An increased number of suspected outbreaks of gastroenteritis linked to bathing water were reported to the  Finnish food- and waterborne outbreak (FWO) registry  in July and August 2014. The investigation reports were  assessed by a national outbreak investigation panel.  Eight confirmed outbreaks were identified among the  15 suspected outbreaks linked to bathing water that  had been reported to the FWO registry. According to  the outbreak investigation reports, 1,453 persons  fell ill during these outbreaks. Epidemiological and  microbiological data revealed noroviruses as the main  causative agents. During the outbreaks, exceptionally  warm weather had boosted the use of beaches. Six of  eight outbreaks occurred at small lakes; for those, the  investigation strongly suggested that the beach users  were the source of contamination. In one of those  eight outbreaks, an external source of contamination  was identified and elevated levels of faecal indicator  bacteria (FIB) were noted in water. In the remaining  outbreaks, FIB analyses were insufficient to describe  the hygienic quality of the water. Restrictions against bathing proved effective in controlling the outbreaks.  In spring 2015, the National Institute for Health and  Welfare(THL)and the National Supervisory Authority for Welfare and Health (Valvira) published guidelines for outbreak control to prevent bathing water outbreaks. In July 2014, THL received primary information on several suspected outbreaks linked to bathing water via the media, while no notifications were reported to  the FWO registry. This resulted in direct contacts with  the health authorities, and a reminder about notifying outbreaks related to bathing water was posted in  a THL Infectious Disease Bulletin sent to the municipal  health authorities. The message was also distributed  to municipal environmental authorities by the National  Supervisory Authority for Welfare and Health (Valvira).  Following these reminders, several notifications were  reported to the FWO registry. We identified outbreaks  caused by bathing water from the FWO registry for  2014 and reviewed the epidemiological and microbio- logical data in order to assess and compile guidelines  for outbreak control to prevent similar outbreaks in the  future. Methods Epidemiological investigation We reviewed outbreak notifications and investigation  reports from the FWO registry for 2014. Outbreaks with  a suspected link to bathing water were included in this  study. We evaluated the strength of association for  waterborne outbreaks based on classification criteria  (Table 1) modified from those presented by Tillett et al.  [12] and on information collected from local investigation reports (i.e. time and place of swimming, number  of ill persons, clinical and microbiological findings). Microbiological investigation Description of the laboratories and their roles Analyses of enteric virus were carried out in four  laboratories. Clinical samples were analysed at the  Helsinki University Hospital (HUSLAB) and/or at the  Viral Infection Unit of the National Institute for Health  and Welfare (THL). Water samples were analysed either  at the Water and Health Unit of the National Institute  for Health and Welfare (THL) or at the Department of  Food Hygiene and Environmental Health, University of  Helsinki (UH). Surface samples were analysed at the  UH. Pathogenic bacteria, faecal indicator bacteria (FIB)  and water temperature analyses were conducted in  local clinical and/or environmental laboratories. Clinical samples Viruses were analysed in patients stools for seven out- breaks. At the HUSLAB laboratory, noroviruses were  analysed according to Kanerva et al. [13]. For astrovi- ruses, viral RNA was extracted from a 10% suspension  of the stool using MagNa Pure LC (Roche, Germany).  After RT-PCR, the amplified DNA was detected by liquid  hybridisation using an astrovirus-specific probe [14].  At the THL laboratory, norovirus RNAs were extracted  using the RNeasy Mini Kit (Qiagen, Germany) and the  polymerase/capsid gene junction was amplified as pre- viously described [14]. Genotyping analysis was done  for several norovirus isolates at the THL laboratory.  Viral RNA was amplified in polymerase region A using  a one-step RT-PCR kit (Qiagen) according to Vinj et al.  [15]. Sequences were analysed using Geneious soft- ware. NoroNet online software was used for genotyp- ing. For three outbreaks, stool specimens were tested  for pathogenic bacteria (Campylobacter,Salmonella,  Shigella and Yersinia) by routine methods [16]. Water samples At the THL laboratory, noroviruses and adenoviruses  were concentrated from 0.52 L water samples as  Table1 Classification criteria used for evaluating the strength of  association for waterborne outbreaks, Finland, 2014 A: Same pathogen identified in  patients and in the environment B: Water quality failure or other  deviation in the quality of  environment C: Association between illness  and environment shown in  analytical epidemiological  investigation D: Descriptive epidemiological  investigation suggests that  the outbreak is related to the  environment and excludes  other obvious exposures Strong association: A + C or A + D or B + C. Probable association:  B + D or C or A. Possible association: B or D. Criteria modified from Tillett et al. [12]. 3 www.eurosurveillance.org previously described [17] and using glass fibre pre- filters (Millipore). Viral nucleic acids were extracted  and detected using RT-qPCR and qPCR methods, as  previously described [18,19], with the exception of  using Taqman Environmental Master Mix 2.0 (Life  Technologies) in the adenovirus qPCR. At the UH laboratory, noroviruses and adenoviruses  were concentrated by using membrane disks HA and  Nanoceram to filter a total volume of 4.5 L of water.  When necessary, a prefilter (Waterra) was used, oth- erwise the protocol was as described in Maunula et  al. [14]. As a modification, Taqman primerprobe sets  were applied as published in ISO/TS 152162 [20] for  norovirus GI and GII. Mengovirus was added as a pro- cess control. MPN of E. coli and CFU of intestinal enterococci were  analysed according to standards ISO 93082 and ISO  78992, respectively [21,22]. Surface samples In outbreak IV, 10 environmental swabs were taken  from the toilet facilities (toilets for females, toilets for  males and two latrines). Swabs taken from taps, door  handles and toilet seats were analysed for noroviruses  according to Rnnqvist et al. using nucleic acid detec- tion by RT-qPCR [23]. For adenovirus investigation, a  primerprobe set from Jothikumar et al. was included  [24]. Statistical analyses The statistical analyses were conducted using SPSS 22  software for Windows. The related samples Wilcoxon  signed-rank test was used to test the significance of  temperature and FIB analyses, while comparing the  outbreak samples with frequent-monitoring samples  collected during the summer. Differences were consid- ered significant if the p value was < 0.05. Results Review of the outbreak notifications and  investigation reports In 2014, 15 outbreaks suspected to be caused by bath- ing water were reported to the FWO registry. We identi- fied eight outbreaks in which an association between  bathing water and the illness could be confirmed  based on classification criteria (Table 1). These out- breaks occurred on public beaches in different parts of  Finland in July and August, 2014 (Table 2; Table 3). Six of eight confirmed outbreaks occurred at rather  small lakes or ponds (< 141 ha) and eight of 13 beaches  were categorised as large public beaches with more  than 100 bathers per day (Table 2). According to the  BWD classification criteria based on the last four  bathing seasons, all these large public beaches were  classified as excellent, except for one beach that was  opened in 2012 and therefore did not have data for  classification. Restrictions against bathing were set for each beach  (Table 2). The length of these restrictions varied from  2 days to more than 3 weeks and for one beach, the  advice against bathing was set for the rest of the  bathing season. Seven of eight outbreaks occurred at  inland lakes where no clear source of contamination  was identified according to the bathing water profiles  and/or outbreak investigation reports, although for  five of these outbreaks at inland lakes, non-specific  quality deviations were reported (Table 3). In the one  Table2 Description of beaches with outbreaks linked to recreational water, Finland, summer 2014 (n = 13) Outbreak Type Size (ha) Category Estimated number  of bathers/day EU BWD  classification  (2014)a Estimated outbreak  start time Restriction against  bathing I Lake 2,420 Small < 100 NA 26 July 16 August II Lake 2.9 Large 150500 Excellent 25 July 29 July21 August IIIb Lake 5.5141 2/6 small  4/6 large < 100  > 100 NA  Excellent 2427 July 28 July12 August IV Lake 16.6 Large 1002,000 Excellent 24 July 31 July31 August  (until the end of the  bathing season) V Lake 9.7 Small < 100 NA 3 August 1522 August VI Lake 71.1 Large  150 Excellent 5 August 1121 August VII Sea 393,00,000 Small < 100 NA NK 1315 August and  19 August9  September VIII Lake/pond 0.8 Large 1,000 NAc 27 July 621 August EU BWD: European Unions Bathing Water Directive [5]; NA: not available; NK: not known. a Based on frequent monitoring during the last four bathing seasons [5]. b Combined results from six beaches. c New beach, no classification. 4 www.eurosurveillance.org coastal sea water outbreak, a wastewater overflow was  identified as a potential source of contamination. According to the outbreak investigation reports, 1,453  persons fell ill in these outbreaks (Table 3). The most  common symptoms were vomiting, diarrhoea, stomach  pain, and fever. Information on the incubation period  was available for four outbreaks, the median incuba- tion period ranging from 20 to 62 hours. The dura- tion of illness was reported for five outbreaks, with  a median ranging from 19 to 60 hours. None of the  patients required hospital care. Patient samples were collected in seven outbreaks and  tested for gastrointestinal pathogenic viruses and bacteria. Several types of norovirus were identified, with  norovirus GI.2 detected in three outbreaks (Table 3). In  addition, norovirus GI.4, GII.2 and GII.4 were detected  in patient samples. In one patient, astrovirus was identified. According to outbreak investigation reports,  pathogenic bacteria were analyzed in three investigations (outbreaks III, IV and VIII). Campylobacter was  found in one patient (outbreak III). Salmonella, Shigella  or Yersinia spp. were not found in any of the specimens  tested. Water samples were collected for noro- and adenovi- rus analyses in seven outbreaks, and noro- and/or  adenoviruses were detected in the samples from three  outbreaks (Table 3). In the remaining outbreak, these  analyses were not requested by the municipal health  protection authority. FIB were analysed from water in  all outbreaks. In addition, water quality monitoring was  carried out at every beach according to EU BWD and  national regulations. Elevated levels of both FIB were  found in two of the outbreaks (VII and VIII; Table 4), but  only in outbreak VII did the number of E. coli exceed  the limit for management actions, with maximum con- centrations of 1,100 and 190 CFU/100 mL for E. coli  and enterococci, respectively. Elevated levels of ente- rococci were also noted in outbreak I. In the remain- ing outbreaks, the levels of FIB were low. Overall, no  statistical difference in the levels of E. coli (p = 0.8) or  enterococci (p = 0.086) were noted between the out- break samples (n = 14) and the frequent-monitoring  samples (n = 42), excluding the samples from outbreak  VII, where a clear contamination source was noted. At one outbreak (IV), 10 surface samples from the toi- let area were analysed, and norovirus GII was found on  the tap of the womens toilet. Adenoviruses were not  detected in the surface samples. Water temperature During the outbreak period, exceptionally warm  weather raised the temperature of the bathing water  by several degrees (Table 4). The average tempera- ture of the bathing water samples collected during the  outbreaks was 24.3  1.3 C (n = 16), while the average  temperature of other frequent-monitoring samples col- lected at these beaches in summer 2014 (2 June to 26  August) was 19.4  3.6 C (n = 47; p = 0.002). Table3 Strength of association for waterborne outbreaks, number of patients, virological findings and observed quality deviations,  Finland, summer 2014 (n = 1,453 patients) Outbreak Strength of  associationa No. of  patients Viruses found  in patients No. of virus findings per  water samples tested Viruses found in  water Observed quality  deviation I Possible  (D) 40 NA 0/1 ND Not observed II Probable  (A + B) 85 Norovirus GI.2 2/4 Adenovirus,  norovirus GI Untidy toilets IIIb Strong  (B + C) 819b  1,093c Norovirus GI.2,  GI.4, GII.2 0/3 ND Untidy toilets,  defecation in water IV Strong  (A + B + D) 185 Norovirus GII 0/1 ND Untidy toilets V Probable  (A) 4 Norovirus GI.2  and GII.4 1/2 Norovirus GII Not observed VI Possible  (B) 17 Norovirus (not  typed) 0/2 ND Untidy toilets,  used nappies in  water VII Possible  (B) 2 Norovirus GI NA NA Wastewater  overflow VIII Possible  (B) 27 Astrovirus 1/3 Adenovirus Faeces on the dock NA: not analysed; ND: not detected. a Letters refer to classification criteria detailed in Table 1. b Combined results from six beaches that were investigated in detail. c Total number from all 32 suspected beaches from which the local health authority received notifications of illness. 5 www.eurosurveillance.org Discussion In 2014, an increased number of suspected outbreaks  linked to bathing water were reported to the Finnish  FWO registry. Reminders about the need to notify  outbreaks borne by bathing water were sent to the  municipal authorities and probably triggered the fol- lowing notifications seeing as only one outbreak linked  to bathing water had been reported during the period  2012 to 2013. In addition, the publicity around out- breaks in 2014 probably made the beach users more  alert so that they reported their suspicions of bath- ing water-related sickness to the health authorities.  Generally, it could be difficult to attribute individually  reported gastroenteritis cases to a particular bathing  activity and therefore these outbreaks may remain  undocumented. Nearly 1,500 persons fell ill during the outbreaks linked  to bathing water in 2014. Although the exact number  of people visiting the beaches was not known, some  municipal investigation reports estimated that hun- dreds to thousands of persons per day had been swim- ming at each beach during the outbreak period before  restrictions against bathing were set. In the summer of  2014, the period of continuous hot weather in Finland,  with temperatures of more than 25 C, was exception- ally long and lasted for 38 days [25]. Because of this  heatwave, it is likely that more people than usual were  visiting the beaches and spent more time in the water.  A previous study noted a positive correlation between  the number of days with temperatures over 25 C and  the number of outbreaks per bathing season [26]. Some  investigation reports also stated that the toilets at the  beaches were untidy, rubbish bins were overloaded,  and used nappies were floating in the water, indicating  overcrowded conditions. In 2015, no outbreaks linked  to bathing water were reported. This was probably due  in part to the weather conditions, namely 3 days with  temperatures over 25 C in July 2015, compared with 26  such days in July 2014. In Helsinki, the average tem- perature and precipitation in July differed considerably  between 2015 and 2014 (16.2 C/76.1 mm vs 20 C/12.5  mm) [27]. Most of the beaches were small, suggesting that the  volume of users exceeded the self-cleaning capacity  of the beach. For example, the volume of the smallest  lake (outbreak VIII) is 20,800 m3. In theory, if a single  infected person excreted large numbers of noroviruses  (up to 1011 genomic copies/g) [28], and if these viruses  were evenly diluted in the total volume of the lake, 1 g  of faeces would result in a virus concentration of nearly  5,000 genomic copies/L. Considering the low infectious  dose of norovirus (as few as 18 virus particles) [29] and  the average ingestion of water while swimming (37 mL  and 16 mL for children and adults, respectively, per  Table4 Levels of faecal indicator bacteria and water temperature in outbreak samples (n = 17) and frequent-monitoring samples  (n = 47), Finland, summer 2014 Outbreak No. of analysed water samples Escherichia coli   MPN/100 mL Intestinal enterococci  CFU/100 mL Temperature  C I  Outbreak samples  Monitoring samples   1  3   6  8  6   190  4  2   25.7  22.1  3.3 II  Outbreak samples  Monitoring samples   2  6   39  26  72  72   9  8  6  4   25.0  1.4  20.5  4.4 IIIa  Outbreak samples  Monitoring samples   5  18   14  10  19  4   3  3  15  22   25.2  0  19.0  3.8 IV  Outbreak samples  Monitoring samples   1  4   9  3  3   7  1  2   24.0  19.8  4.2 V  Outbreak samples  Monitoring samples   1  2   12  34  47   22  6  8   24.0  19.3  2.5 VI  Outbreak samples  Monitoring samples   2  4   4  1  1  0   3  2  1  1   23.0  0  17.5  3.7 VII  Outbreak samples  Monitoring samples   3  5   670  580  2  4   110  98  4  4   22.3  1b  20.2  3.5 VIII  Outbreak samples  Monitoring samples   2  5   130  120  17  5   48  46  8  7   23.9  1  18.1  2.2 CFU: colony-forming units; MPN: most probable number. a Combined results from the five beaches for which indicator bacteria were analysed. b Average from n = 2 samples. 6 www.eurosurveillance.org 45 min swimming session [30]), it is obvious that the  bathing water at this particular beach would have the  potential to cause a considerable number of infections. Norovirus was detected in ill persons in most of the out- breaks. The symptoms reported by municipal authori- ties fit the clinical picture of a norovirus illness [31]. In  three outbreaks, norovirus GI.2 was identified. In addi- tion, also GI.4, GII.2 and GII.4 were detected in patient  samples. The prevalence of GI in these outbreaks is  consistent with the observation that GI genotypes are  more frequently involved in food- or waterborne out- breaks than GII, which could imply that GI is more sta- ble in the environment [32,33]. Genotype GII.4 is the  most common genotype causing infections in humans  and is more likely to be associated with person-to-per- son transmission [34]. In two outbreaks, norovirus GI and GII were found in  bathing water and in one outbreak, GII was determined  in a swab taken from the tap of the toilet, but the num- ber of particles obtained was too small to allow typ- ing of these viruses. Therefore, an exact comparison  between patient and water samples could not be car- ried out. In two outbreaks, adenovirus was found in  water. Adenoviruses are commonly found in human  wastewater and owing to their high stability in aqueous  environments, they are recognised as good viral indi- cators of human sewage pollution [19,35,36]. Moreover,  adenoviruses can spread via contaminated water  and they have been linked to waterborne outbreaks  [14,37,38]. Since adenoviruses most often result in  subclinical disease, and symptomatic infections tend  to be mild and self-resolving, most infections remain  undocumented [39]. In the outbreaks of this study, no  adenoviruses were identified in ill persons. In Finland, the hygienic quality of the bathing water is  evaluated according to BWD and national regulations  [3-5]. According to Finnish legislation, the minimum  number of bathing water samples to be taken during  a bathing season is three for small public beaches  and four for large public beaches. The legislation con- tains rules how to monitor and manage bathing waters,  indicates microbiological threshold values, regulates  measures to be taken when bathing water fails to meet  the quality and requires the dissemination of informa- tion about bathing water quality. In Finland, the concen- trations of FIB in bathing water are typically very low;  70% of the E. coli and 58% of the intestinal enterococci  concentrations were < 10 CFU or MPN/100 mL in bathing  water samples collected from all large public beaches  (n = 302) during the seasons from 2013 to 2015 (data  not shown). In this study, the microbiological thresh- old for management actions was exceeded only in one  of eight outbreaks. For this outbreak, a clear external  contamination source was identified as 2,0003,000  m3 of raw wastewater had overflowed near the bath- ing site. In the other outbreaks, the levels of FIB were  low and the bathing water quality was classified as  excellent according to the BWD criteria. The sources of  contamination in these outbreaks were most probably  the bathers and other beach users. This suggestion  is supported by the observed pollution of the beach  environment. The poor indicator value of FIB in these outbreaks raises  questions about the current practices for assessing  bathing water quality. This finding is consistent with  a recent study showing high prevalence of adenovi- ruses (75%) in bathing water samples, which neverthe- less complied with the regulations for recreational use  [40]. Moreover, Boehm et al. reviewed the lack of cor- relation between FIB and human pathogen concentra- tions and between FIB and human health, especially in  recreational areas of non-point-source contamination  [41]. It is also widely known that pathogenic microbes,  especially enteric viruses, survive substantially bet- ter than the currently used FIB in water environments.  Therefore, new candidates, such as Clostridium per- fringens, coliphages, Bacteroides and human enteric  viruses as well as new genomic approaches, e.g.  metagenomics, have been proposed for water quality  assessment [41-43]. However, during the summer, the  higher temperature of bathing water and the increased  amount of ultraviolet light have a negative impact on  microbe survival. In this study, noro- and adenoviruses  in outbreak II were detected in the water on at least  six days but fewer than 12 days. These relatively short  contamination episodes may remain undetected with  routine FIB sampling. In most of the outbreaks, the  quality of bathing water was questioned only after people visiting the beaches fell ill, and restrictions against  bathing were set for the beaches only then. The length  of the restrictions was determined according to the  results of water analyses and proved effective in con- trolling of the outbreaks. Investigation reports of outbreaks linked to bathing  water were assessed by a panel that included experts  from THL, Valvira and UH. By using agreed criteria,  reports can be assessed more consistently over time  [12]. When the same pathogen has been identified in  patients and in the beach environment, results from  the analytical epidemiological study point towards a  certain source and water quality failures have been  detected, outbreaks are often easy to categorise. More  discussion in the panel will be needed on the relation  between illness and the beach environment when pol- lution of the beach is mentioned but no obvious other  exposures are described in outbreak reports. In this  study, eight outbreaks were identified among the 15  outbreaks suspected to be caused by bathing water  that were reported to the FWO registry. Four outbreaks  were classified as having a strong or probable associa- tion with the beach environment, and four as having a  possible association. Analytical epidemiological inves- tigations were lacking in all but one investigation, indi- cating that more training and practical experience in  analytical epidemiology may be needed in the munici- pal outbreak investigation groups. 7 www.eurosurveillance.org Because of an increase in the number of bathing water  outbreaks in the summer of 2014, THL and Valvira pub- lished guidelines for outbreak control in spring 2015 to  prevent bathing water outbreaks. If, based on the labo- ratory or epidemiological findings, the water is consid- ered to be contaminated, visitors should be informed  about a bathing prohibition or advice against bath- ing should be posted by means of the international  symbols presented in the Commission Implementing  Decision (2011/321/EU) [44]. To prevent outbreaks,  rooms intended for washing and dressing as well as  toilets at the beach should be kept clean, and soap,  hand towels and toilet paper should be available.  Visitors should be encouraged to wash their hands or  use freshen-up towels. Nappies should not be changed  and the babies bottoms should not be washed in the  bathing water, and people with gastrointestinal illness  should avoid swimming. In the case of an outbreak  suspicion, municipal authorities should notify the FWO  registry and an outbreak investigation, including epi- demiological and microbiological analyses, should be  initiated. Acknowledgements Appreciation is given to the municipal health authorities for  their investigations and assistance. We acknowledge the  help of the personnel at the National Institute for Health  and Welfare and the University of Helsinki. The research at  THL was partly supported by the personal research grant to  Ari Kauppinen from the Doctoral School of the University of  Eastern Finland. The research at UH was partly supported by  EU project Aquavalens (311846). Conflict of interest None declared. Authors contributions Ari Kauppinen, Haider Al-Hello, Outi Zacheus, Jaana  Kilponen, Leena Maunula, Sari Huusko, Ilkka Miettinen,  Soile Blomqvist and Ruska Rimhanen-Finne participated in  the national outbreak evaluation panel and the design of  the study. Ruska Rimhanen-Finne coordinated the national  panel. Ari Kauppinen was responsible for performing the  data analyses and virus analyses from water performed at  THL. 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What pathogen was connected to the outbreak?
{'answer_id': 273717, 'document_id': 445540, 'question_id': 142258, 'text': 'noroviruses', 'answer_start': 567, 'answer_category': 'SHORT'}