISIRI. Milk and milk products – guidance on sampling - 3th. revision 326. Iran: The Institute of Standards & Industrial Research of Iran. 2009. https://standard.inso.gov.ir/Search.aspx?standardnumber=326&subject:1-47
22. ISIRI. Milk and milk products-Detection of Salmonella-4st. Revision 4413. Iran: The Institute of Standards & Industrial Research of Iran. 2010. https://standard.inso.gov.ir/StandardView.aspx?Id=52720&subject
23. De Medici D, Croci L, Delibato E, Di Pasquale S, Filetici E, Toti L. Evaluation of DNA extraction methods for use in combination with SYBR green I real-time PCR to detect Salmonella enterica serotype enteritidis in poultry. Appl Environ Microbiol 2003; 69: 3456-3461.
24. Ferretti R, Mannazzu I, Cocolin L, Comi G, Clementi F. Twelve-hour PCR-based method for detection of Salmonella spp. in food. Appl Environ Microbiol 2001; 67: 977-978.
25. Poulou A, Grivakou E, Vrioni G, Koumaki V, Pittaras T, Pournaras S, et al. Modified CLSI extended-spectrum β-lactamase (ESBL) confirmatory test for phenotypic detection of ESBLs among Enterobacteriaceae producing various β-lactamases. J Clin Microbiol 2014; 52: 1483-1489.
26. Elafify M, Darwish WS, El-Toukhy M, Badawy BM, Mohamed RE, Shata RR. Prevalence of multidrug resistant Salmonella spp. in dairy products with the evaluation of the inhibitory effects of ascorbic acid, pomegranate peel extract, and D-tryptophan against Salmonella growth in cheese. Int J Food Microbiol 2022; 364: 109534.
27. Liu B-G, Xie M, Gong Y-T, Dong Y, Zheng G-M, Wu H, et al. Prevalence, resistance phenotypes, and fluoroquinolone resistance genes of Salmonella isolates from raw milk of healthy dairy cows in Henan province, China. Eur Rev Med Pharmacol Sci 2022; 26: 6837-6844.
28. Hassani S, Moosavy M-H, Gharajalar SN, Khatibi SA, Hajibemani A, Barabadi Z. High prevalence of antibiotic resistance in pathogenic foodborne bacteria isolated from bovine milk. Sci Rep 2022; 12: 3878.
29. Artursson K, Schelin J, Thisted Lambertz S, Hansson I, Olsson Engvall E. Foodborne pathogens in unpasteurized milk in Sweden. Int J Food Microbiol 2018; 284: 120-127.
30. Bedassa A, Nahusenay H, Asefa Z, Sisay T, Girmay G, Kovac J, et al. Prevalence and associated risk factors for Salmonella enterica contamination of cow milk and cottage cheese in Ethiopia. Int J Food Contam 2023; 10: 2.
31. Soto-Varela ZE, Gutiérrez CG, De Moya Y, Mattos R, Bolívar-Anillo HJ, Villarreal JL. Molecular detection of Salmonella spp., Listeria spp. and Brucella spp. in fresh artisanal cheese marketed in the city of Barranquilla: A pilot study. Biomedica 2018;38:30-36.
32. Ahmed AM, Shimamoto T. Isolation and molecular characterization of Salmonella enterica, Escherichia coli O157: H7 and Shigella spp. from meat and dairy products in Egypt. Int J Food Microbiol 2014; 168-169: 57-62.
33. Esho FK, Enkhtuya B, Kusumoto A, Kawamoto K. Microbial assessment and prevalence of foodborne pathogens in natural cheeses in Japan. Biomed Res Int 2013; 2013: 205801.
34. Van Asselt ED, Van der Fels-Klerx HJ, Marvin HJP, Van Bokhorst-van de Veen H, Groot MN. Overview of food safety hazards in the European dairy supply chain. Compr Rev Food Sci Food Saf 2017; 16: 59-75.
35. Kruy SL, Soares JL, Ping S, Sainte-Marie FF. Microbiological quality of" ice, ice cream. sorbet" sold on the streets of Phnom Penh; April 1996-April 1997. Bull Soc Pathol Exot 2001; 94: 411-414.
36. Ahmadi SA, Panda AK. Prevalence of Escherichia coli and Salmonella spp. in ready-to-eat milk and milk products in Himachal Pradesh. J Vet Public Health 2015; 13: 34-38.
37. Reddy SP, Wang H, Adams JK, Feng PC. Prevalence and characteristics of Salmonella serotypes isolated from fresh produce marketed in the United States. J Food Prot 2016; 79: 6-16.
38. Ehsani A, Hashemi M, Hosseini Jazani N, Aliakbarlu J, Shokri S, Naghibi SS. Effect of Echinophora platyloba DC. essential oil and lycopene on the stability of pasteurized cream obtained from cow milk. Vet Res Forum 2016; 7: 139-148.
39. Sharifzadeh A, Hajsharifi-Shahreza M, Ghasemi-Dehkordi P. Evaluation of microbial contamination and chemical qualities of cream-filled pastries in confectioneries of Chaharmahal Va Bakhtiari Province (Southwestern Iran). Osong Public Health Res Perspect 2016; 7: 346-350.
40. McLauchlin J, Aird H, Elliott A, Forester E, Jørgensen F, Willis C. Microbiological quality of raw drinking milk and unpasteurised dairy products: results from England 2013–2019. Epidemiol Infect 2020; 148: e135.
41. Busani L, Cigliano A, Taioli E, Caligiuri V, Chiavacci L, Di Bella C, et al. Prevalence of Salmonella enterica and Listeria monocytogenes contamination in foods of animal origin in Italy. J Food Prot 2005; 68: 1729-1733.
42. Rios-Muñiz D, Cerna-Cortes JF, Lopez-Saucedo C, Angeles-Morales E, Bobadilla-Del Valle M, Ponce-DE Leon A, et al. Isolation of Staphylococcus aureus, uropathogenic Escherichia coli, and nontuberculous Mycobacteria strains from pasteurized cheeses and Unpasteurized cream sold at Traditional open markets in Mexico city. J Food Prot 2022; 85: 1848-1854.
43. Asfaw Geresu M, Assefa Wayuo B, Mamo Kassa G. Occurrence and antimicrobial susceptibility profile of Salmonella isolates from animal origin food items in selected areas of Arsi zone, southeastern Ethiopia, 2018/19. Int J Microbiol 2021; 2021: 6633522.
44. Ombarak RA, Hinenoya A, Elbagory AM, Yamasaki S. Prevalence and molecular characterization of antimicrobial resistance in Escherichia coli isolated from raw milk and raw milk cheese in Egypt. J Food Prot 2018; 81: 226-232.
45. Ejo M, Garedew L, Alebachew Z, Worku W. Prevalence and antimicrobial resistance of Salmonella isolated from animal-origin food items in Gondar, Ethiopia. Biomed Res Int 2016; 2016: 4290506.
46. Sobur MA, Sabuj AAM, Sarker R, Rahman AT, Kabir SL, Rahman MT. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance. Vet World 2019;12:984.
47. Blau DM, McCluskey BJ, Ladely SR, Dargatz DA, Fedorka-Cray PJ, Ferris KE, et al. Salmonella in dairy operations in the United States: prevalence and antimicrobial drug susceptibility. J Food Prot 2005; 68: 696-702.
48. Obaidat MM, Stringer AP. Prevalence, molecular characterization, and antimicrobial resistance profiles of Listeria monocytogenes, Salmonella enterica, and Escherichia coli O157: H7 on dairy cattle farms in Jordan. J Dairy Sci 2019; 102: 8710-8720.
49. Addis Z, Kebede N, Worku Z, Gezahegn H, Yirsaw A, Kassa T. Prevalence and antimicrobial resistance of Salmonella isolated from lactating cows and in contact humans in dairy farms of Addis Ababa: a cross sectional study. BMC Infect Dis 2011; 11: 222.
50. Van Kessel JS, Sonnier J, Zhao S, Karns JS. Antimicrobial resistance of Salmonella enterica isolates from bulk tank milk and milk filters in the United States. J Food Prot 2013; 76: 18-25.
Files | ||
Issue | Vol 16 No 6 (2024) | |
Section | Original Article(s) | |
DOI | https://doi.org/10.18502/ijm.v16i6.17248 | |
Keywords | ||
Dairy products; invA; Cow’s milk; Salmonella; Antimicrobial resistance |
Rights and permissions | |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |