Clostridium difficile contamination of public tap water distribution system during a waterborne outbreak in Finland

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1 481648SJP / Clostridium difficile contamination 2013 Scandinavian Journal of Public Health, 2013; 41: ORIGINAL ARTICLE Clostridium difficile contamination of public tap water distribution system during a waterborne outbreak in Finland SAARA M. KOTILA 1, TARJA PITKÄNEN 2, JON BRAZIER 4, ERKKI EEROLA 5, JARI JALAVA 3, MARKKU KUUSI 1, EIJA KÖNÖNEN 1, JANNE LAINE 1,6, ILKKA T. MIETTINEN 2, RISTO VUENTO 7 & ANNI VIROLAINEN 1 1 National Institute for Health and Welfare (THL), Department of Infectious Disease Surveillance and Control, Bacteriology Unit/Epidemiologic Surveillance and Response Unit, Helsinki, Finland, 2 National Institute for Health and Welfare, Department of Environmental Health, Water and Health Unit, Kuopio, Finland, 3 Department of Infectious Disease Surveillance and Control, Antimicrobial Resistance Unit, Turku, Finland, 4 Anaerobe Reference Laboratory, NPHS Microbiology Cardiff, University Hospital of Wales, United Kingdom, 5 Faculty of Medicine/Institute of Microbiology and Pathology, Medical Microbiology and Immunology, Turku, Finland, 6 Tampere University Hospital, Department of Infectious Diseases, Finland, and 7 Centre for Laboratory Medicine, Tampere, Finland Abstract Aims: In November through December 2007, the drinking water distribution system in the town of Nokia, Finland, was contaminated with treated sewage effluent that resulted in a large gastroenteritis outbreak in the community. The aim of the present study was to investigate if the contaminated water in this outbreak was also a potential source of Clostridium difficile infections. Methods: Samples from the contaminated tap water and treated sewage effluent were collected. Stool samples from a portion of patients that fell ill during the outbreak were examined for C. difficile. PCR ribotyping was performed on toxin positive C. difficile isolates and the genetic profiles of the water and patient isolates were compared. Results: Twelve toxin-positive C. difficile isolates were found in water samples: five from contaminated tap water and seven from treated sewage effluent. Among these, four and five distinct PCR ribotype profiles were identified, respectively. Four PCR ribotype profiles were found among nine human faecal C. difficile isolates. Two isolates, one from tap water and one from a patient, had an indistinguishable PCR ribotype profile. Conclusions: Our findings demonstrate for the first time C. difficile contamination of a tap water distribution system and waterborne transmission of toxigenic C. difficile seems possible. Key Words: Clostridium difficile infection, Clostridium difficile spores, PCR ribotyping, waterborne outbreak Acronyms and abbreviations ARL Anaerobe Reference Laboratory, Cardiff, UK CCEY Cycloserine-cefoxitin-egg yolk CCFA Cycloserine-cefoxitin-fructose agar CDI C. difficile infection CFU Colony-forming unit EIA Enzyme immunoassay TcdA C. difficile toxin A TcdB C. difficile toxin B THL National Institute for Health and Welfare, Finland Introduction Toxigenic Clostridium difficile is a well-recognized nosocomial pathogen associated with diarrheal disease in patients treated with antibiotics. Communityacquired cases are known to occur [1 3], but little is known about how people become infected with this organism. Recent reports have indicated that C. difficile spores can be present in faeces of certain farm animals and that these spores may contaminate meat products suggesting a zoonotic route of acquisition [4 6]. C. difficile spores may be present in the soil and Correspondence: Tarja Pitkänen, National institute for Health and Welfare, Department of Environmental Health, Water and Health Unit, PO Box 95, FI , Kuopio, Finland. tarja.pitkanen@thl.fi Accepted 10 February the Nordic Societies of Public Health DOI: /

2 542 S. M. Kotila et al. have been recovered from chlorinated, river, lake and sea water samples in the environment of South Wales, UK [7]. The potential of water as a source of C. difficile infection (CDI) was demonstrated in Zimbabwe where vegetative C. difficile cells were isolated from soil and groundwater wells heavily contaminated with chicken faeces [8]. Recently, C. difficile was shown to be widely distributed in Slovenian rivers, especially in proximity of dense populations; however, the presence of C. difficile seemed to be transient and the PCR ribotype distribution changed constantly [9]. To our knowledge, no studies investigating the possibility of drinking-water sources as a mode of transmission for C. difficile spores and subsequent CDI in urban communities have ever been published. In this study, we demonstrate that C. difficile spores were present in drinking water during an outbreak caused by faecal contamination of a public water supply. In late November through early December 2007, the drinking water distribution system for 10,000 people in the town of Nokia, Finland, became massively contaminated with sewage effluent from a municipal wastewater treatment plant [10 14]. Investigations later revealed that the contamination was caused by human error and that it took over two days before the contamination was noticed. In the meantime, over 8000 people in the community of Nokia became ill, and about 1000 of these sought medical care for symptoms of gastroenteritis [10]. In addition to cases of diarrheal disease with faecal samples positive for common intestinal pathogens, such as Salmonella sp., Campylobacter sp., Giardia sp., norovirus and rotavirus, there were 17 cases associated with C. difficile. The water samples also contained a wide range of pathogens that mostly matched with those found in the patients [13,15]. Methods Since the routine water bacteriological examinations had revealed that the counts of fecal indicator bacteria in the tap water were extremely high during the contamination event (Escherichia coli count over 10 4 /100 ml, Pitkänen et al., unpublished results), C. difficile spores were searched for in the contaminated tap water and the treated sewage effluent, the latter identified as the contamination source. The isolates from water were compared to those recovered from the symptomatic patients using molecular typing techniques described below. Isolation of C. difficile from water samples The first sample from the contaminated tap water was taken on 1 December 2007, 3 days after the onset of contamination. The tap water sampling continued through December 2007 from several locations of the distribution system. A sample from treated sewage effluent was collected on 3 December, when flushing and intensive chlorination measures to clean the drinking water pipeline had started [16] and may have had an effect on microbial concentrations in sewage. The water samples were stored at 4 C, in the dark, for 4 weeks prior to the examination. C. difficile was cultured from heat-treated water samples following the procedure of the international standard ISO :1986 [17]. This entailed heating samples at (75 ± 5) C for 15 minutes to kill non-spore-forming bacteria and the vegetative forms of spore-forming bacteria like C. difficile. The treated samples in volumes of 100 ml, 10 ml, and 1 ml were passed through a cellulose membrane filter with a pore size of 0.45 microns. Each of the filtrate membranes was placed on a cycloserine-cefoxitin-egg yolk (CCEY) agar medium, which is selective for C. difficile. The plates were incubated at 37 C under anaerobic conditions and examined after 3 days. All potential C. difficile colonies were subcultured on cycloserine-cefoxitinfructose agar (CCFA) plates. C. difficile infection (CDI) diagnosis Stool samples from patients fallen ill between 28 November and 31 December 2007 were examined for enteric pathogens, including C. difficile. The vast majority of the cases were diagnosed only clinically without any laboratory confirmation, but a total of 366 cultures for common enteric pathogens and 65 tests for C. difficile were performed. The number of patient samples tested for C. difficile remained lower than that of common enteric pathogens since C. difficile was not recognized as a potential pathogen at early phases of the outbreak investigation. The main laboratory method for diagnosing CDI was the detection of toxin A (TcdA) and toxin B (TcdB) directly in samples by an enzyme immunoassay (EIA) (Premier toxins A&B, Meridian Bioscience Inc., Cincinnati, OH, USA). Only a few cases were confirmed by culture on selective CCFA plates. In addition, the patients visiting the municipal health centre between 28 November and 31 December 2007 with suspected CDI were registered on a line-list, including the name, personal identity number, date of onset of symptoms, and sampling date, if samples were taken. Detection of toxins and toxin genes All cultured water and patient isolates were tested for TcdA and TcdB by EIA (Premier toxins A&B, Meridian Bioscience Inc., Cincinnati, OH, USA). In

3 Clostridium difficile contamination of public tap water 543 Dice (Opt:1.00%) (Tol 1.0%-1.0%) (H>0.0% S>0.0%) [0.0%-5.8%] [30.4%-100.0%] PCR O'Neill PCR O'Neill Strain PCR ribotype. tap water 2. type 002. sewage effluent 2. type 005. patient 6. type 097. patient 7. type 097. patient 2. patient 3. patient 4. patient 5. patient 9. tap water 1. type 011. type 027. sewage effluent 1. type 001. type 001. sewage effluent 3. type 015 tap. water 3. type 014 patient. 8. type 014. sewage effluent 5. tap water 5. tap water 4. sewage effluent 4. patient 1. type 087. sewage effluent 6. type 205. sewage effluent 7. type 205 Figure 1. Dendrogram of C. difficile isolates from patients and water, including two reference strains (types 001 and 027). Patient isolates 2 and 9 originate from the same patient, as well as isolates 6 and 7, and isolates 3, 4 and 5. addition, an in-house PaLoc-CDT multiplex PCR was used for the detection of toxin genes tcda, tcdb, cdtb and tcdc on selected isolates. The primers were designed according to published sequences of the pathogenicity locus (PaLoc) and binary toxin CDT (cdta and cdtb) genes of C. difficile strains. The primers for the binary toxin were designed so that the cdtb gene with the known deletion was not amplified. PCR ribotyping PCR ribotyping was performed according to the protocol of the Anaerobe Reference Laboratory (ARL), Cardiff, UK [18], using the Cardiff-ECDC culture collection as a set of reference strains. After gel electrophoresis, the band patterns were analysed with the BioNumerics 5.0 software (Applied Maths NV, Belgium) by using the Dice coefficient to analyse the similarity of the banding patterns, and utilizing the unweighted pair group method using arithmetic averages (UPGMA) for cluster analysis. All the PCR ribotyping results, except for one unreculturable strain, were confirmed in ARL, where the isolates were identified using the library of PCR ribotypes [19]. Results Water samples The confirmed C. difficile spore count of samples after 4 weeks of storage was 28 CFU/100 ml in the first tap water sample, and 8 CFU/100 ml in the treated sewage effluent sample. No spores were found from the other tested tap water samples. Of the 22 presumptive C. difficile colonies, 19 were confirmed to be C. difficile and 12 of these were positive for TcdA and TcdB by EIA, and for tcda, tcdb, and tcdc by multiplex PCR: five isolates from the tap water and seven isolates from the sewage effluent, the latter being the contamination source. Among the tap water and effluent isolates, four (types 002, 011, 014, and 020) and five (types 001, 005, 015, 020, and 205) distinct PCR ribotype profiles were identified, respectively (Figure 1). PCR

4 544 S. M. Kotila et al. ribotyping of all of the water and patient isolates was repeated at least twice. The results, except for the isolate tap water 5 (see Figure 1), were also confirmed in ARL. Clinical C. difficile isolates During the epidemic period, 19 patients were detected positive for TcdA and TcdB by EIA. Of these, C. difficile was isolated from three toxin positive samples, originating from two patients. In addition, six toxin positive samples from three deceased patients, obtained during autopsy, were analysed. All isolates tested positive for TcdA and TcdB by EIA and for tcda, tcdb, and tcdc genes by multiplex PCR. Among the nine isolates, four distinct PCR ribotype profiles (types 014, 056, 087 and 097) were found, one PCR ribotype per patient. Two isolates, one from tap water and another from a patient, had an indistinguishable PCR ribotype profile, type 014 (Figure 1). In addition, type 020 was found in both tap water and sewage effluent (two isolates from each). None of the profiles was identical with that of the hypervirulent PCR ribotype 027. Discussion This study reports the detection of an indistinguishable PCR ribotype profile among C. difficile isolates cultured from the faecal-contaminated tap water and from isolates cultured from a stool sample of a symptomatic patient during an enteritis outbreak. Although not conclusively proving any causality between these two observations, it is indicative of the possibility for such an event to occur. This finding resulted from the investigation of a large outbreak that was caused by the accidental funnelling of treated but non-disinfected sewage into the municipal drinking water distribution system in a Finnish community in 2007 [10]. It is known that faecal pathogens and indicator microorganisms are still present in secondary effluents of domestic sewage after conventional treatments and are discharged to the surface waters [20,21]. Moreover, contamination of drinking water by domestic sewage is the most common cause of waterborne outbreaks in affluent nations [22]. In this study, the C. difficile spores were detected from the contaminated tap water and from the sewage effluent sample analysed. There was a period of 2 days between the retrieval of the tap water and sewage effluent samples. During this intermission, flushing and intensive chlorination of the drinking water pipelines was started. The higher spore count in tap water than in sewage effluent sample taken 2 days later reflect the extreme intensity of the contamination but the exact counts may be prone to interpretation since only single grab samples were available. It is highly probable that C. difficile spores are able to survive for long periods of time in water. Indeed, spores of sulphite-reducing clostridia and specifically those of Clostridium perfringens are used as indicators of past faecal pollution of water, since spores of clostridia are extremely resistant to various environmental stresses and are known to survive for considerable periods of time in water [23]. However, other indicators of faecal pollution, such as E. coli and enterococci, are used more frequently than clostridia in water quality monitoring. This is because of their greater quantity in faeces, despite their poorer stability in a water environment compared to clostridium spores. In the present study, only the count of C. difficile spores in contaminated water was estimated, since vegetative cells of C. difficile are unlikely to survive for long in oxygenated conditions. Due to the large amount of water in the municipal distribution system, it was challenging to get a representative sample for detecting C. difficile, not to mention finding a wider selection of the possible different PCR ribotypes present in the water. Indeed, only one ribotype (type 020) was recovered from the treated sewage effluent as well as from the contaminated tap water (two isolates from each). The detection of multiple ribotypes implies that many ribotypes form spores in the tap/waste water environment, although the ribotype distribution among vegetative cells of C. difficile is unknown. Of the PCR ribotypes detected in the water isolates, types 001, 002, 014 and 020 belong to the major PCR ribotypes found in Europe [24]. Type 001 is a common PCR ribotype among the Finnish patient isolates sent for genotyping to the National Institute for Health and Welfare (THL) from severe cases and suspected outbreaks, being second most common type after the hypervirulent type 027 [25]. In addition, types 002, 014 and 020 are encountered frequently in enteritis patients in Finland. Interestingly, the PCR ribotype 014 was recently described as the predominant C. difficile ribotype in Slovenian rivers as well as among patient and animal isolates in the same area [9]. There are no accurate data on the incidence of CDI in 2007 when the Nokia outbreak took place since it did not became a reportable communicable disease in Finland until January Moreover, the main diagnostic focus during the outbreak was on the commonly known intestinal pathogens that may have led to under-diagnosing of CDI as C. difficile was investigated only from patients with preceding antibiotic treatment and a suspicion of CDI. In addition,

5 since the CDI diagnoses during the epidemic period were mainly based on the direct detection of toxin(s) in faeces only (instead of using both culture and toxin detection), there were only a few isolates available for further analyses. However, based on the routine follow-up data of clinical laboratories during the epidemic period, there was an approximately fourfold increase in the number of toxin positive samples from CDI cases in Nokia in December 2007 compared to the equivalent numbers in the periods of and This observation implies the possibility of waterborne transmission. Conclusions Our observation indicates that C. difficile contamination of tap water had occurred during a faecal contamination event of the drinking water distribution system. Demonstrated for the first time, waterborne transmission of C. difficile spores was possible and a potential cause of CDI during the outbreak. In terms of evaluating the importance of this potential transmission route in the aetiology and epidemiology of CDI, a more comprehensive approach is needed. Funding This research received no specific grant from any funding agency in the public, commercial, or not-forprofit sectors. Conflict of interest None declared. References [1] Riley TV, Wetherall F, Bowman J, et al. Diarrheal disease due to Clostridium difficile in general practice. Pathology 1991;23: [2] Bauer MP, Goorhuis A, Koster T, et al. Community-onset Clostridium difficile-associated diarrhoea not associated with antibiotic usage two case reports with review of the changing epidemiology of Clostridium difficile-associated diarrhoea. Neth J Med 2008;66: [3] Wilcox MH, Mooney L, Bendall R, et al. A case-control study of community-associated Clostridium difficile infection. J Antimicrob Chemother 2008;62: [4] Rodriguez-Palacios A, Stampfli HR, Duffield T, et al. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis 2006;12: [5] Pirs T, Ocepek M and Rupnik M. Isolation of Clostridium difficile from food animals in Slovenia. J Med Microbiol 2008;57: [6] Indra A, Lassnig H, Baliko N, et al. Clostridium difficile: a new zoonotic agent? Wien Klin Wochenschr 2009; 121: [7] al Saif N and Brazier JS. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 1996;45: Clostridium difficile contamination of public tap water 545 [8] Simango C. Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. Trans R Soc Trop Med Hyg 2006;100: [9] Zidaric V, Beigot S, Lapajne S, et al. The occurrence and high diversity of Clostridium difficile genotypes in rivers. Anaerobe 2010;16: [10] Accident Investigation Board. Entry of treated wastewater into the drinking water network in Nokia, Finland on November Helsinki, Finland: Onnettomuustutkintakeskus [Accident Investigation Board]; [11] Maunula L, Klemola P, Kauppinen A, et al. Enteric Viruses in a Large Waterborne Outbreak of Acute Gastroenteritis in Finland. Food Environ Virol 2009;1:31 6. [12] Rimhanen-Finne R, Hanninen ML, Vuento R, et al. Contaminated water caused the first outbreak of giardiasis in Finland, 2007: a descriptive study. Scand J Infect Dis 2010;42: [13] Laine J, Huovinen E, Virtanen MJ, et al. An extensive gastroenteritis outbreak after drinking-water contamination by sewage effluent, Finland. Epidemiol Infect 2010;15:1 9. [14] Lienemann T, Pitkanen T, Antikainen J, et al. Shiga toxinproducing Escherichia coli O100:H(-): stx2e in drinking water contaminated by waste water in Finland. Curr Microbiol 2011;62: [15] Kuusi M, Ruotsalainen E, Laine J, et al. Food- and waterborne outbreaks. In: Hulkko T, Lyytikäinen O, Kuusi M, et al. (eds). Infectious diseases in Finland Helsinki, Finland: National Public Health Institute, 2008, p Available at: [16] Miettinen IT, Lepistö O, Pitkänen TM, et al. Waterborne outbreak caused by massive waste water contamination in drinking water distribution network. 15th Health Related Water Microbiology Symposium; 31 May 5 June Naxos, Greece, [17] International Organization for Standardization. ISO Water quality. Detection and enumeration of the spores of sulfitereducing anaerobes (clostridia). Part 2:Method by membrane filtration. Geneva, Switzerland: International Organization for Standardization, [18] O Neill GL, Ogunsola FT, Brazier JS, et al. Modification of a PCR Ribotyping Method for Application as a Routine Typing Scheme for Clostridium difficile. Anaerobe 1996;2: [19] Stubbs SL, Brazier JS, O Neill GL, et al. PCR targeted to the 16S-23S rrna gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 1999;37: [20] Medema GJ, Shaw S, Waite M, et al. Catchment characterization and source water quality. In: Dufour A, Snozzi M, Koster W, et al. (eds). Assessing microbial safety of drinking water: improving approaches and methods. London, UK: IWA Publishing, pp [21] Ferguson CM, Charles K and Deere DA. Quantification of Microbial Sources in Drinking-Water Catchments. Crit Rev Environ Sci Tech 2009;39:1 40. [22] Hrudey SE and Hrudey EJ. Safe drinking water: Lessons from recent outbreaks in affluent nations. London, UK: IWA Publishing, [23] Payment P, Godfree A and Sartory D. Clostridium. In: Bitton G (ed) Encyclopedia of environmental microbiology. New York, NY: Wiley, 2002, pp [24] Barbut F, Mastrantonio P, Delmee M, et al. Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. Clin Microbiol Infect 2007;13: [25] Hulkko T, Lyytikäinen O, Kuusi M, et al. Infectious Diseases in Finland 2008; Report 12/2009. National Institute for Health and Welfare, Available from: URN:NBN:fi-fe

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