Distribution and genotypic diversity of Listeria monocytogenes strains isolated from humans and ruminants with common clinical and pathological phenotypes (neurolisterioses and abortions) (review)

Listeria (L.) monocytogenes is an intracellular food pathogen that causes listeriosis in mammals in the form of sporadic cases or large outbreaks with a high mortality rate among humans and domestic ruminants. The determination of the sequence type (ST) and the clonal complex (CC) by multilocus sequencing (MLST) and other methods in L. monocytogenes strains from different sources allowed us to establish the existence of strains with organ tropism and causing forms of listeriosis common to humans and ruminants. The purpose of the review was to generalize the available data on the distribution and genotypic diversity of L. monocytogenes strains isolated during neurolisteriosis and abortions, their adaptation in the environment to determine a possible link between listeriosis of ruminants and humans. In general, the analysis of the differential distribution of STs/CCs of L. monocytogenes associated with humans and ruminants showed their significant variation, as well as the predominance of CCs (CC1, CC2, CC4, CC6, CC7, CC8, CC14, CC29, CC37, etc.) common to the studied host groups. Neurolisterioses in humans are mainly associated with hypervirulent CC1, CC6, CC4, CC2, in ruminants - CC1 and CC4, as well as CC8-16 and CC412. A special association of ST1 (CC1) with human and bovine neurolisteriosis has been determined, indicating increased neurotropism of ST1. In small ruminants (goats, sheep), neurolisterioses are associated with various STs from phylogenetic lineages I and II. Most of L. monocytogenes strains isolated from abortions belonged to CC1, CC2, CC4, CC6, CC7, CC14 in humans and CC1, CC6, CC4-217, CC37 in ruminants. The detection of common isolates CC1, CC4-CC217, CC6, CC18, CC37 in ruminants and in their natural environment indicates that the farm environment is a reservoir for L. monocytogenes strains. In the Russian Federation, the prevalence of SТ7 isolates among all types of sources obtained on the territory of the country was noted. Future research should be aimed at studying the pathogenicity of L. monocytogenes strains with an increased tendency to cause diseases in humans and ruminants for better understanding the mechanisms of infection and strengthening the control over the spread of the pathogen in various ecological niches. 

1. European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). The European Union One Health 2018. Zoonoses Report. EFSA J. 2019;17(12):e05926. DOI: https://doi.org/10.2903/j.efsa.2019.5926

2. Oevermann A., Zurbriggen A., Vandevelde M. Rhombencephalitis Caused by Listeria monocytogenes in Humans and Ruminants: A Zoonosis on the Rise? Interdiscip. Perspect. Infect. Dis. 2010;632513. DOI: https://doi.org/10.1155/2010/632513

3. Goulet V., Hedberg C., Le Monnier A., de Valk H. Increasing incidence of listeriosis in France and other European countries. Emerging Infectious Diseases. 2008;14(5):734-740. DOI: https://doi.org/10.3201/eid1405.071395

4. Adgamov R., Zaytseva E., Thiberge J. M., Brisse B., Ermolaeva S. Genetically related Listeria monocytogenes strains isolated from lethal human cases and wild animals. In: Genetic Diversity in Microorganisms. Rijeka, Croatia: InTech, 2012. pp. 235-250. DOI: https://doi.org/10.5772/32913

5. Walland J., Lauper J., Frey J., Imhof R., Stephan R., Seuberlich T., Oevermann A. Listeria monocytogenes infection in ruminants: Is there a link to the environment, food and human health? A review. Schweiz. Arch. Tierheilkd. 2015;157(6):319-328. DOI: https://doi.org/10.17236/sat00022

6. Dreyer M., Aguilar-Bultet L., Rupp S., Guldimann C., Stephan R., Schock A., Otter A., Schupbach G., Brisse S., Lecuit M., Frey J., Oevermann A. Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis. Sci. Rep. 2016;6:36419. DOI: https://doi.org/10.1038/srep36419

7. Papić B., Pate M., Félix B., Kušar D. Genetic diversity of Listeria monocytogenes strains in ruminant abortion and rhomenchephalitis cases in comparison with the natural environment. BMC Microbiol. 2019;19:299. DOI: https://doi.org/10.1186/s12866-019-1676-3

8. Vazquez-Boland J. A., Kuhn M., Berche P., Chakraborty T., Domínguez-Bernal G., Goebel W., GonzálezZorn B., Wehland J., Kreft J. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 2001;14(3):584-640. DOI: https://doi.org/10.1128/CMR.14.3.584-640.2001

9. Precht C., Vermathen P., Henke D., Staudacher A., Lauper J., Seuberlich T., Oevermann A., SchweizerGorgas D. Correlative Magnetic Resonance Imaging and Histopathology in Small Ruminant Listeria Rhombencephalitis. Front Neurol. 2020;11:518697. DOI: https://doi.org/10.3389/fneur.2020.518697

10. Oevermann A., Botteron C., Seuberlich T., Nicolier A., Friess M., Doherr M. G., Heim D., Hilbe M., Zimmer K., Zurbriggen A., Vandevelde M. Neuropathological survey of fallen stock: Active surveillance reveals high prevalence of encephalitic listeriosis in small ruminants. Vet. Microbiol. 2008;130(3-4):320-329. DOI: https://doi.org/10.1016/j.vetmic.2008.01.015

11. Bartt R. Listeria and atypical presentations of Listeria in the central nervous system. Semin. Neurol. 2000;20(3):361-374. DOI: https://doi.org/10.1055/s-2000-9398

12. Swaminathan B., Gerner-Smidt P. The epidemiology of human listeriosis. Microbes. Infect. 2007;9(10):1236-1243. DOI: https://doi.org/10.1016/j.micinf.2007.05.011

13. Dell’Armelina Rocha P. R., Lomonaco S., Bottero M. T., Dalmasso A., Dondo A., Grattarola C., Zuccon F., Iulini B., Knabel S. J., Capucchio M. T., Casalone C. Ruminant rhombencephalitis-associated Listeria monocytogenes strains constitute a genetically homogeneous group related to human outbreak strains. Appl. Environ. Microbiol. 2013;79(9):3059-3066. DOI: https://doi.org/10.1128/AEM.00219-13

14. EFSA, ECDC. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J. 2012;10(3):2597. DOI: https://doi.org/10.2903/j.efsa.2012.2597

15. Jensen A. K., Björkman J. T., Ethelberg S., Kiil K., Kemp M., Nielsen E. M. Molecular typing and epidemiology of human listeriosis cases, Denmark, 2002-2012. Emerg Infect Dis. 2016;22(4):625-633. DOI: https://doi.org/10.3201/eid2204.150998

16. Kuch A., Goc A., Belkiewicz K., Filipello V., Ronkiewicz P., Gołębiewska A., Wróbel I., Kiedrowska M., Waśko I., Hryniewicz W., Lomonaco S., Skoczyńska A. Molecular diversity and antimicrobial susceptibility of Listeria monocytogenes isolates from invasive infections in Poland (1997-2013). Sci Rep. 2018;8(1):14562. DOI: https://doi.org/10.1038/s41598-018-32574-0

17. EFSA, ECDC. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J. 2017;15(12):e05077. DOI: https://doi.org/10.2903/j.efsa.2017.5077

18. Painset A., Björkman J. T., Kiil K., Guillier L., Mariet J. F., Félix B., Amar C., Rotariu O., Roussel S., Perez-Reche F., Brisse S., Moura A., Lecuit M., Forbes K., Strachan N., Grant K., Møller-Nielsen E., Dallman T. J. LiSEQ − whole-genome sequencing of a cross-sectional survey of Listeria monocytogenes in ready-to-eat foods and human clinical cases in Europe. Microb. Genom. 2019;5(2):е000257. DOI: https://doi.org/10.1099/mgen.0.000257

19. Petrovic V., Petrovic M., Dragovac G., Ristic M., Medic S., Ilic S., Rachevic S., Shtrbac M. Infectious Diseases in Vojvodina in 2018. Institute of Public Health of Vojvod: Novi Sad, Serbia. 2019. pp. 97-98.

20. Lüth S., Halbedel S., Rosner B., Wilking H., Holzer A., Roedel A., Dieckmann R., Vincze S., Prager R., Flieger A., Al Dahouk S., Kleta S. Backtracking and forward checking of human listeriosis clusters identified a multiclonal outbreak linked to Listeria monocytogenes in meat products of a single producer. Emerg. Microbes Infect. 2020;9(1):1600-1608. DOI: https://doi.org/10.1080/22221751.2020.1784044

21. Goulet V., King L. A., Vaillant V., de Valk H. What is the incubation period for listeriosis? BMC Infect Dis. 2013;10:11. DOI: https://doi.org/10.1186/1471-2334-13-11

22. Félix B., Feurer C., Maillet A., Guillier L., Boscher E., Kerouanton A., Denis M., Roussel S. Population Genetic Structure of Listeria monocytogenes Strains Isolated From the Pig and Pork Production Chain in France. Front. Microbiol. 2018;9:684. DOI: https://doi.org/10.3389/fmicb.2018.00684

23. 7 Kovalev V. A., Filatov N. N., Aleshina E. N., Simonova E. G. Zabolevaemost' listeriozom v Rossiyskoy Federatsii. [Sickness of listeriosis in Russian Federation]. Nauka molodykh (Eruditio Juvenium) = Science of the young (Eruditio Juvenium). 2019;7(4):509-517. (In Russ.). DOI: https://doi.org/10.23888/HMJ201974509-517

24. Smith A. M., Tau N. P., Smouse S. L., Allam M., Ismail A., Ramalwa N. R., Disenyeng, B., Ngomane M., Thomas J. Outbreak of Listeria monocytogenes in South Africa, 2017–2018: Laboratory Activities and Experiences Associated with Whole-Genome Sequencing Analysis of Isolates. Foodborne Pathog. Dis. 2019;16(7):524-530. DOI: https://doi.org/10.1089/fpd.2018.2586

25. Outbreak investigation of Listeria monocytogenes: enoki mushrooms (March 2020). URL: https://www.fda.gov/food/outbreaks-foodborne-illness/outbreak-investigation-listeria-monocytogenes-enokimushrooms-march-2020

26. Whitworth J. Officials Report More Patients in Listeria Outbreak Linked to Cheese. URL: https://www.foodsafetynews.com/2020/05/more-patients-reported-in-listeria-outbreak-linked-to-cheese

27. Orsi R. H., den Bakker H. C., Wiedmann M. Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics. Int. J. Med. Microbiol. 2011;301(2):79-96. DOI: https://doi.org/10.1016/j.ijmm.2010.05.002

28. Truchet L., Walland J., Wüthrich D., Boujon C. L., Posthaus H. Neuropathological survey reveals underestimation of the prevalence of neuroinfectious diseases in cattle in Switzerland. Vet Microbiol. 2017;208:137-145. DOI: https://doi.org/10.1016/j.vetmic.2017.07.027

29. Kotzamanidis C., Papadopoulos T., Vafeas G., Tsakos P., Giantzi V., Zdragas A. Characterization of Listeria monocytogenes from encephalitis cases of small ruminants from different geographical regions, in Greece. Journal of Applied Microbiology. 2019;126(5):1373-1382. DOI: https://doi.org/10.1111/jam.14244

30. Papić B., Kušar D., Zdovc I., Golob M., Pate M. Retrospective investigation of listeriosis outbreaks in small ruminants using different analytical approaches for whole genome sequencing-based typing of Listeria monocytogenes. Infection, Genetics and Evolution. 2020;77:104047. DOI: https://doi.org/10.1016/j.meegid.2019.104047

31. Karaulov A. K., Varkentin A. V., Petrova O. N., Semenova N. A., Batashova D. S., Korennoy F. I. Epizooticheskaya situatsiya v Rossiyskoy Federatsii 2020 god. Informatsionno-analiticheskiy tsentr Rossel'-khoznadzora. [Epizootic situation in the Russian Federation in 2020. Information and Analytical Center of the Rosselkhoznadzor]. (In Russ.). URL: https://fsvps.gov.ru/fsvps-docs/ru/iac/rf/2020/iac2020_all.pdf

32. BIGSdb-Pasteur MLST database. URL: https://bigsdb.web.pasteur.fr/listeria/listeria.html (accessed on 16.12.2021).

33. Stessl B., Wagner M., Ruppitsch W. Multilocus Sequence Typing (MLST) and Whole Genome Sequencing (WGS) of Listeria monocytogenes and Listeria innocua. Methods Mol. Biol. 2021;2220:89-103. DOI: https://doi.org/10.1007/978-1-0716-0982-8_7

34. Camargo A. C., Woodward J. J., Nero L. A. The Continuous Challenge of Characterizing the Food-borne Pathogen Listeria monocytogenes. Foodborne Pathog. Dis. 2016;13(8): 405-416. DOI: https://doi.org/10.1089/fpd.2015.2115

35. Bakker den H. C., Fortes E. D., Wiedmann M. Multilocus sequence typing of out-break-associated Listeria monocytogenes isolates to identify epidemic clones. Foodborne pathogens and disease. 2010;7(3):257-265. DOI: https://doi.org/10.1089/fpd.2009.0342

36. Jeffers G. T., Bruce J. L., McDonough P. L., Scarlett J., Boor K. J., Wiedmann M. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology. 2001;147(5):1095-1104. DOI: https://doi.org/10.1099/00221287-147-5-1095

37. Ho A. J., Ivanek R., Grohn Y. T., Nightingale K. K., Wiedmann M. Listeria monocytogenes fecal shedding in dairy cattle shows high levels of day-to-day variation and includes outbreaks and sporadic cases of shedding of specific L. monocytogenes subtypes. Prev. Vet. Med. 2007;80(4):287-305. DOI: https://doi.org/10.1016/j.prevetmed.2007.03.005

38. Dreyer M., Thomann A., Böttcher S., Frey J., Oevermann A. Outbreak investigation identifies a single Listeria monocytogenes strain in sheep with different clinical manifestations, soil and water. Vet. Microbiol. 2015;179(1-2):69-75. DOI: https://doi.org/10.1016/j.vetmic.2015.01.025

39. Maury M. M., Bracq-Dieye H., Huang L., Vales G., Lavina M., Thouvenot P., Disson O., Leclercq A., Brisse S., Lecuit M. Hypervirulent Listeria monocytogenes clones’ adaption to mammalian gut accounts for their association with dairy products. Nat. Commun. 2019;10(1):2488. DOI: https://doi.org/10.1038/s41467-019-10380-0

40. Esteban J. I., Oporto B., Aduriz G., Juste R. A., Hurtado A. Faecal shedding and strain diversity of Listeria monocytogenes in healthy ruminants and swine in Northern Spain. BMC Vet. Res. 2009;(5):2. DOI: https://doi.org/10.1186/1746-6148-5-2

41. Terentjeva M., Šteingolde Ž., Meistere I., Elferts D., Avsejenko J., Streikiša M., Gradovska S., Alksne L., Ķibilds J., Bērziņš A. Prevalence, Genetic Diversity and Factors Associated with Distribution of Listeria monocytogenes and Other Listeria spp. in Cattle Farms in Latvia. Pathogens. 2021;10(7):851. DOI: https://doi.org/10.3390/pathogens10070851

42. Castro H., Jaakkonen A., Hakkinen M., Korkeala H., Lindström M. Occurrence, persistence, and contamination routes of Listeria monocytogenes genotypes on three Finnish dairy cattle farms: A Longitudinal study. Appl. Environ. Microbiol. 2018;84(4):е02000-17. DOI: https://doi.org/10.1128/AEM.02000-17

43. Kim S. W., Haendiges J., Keller E. N., Myers R., Kim A., Lombard J. E., Karns J. S., Van Kessel J. A. S., Haley B. J. Genetic diversity and virulence profiles of Listeria monocytogenes recovered from bulk tank milk, milk filters, and milking equipment from dairies in the United States (2002 to 2014). PLoS One. 2018;13(5):e0197053. DOI: https://doi.org/10.1371/journal.pone.0197053

44. Bandelj P., Jamnikar-Ciglenecki U., Ocepek M., Blagus R., Vengust M. Risk factors associated with fecal shedding of Listeria monocytogenes by dairy cows and calves. J. Vet. Intern. Med. 2018;32(5):1773-1779. DOI: https://doi.org/10.1111/jvim.15234

45. Knabel S. J., Reimer A., Verghese B., Lok M., Ziegler J., Farber J., Pagotto F., Graham M., Nadon C. A., Gilmour M. W. Sequence typing confirms that a predominant Listeria monocytogenes clone caused human listeriosis cases and outbreaks in Canada from 1988 to 2010. J. Clin. Microbiol. 2012;50(5):1748-1751. DOI: https://doi.org/10.1128/JCM.06185-11

46. Chen Y., Gonzalez-Escalona N., Hammack T. S., Allard M. W., Strain E. A., Brown E. W. Core genome multilocus sequence typing for identification of globally distributed clonal groups and differentiations of outbreaks of strains of Listeria monocytogenes. Appl. Environ. Microbiol. 2016;82(20):6258-6272. DOI: https://doi.org/10.1128/AEM.01532-16

47. Raschle S., Stephan R., Stevens M. J. A., Cernela N., Zurfluh K., Muchaamba F., Nüesch-Inderbinen M. Environmental dissemination of pathogenic Listeria monocytogenes in flowing surface waters in Switzerland. Sci. Rep. 2021;11:9066. DOI: https://doi.org/10.1038/s41598-021-88514-y

48. Moura A., Criscuolo A., Pouseele H., Maury M. M., Leclercq A., Tarr C., Björkman J. T., Dallman T., Reimer A., Enouf V., Larsonneur E., Carleton H., Bracq-Dieye H., Katz L. S., Jones L., Touchon M., Tourdjman M., Walker M., Stroika S., Cantinelli T., Chenal-Francisque V., Kucerova Z., Rocha E. P., Nadon C., Grant K., Nielsen E. M., Pot B., Gerner-Smidt P., Lecuit M., Brisse S. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol. 2016;(2):16185. DOI: https://doi.org/10.1038/nmicrobiol.2016.185

49. Althaus D., Lehner A., Brisse S., Maury M., Tasara T., Stephan R. Characterization of Listeria monocytogenes strains isolated during 2011-2013 from human infections in Switzerland. Foodborne Pathogens and Disease. 2014;11(10):753-758. DOI: https://doi.org/10.1089/fpd.2014.1747

50. Maury M. M., Tsai Y. H., Charlier C., Touchon M., Chenal-Francisque V., Leclercq A., Criscuolo A., Gaultier C., Roussel S., Brisabois A., Disson O., Rocha E. P. C., Brisse S., Lecuit M. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nature genetics. 2016;48:308-313. DOI: https://doi.org/10.1038/ng.3501

51. Bespalova T. Y., Mikhaleva T. V., Meshcheryakova N. Y., Kustikova O. V., Matovic K., Dmitri´c M., Zaitsev S. S., Khizhnyakova M. A., Feodorova V. A. Novel Sequence Types of Listeria monocytogenes of Different Origin Obtained in the Republic of Serbia. Microorganisms. 2021;9(6):1289. DOI: https://doi.org/10.3390/microorganisms9061289

52. Aguilar-Bultet L., Nicholson P., Rychener L., Dreyer M., Gözel B., Origgi F. C., Oevermann A., Frey J., Falquet L. Genetic separation of Listeria monocytogenes causing central nervous system infections in animals. Front Cell Infect Microbiol. 2018;8:20. DOI: https://doi.org/10.3389/fcimb.2018.00020

53. Koopmans M. M., Engelen-Lee J., Brouwer M. C., Jaspers V., Man W. K., Vall Seron M., van de Beek D. Characterization of a Listeria monocytogenes meningitis mouse model. J. Neuroinflammation. 2018;15(1):257. DOI: https://doi.org/10.1186/s12974-018-1293-3

54. Voronina O. L., Kunda M. S., Ryzhova N. N., Kutuzova A. V., Aksenova E. I., Karpova T. I., Tartakovskiy I. S., Yushchuk N. D., Klimova E. A., Karetkina G. N., Chemeris O. Yu., Gruzdeva O. A., Melkumyan A. R., Orlova O. E., Burmistrova E. N. Listerioz. Genotipirovanie kak klyuch k vyyavleniyu vozmozhnogo istochnika zarazheniya. [Listeriosis: genotyping as a key for identification a possible source of infection]. Klinicheskaya mikrobiologiya i antimikrobnaya khimioterapiya = Clinical Microbiology and Antimicrobial Chemotherapy. 2019;21(4):261-273. (In Russ.). DOI: https://doi.org/10.36488/cmac.2019.4.261-273

55. Cardenas-Alvarez M.X., Townsend Ramsett M.K., Malekmohammadi S., Bergholz T.M. Evidence of hypervirulence in Listeria monocytogenes clonal complex 14. J Med Microbiol. 2019;68(11):1677-1685. DOI: https://doi.org/10.1099/jmm.0.001076

56. Voronina O. L., Tartakovskiy I. S., Yushchuk N. D., Ryzhova N. N., Aksenova E. I., Kunda M. S., Kutuzova A. V., Melkumyan A. R., Karpova T. I., Gruzdeva O. A., Klimova E. A., Karetkina G. N., Chemeris O. Yu., Tarasova T. A., Dronina Yu. E., Orlova O. E., Burmistrova E. N., Tsibin A. N. Analiz sporadicheskikh sluchaev invazivnogo listerioza v megapolise. [Analysis of sporadic cases of invasive listeriosis in a metropolis]. Zhurnal mikrobiologii, epidemiologii i immunobiologii = Journal of Microbiology, Epidemiology and Immunobiology. 2020;97(6):546-555. (In Russ.). DOI: https://doi.org/10.36233/0372-9311-2020-97-6-5

57. Psareva E. K., Egorova I. Y., Liskova E. A., Razheva I. V., Gladkova N. A., Sokolova E. V., Potemkin E. E., Zhurilov P. А., Mikhaleva T. V., Blokhin A. А., Chalenko Y. М., Kolbasov D. V., Ermolaeva S. A. Retrospective Study of Listeria monocytogenes isolated in the territory of inner Eurasia from 1947 to 1999. Pathogens. 2019;8(4):184. DOI: https://doi.org/10.3390/pathogens8040184

58. Voronina O. L., Ryzhova N. N., Kunda M. S., Kurnaeva M. A., Semenov A. N., Aksenova E. I., Egorova I. Y., Kolbasov D. V., Ermolaeva S. A., Gintsburg A. L. Diversity and Pathogenic Potential of Listeria monocytogenes Isolated from Environmental Sources in the Russian Federation. IJMER. 2015;5(3):5-15. URL: https://www.researchgate.net/publication/274510695_Diversity_and_Pathogenic_Potential_of_Listeria_monocytoge nes_Isolated_from_Environmental_Sources_in_the_Russian_Federation

59. Ragon M., Wirth T., Hollandt F., Lavenir R., Lecuit M., Le Monnier A., Brisse S. A new perspective on listeria monocytogenes evolution. PLoS Pathog. 2008;4(9):e1000146. DOI: https://doi.org/10.1371/journal.ppat.1000146

60. Steckler A. J., Cardenas-Alvarez M. X., Townsend Ramsett M. K., Dyer N., Bergholz T. M. Genetic characterization of Listeria monocytogenes from ruminant listeriosis from different geographical regions in the U.S. Vet Microbiol. 2018;215:93-97. DOI: https://doi.org/10.1016/j.vetmic.2017.12.021