Belgium; Vibrio spp.; bathing water; recreational water; vibriosis; Humans; Seasons; Vibrio/genetics; Vibrio cholerae/genetics; Vibrio Infections/epidemiology; Pollution; Public Health, Environmental and Occupational Health
Abstract :
[en] In recent years, a global increase in the number of reports of human vibriosis involving V. cholerae non-O1/O139 (NOVC) and other Vibrio spp. has been observed. In this context, the Belgian National Reference Center for Vibrio conducted an assessment of the presence of Vibrio spp. in recreational waters. Water sampling was performed monthly in different lakes in Wallonia and Flanders, including the North Sea. The collected water was then filtrated and cultured, and Vibrio spp. was quantified according to the Most Probable Number (MPN). Presumptive colonies were confirmed via MALDI-TOF, and PCR for virulence genes was applied if justified. No Vibrio spp. was found in the analyzed water bodies in Wallonia. However, NOVC was isolated from three different lakes in Flanders and from coastal water. In addition, V. alginolyticus and V. parahaemolyticus were also detected in coastal water. No clear impact of the pH and temperature was observed on Vibrio spp. occurrence. Our study demonstrates the presence of Vibrio spp. in different bathing water bodies, mostly in the north of Belgium, and supports the recommendation to include Vibrio spp. as a water quality indicator for bathing water quality assessment to ensure the safety of water recreational users in Belgium.
Disciplines :
Microbiology
Author, co-author :
Sacheli, Rosalie ; Centre Hospitalier Universitaire de Liège - CHU > > Service de microbiologie clinique
Philippe, Camille ; Department of Clinical Microbiology, Belgian National Reference Center Vibrio cholerae and Vibrio parahaemolyticus, Center for Interdisciplinary Research on Medicines (CIRM), University Hospital of Liege, 4000 Liège, Belgium
Meex, Cécile ; Centre Hospitalier Universitaire de Liège - CHU > > Service de microbiologie clinique
MZOUGUI, Samy ; Centre Hospitalier Universitaire de Liège - CHU > > Service de microbiologie clinique
Melin, Pierrette ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Hayette, Marie-Pierre ; Centre Hospitalier Universitaire de Liège - CHU > > Service de microbiologie clinique
Language :
English
Title :
Occurrence of Vibrio spp. in Selected Recreational Water Bodies in Belgium during 2021 Bathing Season.
Publication date :
17 October 2023
Journal title :
International Journal of Environmental Research and Public Health
Percival S.L. Williams D.W. Vibrio Microbiology of Waterborne Diseases: Microbiological Aspects and Risks 2nd ed. Elsevier London, UK 2013 9780124158467
Deshayes S. Daurel C. Cattoir V. Parienti J.-J. Quilici M.-L. de La Blanchardière A. Non-O1, Non-O139 Vibrio cholerae Bacteraemia: Case Report and Literature Review SpringerPlus 2015 4 575 10.1186/s40064-015-1346-3 26543710
Lan N.P.H. Nga T.V.T. Yen N.T.T. Dung L.T. Tuyen H.T. Campbell J.I. Whitehorn J. Thwaites G. Van Vinh Chau N. Baker S. Two Cases of Bacteriemia Caused by Nontoxigenic, Non-O1, Non-O139 Vibrio cholerae Isolates in Ho Chi Minh City, Vietnam J. Clin. Microbiol. 2014 52 3819 3821 10.1128/JCM.01915-14
Maraki S. Christidou A. Anastasaki M. Scoulica E. Non-O1, Non-O139 Vibrio cholerae Bacteremic Skin and Soft Tissue Infections Infect. Dis. 2016 48 171 176 10.3109/23744235.2015.1104720 26503346
Chowdhury G. Joshi S. Bhattacharya S. Sekar U. Birajdar B. Bhattacharyya A. Shinoda S. Ramamurthy T. Extraintestinal Infections Caused by Non-toxigenic Vibrio cholerae Non-O1/Non-O139 Front. Microbiol. 2016 7 144 10.3389/fmicb.2016.00144 26904017
Hirk S. Huhulescu S. Allerberger F. Lepuschitz S. Rehak S. Weil S. Gschwandtner E. Hermann M. Neuhold S. Zoufaly A. et al. Necrotizing Fasciitis Due to Vibrio cholerae Non-O1/Non-O139 after Exposure to Austrian Bathing Sites Wien. Klin. Wochenschr. 2016 128 141 145 10.1007/s00508-015-0944-y 26825075
Crowe S.J. Newton A.E. Gould L.H. Parsons M.B. Stroika S. Bopp C.A. Freeman M. Greene K. Mahon B.E. Vibriosis, Not Cholera: Toxigenic Vibrio cholerae Non-O1, Non-O139 Infections in the United States, 1984–2014 Epidemiol. Infect. 2016 144 3335 3341 10.1017/S0950268816001783
Homsy P. Skogberg K. Jahkola T. Three Cases of Fulminant Cellulitis Caused by Non-O1, Non-O139 Vibrio cholerae in Southern Finland Infect. Dis. 2020 52 506 510 10.1080/23744235.2020.1756399
Hao Y. Wang Y. Bi Z. Sun B. Jin Y. Bai Y. Chen B. Shao C. Sun X. Lu Z. A Case of Non-O1/Non-O139 Vibrio cholerae Septicemia and Meningitis in a Neonate Int. J. Infect. Dis. 2015 35 117 119 10.1016/j.ijid.2015.05.004
De Keukeleire S. Hoste P. Crivits M. Hammami N. Piette A. Atypical Manifestation of Vibrio cholerae: Fear the Water! Acta Clin. Belg. 2018 73 462 464 10.1080/17843286.2018.1483563
Frank C. Littman M. Alpers K. Hallauer J. Vibrio Vulnificus Wound Infections after Contact with the Baltic Sea, Germany Eurosurveillance 2006 11 3024 10.2807/esw.11.33.03024-en
Brehm T.T. Dupke S. Hauk G. Fickenscher H. Rohde H. Berneking L. [Nicht-Cholera-Vibrionen—Derzeit Noch Seltene, aber Wachsende Infektionsgefahr in Nord- und Ostsee]. Non-Cholera Vibrio Species—Currently Still Rare but Growing Danger of Infection in the North Sea and the Baltic Sea Internist 2021 62 876 886 10.1007/s00108-021-01086-x 34269833
Fleischmann S. Herrig I. Wesp J. Stiedl J. Reifferscheid G. Strauch E. Alter T. Brennholt N. Prevalence and Distribution of Potentially Human Pathogenic Vibrio spp. on German North and Baltic Sea Coasts Front. Cell. Infect. Microbiol. 2022 12 846819 10.3389/fcimb.2022.846819 35937704
Centers for Disease Control and Prevention Questions and Answers|Vibrio Illness (Vibriosis) Available online: https://www.cdc.gov/vibrio/faq.html (accessed on 12 September 2023)
Hwang S. Kim Y. Jung H. Chang H.-H. Kim S.-J. Park H.-K. Lee J.-M. Kim H.-I. Kim S.-W. A Fatal Case of Bacteremia Caused by Vibrio cholerae Non-O1/O139 Infect. Chemother. 2021 53 384 390 10.3947/ic.2020.0301 32869555
Raszl S.M. Froelich B.A. Vieira C.R.W. Blackwood A.D. Noble R.T. Vibrio Parahaemolyticus and Vibrio Vulnificus in South America: Water, Seafood and Human Infections J. Appl. Microbiol. 2016 121 1201 1222 10.1111/jam.13246
Igbinosa E.O. Okoh A.I. Vibrio Fluvialis: An Unusual Enteric Pathogen of Increasing Public Health Concern Int. J. Environ. Res. Public Health 2010 7 3628 3643 10.3390/ijerph7103628
Shravan Y. Gill R. Vaswani V. Lakhani S. Lakhani J. Vibrio fluvialis—Unusual Case of Cellulitis Leading to Sepsis Asian J. Res. Infect. Dis. 2021 6 1 8 10.9734/ajrid/2021/v6i430200
Ramamurthy T. Chowdhury G. Pazhani G.P. Shinoda S. Vibrio fluvialis: An Emerging Human Pathogen Front. Microbiol. 2014 5 91 10.3389/fmicb.2014.00091
Schets F.M. van den Berg H.H. Demeulmeester A.A. van Dijk E. Rutjes S.A. van Hooijdonk H.J. de Roda Husman A.M. Vibrio alginolyticus Infections in The Netherlands after Swimming in the North Sea Eurosurveillance 2006 11 3077 10.2807/esw.11.45.03077-en
Morris J.G. Wilson R. Hollis D.G. Weaver R.E. Miller H.G. Tacket C.O. Hickman F.W. Blake P.A. Illness Caused by Vibrio damsela and Vibrio hollisae Lancet 1982 319 1294 1297 10.1016/S0140-6736(82)92853-7
Perez-Tirse J. Levine J.F. Mecca M. Vibrio damsela: A Cause of Fulminant Septicemia Arch. Intern. Med. 1993 153 1838 1840 10.1001/archinte.1993.00410150128012 8333818
Bross M.H. Soch K. Morales R. Mitchell R.B. Vibrio vulnificus Infection: Diagnosis and Treatment Am. Fam. Physician 2007 76 539 544 17853628
ECDC Geoportal: Vibrio Map Viewer Available online: https://geoportal.ecdc.europa.eu/vibriomapviewer/ (accessed on 10 August 2023)
Decision C. 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 2006 L064 37 51
Schets F.M. van den Berg H.H.J.L. Marchese A. Garbom S. de Roda Husman A.M. Potentially Human Pathogenic Vibrios in Marine and Fresh Bathing Waters Related to Environmental Conditions and Disease Outcome Int. J. Hyg. Environ. Health 2011 214 399 406 10.1016/j.ijheh.2011.05.003
Barrera-Escorcia G. Wong-Chang I. Fernández-Rendón C.L. Botello A.V. Gómez-Gil B. Lizárraga-Partida M.L. Quantification of Vibrio Species in Oysters from the Gulf of Mexico with Two Procedures Based on MPN and PCR Environ. Monit. Assess. 2016 188 602 10.1007/s10661-016-5620-9
Alexander M. Most-Probable-Number Method for Microbial Populations Methods of Soil Analysis, Part 2: Chemical and Microbiological Properties American Society of Agronomy Madison, WI, USA 2016 9780891182047
Blackstone G.M. Nordstrom J.L. Bowen M.D. Meyer R.F. Imbro P. DePaola A. Use of a Real Time PCR Assay for Detection of the ctxA Gene of Vibrio cholerae in an Environmental Survey of Mobile Bay J. Microbiol. Methods 2007 68 254 259 10.1016/j.mimet.2006.08.006
Bej A.K. Patterson D.P. Brasher C.W. Vickery M.C. Jones D.D. Kaysner C.A. Detection of Total and Hemolysin-Producing Vibrio parahaemolyticus in Shellfish Using Multiplex PCR Amplification of tl, tdh and trh J. Microbiol. Methods 1999 36 215 225 10.1016/S0167-7012(99)00037-8
Dormann W. The Surface Salinity of the North Sea and Baltic Sea Area Terrestrial Coastal Ecosystems in Germany and Climate Change. Ecological Studies Mossakowski D. Irmler U. Springer Cham, Switzerland 2023 Volume 245 10.1007/978-3-031-12539-3_7
Van Landuyt H.W. Van Hulle B.M. Fossépré J.M. Verschraegen G. The Occurrence of Vibrio spp. at the Belgian Coast Acta Clin. Belg. 1985 40 12 16 10.1080/22953337.1985.11719044
Banakar V. de Magny G.C. Jacobs J. Murtugudde R. Huq A. Wood R.J. Colwell R.R. Temporal and Spatial Variability in the Distribution of Vibrio vulnificus in the Chesapeake Bay: A Hindcast Study Ecohealth 2011 8 456 467 10.1007/s10393-011-0736-4
Caburlotto G. Bianchi F. Gennari M. Ghidini V. Socal G. Aubry F.B. Bastianini M. Tafi M.C. Lleo M.M. Integrated Evaluation of Environmental Parameters Influencing Vibrio Occurrence in the Coastal Northern Adriatic Sea (Italy) Facing the Venetian Lagoon Microb. Ecol. 2012 63 20 31 10.1007/s00248-011-9920-x
Martinez-Urtaza J. Lozano-Leon A. Varela-Pet J. Trinanes J. Pazos Y. Garcia-Martin O. Environmental Determinants of the Occurrence and Distribution of Vibrio parahaemolyticus in the Rias of Galicia, Spain Appl. Environ. Microbiol. 2008 74 265 274 10.1128/AEM.01307-07 17981951
Hsieh J.L. Fries J.S. Noble R.T. Dynamics and Predictive Modelling of Vibrio spp. in the Neuse River Estuary, North Carolina, USA Environ. Microbiol. 2008 10 57 64 10.1111/j.1462-2920.2007.01429.x 18211266
Lamon S. Consolati S.G. Fois F. Cambula M.G. Pes M. Porcheddu G. Agus V. Esposito G. Mureddu A. Meloni D. Occurrence, Seasonal Distribution, and Molecular Characterization of Vibrio vulnificus, Vibrio cholerae, and Vibrio parahaemolyticus in Shellfish (Mytilus galloprovincialis and Ruditapes decussatus) Collected in Sardinia (Italy) J. Food Prot. 2019 82 1851 1856 10.4315/0362-028X.JFP-19-021 31603702
Oberbeckmann S. Fuchs B.M. Meiners M. Wichels A. Wiltshire K.H. Gerdts G. Seasonal Dynamics and Modeling of a Vibrio Community in Coastal Waters of the North Sea Microb. Ecol. 2012 63 543 551 10.1007/s00248-011-9990-9 22202887
Oberbeckmann S. Wichels A. Wiltshire K.H. Gerdts G. Occurrence of Vibrio parahaemolyticus and Vibrio alginolyticus in the German Bight over a Seasonal Cycle Antonie Leeuwenhoek Int. J. Gen. Mol. Microbiol. 2011 100 291 307 10.1007/s10482-011-9586-x
Kaneko T. Colwell R.R. Ecology of Vibrio Parahaemolyticus in Chesapeake Bay J. Bacteriol. 1973 113 24 32 10.1128/jb.113.1.24-32.1973
Lutz C. Erken M. Noorian P. Sun S. McDougald D. Environmental Reservoirs and Mechanisms of Persistence of Vibrio cholerae Front. Microbiol. 2013 4 375 10.3389/fmicb.2013.00375
Ogg J.E. Ryder R.A. Smith L.H. Isolation of Vibrio cholerae from Aquatic Birds in Colorado and Utah Appl. Environ. Microbiol. 1989 55 95 99 10.1128/aem.55.1.95-99.1989
Laviad-Shitrit S. Izhaki I. Halpern M. Accumulating Evidence Suggests that Some Waterbird Species are Potential Vectors of Vibrio cholerae PLoS Pathog. 2019 15 e1007814 10.1371/journal.ppat.1007814
Iwamoto M. Ayers T. Mahon B.E. Swerdlow D.L. Epidemiology of Seafood-Associated Infections in the United States Clin. Microbiol. Rev. 2010 23 399 411 10.1128/CMR.00059-09 20375359
Schmid-Hempel P. Frank S.A. Pathogenesis, Virulence, and Infective Dose PLoS Pathog. 2007 3 e147 10.1371/journal.ppat.0030147 17967057
Caburlotto G. Ghidini V. Gennari M. Tafi M.C. Lleo M.M. Isolation of a Vibrio parahaemolyticus Pandemic Strain from a Marine Water Sample Obtained in the Northern Adriatic Eurosurveillance 2008 13 5 6 10.2807/ese.13.11.08068-en 18768128
Musie W. Gonfa G. Fresh Water Resource, Scarcity, Water Salinity Challenges and Possible Remedies: A Review Heliyon 2023 9 e18685 10.1016/j.heliyon.2023.e18685 37554830
Hervio-Heath D. Colwell R.R. Derrien A. Robert-Pillot A. Fournier J.M. Pommepuy M. Occurrence of Pathogenic Vibrios in Coastal Areas of France J. Appl. Microbiol. 2002 92 1123 1135 10.1046/j.1365-2672.2002.01663.x 12010553
Harrison J. Nelson K. Morcrette H. Morcrette C. Preston J. Helmer L. Titball R.W. Butler C.S. Wagley S. The Increased Prevalence of Vibrio Species and the First Reporting of Vibrio jasicida and Vibrio rotiferianus at UK Shellfish Sites Water Res. 2022 211 117942 10.1016/j.watres.2021.117942
Sterk A. Schets F.M. Husman A.M.d.R. de Nijs T. Schijven J.F. Effect of Climate Change on the Concentration and Associated Risks of Vibrio spp. in Dutch Recreational Waters Risk Anal. 2015 35 1717 1729 10.1111/risa.12365
Valáriková J. Korcová J. Ziburová J. Rosinský J. Čížová A. Bieliková S. Sojka M. Farkaš P. Potential Pathogenicity and Antibiotic Resistance of aquatic Vibrio isolates from Freshwater in Slovakia Folia Microbiol. 2020 65 545 555 10.1007/s12223-019-00760-w
Brehm T.T. Berneking L. Martins M.S. Dupke S. Jacob D. Drechsel O. Bohnert J. Becker K. Kramer A. Christner M. et al. Heatwave-Associated Vibrio Infections in Germany, 2018 and 2019 Eurosurveillance 2021 26 2002041 10.2807/1560-7917.ES.2021.26.41.2002041
Brehm T.T. Berneking L. Rohde H. Chistner M. Schlickewei C. Martins M.S. Schmiedel S. 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 20 104 10.1186/s12879-020-4789-2
Klontz K.C. Fatalities Associated With Vibrio parahaemolyticus and Vibrio cholerae Non-O1 Infections in Florida (1981 to 1988) South. Med. J. 1990 83 500 502 10.1097/00007611-199005000-00006 2343327
Farmachidi J.-P. Sobesky R. Boussougant Y. Quilici M.-L. Coffin B. Septicaemia and Liver Abscesses Secondary to Non-O1/Non-O139 Vibrio cholerae Colitis Eur. J. Gastroenterol. Hepatol. 2003 15 699 700 10.1097/00042737-200306000-00018
Patel N.M. Wong M. Little E. Ramos A.X. Kolli G. Fox K.M. Melvin J. Moore A. Manch R. Vibrio choleraenon-O1 Infection in Cirrhotics: Case Report and Literature Review Transpl. Infect. Dis. 2009 11 54 56 10.1111/j.1399-3062.2008.00339.x
Zhang X. Lu Y. Qian H. Liu G. Mei Y. Jin F. Xia W. Ni F. Non-O1, Non-O139 Vibrio cholerae (NOVC) Bacteremia: Case Report and Literature Review, 2015–2019 Infect. Drug Resist. 2020 13 1009 1016 10.2147/IDR.S245806 32308442
Zmeter C. Tabaja H. Sharara A.I. Kanj S.S. Non-O1, Non-O139 Vibrio cholerae Septicemia at A Tertiary Care Center in Beirut, Lebanon; a Case Report and Review J. Infect. Public Health 2018 11 601 604 10.1016/j.jiph.2018.01.001
Daboul J. Weghorst L. DeAngelis C. Plecha S.C. Saul-McBeth J. Matson J.S. Characterization of Vibrio cholerae isolates from Freshwater Sources in Northwest Ohio PLoS ONE 2020 15 e0238438 10.1371/journal.pone.0238438 32881972
Špačková M. Košťálová J. Fabiánová K. Non-O1/Non-O139 Vibrios—Occurrence Not Only in Europe in Recent Years Epidemiol. Mikrobiol. Imunol. 2021 70 131 138 34412489
Kirschner A.K.T. Schauer S. Steinberger B. Wilhartitz I. Grim C.J. Huq A. Colwell R.R. Herzig A. Sommer R. Interaction of Vibrio cholerae Non-O1/Non-O139 with Copepods, Cladocerans and Competing Bacteria in the Large Alkaline Lake Neusiedler See, Austria Microb. Ecol. 2011 61 496 506 10.1007/s00248-010-9764-9
Hasrimi A.N. Budiharjo A. Jannah S.N. Detection of Tlh and Tdh Genes in Vibrio Parahaemolyticus Inhabiting Farmed Water Ecosystem Used for L. Vannamei Aquaculture J. Phys. Conf. Ser. 2018 1025 012058 10.1088/1742-6596/1025/1/012058
Baker-Austin C. Trinanes J.A. Taylor N.G.H. Hartnell R. Siitonen A. Martinez-Urtaza J. Emerging Vibrio Risk at High Latitudes in Response to Ocean Warming Nat. Clim. Chang. 2013 3 73 77 10.1038/nclimate1628
Baker-Austin C. Trinanes J. Gonzalez-Escalona N. Martinez-Urtaza J. Non-Cholera Vibrios: The Microbial Barometer of Climate Change Trends Microbiol. 2017 25 76 84 10.1016/j.tim.2016.09.008
Baker-Austin C. Trinanes J.A. Salmenlinna S. Löfdahl M. Siitonen A. Taylor N.G.H. Martinez-Urtaza J. Heat Wave–Associated Vibriosis, Sweden and Finland, 2014 Emerg. Infect. Dis. 2016 22 1216 1220 10.3201/eid2207.151996
Ford C.L. Powell A. Lau D.Y.L. Turner A.D. Dhanji-Rapkova M. Martinez-Urtaza J. Baker-Austin C. Isolation and Characterization of Potentially Pathogenic Vibrio Species in a Temperate, Higher Latitude Hotspot Environ. Microbiol. Rep. 2020 12 424 434 10.1111/1758-2229.12858
Vezzulli L. Brettar I. Pezzati E. Reid P.C. Colwell R.R. Höfle M.G. Pruzzo C. Long-Term Effects of Ocean Warming on the Prokaryotic Community: Evidence from the Vibrios ISME J. 2012 6 21 30 10.1038/ismej.2011.89
Vezzulli L. Grande C. Reid P.C. Hélaouët P. Edwards M. Höfle M.G. Brettar I. Colwell R.R. Pruzzo C. Climate Influence on Vibrio and Associated Human Diseases during the Past Half-Century in the Coastal North Atlantic Proc. Natl. Acad. Sci. USA 2016 113 E5062 E5071 10.1073/pnas.1609157113 27503882
Vezzulli L. Colwell R.R. Pruzzo C. Ocean Warming and Spread of Pathogenic Vibrios in the Aquatic Environment Microb. Ecol. 2013 65 817 825 10.1007/s00248-012-0163-2 23280498
Froelich B.A. Daines D.A. In Hot Water: Effects of Climate Change on Vibrio–Human Interactions Environ. Microbiol. 2020 22 4101 4111 10.1111/1462-2920.14967 32114705
World Health Organization Guidelines on Recreational Water Quality World Health Organization Geneva, Switzerland 2021 Volume 1
Federal Maritime and Hydrographic Agency (BSH) Hamburg, Germany Available online: https://www.bsh.de/EN/The_BSH/ (accessed on 12 August 2023)