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Abstract

Background

spp. are aquatic bacteria that prefer warm seawater with moderate salinity. In humans, they can cause gastroenteritis, wound infections, and ear infections. During the summers of 2018 and 2019, unprecedented high sea surface temperatures were recorded in the German Baltic Sea.

Aim

We aimed to describe the clinical course and microbiological characteristics of infections in Germany in 2018 and 2019.

Methods

We performed an observational retrospective multi-centre cohort study of patients diagnosed with domestically-acquired infections in Germany in 2018 and 2019. Demographic, clinical, and microbiological data were assessed, and isolates were subjected to whole genome sequencing and antimicrobial susceptibility testing.

Results

Of the 63 patients with infections, most contracted the virus between June and September, primarily in the Baltic Sea: 44 (70%) were male and the median age was 65 years (range: 2–93 years). Thirty-eight patients presented with wound infections, 16 with ear infections, six with gastroenteritis, two with pneumonia (after seawater aspiration) and one with primary septicaemia. The majority of infections were attributed to (non–O1/non-O139) (n = 30; 48%) or (n = 22; 38%). Phylogenetic analyses of 12 available isolates showed clusters of three identical strains of , which caused wound infections, suggesting that some clonal lines can spread across the Baltic Sea.

Conclusions

During the summers of 2018 and 2019, severe heatwaves facilitated increased numbers of infections in Germany. Since climate change is likely to favour the proliferation of these bacteria, a further increase in -associated diseases is expected.

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/content/10.2807/1560-7917.ES.2021.26.41.2002041
2021-10-14
2024-03-28
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2021.26.41.2002041
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References

  1. Farmer JJ. The Family Vibrionaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, editors. The prokaryotes: Volume 6: proteobacteria: gamma subclass. New York, NY: Springer New York; 2006. p. 495-507.
  2. Baker-Austin C, Trinanes J, Gonzalez-Escalona N, Martinez-Urtaza J. Non-cholera Vibrios: the microbial barometer of climate change. Trends Microbiol. 2017;25(1):76-84.  https://doi.org/10.1016/j.tim.2016.09.008  PMID: 27843109 
  3. Clemens JD, Nair GB, Ahmed T, Qadri F, Holmgren J. Cholera. Lancet. 2017;390(10101):1539-49.  https://doi.org/10.1016/S0140-6736(17)30559-7  PMID: 28302312 
  4. Muhling BA, Jacobs J, Stock CA, Gaitan CF, Saba VS. Projections of the future occurrence, distribution, and seasonality of three Vibrio species in the Chesapeake Bay under a high-emission climate change scenario. Geohealth. 2017;1(7):278-96.  PMID: 32158993 
  5. Baker-Austin C, Trinanes JA, Taylor NGH, Hartnell R, Siitonen A, Martinez-Urtaza J. Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Chang. 2012;3(1):73-7.  https://doi.org/10.1038/nclimate1628 
  6. Baker-Austin C, Oliver JD, Alam M, Ali A, Waldor MK, Qadri F, et al. Vibrio spp. infections. Nat Rev Dis Primers. 2018;4(1):8.  https://doi.org/10.1038/s41572-018-0005-8  PMID: 30002421 
  7. Marinello S, Marini G, Parisi G, Gottardello L, Rossi L, Besutti V, et al. Vibrio cholerae non-O1, non-O139 bacteraemia associated with pneumonia, Italy 2016. Infection. 2017;45(2):237-40.  https://doi.org/10.1007/s15010-016-0961-4  PMID: 27837335 
  8. Thodis E, Kriki P, Kakagia D, Passadakis P, Theodoridis M, Mourvati E, et al. Rigorous Vibrio vulnificus soft tissue infection of the lower leg in a renal transplant patient managed by vacuum therapy and autologous growth factors. J Cutan Med Surg. 2009;13(4):209-14.  https://doi.org/10.2310/7750.2008.08033  PMID: 19706229 
  9. Brehm TT, Berneking L, Rohde H, Chistner M, Schlickewei C, Sena Martins M, et al. Wound infection with Vibrio harveyi following a traumatic leg amputation after a motorboat propeller injury in Mallorca, Spain: a case report and review of literature. BMC Infect Dis. 2020;20(1):104.  https://doi.org/10.1186/s12879-020-4789-2  PMID: 32019500 
  10. Reilly GD, Reilly CA, Smith EG, Baker-Austin C. Vibrio alginolyticus-associated wound infection acquired in British waters, Guernsey, July 2011. Euro Surveill. 2011;16(42):19994.  https://doi.org/10.2807/ese.16.42.19994-en  PMID: 22027377 
  11. Engel MF, Muijsken MA, Mooi-Kokenberg E, Kuijper EJ, van Westerloo DJ. Vibrio cholerae non-O1 bacteraemia: description of three cases in the Netherlands and a literature review. Euro Surveill. 2016;21(15).  https://doi.org/10.2807/1560-7917.ES.2016.21.15.30197  PMID: 27104237 
  12. De Keukeleire S, Hoste P, Crivits M, Hammami N, Piette A. Atypical manifestation of Vibrio cholerae: fear the water! Acta Clin Belg. 2018;73(6):462-4.  https://doi.org/10.1080/17843286.2018.1483563  PMID: 29916306 
  13. Stypulkowska-Misiurewicz H, Pancer K, Roszkowiak A. Two unrelated cases of septicaemia due to Vibrio cholerae non-O1, non-O139 in Poland, July and August 2006. Euro Surveill. 2006;11(11):E061130.2. PMID: 17213560 
  14. Dalsgaard A, Frimodt-Møller N, Bruun B, Høi L, Larsen JL. Clinical manifestations and molecular epidemiology of Vibrio vulnificus infections in Denmark. Eur J Clin Microbiol Infect Dis. 1996;15(3):227-32.  https://doi.org/10.1007/BF01591359  PMID: 8740858 
  15. Martinez-Urtaza J, Trinanes J, Abanto M, Lozano-Leon A, Llovo-Taboada J, Garcia-Campello M, et al. Epidemic dynamics of Vibrio parahaemolyticus illness in a hotspot of disease emergence, Galicia, Spain. Emerg Infect Dis. 2018;24(5):852-9.  https://doi.org/10.3201/eid2405.171700  PMID: 29664388 
  16. Baker-Austin C, Trinanes JA, Salmenlinna S, Löfdahl M, Siitonen A, Taylor NG, et al. Heat wave-associated Vibriosis, Sweden and Finland, 2014. Emerg Infect Dis. 2016;22(7):1216-20.  https://doi.org/10.3201/eid2207.151996  PMID: 27314874 
  17. Frank C, Littman M, Alpers K, Hallauer J. Vibrio vulnificus wound infections after contact with the Baltic Sea, Germany. Euro Surveill. 2006;11(8):E060817.1.  https://doi.org/10.2807/esw.11.33.03024-en  PMID: 16966781 
  18. Hoyer J, Engelmann E, Liehr RM, Distler A, Hahn H, Shimada T. Septic shock due to Vibrio vulnificus serogroup 04 wound infection acquired from the Baltic Sea. Eur J Clin Microbiol Infect Dis. 1995;14(11):1016-8.  https://doi.org/10.1007/BF01691388  PMID: 8654441 
  19. Kuhnt-Lenz K, Krengel S, Fetscher S, Heer-Sonderhoff A, Solbach W. Sepsis with bullous necrotizing skin lesions due to vibrio vulnificus acquired through recreational activities in the Baltic Sea. Eur J Clin Microbiol Infect Dis. 2004;23(1):49-52.  https://doi.org/10.1007/s10096-003-1056-6  PMID: 14655036 
  20. Ruppert J, Panzig B, Guertler L, Hinz P, Schwesinger G, Felix SB, et al. Two cases of severe sepsis due to Vibrio vulnificus wound infection acquired in the Baltic Sea. Eur J Clin Microbiol Infect Dis. 2004;23(12):912-5.  https://doi.org/10.1007/s10096-004-1241-2  PMID: 15599654 
  21. Lee LH, Ab Mutalib NS, Law JW, Wong SH, Letchumanan V. Discovery on antibiotic resistance patterns of Vibrio parahaemolyticus in Selangor reveals carbapenemase producing Vibrio parahaemolyticus in marine and freshwater fish. Front Microbiol. 2018;9:2513.  https://doi.org/10.3389/fmicb.2018.02513  PMID: 30410472 
  22. Bier N, Schwartz K, Guerra B, Strauch E. Survey on antimicrobial resistance patterns in Vibrio vulnificus and Vibrio cholerae non-O1/non-O139 in Germany reveals carbapenemase-producing Vibrio cholerae in coastal waters. Front Microbiol. 2015;6:1179.  https://doi.org/10.3389/fmicb.2015.01179  PMID: 26579088 
  23. Dupke S, Akinsinde KA, Grunow R, Iwalokun BA, Olukoya DK, Oluwadun A, et al. Characterization of Vibrio cholerae strains isolated from the Nigerian cholera outbreak in 2010. J Clin Microbiol. 2016;54(10):2618-21.  https://doi.org/10.1128/JCM.01467-16  PMID: 27487957 
  24. Clinical and Laboratory Standards Institute (CLSI). Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria. Guideline - Second Edition. Pennsylvania: CLSI. 2010;30(18). M45-A2.
  25. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-77.  https://doi.org/10.1089/cmb.2012.0021  PMID: 22506599 
  26. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068-9.  https://doi.org/10.1093/bioinformatics/btu153  PMID: 24642063 
  27. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67(5):1613-7.  https://doi.org/10.1099/ijsem.0.001755  PMID: 28005526 
  28. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725-9.  https://doi.org/10.1093/molbev/mst197  PMID: 24132122 
  29. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406-25. PMID: 3447015 
  30. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 2005;33(Database issue):D325-8.  https://doi.org/10.1093/nar/gki008  PMID: 15608208 
  31. National Centers for Environmental Information. National Oceanic and Atmospheric Administration (NCEI.NOAA). NOAA 0.25-degree daily optimum interpolation sea surface temperature (OISST), version 2.1. Washington: NCEI.NOAA. [Accessed: 6 Nov 2020]. Available from: https://www.ncei.noaa.gov/metadata/geoportal/rest/metadata/item/gov.noaa.ncdc:C01606/html
  32. Shaw KS, Rosenberg Goldstein RE, He X, Jacobs JM, Crump BC, Sapkota AR. Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticus recovered from recreational and commercial areas of Chesapeake Bay and Maryland Coastal Bays. PLoS One. 2014;9(2):e89616.  https://doi.org/10.1371/journal.pone.0089616  PMID: 24586914 
  33. Lin HV, Massam-Wu T, Lin CP, Wang YA, Shen YC, Lu WJ, et al. The Vibrio cholerae var regulon encodes a metallo-β-lactamase and an antibiotic efflux pump, which are regulated by VarR, a LysR-type transcription factor. PLoS One. 2017;12(9):e0184255.  https://doi.org/10.1371/journal.pone.0184255  PMID: 28898293 
  34. López-Pérez M, Jayakumar JM, Haro-Moreno JM, Zaragoza-Solas A, Reddi G, Rodriguez-Valera F, et al. Evolutionary model of cluster divergence of the emergent marine pathogen Vibrio vulnificus: from genotype to ecotype. MBio. 2019;10(1):e02852-18.  https://doi.org/10.1128/mBio.02852-18  PMID: 30782660 
  35. Nonaka L, Suzuki S. New Mg2+-dependent oxytetracycline resistance determinant tet 34 in Vibrio isolates from marine fish intestinal contents. Antimicrob Agents Chemother. 2002;46(5):1550-2.  https://doi.org/10.1128/AAC.46.5.1550-1552.2002  PMID: 11959596 
  36. Zhang Z, Yu YX, Jiang Y, Wang YG, Liao MJ, Rong XJ, et al. First report of isolation and complete genome of Vibrio rotiferianus strain SSVR1601 from cage-cultured black rockfish (Sebastes schlegelii) associated with skin ulcer. J Fish Dis. 2019;42(5):623-30.  https://doi.org/10.1111/jfd.12963  PMID: 30851004 
  37. Dechet AM, Yu PA, Koram N, Painter J. Nonfoodborne Vibrio infections: an important cause of morbidity and mortality in the United States, 1997-2006. Clin Infect Dis. 2008;46(7):970-6.  https://doi.org/10.1086/529148  PMID: 18444811 
  38. Heng S-P, Letchumanan V, Deng C-Y, Ab Mutalib N-S, Khan TM, Chuah L-H, et al. Vibrio vulnificus: an environmental and clinical burden. Front Microbiol. 2017;8:997.  https://doi.org/10.3389/fmicb.2017.00997  PMID: 28620366 
  39. Merkel SM, Alexander S, Zufall E, Oliver JD, Huet-Hudson YM. Essential role for estrogen in protection against Vibrio vulnificus-induced endotoxic shock. Infect Immun. 2001;69(10):6119-22.  https://doi.org/10.1128/IAI.69.10.6119-6122.2001  PMID: 11553550 
  40. Hirk S, Huhulescu S, Allerberger F, Lepuschitz S, Rehak S, Weil S, et al. Necrotizing fasciitis due to Vibrio cholerae non-O1/non-O139 after exposure to Austrian bathing sites. Wien Klin Wochenschr. 2016;128(3-4):141-5.  https://doi.org/10.1007/s00508-015-0944-y  PMID: 26825075 
  41. Semenza JC, Trinanes J, Lohr W, Sudre B, Löfdahl M, Martinez-Urtaza J, et al. Environmental suitability of Vibrio infections in a warming climate: an early warning system. Environ Health Perspect. 2017;125(10):107004.  https://doi.org/10.1289/EHP2198  PMID: 29017986 
  42. Kniebusch M, Meier HEM, Neumann T, Börgel F. Temperature variability of the Baltic Sea since 1850 and attribution to atmospheric forcing variables. J Geophys Res Oceans. 2019;124(6):4168-87.  https://doi.org/10.1029/2018JC013948 
  43. Stramska M, Białogrodzka J. Spatial and temporal variability of sea surface temperature in the Baltic Sea based on 32-years (1982-2013) of satellite data. Oceanologia. 2015;57(3):223-35.  https://doi.org/10.1016/j.oceano.2015.04.004 
  44. Semenza JC, Herbst S, Rechenburg A, Suk JE, Höser C, Schreiber C, et al. Climate change impact assessment of food- and waterborne diseases. Crit Rev Environ Sci Technol. 2012;42(8):857-90.  https://doi.org/10.1080/10643389.2010.534706  PMID: 24808720 
  45. Böer SI, Heinemeyer EA, Luden K, Erler R, Gerdts G, Janssen F, et al. Temporal and spatial distribution patterns of potentially pathogenic Vibrio spp. at recreational beaches of the German north sea. Microb Ecol. 2013;65(4):1052-67.  https://doi.org/10.1007/s00248-013-0221-4  PMID: 23563708 
  46. Lee TH, Kim MH, Lee CS, Lee JH, Rhee JH, Chung KM. Protection against Vibrio vulnificus infection by active and passive immunization with the C-terminal region of the RtxA1/MARTXVv protein. Vaccine. 2014;32(2):271-6.  https://doi.org/10.1016/j.vaccine.2013.11.019  PMID: 24252692 
  47. Stevens DL, Bisno AL, Chambers HF, Dellinger EP, Goldstein EJ, Gorbach SL, et al. , Infectious Diseases Society of America. Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the Infectious Diseases Society of America. Clin Infect Dis. 2014;59(2):e10-52.  https://doi.org/10.1093/cid/ciu296  PMID: 24973422 
  48. Roig FJ, González-Candelas F, Sanjuán E, Fouz B, Feil EJ, Llorens C, et al. Phylogeny of Vibrio vulnificus from the analysis of the core-genome: implications for intra-species taxonomy. Front Microbiol. 2018;8:2613.  https://doi.org/10.3389/fmicb.2017.02613  PMID: 29358930 
  49. Newton A, Kendall M, Vugia DJ, Henao OL, Mahon BE. Increasing rates of vibriosis in the United States, 1996-2010: review of surveillance data from 2 systems. Clin Infect Dis. 2012;54 Suppl 5(0 5):S391-5.
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