The effect of environmental conditions on the occurrence of Campylobacter jejuni and Campylobacter coli in wastewater and surface waters
Language English Country Great Britain, England Media print-electronic
Document type Journal Article
Grant support
GA18-16549S
Grantová Agentura České Republiky
PubMed
34192401
PubMed Central
PMC9290866
DOI
10.1111/jam.15197
Knihovny.cz E-resources
- Keywords
- Campylobacter, ammonium salts, chloride salts, seasons, waters,
- MeSH
- Campylobacter coli * MeSH
- Campylobacter jejuni * MeSH
- Campylobacter * MeSH
- Campylobacter Infections * epidemiology MeSH
- Humans MeSH
- Wastewater MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Waste Water MeSH
AIMS: The purpose of the study was to evaluate the occurrence of Campylobacter jejuni and Campylobacter coli in the aquatic environment based on the water origin, seasonality and physico-chemical properties. METHODS AND RESULTS: The occurrence of C. jejuni and C. coli was determined in waste (29) or surface (56) waters in four different seasons. The air and water temperatures were measured during sampling and chemical analyses of water samples for ammonium, chloride, chlorine, nitrite, nitrate, phosphate and iron were performed. The thermotolerant Campylobacter spp. were more frequently detected in wastewater (59%; 17 positive samples) compared to surface water (38%; 21 positive samples), with the highest rate in autumn (67% of samples positive) and with a higher C. coli occurrence than C. jejuni (31% vs. 26%). Ammonium (above 0.2 mg/L) and chloride ion concentrations (above 60 mg/L) favour C. jejuni. Similarly, C. coli occurrence in water was supported by ammonium (above 0.2 mg/L), chloride (above 60 mg/L) and in addition by phosphate ion concentrations (below 0.7 mg/L). CONCLUSIONS: Campylobacter presence in water is influenced by physico-chemical parameters such as concentrations of ammonium and chloride ions. SIGNIFICANCE AND IMPACT OF THE STUDY: Water environment is an alternative source of Campylobacter. The concentration of ammonium and chloride ions can be used as a basis for successful prediction of the potential occurrence of C. jejuni and C. coli in wastewater and surface water in future.
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Bang, D.D. , Wedderkopp, A. , Pedersen, K. & Madsen, M. (2002) Rapid PCR using nested primers of the 16s rRNA and the hippuricase (hipO) genes to detect Campylobacter jejuni and Campylobacter coli in environmental samples. Molecular and Cellular Probes, 16, 359–369. 10.1006/mcpr.2002.0434. PubMed DOI
Bartholomew, N. , Brunton, C. , Mitchell, P. , Williamson, J. & Gilpin, B. (2014) A waterborne outbreak of campylobacteriosis in the South Island of New Zealand due to a failure to implement a multi‐barrier approach. Journal of Water and Health, 12, 555–563. 10.2166/wh.2014.155. PubMed DOI
Berndtson, E. , Danielsson‐Tham, M.L. & Engvall, A. (1996) Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. International Journal of Food Microbiology, 32, 35–47. 10.1016/0168-1605(96)01102-6. PubMed DOI
Braeye, T. , De Schrijver, K. , Wollants, E. , Van Ranst, M. & Verhaegen, J. (2015) A large community outbreak of gastroenteritis associated with consumption of drinking water contaminated by river water, Belgium, 2010. Epidemiology and Infection, 143, 711–719. 10.1017/S0950268814001629. PubMed DOI PMC
Chmielewski, R.A.N. & Frank, J.F. (2003) Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2, 22–32. 10.1111/j.1541-4337.2003.tb00012.x. PubMed DOI
Cook, K.L. & Bolster, C.H. (2007) Survival of Campylobacter jejuni and Escherichia coli in groundwater during prolonged starvation at low temperatures. Journal of Applied Microbiology, 103, 573–583. 10.1111/j.1365-2672.2006.03285.x. PubMed DOI
Donlan, R.M. & Costerton, J.W. (2002) Biofilms: Survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15, 167–193. 10.1128/CMR.15.2.167-193.2002. PubMed DOI PMC
EFSA . 2019. The European Union One Health 2018 Zoonoses Report. 10.2903/j.efsa.2019.5926 PubMed DOI PMC
Epps, S.V.R. , Harvey, R.B. , Hume, M.E. , Phillips, T.D. , Anderson, R.C. & Nisbet, D.J. (2013) Foodborne campylobacter: infections, metabolism, pathogenesis and reservoirs. International Journal of Environmental Research and Public Health, 10, 6292–6304. 10.3390/ijerph10126292. PubMed DOI PMC
Gaardbo Kuhn, K. , Falkenhorst, G. , Emborg, H.‐D. , Ceper, T. , Torpdahl, M. , Krogfelt, K.A. et al. (2017) Epidemiological and serological investigation of a waterborne Campylobacter jejuni outbreak in a Danish town. Epidemiology and Infection, 145, 701–709. 10.1017/S0950268816002788. PubMed DOI PMC
Gilpin, B.J. , Walker, T. , Paine, S. , Sherwood, J. , Mackereth, G. , Wood, T. et al. (2020) A large scale waterborne Campylobacteriosis outbreak, Havelock North, New Zealand. Journal of Infection, 81, 390–395. 10.1016/j.jinf.2020.06.065 PubMed DOI
Gölz, G. , Rosner, B. , Hofreuter, D. , Josenhans, C. , Kreienbrock, L. , Löwenstein, A. et al. (2014) Relevance of Campylobacter to public health‐The need for a One Health approach. International Journal of Medical Microbiology, 304, 817–823. 10.1016/j.ijmm.2014.08.015. PubMed DOI
Hartnett, E. , Kelly, L. , Newell, D. , Wooldridge, M. & Gettinby, G. (2001) A quantitative risk assessment for the occurrence of campylobacter in chickens at the point of slaughter. Epidemiology and Infection, 127, 195–206. 10.1017/s0950268801005866. PubMed DOI PMC
Hyllestad, S. , Iversen, A. , MacDonald, E. , Amato, E. , Borge, B.A.S. , Boe, A. et al. (2020) Large waterborne Campylobacter Outbreak: use of multiple approaches to investigate contamination of the drinking water supply system, Norway, June 2019. Eurosurveillance, 25, 1–10. 10.2807/1560-7917.ES.2020.25.35.2000011. PubMed DOI PMC
Igwaran, A. & Okoh, A.I. (2019) Human campylobacteriosis: a public health concern of global importance. Heliyon, 5, e02814 10.1016/j.heliyon.2019.e02814. PubMed DOI PMC
International Organization for Standardisation (2019) Water quality — Detection and enumeration of thermotolerant Campylobacter spp. ‐ ISO 17995:2019. ISO.
Kirk, M.D. , Pires, S.M. , Black, R.E. , Caipo, M. , Crump, J.A. , Devleesschauwer, B. et al. (2015) World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med, 12, 1–21. 10.1371/journal.pmed.1001921. PubMed DOI PMC
Koga, M. , Ang, C.W. , Yuki, N. , Jacobs, C. , Herbrink, P. , Van Der Meché, G.A. et al. (2001) Comparative study of preceding Campylobacter jejuni infection in Guillain‐Barré syndrome in Japan and The Netherlands. Journal of Neurology, Neurosurgery and Psychiatry, 70, 693–695. 10.1136/jnnp.70.5.693. PubMed DOI PMC
Linton, D. , Lawson, A.J. , Owen, R.J. & Stanley, J. (1997) PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. Journal of Clinical Microbiology, 35, 2568–2572. 10.1128/jcm.35.10.2568-2572.1997. PubMed DOI PMC
Mouly, D. , Van Cauteren, D. , Vincent, N. , Vaissiere, E. , Beaudeau, P. , Ducrot, C. et al. (2016) Description of two waterborne disease outbreaks in France: a comparative study with data from cohort studies and from health administrative databases. Epidemiology and Infection, 144, 591–601. 10.1017/S0950268815001673. PubMed DOI
Mughini‐Gras, L. , Penny, C. , Ragimbeau, C. , Schets, F.M. , Blaak, H. , Duim, B. et al. (2016) Quantifying potential sources of surface water contamination with Campylobacter jejuni and Campylobacter coli . Water Research, 101, 36–45. 10.1016/j.watres.2016.05.069. PubMed DOI
Mulder, A.C. , Franz, E. , de Rijk, S. , Versluis, M.A.J. , Coipan, C. , Buij, R. et al. (2020) Tracing the animal sources of surface water contamination with Campylobacter jejuni and Campylobacter coli . Water Research, 187, 10.1016/j.watres.2020.116421. PubMed DOI
Nachamkin, I. , Szymanski, C. & Blaser, M.J. (2008) Campylobacter, 3rd Edition. ASM Press. 10.1128/9781555815554. DOI
Nygård, K. , Andersson, Y. , Røttingen, J.A. , Svensson, Å. , Lindbäck, J. , Kistemann, T. et al. (2004) Association between environmental risk factors and campylobacter infections in Sweden. Epidemiology and Infection, 132, 317–325. 10.1017/S0950268803001900. PubMed DOI PMC
Obiri‐Danso, K. , Paul, N. & Jones, K. (2001) The effects of UVB and temperature on the survival of natural populations and pure cultures of Campylobacter jejuni, Camp. coli, Camp. lari and urease‐positive thermophilic campylobacters (UPTC) in surface waters. Journal of Applied Microbiology, 90, 256–267. 10.1046/j.1365-2672.2001.01239.x. PubMed DOI
Olin, A.C. , Aldenbratt, A. , Ekman, A. , Ljungkvist, G. , Jungersten, L. , Alving, K. et al. (2001) Increased nitric oxide in exhaled air after intake of a nitrate‐rich meal. Respiratory Medicine, 95, 153–158. 10.1053/rmed.2000.1010. PubMed DOI
Pattis, I. , Moriarty, E. , Billington, C. , Gilpin, B. , Hodson, R. & Ward, N. (2017) Concentrations of Campylobacter spp., Escherichia coli, Enterococci, and Yersinia spp. in the feces of farmed red deer in New Zealand. Journal of Environmental Quality, 46, 819–827. 10.2134/jeq2017.01.0002. PubMed DOI
Pittman, M.S. , Elvers, K.T. , Lee, L. , Jones, M.A. , Poole, R.K. , Park, S.F. et al. (2007) Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Molecular Microbiology, 63, 575–590. 10.1111/j.1365-2958.2006.05532.x. PubMed DOI
Rollins, D.M. & Colwell, R.R. (1986) Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Applied and Environment Microbiology, 52, 531–538. 10.1128/aem.52.3.531-538.1986. PubMed DOI PMC
Sales‐Ortells, H. , Agostini, G. & Medema, G. (2015) Quantification of waterborne pathogens and associated health risks in urban water. Environmental Science and Technology, 49, 6943–6952. 10.1021/acs.est.5b00625. PubMed DOI
Schönberg‐Norio, D. , Takkinen, J. , Hänninen, M.‐L. , Katila, M.‐L. , Kaukoranta, S.‐S. , Mattila, L. et al. (2004) Swimming and Campylobacter infections. Emerging Infectious Diseases, 10, 1474–1477. 10.3201/eid1008.030924. PubMed DOI PMC
Schullehner, J. , Stayner, L. & Hansen, B. (2017) Nitrate, nitrite, and ammonium variability in drinking water distribution systems. International Journal of Environmental Research and Public Health, 14, 1–9. 10.3390/ijerph14030276. PubMed DOI PMC
Shagieva, E. , Teren, M. , Michova, H. , Strakova, N. , Karpiskova, R. & Demnerova, K. (2020) Adhesion, biofilm formation, and luxS sequencing of Campylobacter jejuni isolated from water in the Czech Republic. Frontiers in Cellular and Infection Microbiology, 10, 1–9. 10.3389/fcimb.2020.596613. PubMed DOI PMC
Sheppard, S.K. , Dallas, J.F. , MacRae, M. , McCarthy, N.D. , Sproston, E.L. , Gormley, F.J. et al. (2009) Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. International Journal of Food Microbiology, 134, 96–103. 10.1016/j.ijfoodmicro.2009.02.010. PubMed DOI PMC
Sheppard, S.K. & Maiden, M.C.J. (2015) The evolution of Campylobacter jejuni and Campylobacter coli . Cold Spring Harbor Perspectives in Biology, 7, 1–13. 10.1101/cshperspect.a018119. PubMed DOI PMC
Smith, M.A. , Finel, M. , Korolik, V. & Mendz, G.L. (2000) Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori . Archives of Microbiology, 174, 1–10. 10.1007/s002030000174. PubMed DOI
Strakova, N. , Korena, K. , Gelbicova, T. , Kulich, P. & Karpiskova, R. (2021). A rapid culture method for the detection of campylobacter from water environments. International Journal of Environmental Research and Public Health, 18(11), 6098–10.3390/ijerph18116098. PubMed DOI PMC
Teren, M. , Turonova Michova, H. , Vondrakova, L. & Demnerova, K. (2019) Molecules autoinducer 2 and cjA and their impact on gene expression in Campylobacter jejuni . Journal of Molecular Microbiology and Biotechnology, 28, 207–215. 10.1159/000495411. PubMed DOI
The European Union One Health (2019) Zoonoses Report, 2019. 10.2903/j.efsa.2019.5926 PubMed DOI PMC
Thomas, C. , Hill, D. & Mabey, M. (2002) Culturability, injury and morphological dynamics of thermophilic Campylobacter spp. within a laboratory‐based aquatic model system. Journal of Applied Microbiology, 92, 433–442. 10.1046/j.1365-2672.2002.01550.x. PubMed DOI
Tribble, D.R. , Baqar, S. , Scott, D.A. , Oplinger, M.L. , Trespalacios, F. , Rollins, D. et al. (2010) Assessment of the duration of protection in Campylobacter jejuni experimental infection in humans. Infection and Immunity, 78, 1750–1759. 10.1128/IAI.01021-09. PubMed DOI PMC
Winters, D.K. , O’Leary, A.E. & Slavik, M.F. (1998) Polymerase chain reaction for rapid detection of Campylobacter jejuni in artificially contaminated foods. Letters in Applied Microbiology, 27, 163–167. 10.1046/j.1472-765X.1998.00411.x. PubMed DOI
Genotyping of Campylobacter jejuni and prediction tools of its antimicrobial resistance