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Background: Salmonella enterica subsp. enterica serovar Agona (antigenic formula 1,4,[5],12:f,g,s:[1,2]) is a serovar of the O:4 (B) serogroup. S. Agona is among the 15th most common serovars in humans the U.S., and the 4th most common serovar in clinical non-human sources. This serovar was first isolated from cattle in Ghana in 1952, since then numerous outbreaks in the U.S. and Europe have occurred. Multi Locus Sequence Typing (MLST) has identified only four sequence types. Genome sequencing of 73 strains from multiple countries and sources was recently reported by Zhou et al., 2013.  Animal reservoir: Different animal species, including turkey, swine and cattle are reservoirs of S. Agona. Geographical distribution: Serovar Agona is among the 10th most common serovars in North and South America, Europe, and Asia. In China, it is among the 10th most common serovars.

Outbreaks: Outbreaks linked to Salmonella Agona have been associated with different foods, including cereal, meat and fruits.

Year

Location

Associated source

Number of cases

2022

Sweden

Cucumbers (suspected)

35

2011

US-multistate

Imported Papayas

106

2008

US-multistate

Rice & Wheat Puff Cereal

28

2008

Europe (6 countries)

Meat, cocked sandwich

148

2008

Europe

Meat

119

2004

France

Infant formula

141

2002

Germany

Tea, aniseed herbal

42

1998

US-multistate

Toasted Oats Cereal

209

nontyphoidal Salmonella serotype isolated from human infections in China and is also among the top 20 most frequently reported Salmonella serotypes in the United States.

NCBI PD link for serovar Agona: https://www.ncbi.nlm.nih.gov/pathogens/isolates/#(taxgroup_name:%22Salmonella%20enterica%22)%20AND%20computed_types:(%22serotype=Agona%22)

Genetic characteristics: Serovar Agona has been found to be polyphyletic with one lineage identified and one stand-alone singleton that does not cluster with any other Salmonella Agona isolatesRelevant genetic characteristics: Whole genome sequences for 74 strains of S. Agona have been deposited at GenBank as of October, 2013. Genomic characteristics of the sequenced S. Agona include (i) a genome size ranging from 4.70 to 4.95 Mb, (ii) a mol G+C% of approx. 52, and (iii) 4,658 to 4,934 predicted genes. Comparative genomics of 73 of the sequenced strains identified three lineages of S. serovar Agona that emerged approx. 80 90 years ago.  S. Agona has Serovar Agona has an accessory genome of approx. 1.3 Mb; this accessory genome includes (i) multiple prophages (P2-like, Fels-like, Lambda-like), (ii) antibiotic resistance plasmids (e.g., IncI1 plasmids), (iii) genomic islands, (iv) transposons, and (v) chromosomal integrons.Phylogenetic  Phylogenetic and pan-genomic analyses that included one of the sequenced S. Agona serovar Agona strains and other Salmonella serovars concluded that S. serovar Agona belongs to clade A, according to den Bakker et al. (2011) classification and it contains 133 gene families unique to this serovar.  

Genome sequences available:

. Bartsch reported the MDR isolate, 18-SA00377, isolated in Germany in 2018, harbored pSE18-SA00377-1 plasmid (295,499 bp) carrying 16 ARGsSong et al. analyzed 209 Agona isolates obtained from food-producing animals during 2010–2020 in South Korea  and found that resistance to ampicillin, chloramphenicol, streptomycin, tetracycline, and trimethoprim/sulfamethoxazole was the most frequently observed MDR pattern (60.6%, 86/142) in isolates from chickens and ducks. Among the three sequence types (STs) detected-ST13, ST11, and ST292-ST13 was predominant. In a UK study, Waters et al. identified an increase in SNP variation in 207 Agona isolates associated with acute and persistent infections potentially reflecting a population expansion after acute S. Agona infection. 

Animal reservoir: Multiple animal species, including turkey, swine and cattle are reservoirs of serovar Agona.

Geographical distribution: Serovar Agona has been reported worldwide such as the US, the UK, and China.

Human outbreaks: Numerous outbreaks linked to Salmonella Agona have been associated with a variety of foods, including cereal, meat and fruits. Some examples are shown below. 

Year

Location

Associated source

Number of cases

2022

Europe: multi-country

Cucumbers

72

2011

US: multistate

Imported Papayas from Mexico

106

2008

US: multistate

Rice & Wheat Puff Cereal

28

2008

Europe: multi-country

Meat

119

2004

France

Infant formula

141

2002

Germany

Tea, aniseed herbal

42

1998

US: multistate

Toasted Oats Cereal

209

Border rejections: Multiple border rejections associated with serovar Agona have been reported. Here we selected two as examples.

Year

Exporting country

Importing country

Associated source

Product category

2024Poland

Italy

Turkey meat

Poultry meat and poultry meat products

2022China

Sweden

Organic soybean cake

Feed materials

Recalls: Multiple recalls associated with serovar Agona have been reported. Here we selected two as examples.

YearLocationRecalled foodType
2017FranceInfant formula1Ultra-processed food
1998US: multistateToasted Oats Cereal2Ready-to-Eat food

1 This recall was caused by an outbreak of Salmonella enterica serovar Agona associated with infant formula products manufactured by the Lactalis Nutrition Santé group in France.

2 This recall was caused by an multistate outbreak of Salmonella serovar Agona infections linked to toasted oats cereal manufactured by Malt-O-Meal. 

Relevant links:

  1. https://pubmed
  2. Salmonella enterica subsp. enterica serovar Agona str. SL483 http://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=454166&lvl=3&lin=f&keep=1&srchmode=1&unlock
  3. Salmonella enterica subsp. enterica serovar Agona str. SH08SF124 http://www.ncbi.nlm.nih.gov/assembly/526088/
  4. Salmonella enterica subsp. enterica serovar Agona str. SH10GFN094 http://www.ncbi.nlm.nih.gov/assembly/526108/
  5. Salmonella enterica subsp. enterica serovar Agona str. SH11G1113 http://www.ncbi.nlm.nih.gov/assembly/526068/
  6. Salmonella enterica subsp. enterica serovar Agona str. 73.H.09 http://www.ncbi.nlm.nih.gov/assembly/689058/
  7. Salmonella enterica subsp. enterica serovar Agona str. 72.A.52 http://www.ncbi.nlm.nih.gov/assembly/689078/
  8. Salmonella enterica subsp. enterica serovar Agona str. 71.E.05 http://www.ncbi.nlm.nih.gov/assembly/689098/
  9. Salmonella enterica subsp. enterica serovar Agona str. 70.E.05 http://www.ncbi.nlm.nih.gov/assembly/689118/
  10. Salmonella enterica subsp. enterica serovar Agona str. 69.H.06 http://www.ncbi.nlm.nih.gov/assembly/689138/
  11. Salmonella enterica subsp. enterica serovar Agona str. 68.U.05 http://www.ncbi.nlm.nih.gov/assembly/689158/
  12. Salmonella enterica subsp. enterica serovar Agona str. 67.H.09 http://www.ncbi.nlm.nih.gov/assembly/689318/
  13.  Salmonella enterica subsp. enterica serovar Agona str. 66.F.99 http://www.ncbi.nlm.nih.gov/assembly/689178/
  14. Salmonella enterica subsp. enterica serovar Agona str. 65.H.72 http://www.ncbi.nlm.nih.gov/assembly/653108/
  15. Salmonella enterica subsp. enterica serovar Agona str. 64.H.00 http://www.ncbi.nlm.nih.gov/assembly/689198/
  16. Salmonella enterica subsp. enterica serovar Agona str. 63.H.87 http://www.ncbi.nlm.nih.gov/assembly/689218/
  17. Salmonella enterica subsp. enterica serovar Agona str. 62.H.72 http://www.ncbi.nlm.nih.gov/assembly/689238/
  18.  Salmonella enterica subsp. enterica serovar Agona str. 61.O.08 http://www.ncbi.nlm.nih.gov/assembly/689258/
  19. Salmonella enterica subsp. enterica serovar Agona str. 60.O.08 http://www.ncbi.nlm.nih.gov/assembly/689278/
  20. Salmonella enterica subsp. enterica serovar Agona str. 59.F.08 http://www.ncbi.nlm.nih.gov/assembly/689298/
  21. Salmonella enterica subsp. enterica serovar Agona str. 58.E.08 http://www.ncbi.nlm.nih.gov/assembly/676478/
  22. Salmonella enterica subsp. enterica serovar Agona str. 57.A.08 http://www.ncbi.nlm.nih.gov/assembly/677478/
  23. Salmonella enterica subsp. enterica serovar Agona str. 56.O.08 http://www.ncbi.nlm.nih.gov/assembly/676498/
  24. Salmonella enterica subsp. enterica serovar Agona str. 55.U.08 http://www.ncbi.nlm.nih.gov/assembly/676518/
  25. Salmonella enterica subsp. enterica serovar Agona str. 54.O.08 http://www.ncbi.nlm.nih.gov/assembly/676538/
  26. Salmonella enterica subsp. enterica serovar Agona str. 53.F.08 http://www.ncbi.nlm.nih.gov/assembly/676558/
  27. Salmonella enterica subsp. enterica serovar Agona str. 52.F.08 http://www.ncbi.nlm.nih.gov/assembly/676578/
  28. Salmonella enterica subsp. enterica serovar Agona str. 51.E.09 http://www.ncbi.nlm.nih.gov/assembly/676598/
  29. Salmonella enterica subsp. enterica serovar Agona str. 50.E.08 http://www.ncbi.nlm.nih.gov/assembly/676618/
  30. Salmonella enterica subsp. enterica serovar Agona str. 49.E.09 http://www.ncbi.nlm.nih.gov/assembly/677498/
  31. Salmonella enterica subsp. enterica serovar Agona str. 48.E.08 http://www.ncbi.nlm.nih.gov/assembly/676638/
  32. Salmonella enterica subsp. enterica serovar Agona str. 46.E.09 http://www.ncbi.nlm.nih.gov/assembly/676658/
  33. Salmonella enterica subsp. enterica serovar Agona str. 45.E.09 http://www.ncbi.nlm.nih.gov/assembly/676678/
  34. Salmonella enterica subsp. enterica serovar Agona str. 44.E.09 http://www.ncbi.nlm.nih.gov/assembly/676698/
  35. Salmonella enterica subsp. enterica serovar Agona str. 43.E.09 http://www.ncbi.nlm.nih.gov/assembly/676718/
  36. Salmonella enterica subsp. enterica serovar Agona str. 42.E.09 http://www.ncbi.nlm.nih.gov/assembly/676738/
  37. Salmonella enterica subsp. enterica serovar Agona str. 41.E.09 http://www.ncbi.nlm.nih.gov/assembly/676778/
  38. Salmonella enterica subsp. enterica serovar Agona str. 40.E.08 http://www.ncbi.nlm.nih.gov/assembly/676758/
  39. Salmonella enterica subsp. enterica serovar Agona str. 39.O.03 http://www.ncbi.nlm.nih.gov/assembly/677518/
  40. Salmonella enterica subsp. enterica serovar Agona str. 38.O.03 http://www.ncbi.nlm.nih.gov/assembly/676798/
  41. Salmonella enterica subsp. enterica serovar Agona str. 37.F.02 http://www.ncbi.nlm.nih.gov/assembly/676818/
  42. Salmonella enterica subsp. enterica serovar Agona str. 36.H.00 http://www.ncbi.nlm.nih.gov/assembly/676838/Salmonella enterica subsp. enterica serovar Agona str. 35.H.08 http13902866/
  43. https://www.ncbi.nlm.nih.gov/assembly/676858/
  44. Salmonella enterica subsp. enterica serovar Agona str. 34.H.09 http://www.ncbi.nlm.nih.gov/assembly/676878/
  45. liebertpub.com/doi/full/10.1089/fpd.2010.0827?casa_token=r5_H4WYgMn0AAAAA%3A5MU6aDnk2JmPoDATaXDvLO7TXqqWkEc57PaWFHA6ef0LkN2mJecTbfXy73ZKQ06d-5LnTu3a6w
  46. https://pmcSalmonella enterica subsp. enterica serovar Agona str. 33.A.05 http://www.ncbi.nlm.nih.gov/assemblyarticles/676898PMC3739514/Salmonella enterica subsp. enterica serovar Agona str. 31.A.00 http
  47. https://www.ncbi.nlm.nih.gov/assembly/676918/
  48. Salmonella enterica subsp. enterica serovar Agona str. 31.H.09 http://www.ncbi.nlm.nih.gov/assembly/676938/
  49. Salmonella enterica subsp. enterica serovar Agona str. 30.H.04 http://www.ncbi.nlm.nih.gov/assembly/677538/
  50. Salmonella enterica subsp. enterica serovar Agona str. 29.O.08 http://www.ncbi.nlm.nih.gov/assembly/676958/
  51. Salmonella enterica subsp. enterica serovar Agona str. 28.O.08 http://www.ncbi.nlm.nih.gov/assembly/676978/
  52. Salmonella enterica subsp. enterica serovar Agona str. 27.O.98 http://www.ncbi.nlm.nih.gov/assembly/676998/
  53. Salmonella enterica subsp. enterica serovar Agona str. 26.F.98 http://www.ncbi.nlm.nih.gov/assembly/677558/
  54. Salmonella enterica subsp. enterica serovar Agona str. 24.H.04 http://www.ncbi.nlm.nih.gov/assembly/677018/
  55. Salmonella enterica subsp. enterica serovar Agona str. 23.F.01 http://www.ncbi.nlm.nih.gov/assembly/677038/
  56. Salmonella enterica subsp. enterica serovar Agona str. 22.H.04 http://www.ncbi.nlm.nih.gov/assembly/677058/
  57. Salmonella enterica subsp. enterica serovar Agona str. 21.H.10 http://www.ncbi.nlm.nih.gov/assembly/677078/
  58. frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2025.1547190/full
  59. https://journals.asm.org/doi/10.1128/aem.00591-19#:~:text=Agona%20is%20ranked%20among%20the,and%20different%20animal%2Dbased%20foods.
  60. https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1003471
  61. https://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-12-425
  62. https://pmcSalmonella enterica subsp. enterica serovar Agona str. 20.H.06 http://www.ncbi.nlm.nih.gov/assemblyarticles/677098PMC3175032/Salmonella enterica subsp. enterica serovar Agona str. 19.F.03
  63. httphttps://wwwpmc.ncbi.nlm.nih.gov/assemblyarticles/677118PMC10686068/Salmonella enterica subsp. enterica serovar Agona str. 18.H.07 http
  64. https://www.ncbi.nlm.nih.gov/assembly/677138/
  65. Salmonella enterica subsp. enterica serovar Agona str. 17.H.06 http://www.ncbi.nlm.nih.gov/assembly/677158/
  66. Salmonella enterica subsp. enterica serovar Agona str. 15.H.03 http://www.ncbi.nlm.nih.gov/assembly/677178/
  67. liebertpub.com/doi/10.1089/fpd.2023.0117?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub%20%200pubmed
  68. https://pmcSalmonella enterica subsp. enterica serovar Agona str. 14.E.05 http://www.ncbi.nlm.nih.gov/assemblyarticles/677198PMC11556752/Salmonella enterica subsp. enterica serovar Agona str. 13.E.05 http
  69. https://www.ncbi.nlm.nih.gov/assembly/677218/
  70. Salmonella enterica subsp. enterica serovar Agona str. 12.A.06 http://www.ncbi.nlm.nih.gov/assembly/677238/
  71. Salmonella enterica subsp. enterica serovar Agona str. 11.A.05 http://www.ncbi.nlm.nih.gov/assembly/677258/
  72. Salmonella enterica subsp. enterica serovar Agona str. 10.A.05 http://www.ncbi.nlm.nih.gov/assembly/677458/
  73. Salmonella enterica subsp. enterica serovar Agona str. 09.F.08 http://www.ncbi.nlm.nih.gov/assembly/677278/
  74. Salmonella enterica subsp. enterica serovar Agona str. 08.A.05 http://www.ncbi.nlm.nih.gov/assembly/677298/
  75. Salmonella enterica subsp. enterica serovar Agona str. 07.O.05 http://www.ncbi.nlm.nih.gov/assembly/677318/
  76. foodsafetynews.com/2022/12/cucumbers-linked-to-multi-country-salmonella-outbreak/
  77. https://archive.cdc.gov/www_cdc_gov/salmonella/2011/papayas-8-29-2011.html
  78. https://archive.cdc.gov/www_cdc_gov/salmonella/2008/rice-wheat-puff-cereal-5-13-2008.html
  79. https://www.researchgate.net/publication/23228196_A_multi-country_outbreak_of_Salmonella_Agona_February_-_August_2008
  80. https://pubmedSalmonella enterica subsp. enterica serovar Agona str. 06.O.05 http://www.ncbi.nlm.nih.gov/assembly17259878/677338/Salmonella enterica subsp. enterica serovar Agona str. 05.O.06
  81. httpshttp://wwwpmc.ncbi.nlm.nih.gov/assemblyarticles/677358PMC3371796/Salmonella enterica subsp. enterica serovar Agona str. 04.O.05
  82. httphttps://www.ncbi.nlm.nihcdc.gov/assemblymmwr/677378/
  83. Salmonella enterica subsp. enterica serovar Agona str. 03.O.05 http://www.ncbi.nlm.nih.gov/assembly/677398/
  84. Salmonella enterica subsp. enterica serovar Agona str. 02.O.05 http://www.ncbi.nlm.nih.gov/assembly/677418/
  85. Salmonella enterica subsp. enterica serovar Agona str. 01.O.05 http://www.ncbi.nlm.nih.gov/assembly/677438/

Relevant links and references:

  1. preview/mmwrhtml/00053368.htm
  2. https://webgate.ec.europa.eu/rasff-window/screen/notification/722223
  3. https://webgate.ec.europa.eu/rasff-window/screen/notification/559290
  4. https://www.who.int/emergencies/disease-outbreak-news/item/22-december-2017-salmonella-agona-infections-france-en
  5. http://www.cdc.gov/salmonella/agona-papayas/index.html
  6. http://www.ncbi.nlm.nih.gov/pubmed/20950515
  7. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=18956
  8. http://genomea.asm.org/content/1/1/e00203-12.full
  9. http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1003471