Serovars, virulence factors, and antimicrobial resistance profile of non-typhoidal Salmonella in the human-dairy interface in Northwest Ethiopia: A one health approach.

Achenef Melaku Beyene, Yismaw Alemie, Mucheye Gizachew, Ahmed E Yousef, Bereket Dessalegn, Abebe Belete Bitew, Amare Alemu, Waktole Gobena, Kornschober Christian, Baye Gelaw
Author Information
  1. Achenef Melaku Beyene: Department of Medical Microbiology, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia. ORCID
  2. Yismaw Alemie: Department of Pathobiology, College of Veterinary Medicine and Animal Sciences, University of Gondar, Gondar, Ethiopia.
  3. Mucheye Gizachew: Department of Medical Microbiology, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia.
  4. Ahmed E Yousef: Department of Food Science and Technology, The Ohio State University, Columbus, Ohio, United States of America.
  5. Bereket Dessalegn: Department of Pathobiology, College of Veterinary Medicine and Animal Sciences, University of Gondar, Gondar, Ethiopia.
  6. Abebe Belete Bitew: Department of Veterinary Epidemiology and Public Health, College of Veterinary Medicine and Animal Sciences, University of Gondar, Gondar, Ethiopia.
  7. Amare Alemu: Infectious Diseases Directorate, Tuberculosis and Other Bacterial Diseases division, Ethiopian Public Health Institute, Addis Ababa, Ethiopia.
  8. Waktole Gobena: Food Microbiology Laboratory, Ethiopian Public Health Institute, Addis Ababa, Ethiopia.
  9. Kornschober Christian: AGES: Agency for Health and Food Safety, National Reference Laboratory for Salmonella, Institute for Medical Microbiology and Hygiene, Graz, Austria.
  10. Baye Gelaw: Department of Medical Microbiology, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia.

Abstract

Non-typhoidal Salmonella (NTS) is a zoonotic pathogen that exerts huge public health and economic impacts in the world. The severity of illness is mainly related to the serovars involved, the presence of virulence genes, and antimicrobial resistance (AMR) patterns. However, data are scarce on serovars, virulence genes, and AMR among NTS identified from the human-dairy interface in Northwest Ethiopia. Thus, this study investigated the serovars, common virulence genes, and AMR patterns of NTS isolates in the area. The study was conducted from June 2022 to August 2023 among randomly selected 58 dairy farms. A total of 362 samples were processed to detect NTS using standard bacteriological methods. The presumptive positive colonies were confirmed by Matrix-Assisted Laser Desorption Ionization-Time-of-Flight (MALDi-ToF). Polymerase chain reaction (PCR) was used to detect virulence genes, including invA and spvC. A slide agglutination test according to the White-Kauffmann-Le Minor scheme was employed to identify the serovars of the NTS isolates. The Kirby-Bauer disk diffusion method was used to assess the antimicrobial susceptibility patterns. Of the processed samples (362), 28 (7.7%) NTS isolates were detected. When distributed among samples, the proportions were 11.9%, 10.5%, 10.3%, 5.2%, 4.3%, and 1.7% among cows' feces, dairy farm sewage, pooled raw milk, milk container swabs, milkers' stool, and milkers' hand swab samples, respectively. Six serovars were detected with the dominancy of S. Uganda (39.3%), followed by S. enterica subsp. diarizonae (25.0%) and S. Typhimurium (21.4%). Among the 28 NTS isolates, 100% and 21.4% had the virulence genes invA and spvC, respectively. The susceptibility profile showed that 89.3% of the NTS isolates were resistant to at least one antimicrobial agent and 46.4% were resistant to three or more classes of antimicrobials (multidrug-resistant). Among antimicrobials, isolates were highly resistant to ampicillin (57.1%), followed by tetracycline (42.9%) and chloramphenicol (35.7%). On the other hand, the NTS isolates were 100%, 96.4%, and 96.4% susceptible to ceftriaxone, azithromycin, and norfloxacin, respectively. In conclusion, we detected NTS from humans, dairy cows, raw milk, dairy utensils, and the environment (sewage), showing the potential of the human-dairy farm-environment nexus in the NTS circulation. These further highlight that the interface is a good point of intervention in the control and prevention of NTS infection. The susceptibility profiles of the isolate necessitate interventions including the prudent use of the antimicrobials.

References

  1. Trends Microbiol. 2012 Jul;20(7):320-7 [PMID: 22591832]
  2. Vet Sci. 2018 Apr 08;5(2): [PMID: 29642473]
  3. Indian J Psychol Med. 2013 Apr;35(2):121-6 [PMID: 24049221]
  4. Animals (Basel). 2023 Nov 27;13(23): [PMID: 38067017]
  5. J Urban Health. 2006 Nov;83(6 Suppl):i98-112 [PMID: 16937083]
  6. Front Microbiol. 2023 May 15;14:1162657 [PMID: 37256054]
  7. Int J Microbiol. 2023 Feb 23;2023:6837797 [PMID: 36875709]
  8. BMC Infect Dis. 2015 Nov 04;15:497 [PMID: 26537951]
  9. Wellcome Open Res. 2020 Oct 9;5:237 [PMID: 34017923]
  10. Appl Environ Microbiol. 2001 Feb;67(2):977-8 [PMID: 11157272]
  11. BMC Microbiol. 2014 Nov 15;14:270 [PMID: 25398272]
  12. Biomed Res Int. 2016;2016:4290506 [PMID: 28074185]
  13. Indian J Microbiol. 2017 Mar;57(1):1-10 [PMID: 28148975]
  14. J Dairy Sci. 2013 Sep;96(9):5756-61 [PMID: 23810596]
  15. Res Microbiol. 2010 Jan-Feb;161(1):26-9 [PMID: 19840847]
  16. J Epidemiol Glob Health. 2023 Dec;13(4):637-652 [PMID: 37883006]
  17. Trop Anim Health Prod. 2009 Oct;41(7):1143-50 [PMID: 19083118]
  18. Front Microbiol. 2011 Jun 14;2:129 [PMID: 21716657]
  19. BMC Microbiol. 2022 Mar 31;22(1):84 [PMID: 35361106]
  20. J Appl Microbiol. 2015 Jan;118(1):152-60 [PMID: 25358641]
  21. PLoS One. 2024 May 21;19(5):e0303872 [PMID: 38771780]
  22. PLoS One. 2024 May 7;19(5):e0301697 [PMID: 38713729]
  23. Gut Pathog. 2023 Mar 30;15(1):16 [PMID: 36998086]
  24. J Food Prot. 2022 Dec 1;85(12):1790-1796 [PMID: 36150093]
  25. Lancet. 2012 Jun 30;379(9835):2489-2499 [PMID: 22587967]
  26. Int J Food Microbiol. 2019 Jan 2;288:3-12 [PMID: 29803313]
  27. Clin Microbiol Infect. 2012 Mar;18(3):268-81 [PMID: 21793988]
  28. BMC Infect Dis. 2015 Feb 21;15:84 [PMID: 25887706]
  29. Microorganisms. 2021 Apr 28;9(5): [PMID: 33924919]
  30. Front Microbiol. 2014 Aug 04;5:391 [PMID: 25136336]
  31. Front Microbiol. 2017 Sep 08;8:1723 [PMID: 28943871]
  32. Front Microbiol. 2018 Jan 11;8:2697 [PMID: 29379488]
  33. PLoS One. 2022 Mar 16;17(3):e0265271 [PMID: 35294487]
  34. Int J Food Contam. 2023;10(1):2 [PMID: 36811093]
  35. Biomed Res Int. 2017;2017:3782182 [PMID: 28540296]
  36. Ann Agric Environ Med. 2023 Mar 31;30(1):9-14 [PMID: 36999850]
  37. Front Microbiol. 2019 Sep 06;10:2091 [PMID: 31555256]
  38. J Thorac Dis. 2015 Nov;7(11):E537-40 [PMID: 26716051]
  39. One Health. 2022 Apr 20;14:100390 [PMID: 35686143]
  40. Biomed Res Int. 2021 Sep 18;2021:6177741 [PMID: 34589548]
  41. BMC Res Notes. 2015 Apr 21;8:163 [PMID: 25896925]
  42. Lancet Infect Dis. 2019 Dec;19(12):1312-1324 [PMID: 31562022]
  43. Appl Environ Microbiol. 2019 Jul 1;85(14): [PMID: 31053586]
  44. BMC Microbiol. 2016 Feb 16;16:20 [PMID: 26879347]
  45. Iran J Basic Med Sci. 2021 Jul;24(7):914-921 [PMID: 34712421]
  46. Microbes Infect. 2000 Feb;2(2):145-56 [PMID: 10742687]
  47. Trop Med Infect Dis. 2023 Oct 27;8(11): [PMID: 37999606]
  48. BMJ Glob Health. 2021 Aug;6(8): [PMID: 34341020]
  49. Vet World. 2015 Jan;8(1):121-4 [PMID: 27047008]
  50. J Dairy Sci. 2020 Nov;103(11):9715-9729 [PMID: 33076183]
  51. FEMS Microbiol Rev. 2012 May;36(3):600-15 [PMID: 22335190]
  52. PLoS Med. 2015 Dec 03;12(12):e1001923 [PMID: 26633896]

MeSH Term

Ethiopia
Humans
Animals
Virulence Factors
Salmonella
Salmonella Infections
Anti-Bacterial Agents
Cattle
Serogroup
One Health
Drug Resistance, Bacterial
Microbial Sensitivity Tests
Dairying
Salmonella Infections, Animal

Chemicals

Virulence Factors
Anti-Bacterial Agents

Word Cloud

Created with Highcharts 10.0.0NTSisolatesvirulenceserovarsgenes4%antimicrobialamongdairysamples3%AMRpatternshuman-dairyinterfacesusceptibility7%detectedmilkrespectivelySresistantantimicrobialsSalmonellahealthresistanceNorthweststudy362processeddetectusedincludinginvAspvC289%10sewagerawmilkers'handfollowed21Among100%profileone96Non-typhoidalzoonoticpathogenexertshugepubliceconomicimpactsworldseverityillnessmainlyrelatedinvolvedpresenceHoweverdatascarceidentifiedEthiopiaThusinvestigatedcommonareaconductedJune2022August2023randomlyselected58farmstotalusingstandardbacteriologicalmethodspresumptivepositivecoloniesconfirmedMatrix-AssistedLaserDesorptionIonization-Time-of-FlightMALDi-ToFPolymerasechainreactionPCRslideagglutinationtestaccordingWhite-Kauffmann-LeMinorschemeemployedidentifyKirby-Bauerdiskdiffusionmethodassess7distributedproportions115%52%41cows'fecesfarmpooledcontainerswabsstoolswabSixdominancyUganda39entericasubspdiarizonae250%Typhimuriumshowed89leastagent46threeclassesmultidrug-resistanthighlyampicillin571%tetracycline42chloramphenicol35susceptibleceftriaxoneazithromycinnorfloxacinconclusionhumanscowsutensilsenvironmentshowingpotentialfarm-environmentnexuscirculationhighlightgoodpointinterventioncontrolpreventioninfectionprofilesisolatenecessitateinterventionsprudentuseSerovarsfactorsnon-typhoidalEthiopia:approach

Similar Articles

Cited By