Why is it important for us to isolate a single colony of bacteria from the chicken farm sample

1. Shao D., Shi Z., Wei J., Ma Z. A brief review of foodborne zoonoses in China. Epidemiology and Infection . 2011;139(10):1497–1504. doi: 10.1017/S0950268811000872. [PubMed] [CrossRef] [Google Scholar]

2. Jackson B. R., Griffin P. M., Cole D., Walsh K. A., Chai S. J. Outbreak-associatedSalmonella entericaSerotypes and food commodities, United States, 1998-2008. Emerging Infectious Diseases . 2013;19(8):1239–1244. doi: 10.3201/eid1908.121511. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

3. Smith J. L., Fratamico P. M. Factors involved in the emergence and persistence of food-borne diseases. Journal of Food Protection . 1995;58(6):696–708. doi: 10.4315/0362-028X-58.6.696. [PubMed] [CrossRef] [Google Scholar]

4. Ward L. R. Salmonella enteritidis epidemic. Science . 2000;287(5459):1753c–11753. doi: 10.1126/science.287.5459.1753c. [PubMed] [CrossRef] [Google Scholar]

5. Youn S. Y., Jeong O. M., Choi B. K., Jung S. C., Kang M. S. Comparison of the antimicrobial and sanitizer resistance ofSalmonellaIsolates from chicken slaughter processes in Korea. Journal of Food Science . 2017;82(3):711–717. doi: 10.1111/1750-3841.13630. [PubMed] [CrossRef] [Google Scholar]

6. Márquez M. L. F., Burgos M. J. G., Pulido R. P., Gálvez A., López R. L. Correlations among resistances to different antimicrobial compounds in Salmonella strains from hen eggshells. Journal of Food Protection . 2018;81(2):178–185. doi: 10.4315/0362-028X.JFP-17-200. [PubMed] [CrossRef] [Google Scholar]

7. Nhung N. T., Chansiripornchai N., Carrique-Mas J. J. Antimicrobial resistance in bacterial poultry pathogens: a review. Frontiers in Veterinary Science . 2017;4 doi: 10.3389/fvets.2017.00126. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

8. Carrique-Mas J. J., Davies R. H. Sampling and bacteriological detection of Salmonella in poultry and poultry premises: a review. Revue scientifique et technique (International Office of Epizootics) . 2008;27(3):665–677. doi: 10.20506/rst.27.3.1829. [PubMed] [CrossRef] [Google Scholar]

9. Singer R. S., Mayer A. E., Hanson T. E., Isaacson R. E. Do microbial interactions and cultivation media decrease the accuracy of Salmonella surveillance systems and outbreak investigations? Journal of Food Protection . 2009;72(4):707–713. doi: 10.4315/0362-028X-72.4.707. [PubMed] [CrossRef] [Google Scholar]

10. International Organization for Standardization. Horizontal method for the detection, enumeration and serotyping of Salmonella . 2017.

11. Abdelhai M. H. Comparative study of rapid DNA extraction methods of pathogenic bacteria. American Journal of Bioscience and Bioengineering . 2016;4(1):p. 1. doi: 10.11648/j.bio.20160401.11. [CrossRef] [Google Scholar]

12. Pathmanathan S. G., Cardona-Castro N., Sánchez-Jiménez M. M., Correa-Ochoa M. M., Puthucheary S. D., Thong K. L. Simple and rapid detection of Salmonella strains by direct PCR amplification of the hilA gene. Journal of Medical Microbiology . 2003;52(9):773–776. doi: 10.1099/jmm.0.05188-0. [PubMed] [CrossRef] [Google Scholar]

13. Bäumler A. J., Heffron F., Reissbrodt R. Rapid detection of Salmonella enterica with primers specific for iroB. Journal of Clinical Microbiology . 1997;35(5):1224–1230. doi: 10.1128/jcm.35.5.1224-1230.1997. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

14. EUCAST. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. 2020, http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_5.0_Breakpoint_Table_01.pdf.

15. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. CLSI Document VET01 5th Edition. Jun 2018 . Clinical & Laboratory Standards Institute (CLSI); 2018. [Google Scholar]

16. Rawat D., Nair D. Extended-spectrum ß-lactamases in Gram negative bacteria. Journal of Global Infectious Diseases . 2010;2(3):p. 263. doi: 10.4103/0974-777x.68531. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

17. Magiorakos A. P., Srinivasan A., Carey R. B., et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection . 2012;18(3):268–281. doi: 10.1111/j.1469-0691.2011.03570.x. [PubMed] [CrossRef] [Google Scholar]

18. Zhang G., Ma L., Patel N., Swaminathan B., Wedel S., Doyle M. P. Isolation of Salmonella Typhimurium from outbreak-associated cake mix. Journal of Food Protection . 2007;70(4):997–1001. doi: 10.4315/0362-028X-70.4.997. [PubMed] [CrossRef] [Google Scholar]

19. Miller R. G., Tate C. R., Mallinson E. T., Scherrer J. A. Xylose-Lysine-Tergitol 4: An Improved Selective Agar Medium for the Isolation of Salmonella. Poultry Science . 1991;70(12):2429–2432. doi: 10.3382/ps.0702429. [PubMed] [CrossRef] [Google Scholar]

20. Dusch H., Altwegg M. Evaluation of five new plating media for isolation of Salmonella species. Journal of Clinical Microbiology . 1995;33(4):802–804. doi: 10.1128/jcm.33.4.802-804.1995. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

21. Moussa I. M., I M., Gassem, et al. Using molecular techniques for rapid detection of Salmonella serovars in frozen chicken and chicken products collected from Riyadh, Saudi Arabia. African Journal of Biotechnology . 2010;9(5):612–619. doi: 10.5897/AJB09.1761. [CrossRef] [Google Scholar]

22. Paião F. G., Arisitides L. G. A., Murate L. S., Vilas-Bôas G. T., Vilas-Boas L. A., Shimokomaki M. Detection of Salmonella spp, Salmonella Enteritidis and Typhimurium in naturally infected broiler chickens by a multiplex PCR-based assay. Brazilian Journal of Microbiology . 2013;44(1):37–42. doi: 10.1590/S1517-83822013005000002. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

23. Gwida M. M., Al-Ashmawy M. A. M. Culture versus PCR for salmonella species identification in some dairy products and dairy handlers with special concern to its zoonotic importance. Veterinary Medicine International . 2014;2014:5. doi: 10.1155/2014/502370.502370 [PMC free article] [PubMed] [CrossRef] [Google Scholar]

24. Gautam R. K., Kakatkar A. S., Karani M. N., Bandekar J. R. Salmonella in Indian ready-to-cook poultry: antibiotic resistance and molecular characterization. Microbiology Research . 2017;8(1):15–19. doi: 10.4081/mr.2017.6882. [CrossRef] [Google Scholar]

25. Bhuvaneswa M., Shanmughap S., Natarajase K. Prevalence of multidrug-resistant (MDR) Salmonella enteritidis in poultry and backyard chicken from Tiruchirappalli, India. Microbiology Journal . 2015;5(2):28–35. doi: 10.3923/mj.2015.28.35. [CrossRef] [Google Scholar]

26. Cui M., Xie M., Qu Z., et al. Prevalence and antimicrobial resistance of Salmonella isolated from an integrated broiler chicken supply chain in Qingdao, China. Food Control . 2016;62:270–276. doi: 10.1016/j.foodcont.2015.10.036. [CrossRef] [Google Scholar]

27. Kalaba V., Golić B., Sladojević Ž., Kalaba D. Incidence ofSalmonellaInfantis in poultry meat and products and the resistance of isolates to antimicrobials. IOP Conference Series: Earth and Environmental Science . 2017;85(1):p. 012082. doi: 10.1088/1755-1315/85/1/012082. [CrossRef] [Google Scholar]

28. Tessema K., Bedu H., Ejo M., Hiko A. Prevalence and antibiotic resistance of salmonella species isolated from chicken eggs by standard bacteriological method. Journal of Veterinary Science & Technology . 2017;8(1):1–5. doi: 10.4172/2157-7579.1000421. [CrossRef] [Google Scholar]

29. Li S., Zhou Y., Miao Z. Prevalence and antibiotic resistance of non-typhoidal Salmonella isolated from raw chicken carcasses of commercial broilers and spent hens in Tai’an, China. Frontiers in Microbiology . 2017;8:1–6. doi: 10.3389/fmicb.2017.02106. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

30. Sharma J., Kumar D., Hussain S., et al. Prevalence, antimicrobial resistance and virulence genes characterization of nontyphoidal Salmonella isolated from retail chicken meat shops in Northern India. Food Control . 2019;102:104–111. doi: 10.1016/j.foodcont.2019.01.021. [CrossRef] [Google Scholar]

31. Shubham S. Molecular characterization of non-typhoidal Salmonella serovars isolated from commercial broiler farms and retail chicken meat shops with reference to virulence and antimicrobial resistance, [Ph.D. thesis] G.B. Pant University of Agriculture and Technology, Pantnagar - 263145 (Uttarakhand); 2019. [Google Scholar]

32. Zafer A., Di G., Yibar A., Müştak H. K., Şahan Ö. Extended spectrum beta-lactamase activity and multidrug resistance of Salmonella serovars isolated from chicken carcasses from different regions of Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi . 2015;62(2):119–123. doi: 10.1501/vetfak_0000002668. [CrossRef] [Google Scholar]

33. Thung T. Y., Mahyudin N. A., Basri D. F., et al. Prevalence and antibiotic resistance of Salmonella Enteritidis and Salmonella Typhimurium in raw chicken meat at retail markets in Malaysia. Poultry Science . 2016;95(8):1888–1893. doi: 10.3382/ps/pew144. [PubMed] [CrossRef] [Google Scholar]

34. Choi S. W., Ha J. S., Kim B. Y., et al. Prevalence and characterization of Salmonella species in entire steps of a single integrated broiler supply chain in Korea. Poultry Science . 2014;93(5):1251–1257. doi: 10.3382/ps.2013-03558. [PubMed] [CrossRef] [Google Scholar]

35. Zhu Y., Lai H., Zou L., et al. Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. International Journal of Food Microbiology . 2017;259:43–51. doi: 10.1016/j.ijfoodmicro.2017.07.023. [PubMed] [CrossRef] [Google Scholar]

36. Olsen S. J., MacKinnon L. C., Goulding J. S., Bean N. H., Slutsker L. Surveillance for foodborne-disease outbreaks, United States, 1993-1997 . Vol. 49. Centers for Disease Control and Prevention; 2000. (MMWR. CDC surveillance summaries : Morbidity and mortality weekly report. CDC surveillance summaries). [Google Scholar]

37. Jajere S. M. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Veterinary World . 2019;12(4):504–521. doi: 10.14202/vetworld.2019.504-521. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

38. Wang J., Li J., Liu F., Cheng Y., Su J. Characterization of Salmonella enterica isolates from diseased poultry in northern China between 2014 and 2018. Pathogens . 2020;9(2):p. 95. doi: 10.3390/pathogens9020095. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

39. Elkenany R., Elsayed M. M., Zakaria A. I., El-Sayed S. A. E. S., Rizk M. A. Antimicrobial resistance profiles and virulence genotyping of Salmonella enterica serovars recovered from broiler chickens and chicken carcasses in Egypt. BMC Veterinary Research . 2019;15(1):1–9. doi: 10.1186/s12917-019-1867-z. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

40. Arora D., Kumar S., Jindal N., Narang G., Kapoor P. K., Mahajan N. K. Prevalence and epidemiology of Salmonella enterica serovar Gallinarum from poultry in some parts of Haryana, India. Veterinary World . 2015;8(11):1300–1304. doi: 10.14202/vetworld.2015.1300-1304. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

41. Dessie H. K., Bae D. H., Lee Y. J. Characterization of integrons and their cassettes in Escherichia coli and Salmonella isolates from poultry in Korea. Poultry Science . 2013;92(11):3036–3043. doi: 10.3382/ps.2013-03312. [PubMed] [CrossRef] [Google Scholar]

42. Rahmani M., Peighambari S. M., Svendsen C. A., Cavaco L. M., Agersø Y., Hendriksen R. S. Molecular clonality and antimicrobial resistance in Salmonella entericaserovars Enteritidis and Infantis from broilers in three Northern regions of Iran. BMC Veterinary Research . 2013;9(1) doi: 10.1186/1746-6148-9-66. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

43. Mir I. A., Kashyap S. K., Maherchandani S. Isolation, serotype diversity and antibiogram of Salmonella enterica isolated from different species of poultry in India. Asian Pacific Journal of Tropical Biomedicine . 2015;5(7):561–567. doi: 10.1016/j.apjtb.2015.03.010. [CrossRef] [Google Scholar]

44. Malik S., Roy P., Rawat D. A case of extended spectrum beta-lactamase producing salmonella enterica serotype paratyphi A from India. Indian Journal of Pathology & Microbiology . 2015;58(1):113–114. doi: 10.4103/0377-4929.151205. [PubMed] [CrossRef] [Google Scholar]

45. Venkatesh S. Minutes of the 81stmeeting of drugs technical advisory board held on 29th November, 2018 at DGHS, Nirman Bhawan, New Delhi . 2018, https://cdsco.gov.in/opencms/resources/UploadCDSCOWeb/2018/UploadCommitteeFiles/dtab29nov18.pdf.

46. The Union health ministry. Government ban on colistin for use in poultry industry . New Delhi, India: 2019. , https://www.hindustantimes.com/india-news/centre-bans-antibiotic-drug-colistin-for-use-in-poultry-industry/story-xzX7oxDAGeeQVP2WsqnTwL.html. [Google Scholar]

47. Uddin M. B., Hossain S. M. B., Hasan M., et al. Multidrug antimicrobial resistance and molecular detection of MCR-1 gene in salmonella species isolated from chicken. Animals . 2021;11(1):206–219. doi: 10.3390/ani11010206. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

48. Manic M. Resistance testing of Salmonella Spp. bacteria isolated from samples derived from poultry on antimicrobial drugs. Journal of Dairy, Veterinary and Animal Research . 2016;3(2):67–71. doi: 10.15406/jdvar.2016.03.00074. [CrossRef] [Google Scholar]

49. Waghamare R. N., Paturkar A. M., Vaidya V. M., et al. 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 . 2018;11(12):1682–1688. doi: 10.14202/vetworld.2018.1682-1688. [PMC free article] [PubMed] [CrossRef] [Google Scholar]


Page 2

Samples collected from different commercial broiler supply chain.

No.Types of samples collected n
Hatchery29
1Swabs from egg setting room (10 swabs from different areas and pooled to one/hatchery)3
2Swabs from incubator/setter (3 swabs from different areas of each incubator and 50% of the incubator present in each hatchery were sampled and pooled)3
3Swabs from air tunnels and fans of incubators/setter (3 swabs from different areas of each incubator and 50% of the incubator present in each hatchery were sampled and pooled)3
4Swabs from hatchers (3 swabs from different areas of each hatcher and samples were pooled)3
5Swabs from hatchers egg tray (ten trays/hatcher and one swab/tray from different areas and samples were pooled)3
6Meconium swabs (ten trays/hatcher and one swab/tray from different areas and samples were pooled)3
7Yolk sac swab of dead chicks (ten dead chicks and samples were pooled)3
8Hand swabs from hatchery workers (two swabs from two workers)5
9Boot socks from hatchery floor3
Commercial broiler farm (CBF)—three samplings—day 1, days 18-20, and days 35-4299
125 ml water from water tank/shed (25 ml in 25 ml 2x BPW)15
225 ml water from 30 different nipples/shed/(25 ml in 25 ml 2x BPW) and pooled15
325 g feed sample from 10 different feed bags/shed and pooled15
425 g feed sample from 30 different feeders/shed and pooled15
5Faecal swabs (30 swabs/shed pooled)15
6Internal (inside the shed) environment samples using sterile boot socks/one pair/shed15
7External (outside the shed) environment samples using sterile boot socks/farm9
Retail meat shops (RMS)54
1Swabs from surface of cutting/chopping board (100 cm2). Swabs were immersed in sterile BPW3
2Swabs from cutter/knife3
3Meat rinsing water (25 ml in 25 ml 2x BPW)3
4Chicken carcasses (5 carcasses/shop)15
5Ileal contents from five carcasses15
6Cecal contents from five carcasses15