Skip to main content

Advertisement

SpringerLink
Log in

Temporal and Spatial Distribution Patterns of Potentially Pathogenic Vibrio spp. at Recreational Beaches of the German North Sea

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The number of reported Vibrio-related wound infections associated with recreational bathing in Northern Europe has increased within the last decades. In order to study the health risk from potentially pathogenic Vibrio spp. in the central Wadden Sea, the seasonal and spatial distribution of Vibrio vulnificus, Vibrio parahaemolyticus, Vibrio alginolyticus and Vibrio cholerae were investigated at ten recreational beaches in this area over a 2-year period. V. alginolyticus and V. parahaemolyticus were found to be omnipresent all year round in the study area, while V. vulnificus occurrence was restricted to summer months in the estuaries of the rivers Ems and Weser. Multiple linear regression models revealed that water temperature is the most important determinant of Vibrio spp. occurrence in the area. Differentiated regression models showed a species-specific response to water temperature and revealed a particularly strong effect of even minor temperature increases on the probability of detecting V. vulnificus in summer. In sediments, Vibrio spp. concentrations were up to three orders of magnitude higher than in water. Also, V. alginolyticus and V. parahaemolyticus were found to be less susceptible towards winter temperatures in the benthic environment than in the water, indicating an important role of sediments for Vibrio ecology. While only a very small percentage of tested V. parahaemolyticus proved to be potentially pathogenic, the presence of V. vulnificus during the summer months should be regarded with care.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Chakraborty S, Nair GB, Shinoda S (1997) Pathogenic vibrios in the natural aquatic environment. Rev Environ Health 12:63–80

    Article  PubMed  CAS  Google Scholar 

  2. Lee WC, Lee MJ, Kom JS, Park SY (2001) Foodborne illness outbreaks in Korea and Japan studies retrospectively. J Food Prot 64:899–902

    PubMed  CAS  Google Scholar 

  3. Su HP, Chiu SI, Tsai JL, Lee CL, Pan TM (2005) Bacterial food-borne illness outbreaks in northern Taiwan, 1995–2001. J Infect Chemother 11(3):146–151

    Article  PubMed  Google Scholar 

  4. Oliver JD (2005) Vibrio vulnificus. In: Belkin S, Colwell RR (eds) Oceans and health: pathogens in the marine environment. Springer, New York, pp 253–276

    Chapter  Google Scholar 

  5. Melhus A, Holmdahl T, Tjernberg I (1995) First documented case of bacteremia with Vibrio vulnificus in Sweden. Scand J Infect Dis 27(1):81–82

    Article  PubMed  CAS  Google Scholar 

  6. Høi L, Larsen JL, Dalsgaard I, Dalsgaard A (1998) Occurrence of Vibrio vulnificus biotypes in Danish marine environments. Appl Environ Microbiol 64(1):7–13

    PubMed  Google Scholar 

  7. Torres L, Escobar S, López AI, Marco ML, Pobo V (2002) Wound infection due to Vibrio vulnificus in Spain. Eur J Clin Microbiol Infect Dis 21:537–538

    Article  PubMed  CAS  Google Scholar 

  8. Schmidt U, Chmel H, Cobbs C (1979) Vibrio alginolyticus infections in humans. J Clin Microbiol 10(5):666–668

    PubMed  CAS  Google Scholar 

  9. Schets FM, van den Berg HH, Demeulmeester AA, van Dijk E, Rutjes SA, van Hooijdonk HJ, de Roda Husman AM (2006) Vibrio alginolyticus infections in the Netherlands after swimming in the North Sea. Euro Surveill 11(45):3077

    Google Scholar 

  10. Sganga G, Cozza V, Spanu T, Spada PL, Fadda G (2009) Global climate change and wound care: case study of an off-season Vibrio alginolyticus infection in a healthy man. Ostomy Wound Mange 55(4):60–62

    Google Scholar 

  11. Pruzzo C, Huq A, Colwell RR, Donelli G (2005) Pathogenic Vibrio species in the marine and estuarine environment. In: Belkin S, Colwell RR (eds) Oceans and health: pathogens in the marine environment. Springer, New York, pp 217–252

    Chapter  Google Scholar 

  12. Kaneko T, Colwell RR (1973) Ecology of Vibrio parahaemolyticus in Chesapeake Bay. J Bacteriol 113(1):24–32

    PubMed  CAS  Google Scholar 

  13. Motes ML, DePaola A, Cook DW, Veazey JE, Hunsucker JC, Garthright WE, Blodgett RJ, Chirtel SJ (1998) Influence of water temperature and salinity on Vibrio vulnificus in Northern Gulf and Atlantic Coast Oysters (Crassostrea virginica). Appl Environ Microbiol 64(4):1459–1465

    PubMed  CAS  Google Scholar 

  14. Randa MA, Polz MF, Lim E (2004) Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl Environ Microbiol 70(9):5469–5476

    Article  PubMed  CAS  Google Scholar 

  15. Hsieh JL, Fries JS, Noble RT (2008) Dynamics and predictive modelling of Vibrio spp. in the Neuse River Estuary, North Carolina, USA. Environ Microbiol 10(1):57–64

    PubMed  Google Scholar 

  16. Martinez-Urtaza J, Lozano-Leon A, Varela-Pet J, Trinanes J, Pazos Y, Garcia-Martin O (2008) Environmental determinants of the occurrence and distribution of Vibrio parahaemolyticus in the Rias of Galicia, Spain. Appl Environ Microbiol 74(1):265–274

    Article  PubMed  CAS  Google Scholar 

  17. Oberbeckmann S, Wichels A, Wiltshire KH, Gerdts G (2011) Occurrence of Vibrio parahaemolyticus and Vibrio alginolyticus in the German Bight over a seasonal cycle. Antonie van Leeuwenhoek 100:291–307

    Article  PubMed  Google Scholar 

  18. Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR (1990) Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56(6):1977–1980

    PubMed  CAS  Google Scholar 

  19. Turner JW, Good B, Cole D, Lipp EK (2009) Plankton composition and environmental factors contribute to Vibrio seasonality. ISME J 3:1082–1092

    Article  PubMed  CAS  Google Scholar 

  20. Bock T, Christensen CN, Eriksen NH, Winter S, Rygaard H, Jörgensen F (1994) The first fatal case of Vibrio vulnificus infection in Denmark. APMIS 104:874–875

    Article  Google Scholar 

  21. Dalsgaard A, Fridmodt-Møller N, Bruun B, Høi L, Larsen JL (1996) Clinical manifestations and molecular epidemiology of Vibrio vulnificus infections in Denmark. Eur J Clin Microbiol Infect Dis 15(3):227–232

    Article  PubMed  CAS  Google Scholar 

  22. Andersson Y, Ekdahl K (2006) Wound infections due to Vibrio cholerae in Sweden after swimming in the Baltic Sea, summer 2006. Euro Surveill 11(8):3013

    Google Scholar 

  23. Lukinmaa S, Mattila K, Lehtinen V, Hakkinen M, Koskela M, Siitonen A (2006) Territorial waters of the Baltic Sea as a source of infections caused by Vibrio cholerae non-O1, non-O139: report of 3 hospitalized cases. Diagn Microbiol Infect Dis 54:1–6

    Article  PubMed  Google Scholar 

  24. Frank C, Littman M, Alpers K, Hallauer J (2006) Vibrio vulnificus wound infections after contact with the Baltic Sea, Germany. Euro Surveill 11(8):3024

    Google Scholar 

  25. Mertens A, Nagler J, Hansen W, Gepts-Friedenreich E (1979) Halophilic, lactose-positive Vibrio in a case of fatal septicemia. J Clin Microbiol 9:233–235

    PubMed  CAS  Google Scholar 

  26. Reilly GD, Reilly CA, Smith EG, Baker-Austin C (2011) Vibrio alginolyticus-associated wound infection acquired in British waters, Guernsey, July 2011. Euro Surveill 16(42):10

    Google Scholar 

  27. Baker-Austin C, Trinanes JA, Taylor NGH, Hartnell R, Siitonen A, Martinez-Urtaza J (2012) Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Chang. doi:10.1038/nclimate1628

    Google Scholar 

  28. Belkin IM (2009) Rapid warming of large marine ecosystems. Prog Oceanogr 81:207–213

    Article  Google Scholar 

  29. MacKenzie BR, Schiedek D (2007) Daily ocean monitoring since the 1860s shows record warming of northern European seas. Global Change Biol 13(7):1335–1347

    Article  Google Scholar 

  30. Wiltshire KH, Malzahn AM, Wirtz K, Greve W, Janisch S, Mangelsdorf P, Manly BFJ, Boersma M (2008) Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland Roads. Limnol Oceanogr 53(4):1294–1302

    Article  Google Scholar 

  31. Vezzulli L, Brettox I, Pezzati E, Reid PC, Colwell RR, Höfle MG, Pruzzo C (2012) Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME J 6:21–30

    Article  PubMed  Google Scholar 

  32. Bauer A, Ostensvik O, Florvag M, Ormen O, Rørvik LM (2006) Occurrence of Vibrio parahaemolyticus, V. cholerae, and V. vulnificus in Norwegian Blue Mussels (Mytilus edulis). Appl Environ Microbiol 72(4):3058–3061

    Article  PubMed  CAS  Google Scholar 

  33. Eiler A, Johansson M, Bertilsson S (2006) Environmental infuences on Vibrio populations in northern temperate and boreal coastal waters (Baltic and Skagerrak Seas). Appl Environ Microbiol 72(9):6004–6011

    Article  PubMed  CAS  Google Scholar 

  34. Lhafi SK, Kühne M (2007) Occurrence of Vibrio spp. in blue mussels (Mytilus edulis) from the German Wadden Sea. Int J Food Microb 116(2):297–300

    Article  CAS  Google Scholar 

  35. Ellingsen AB, Rørvik LM (2008) Occurrence of potentially pathogenic Vibrio spp. in Norwegian seawater. In: Ellingsen AB (ed) Vibrio parahaemolyticus, V. cholerae and V. vulnificus in Norway, with special attention to V. parahaemolyticus. Dissertation, Norwegian School of Veterinary Science

  36. Schets FM, van den Berg HHJL, Marchese A, Garbom S, de Roda Husman AM (2011) Potentially human pathogenic vibrios in marine and fresh bathing waters related to environmental conditions and disease outcome. Int J Hyg Envir Health 214(5):399–406

    Article  CAS  Google Scholar 

  37. Collin B, Rehnstam-Holm AS (2011) Occurrence and potential pathogenesis of Vibrio cholerae, Vibrio parahaemolyticus and Vibrio vulnificus on the South Coast of Sweden. FEMS Microbiol Ecol 78:306–313

    Article  PubMed  CAS  Google Scholar 

  38. Bockemühl J, Roch K, Wohlers B, Aleksic V, Aleksic S, Wokatsch R (1986) Seasonal distribution of facultatively enteropathogenic vibrios (Vibrio cholerae, Vibrio mimicus, Vibrio parahaemolyticus) in the freshwater of the Elbe river at Hamburg. J Appl Bacteriol 60:435–442

    Article  PubMed  Google Scholar 

  39. Hervio-Heath D, Colwell RR, Derrien A, Robert-Pillot A, Fournier JM, Pommepuy M (2002) Occurrence of pathogenic vibrios in coastal areas of France. J Appl Microbiol 92:1123–1135

    Article  PubMed  CAS  Google Scholar 

  40. Vezzulli L, Pezzati E, Moreno M, Fabiano M, Pane L, Pruzzo C, The VibrioSea Consortium (2009) Benthic ecology of Vibrio spp. and pathogenic Vibrio species in a coastal Mediterranean environment (La Spezia Gulf, Italy). Microb Ecol 58(4):208–818

    Article  Google Scholar 

  41. Anonymous (2006) ISO 19458:2006–12. Water quality—sampling for microbiological analysis. International Organization for Standardization, Geneva

    Google Scholar 

  42. Oberbeckmann S, Wichels A, Maier T, Kostrzewa M, Raffelberg M, Raffelberg S, Gerdts G (2011) A polyphasic approach for the differentiation of environmental Vibrio isolates from temperate waters. FEMS Microbiol Ecol 75:145–162

    Article  PubMed  CAS  Google Scholar 

  43. Bauer A, Rørvik L (2007) A novel multiplex PCR for the identification of Vibrio parahaemolyticus, Vibrio cholerae and Vibrio vulnificus. Lett Appl Microbiol 45:371–375

    Article  PubMed  CAS  Google Scholar 

  44. Di Pinto A, Ciccarese G, Tantillo G, Catalano D, Forte VT (2005) A collagenase-targeted multiplex PCR assay for identification of Vibrio alginolyticus, Vibrio cholerae, and Vibrio parahaemolyticus. J Food Protect 68(1):150–153 (4)

    Google Scholar 

  45. Tada J, Ohashi T, Nishimura N, Shirasaki Y, Ozaki H, Fukushima S, Takano J, Nishibuchi M, Takeda Y (1992) Detection of the thermostable direct hemolysin gene (tdh) and the thermostable direct hemolysin-related hemolysin gene (trh) of Vibrio parahaemolyticus by polymerase chain-reaction. Mol Cell Probes 6:477–487

    Article  PubMed  CAS  Google Scholar 

  46. Nandi B, Nandi RK, Mukhopadhyay S, Nair GB, Shimada T, Ghose AC (2000) Rapid detection of species-specific identification of Vibrio cholerae using primers targeted to the gene of outer membrane protein ompW. J Clin Microbiol 38:4145–4151

    PubMed  CAS  Google Scholar 

  47. Mantri CK, Mohapatra SS, Ramamurthy T, Ghosh R, Colwell RR, Singh DV (2006) Septaplex PCR assay for rapid identification of Vibrio cholerae including detection of virulence and int SXT genes. FEMS Microbiol Lett 265:208–214

    Article  PubMed  CAS  Google Scholar 

  48. Mohr CF (1856) Neue massanalytische Bestimmung des Chlors in Verbindungen. Ann Chem Pharm 97(3):335–338

    Article  Google Scholar 

  49. Anonymous (1985) DIN 38405–1: 1985–12. German standard methods for the examination of water, waste water and sludge; anions (group D); determination of chloride ions (D 1). Deutsches Institut für Normung e.V, Berlin

    Google Scholar 

  50. Knudsen M (1901) Hydrographical tables. G.E.C. Gad, Copenhagen, p 63

    Google Scholar 

  51. Anonymous (2001) DIN EN 13137:2001–12. Characterization of waste—determination of total organic carbon (TOC) in waste, sludges and sediments. European Committee for Standardization, Brussels, German version

    Google Scholar 

  52. Ackermann F (1980) A procedure for correcting the grain size effect in heavy metal analyses of estuarine and coastal sediments. Environ Technol Lett 1:518–527

    Article  CAS  Google Scholar 

  53. Figge K, Köster R, Thiel H, Wieland P (1980) Schlickuntersuchungen im Wattenmeer der Deutschen Bucht. Zwischenbericht über ein Forschungsprojekt der KFKI. Die Küste 35:187–204

    Google Scholar 

  54. Dick S, Kleine E et al. (2008) A new operational circulation model for the North Sea and the Baltic using a novel vertical co-ordinate—setup and first results. Fifth International Conference on Euro-GOOS, Exeter, EuroGOOS

  55. Dick S, Müller-Navarra S (2002) An operational oil spill model for the North Sea and the Baltic—model features and applications. Third R&D Forum on High-Density Oil Spill Response, Brest, IMO

  56. Van Landuyt HW, Van Hulle BMC, Fossepre JM, Verschraegen G (1985) The occurrence of Vibrio spp. at the Belgian coast. Acta Clin Belg 40:12–16

    PubMed  Google Scholar 

  57. Veenstra J, Rietra PJG, Coster JM, Slaats E, Dirks-Go S (1994) Seasonal variations in the occurrence of Vibrio vulnificus along the Dutch coast. Epidemiol Infect 112:285–290

    Article  PubMed  CAS  Google Scholar 

  58. Ayres PA, Barrow GI (1978) The distribution of Vibrio parahaemolyticus in British coastal waters: report of a collaborative study. J Hyg 80:281–294

    Article  PubMed  CAS  Google Scholar 

  59. Singleton FL, Attwell R, Jangi S, Colwell RR (1982) Effects of temperature and salinity on Vibrio cholerae growth. Appl Environ Microbiol 44(5):1047–1058

    PubMed  CAS  Google Scholar 

  60. Kaneko T, Colwell RR (1978) The annual cycle of V. parahaemolyticus in Chesapeake Bay. Microb Ecol 4:135–155

    Article  Google Scholar 

  61. Tantillo GM, Fontanarosa M, Di Pinto A, Musti M (2004) Updated perspectives on emerging vibrios associated with human infections. Lett Appl Microbiol 39:117–126

    Article  PubMed  CAS  Google Scholar 

  62. Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34(4):415–425

    PubMed  CAS  Google Scholar 

  63. Baross J, Liston J (1970) Occurrence of V. parahaemolyticus and related haemolytic vibrios in marine environments of Washington State. Appl Microbiol 20(2):179–186

    PubMed  CAS  Google Scholar 

  64. Blackwell KD, Oliver JD (2008) The ecology of V. vulnificus, Vibrio cholerae, and Vibrio parahaemolyticus in North Carolina estuaries. J Microbiol 46(2):146–153

    Article  PubMed  Google Scholar 

  65. Thompson JR, Polz MF (2006) Dynamics of Vibrio populations and their role in environmental nutrient cycling. In: Thompson FL, Austin B, Swings J (eds) The biology of vibrios. ASM Press, Washington, DC, pp 190–203

    Google Scholar 

  66. Sherr E, Sherr B (2000) Marine microbes: an overview. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, London, pp 13–46

    Google Scholar 

  67. Martinez-Urtaza J, Bowers JC, Trinanes J, DePaola A (2010) Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses. Food Research International, pp. 1780–1790

  68. Baker-Austin C, Stockley L, Rangdale R, Martinez-Urtaza J (2010) Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environ Microbiol Rep 2(1):7–18

    Article  Google Scholar 

  69. Robert-Pillot A, Guénolé A, Lesne J, Delesmont R, Fournier JM, Quilici ML (2004) Occurrence of the tdh and trh genes in Vibrio parahaemolyticus isolates from waters and raw shellfish collected in two French coastal areas and from seafood imported into France. Int J Food Microbiol 91(3):319–325

    Article  PubMed  CAS  Google Scholar 

  70. Ellingen AB, Jørgensen WS, Monshaugen M, Rørvik LM (2008) Genetic diversity among Norwegian Vibrio parahaemolyticus. J Appl Microbiol 105(6):2195–2202

    Article  Google Scholar 

  71. Nishibuchi M, Kaper JB (1995) Thermostable direct hemolysin gene of Vibrio parahaemolyticus—a virulence gene aquired by a marine bacterium. Infect Immun 63:2093–2099

    PubMed  CAS  Google Scholar 

  72. Caburlotto G, Gennari M, Ghidini V, Tafi MC, Lleo MM (2009) Presence of T3SS2 and other virulence-related genes in tdh-negative Vibrio parahaemolyticus environmental strains isolated from marine samples in the area of the Venetian Lagoon, Italy. FEMS Microbiol Ecol 70(3):506–514

    Article  PubMed  CAS  Google Scholar 

  73. Pruzzo C, Vezzulli L, Colwell RR (2008) Global impact of Vibrio cholerae interactions with chitin. Environ Microbiol 10(6):1400–1410

    Article  PubMed  CAS  Google Scholar 

  74. Han F, Ge B (2010) Multiplex PCR assays for simultaneous detection and characterization of Vibrio vulnificus strains. Lett Appl Microbiol 51(2):234–240

    PubMed  CAS  Google Scholar 

  75. Anonymous (2006) Directive 2006/7/EC of the European Parliament and of the Council of 15 February 2006 concerning the management of bathing water quality and repealing Directive 76/160/EEC. Off J Eur Union L 64:37–51, 4.3.2006

    Google Scholar 

Download references

Acknowledgments

This study was conducted within the German research programme KLIWAS, financed by the Federal Ministry of Transport, Building and Urban affairs. Work at the NLGA was further financially supported by the federal state of Lower Saxony. PCR analyses were performed throughout the German zoonose research network VibrioNet, financed by the Federal Ministry of Education and Research. The National Meterological Service supported our study with provision of weather data. The salinity chart (Fig. 1) was provided by Dr. Uwe Brockmann and Monika Schütt (University of Hamburg). Without the invaluable help of our colleagues at the local health authorities of the administrative districts Aurich, Leer and Cuxhaven, the study would not have been possible. Holger Weigelt and Julia Bachtin are greatly acknowledged for technical assistance with Vibrio and grain size analyses, respectively. Further thanks go to Enoma O. Omoregie for proofreading the manuscript and to two anonymous reviewers for helpful comments and suggestions for improvement.

Author information

Authors and Affiliations

  1. Department G3—Bio-Chemistry, Ecotoxicology, Federal Institute of Hydrology, Am Mainzer Tor 1, 56068, Koblenz, Germany

    Simone I. Böer & Nicole Brennholt

  2. Governmental Institute for Public Health of Lower Saxony, Lüchtenburger Weg 24, 26603, Aurich, Germany

    Ernst-August Heinemeyer & Katrin Luden

  3. Biological Institute Helgoland, Division of Shelf Seas Systems Ecology, Alfred Wegener Institute for Polar and Marine Research, Kurpromenade, 27498, Helgoland, Germany

    René Erler & Gunnar Gerdts

  4. Federal Maritime and Hydrographic Agency, Bernhard-Nocht-Str. 78, 20359, Hamburg, Germany

    Frank Janssen

Authors
  1. Simone I. Böer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ernst-August Heinemeyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katrin Luden
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. René Erler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gunnar Gerdts
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Frank Janssen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nicole Brennholt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simone I. Böer.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 309 kb)

ESM 2

(DOC 64 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Böer, S.I., Heinemeyer, EA., Luden, K. et al. Temporal and Spatial Distribution Patterns of Potentially Pathogenic Vibrio spp. at Recreational Beaches of the German North Sea. Microb Ecol 65, 1052–1067 (2013). https://doi.org/10.1007/s00248-013-0221-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0221-4

Keywords

Search

Navigation