Skip to content
1887

Abstract

is a significant zoonotic pathogen, posing a serious public health threat through its presence in the food supply chain, particularly in poultry production facilities. This study aimed to investigate the genetic diversity, antimicrobial resistance (AMR) profiles and phylogenetic relationships of serovars isolated from various stages of the broiler supply chain in Harare, Zimbabwe. Whole-genome sequencing was employed to analyse 28 isolates from broiler farms, slaughter facilities and retail markets. The overall prevalence of was 5.1% out of 552 samples tested. Contamination rates were higher at slaughter facilities, where 11% of 100 samples tested positive and at retail markets, where 20% of 20 samples were contaminated. In contrast, farms had a significantly lower prevalence, with only 3.0% of 432 samples showing presence. Eight serovars were identified, with subsp. serovar Typhimurium being the most prevalent at 27.6%. Notably, 34.5% of the isolates harboured resistance genes, including , and , and exhibited mutations in the and regions. An extended-spectrum beta-lactamase-producing subsp. serovar Kentucky ST198 strain was isolated from retail chicken cuts. All isolates carried virulence genes such as , and , with present in 47.4% of the isolates. Approximately 31% of the isolates co-harboured antimicrobial, stress tolerance and virulence genes. Genomic analysis identified distinct sequence types while also revealing identical core SNPs in genomes across various stages of the supply chain. This study highlights the transmission of and AMR in the broiler supply chain, emphasizing the urgent need for improved surveillance and intervention strategies to reduce public health risks from contaminated poultry products.

Funding
This study was supported by the:
  • Department of Health and Social Care (Award GB-GOV-10-FF_MA_Zimbabwe)
    • Principal Award Recipient: PeterKatsande
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001550
2025-11-05
2025-12-16

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/11/mgen001550.html?itemId=/content/journal/mgen/10.1099/mgen.0.001550&mimeType=html&fmt=ahah

References

  1. Chen H, Qiu H, Zhong H, Cheng F, Wu Z et al. Non-typhoidal Salmonella infections among children in Fuzhou, Fujian, China: a 10-year retrospective review from 2012 to 2021. Infect Drug Resist 2023; 16:2737–2749 [View Article] [PubMed]
    [Google Scholar]
  2. Centers for Disease Control and Prevention (CDC) Salmonella; 2021 https://www.cdc.gov/salmonella/index.html accessed 20 January 2023
  3. Jeon HJ. Disease Surveillance and Implications on Public Health Decisions: Example of Invasive Salmonellosis in Sub-Saharan Africa Apollo - University of Cambridge Repository; 2023 [View Article]
    [Google Scholar]
  4. Ramtahal MA, Amoako DG, Akebe ALK, Somboro AM, Bester LA et al. A public health insight into Salmonella in poultry in Africa: a review of the past decade, 2010–2020. Microb Drug Resist 2022; 28:710–733 [View Article] [PubMed]
    [Google Scholar]
  5. Mashe T, Gudza-Mugabe M, Tarupiwa A, Munemo E, Mtapuri-Zinyowera S et al. Laboratory characterisation of Salmonella enterica serotype Typhi isolates from Zimbabwe, 2009-2017. BMC Infect Dis 2019; 19:487 [View Article] [PubMed]
    [Google Scholar]
  6. Paglietti B, Falchi G, Mason P, Chitsatso O, Nair S et al. Diversity among human non-typhoidal Salmonella isolates from Zimbabwe. Trans R Soc Trop Med Hyg 2013; 107:487–492 [View Article] [PubMed]
    [Google Scholar]
  7. Di Taranto P, Petruzzi F, Normanno G, Pedarra C, Occhiochiuso G et al. Prevalence and Antimicrobial Resistance of Salmonella Strains Isolated from Chicken Samples in Southern Italy. Microorganisms 2025; 13:270 [View Article] [PubMed]
    [Google Scholar]
  8. Boubendir S, Arsenault J, Quessy S, Thibodeau A, Fravalo P et al. Salmonella contamination of broiler chicken carcasses at critical steps of the slaughter process and in the environment of two slaughter plants: prevalence, genetic profiles, and association with the final carcass status. J Food Prot 2021; 84:321–332 [View Article] [PubMed]
    [Google Scholar]
  9. Oh H, Yoon Y, Yoon J-W, Oh S-W, Lee S et al. Salmonella risk assessment in poultry meat from farm to consumer in Korea. Foods 2023; 12:649 [View Article] [PubMed]
    [Google Scholar]
  10. Shaji S, Selvaraj RK, Shanmugasundaram R. Salmonella Infection in Poultry: A Review on the Pathogen and Control Strategies. Microorganisms 2023; 11:2814 [View Article] [PubMed]
    [Google Scholar]
  11. Adhikari M, Patil K, Acuff JC. Dried and Tested: Inoculation Method Impacts Low-Moisture Food Persistent Bacterial Populations. J Food Prot 2025; 88:100457 [View Article]
    [Google Scholar]
  12. Makaya PV, Matope G, Pfukenyi DM. Distribution of Salmonella serovars and antimicrobial susceptibility of Salmonella Enteritidis from poultry in Zimbabwe. Avian Pathol 2012; 41:221–226 [View Article] [PubMed]
    [Google Scholar]
  13. Mashe T, Thilliez G, Chaibva BV, Leekitcharoenphon P, Bawn M et al. Highly drug resistant clone of Salmonella Kentucky ST198 in clinical infections and poultry in Zimbabwe. NPJ Antimicrob Resist 2023; 1:6 [View Article]
    [Google Scholar]
  14. World Organization for Animal Health (WOAH) Terrestrial manual. In Chapter 3.10.7 – Salmonellosis 2022
    [Google Scholar]
  15. Babraham Bioinformatics FastQC: a quality control tool for high throughput sequence data; 2022 https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ accessed 28 March 2023
  16. MultiQC MultiQC; 2022 https://multiqc.info/ accessed 28 March 2024
  17. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011; 27:863–864 [View Article]
    [Google Scholar]
  18. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  19. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  20. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
    [Google Scholar]
  21. Feldgarden M, Brover V, Gonzalez-Escalona N, Frye JG, Haendiges J et al. AMRFinderPlus and the reference gene catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence. Sci Rep 2021; 11:12728 [View Article] [PubMed]
    [Google Scholar]
  22. [Google Scholar]
  23. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  24. Yoshida CE, Kruczkiewicz P, Laing CR, Lingohr EJ, Gannon VPJ et al. The Salmonella In Silico Typing Resource (SISTR): an open web-accessible tool for rapidly typing and subtyping draft Salmonella genome assemblies. PLoS One 2016; 11:e0147101 [View Article] [PubMed]
    [Google Scholar]
  25. Seeman T. Snippy; 2020 https://github.com/tseemann/snippy
  26. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
    [Google Scholar]
  27. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article]
    [Google Scholar]
  28. Wang J, Li Q, Jiang Y, Wang Z, Jiao X. fosA7: a silent fosfomycin resistance gene in Salmonella?. Lancet Microbe 2024; 5:e211 [View Article] [PubMed]
    [Google Scholar]
  29. Rehman MA, Yin X, Persaud-Lachhman MG, Diarra MS. First detection of a fosfomycin resistance gene, fosA7, in Salmonella enterica serovar Heidelberg isolated from broiler chickens. Antimicrob Agents Chemother 2017; 61:e00410–e00417 [View Article] [PubMed]
    [Google Scholar]
  30. Li M, Wang K, Tang A, Tang A, Chen A et al. Investigation of the genes involved in the outbreaks of Escherichia coli and Salmonella spp. in the United States. Antibiotics 2021; 10:1274 [View Article]
    [Google Scholar]
  31. Asfaw Ali D, Tadesse B, Ebabu A. Prevalence and antibiotic resistance pattern of Salmonella isolated from caecal contents of exotic chicken in Debre Zeit and Modjo, Ethiopia. Int J Microbiol 2020; 2020:1910630 [View Article] [PubMed]
    [Google Scholar]
  32. Sohail MN, Rathnamma D, Priya SC, Isloor S, Naryanaswamy HD et al. Salmonella from farm to table: isolation, characterization, and antimicrobial resistance of Salmonella from commercial broiler supply chain and its environment. Biomed Res Int 2021; 2021:3987111 [View Article] [PubMed]
    [Google Scholar]
  33. Waghamare R, Paturkar A, Vaidya V, Zende R, Chavak M et al. Risk of Salmonella in various poultry farming and processing operations around Mumbai, India. Int J Curr Microbiol App Sci 2020; 9:1024–1034 [View Article]
    [Google Scholar]
  34. Rouger A, Tresse O, Zagorec M. Bacterial contaminants of poultry meat: sources, species, and dynamics. Microorganisms 2017; 5:50 [View Article] [PubMed]
    [Google Scholar]
  35. Zeng H, Reu K, Gabriël S, Mattheus W, Zutter L et al. Salmonella prevalence and persistence in industrialized poultry slaughterhouses. Poult Sci 2021; 100:100991 [View Article]
    [Google Scholar]
  36. Dookeran MM, Baccus-Taylor GS, Akingbala JO, Tameru B, Lammerding AM. Assessing thermal inactivation of Salmonella on cooked broiler chicken carcasses in Trinidad and Tobago. TOPROCJ 2012; 3:12–19 [View Article]
    [Google Scholar]
  37. Assefa A, Dione M, Ilboudo G, Lallogo V, Gemeda BA et al. Quantitative analysis of knowledge, attitude and practice of workers in chicken slaughter slabs toward food safety and hygiene in Ouagadougou, Burkina Faso. Front Sustain Food Syst 2023; 6:1091209 [View Article]
    [Google Scholar]
  38. McKee S. Salmonella control in poultry processing. In 65th Annual Reciprocal Meat Conference 2011
    [Google Scholar]
  39. Karenga D. Salmonella Enteritidis in poultry flocks and abattoirs in Zimbabwe. Zimb Vet J 1997; 28:93–98 [View Article]
    [Google Scholar]
  40. Matope G, Schlundt J, Makaya PV, Aabo S, Baggesen DL. Salmonella Enteritidis in poultry: an emerging zoonosis in Zimbabwe. Zimb Vet J 1998; 29:132–138 [View Article]
    [Google Scholar]
  41. Feasey NA, Hadfield J, Keddy KH, Dallman TJ, Jacobs J et al. Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings. Nat Genet 2016; 48:1211–1217 [View Article] [PubMed]
    [Google Scholar]
  42. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 2009; 19:2279–2287 [View Article] [PubMed]
    [Google Scholar]
  43. Inns T, Ashton PM, Herrera-Leon S, Lighthill J, Foulkes S et al. Prospective use of whole genome sequencing (WGS) detected a multi-country outbreak of Salmonella Enteritidis. Epidemiol Infect 2017; 145:289–298 [View Article] [PubMed]
    [Google Scholar]
  44. Coipan CE, Dallman TJ, Brown D, Hartman H, van der Voort M et al. Concordance of SNP- and allele-based typing workflows in the context of a large-scale international Salmonella Enteritidis outbreak investigation. Microb Genom 2020; 6:1–13 [View Article] [PubMed]
    [Google Scholar]
  45. Ammar AM, Mohamed AA, Abd El-Hamid MI, El-Azzouny MM. Virulence genotypes of clinical Salmonella serovars from broilers in Egypt. J Infect Dev Ctries 2016; 10:337–346 [View Article] [PubMed]
    [Google Scholar]
  46. Mthembu TP, Zishiri OT, El Zowalaty ME. Detection and molecular identification of Salmonella virulence genes in livestock production systems in South Africa. Pathogens 2019; 8:1–13 [View Article] [PubMed]
    [Google Scholar]
  47. Thung TY, Radu S, Mahyudin NA, Rukayadi Y, Zakaria Z et al. Prevalence, virulence genes, and antimicrobial resistance profiles of Salmonella serovars from retail beef in Selangor, Malaysia. Front Microbiol 2018; 8: [View Article]
    [Google Scholar]
  48. Ammendola S, Ajello M, Pasquali P, Kroll JS, Langford PR et al. Differential contribution of sodC1 and sodC2 to intracellular survival and pathogenicity of Salmonella enterica serovar Choleraesuis. Microbes Infect 2005; 7:698–707 [View Article] [PubMed]
    [Google Scholar]
  49. Guillén S, Nadal L, Álvarez I, Mañas P, Cebrián G. Impact of the resistance responses to stress conditions encountered in food and food processing environments on the virulence and growth fitness of non-typhoidal Salmonellae. Foods 2021; 10:617 [View Article]
    [Google Scholar]
  50. Hawkey J, Le Hello S, Doublet B, Granier SA, Hendriksen RS et al. Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. Microb Genom 2019; 5: [View Article]
    [Google Scholar]
  51. Hendriksen RS. Emergence of multidrug-resistant Salmonella Kentucky ST198 with high-level resistance to ciprofloxacin in Europe and North Africa. Antimicrob Agents Chemother 2011; 55:4454–4461
    [Google Scholar]
  52. Le Hello S. Salmonella Kentucky ST198: a microbiological and epidemiological overview of an emerging multidrug-resistant serotype. Lancet Infect Dis 2013; 13:683–692 [View Article]
    [Google Scholar]
  53. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control The European Union One Health 2020 zoonoses report. EFS2 2021; 19:e06971 [View Article]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001550
Loading
/content/journal/mgen/10.1099/mgen.0.001550
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

EXCEL

Supplementary material 3

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error