Zoonoses Public Health. 2020;00:1–7. wileyonlinelibrary.com/journal/zph
|
11 | INTRODUCTION
In July 2018, the Public Health Service (PHS) received several no-tifications via a national reporting system for water-quality and water-related health issues from persons who had become sick following water contact in the vicinity of a natural playground. Reports mostly concerned children who, during the previous weekend, had had water contact in a recreational lake as well as
a nearby natural playground which consists of shallow playground water. The outbreak reached the press and fuelled discussion on local social media in which an unusually large number of geese defecating near the playground were discussed among social media users. Outbreak and symptom characteristics, consisting of an acute-onset and relatively swift disappearance of symptoms of diarrhoea and vomiting, were suggestive of an outbreak with norovirus (NoV) which constitutes the most frequently identified Received: 18 June 2019
|
Revised: 24 December 2019|
Accepted: 10 January 2020DOI: 10.1111/zph.12689
S H O R T C O M M U N I C A T I O N
Norovirus outbreak in a natural playground: A One Health
approach
Gregorius J. Sips
1,2| Mariëlle J. G. Dirven
1| Joke T. Donkervoort
1|
Francien M. van Kolfschoten
1| Claudia M. E. Schapendonk
3| My V. T. Phan
3|
Annemieke Bloem
2| Anna F. van Leeuwen
1| Mariechristine E. Trompenaars
1|
Marion P. G. Koopmans
3| Annemiek A. van der Eijk
3| Miranda de Graaf
3| Ewout B. Fanoy
1This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2020 The Authors. Zoonoses and Public Health published by Blackwell Verlag GmbH.
1Public Health Service Rotterdam-Rijnmond,
Rotterdam, The Netherlands
2Department of Medical Microbiology
and Infectious Diseases, Erasmus Medical Center, Rotterdam, The Netherlands
3Department of Viroscience, Erasmus
Medical Center, Rotterdam, The Netherlands
Correspondence
Ewout B. Fanoy, Public Health Service Rotterdam-Rijnmond, P.O. Box 1130, 3000 BC Rotterdam, The Netherlands.
Email: eb.fanoy@rotterdam.nl
Funding information
This study was financially supported by the EU H2020 grant COMPARE (643476).
Abstract
Norovirus constitutes the most frequently identified infectious cause of disease out-breaks associated with untreated recreational water. When investigating outout-breaks related to surface water, a One Health approach is insightful. Historically, there has been a focus on potential contamination of recreational water by bird droppings and a recent publication demonstrating human noroviruses in bird faeces suggested this should be investigated in future water-related norovirus outbreaks. Here, we describe a One Health approach investigating a norovirus outbreak in a natural play-ground. On social media, a large amount of waterfowl were reported to defecate near these playground premises leading to speculations about their potential involvement. Surface water, as well as human and bird faecal specimens, was tested for human noroviruses. Norovirus was found to be the most likely cause of the outbreak but there was no evidence for transmission via waterfowl. Cases had become known on social media prior to notification to the public health service underscoring the poten-tial of online media as an early warning system. In view of known risk factors, advice was given for future outbreak investigations and natural playground design.
K E Y W O R D S
infectious cause of outbreaks associated with untreated recrea-tional water (de Graaf, Beek, & Koopmans, 2016; Graciaa et al., 2018; Matthews et al., 2012; Rockx et al., 2002).
In the current investigation, a multidisciplinary One Health ap-proach taking into account human, animal and environmental factors was applied to determine the source of the outbreak investigating the role of humans, surface water and waterfowl (World Health Organization, 2017).
2 | MATERIALS AND METHODS
2.1 | Outbreak description
Patient details could be obtained directly because patients had submitted personal notifications to a national reporting system for water-quality and water-related health issues (Meldpunt Water). The PHS was notified of the outbreak on July 4. A timetable demonstrat-ing key events is depicted in Table 1.
To get a more precise overview of outbreak details and proactively screen for further signs of unrest, the PHS monitored public social media via individual queries. On July 4, the day of the notification, a local health-related Facebook-platform posted results of an online request that had started the same day to estimate the total number of sick persons. In this online request, people had been asked to re-port “the number of persons within their household that had become ill following water exposure in the area” and “to actively tag other ill persons.” People were also asked to actively “report the age of all ill persons” (moderator Facebook-platform, personal communication).
2.2 | Patient faeces
N = 7 patients from three families who had submitted personal noti-fications to the national online reporting system were contacted on July 6 and asked to send in stool specimens for NoV-testing using previously published methods (Sukhrie et al., 2011; van Beek et al., 2017). For specimens that were positive in RT-PCR, a fragment of approximately ~1,000 bp overlapping open reading frames 1 and 2 (ORF1 and ORF2) was sequenced, enabling genotyping of both the polymerase and capsid genes using the NoroNet typing tool (Kroneman et al., 2011). For the phylogenetic analyses, norovirus GI.2
capsid sequences were downloaded from ncbi, and not more than two identical sequences per year and location were included (n = 121). Maximum likelihood trees of the capsid gene (260 bp) were inferred by phyml 3.0 software using the general time-reversible nucleotide
substitution model. The trees were visualized in figtree v1.4.3.
2.3 | Water
Following the first disease notifications, the municipality placed warning signs in the swimming area and ordered rapid routine test-ing for indicator bacteria of faecal contamination (Escherichia coli, enterococci) and cyanobacteria of the swimming water of the recre-ational lake. During the summer months, water testing of designated large natural swimming areas, including this specific lake, is routinely performed on a biweekly basis in the Netherlands according to the European Bathing Water Directive (EU BWD) (Schets et al., 2018; The European Parliament & the Council of the European Union, 2006). Rapid testing for faecal indicator bacteria and cyanobacteria of the playground water, which unlike the lake is not included in rou-tine screenings, was initiated as well.
Impacts
• A norovirus outbreak in a natural playground was inves-tigated via a One Health approach testing human fae-cal, water and bird faecal specimens. Incidental human introduction of norovirus was the most likely cause of the outbreak. Geese were reported to defecate near the outbreak site, leading to speculations about their poten-tial involvement, but there was no evidence for trans-mission via waterfowl.
• Monitoring of public social media revealed that cases had become known online prior to notification to the Public Health Service: this underscores the potential of online media as an early warning system. Additional insights concerning, potential, sources of contamination and outbreak magnitude were also obtained.
• Rapid sampling and storage of a variety of environmental specimens is useful so that these can later be tested, not only for typical indicator bacteria, but also for viruses.
Date Key action
30 June 2018 Outbreak onset (date first cases)
4 July 2018 Online enquiry started following outbreak discussion on Facebook-platform Notification to Public Health Service
5 July 2018 Inspection playground Collection water specimens Fixing water pump playground 6 July 2018 Collection human stool specimens 12 July 2018 Collection bird droppings
In close collaboration with local governing bodies, the PHS per-formed a location visit to the playground on July 5 and sampled n = 6 playground water specimens (1 ½ litres each) at four different loca-tions which were transported to the laboratory under cold condi-tions for NoV-testing. Water specimens were concentrated for viral content using polyethylene glycol precipitation (PEG) as previously described (Lewis & Metcalf, 1988; Sima et al., 2011). In brief, 10 ml of 50% PEG 6000 (Sigma-Aldrich) was added to 40 ml of water sample and incubated overnight at 4°C. Subsequently, specimens were cen-trifuged at 13,500 g for 1.5 hr, from which the pellets were re-sus-pended in glycine buffer followed by chloroform-butanol (50%/50% by v/v) treatment. Total nucleic acid from each concentrated water specimen was extracted using High Pure RNA Isolation kit (Roche Diagnostics) and subjected to RT-PCR for NoV-detection.
2.4 | Waterfowl faeces
In light of multiple reports, notably on social media where sus-tained speculations about their potential role in disease trans-mission had arisen, of a continuous unusually large amounts of geese defecating near the playground water, a proactive second location visit was performed on July 12. During this visit, n = 6 faecal specimens were collected from sites directly adjacent to or in the playground water and transported to the laboratory under cold conditions for NoV-testing using previously published meth-ods (Sukhrie et al., 2011; van Beek et al., 2017). Briefly, a faeces
suspension was prepared with 100 mg or 200 μl faecal specimen in 800 μl PBS, and after centrifugation (17,000 g), 200 μl was used for RNA isolation with the High Pure RNA isolation kit (Roche Diagnostics) and subjected to RT-PCR.
3 | RESULTS
3.1 | Outbreak description
The PHS received n = 21 case notifications via the national online reporting system. Reported symptoms consisted of vomiting, di-arrhoea, headache and fever. Symptom onset was acute, within 0–3 days. Symptoms disappeared within 3 days. Secondary cases were also reported, consistent with an infectious aetiology. The first day of disease onset was June 30.
The online query of the local health-related Facebook-platform yielded a total of at least n = 100 sick persons, almost exclusively children (Figure 1, personal communication moderator Facebook-platform, published with permission).
Patients specifically mentioned visits to the natural playground which they suspected to be the likely source. Patient interviewing by the PHS revealed that there had been no food stands at the loca-tion, nor were there other indications of food as a common outbreak source.
The location visit on July 5 revealed the playground area sche-matically depicted in Figure 2. Briefly, a solar-energy-driven water
F I G U R E 1 Number and age distribution of cases notified via an online social media enquiry. X-axis: age distribution; Y-axis: number of cases (total n = 101, n = 55 age unknown) (personal communication moderator Facebook-platform, published with permission)
0 1 2 3 4 5 6 7 8 9 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 Number of cases Age distribution
pump distributes water from a nearby river (A) into a natural play-ground area (B) consisting of two metal water dispensers out of which water flows into a shallow natural playground basin, where mud water is formed, and then into the adjacent lake (C). There were waste bins and, at a nearby beach, public toilets. There were no food trucks. The location visit demonstrated that the water pump designed to refresh the playground basin with fresh river water had broken down. Because of this, a situation with non-refreshed shal-low playground water had existed for an unknown duration. The pump was repaired directly after the outbreak, on July 5, and water was refreshed.
3.2 | Patient faeces
n = 4 patients out of two different families returned stool specimens. 4/4 specimens were positive for NoV GI. One stool specimen, ad-ditionally, tested positive for enterovirus and one for adenovirus genotype non-40/41. All specimens were sequenced to determine the infecting GI genotype, and 4/4 specimens contained NoV geno-type GI.P2-GI.2 as determined by the NoroNet typing tool and phy-logenetic analysis (Figure 3). Norovirus GI-related outbreaks are less frequent compared to GII outbreaks, but GI.P2-G1.2 has previously been detected in outbreaks in the Netherlands (van Beek et al., 2018).
3.3 | Water
Test values for Escherichia coli, enterococci and cyanobacteria on water specimens from the recreational lake as well as from the re-freshed playground water specimens were below cut-off values set by the EU BWD (The European Parliament & the Council of the European Union, 2006). 6/6 playground water specimens tested negative for NoVs GI and GII.
3.4 | Waterfowl faeces
During the second location visit, fuelled by reports of large numbers of defecating geese, significant quantities of thin herbivoral faecal specimens, most likely geese faeces, were spotted near the play-ground water. 6/6 tested faecal specimens were negative for NoVs GI and GII.
4 | DISCUSSION
This outbreak investigation illustrates a number of important considerations.
Norovirus, incidentally introduced by a child, or multiple chil-dren, recreating in the playground water, was the most likely cause of the outbreak. Preventive measures, including installing a water pump, public toilets and waste bins, were taken when designing the playground, and it is difficult to assess the exact role of a de-funct pump, as norovirus is highly infectious in small quantities. However, nearly all risk factors for increased faecal contamination were present in this outbreak setting, that is shallow, poorly cir-culating water, frequented by young children and animals (Graciaa et al., 2018).
In accordance with the 10-steps of outbreak investigation, the outbreak was structurally investigated and followed a One Health approach (Prikazsky, V. (Ed.)).
Monitoring of public social media proved of added value in the outbreak investigation. Interestingly, cases had already become known via social media, enabling an online investigation to be started, before notification to the PHS (Table 1). Although exact reliability can be an issue, previous publications have demon-strated the value of online monitoring strategies as early warning systems (Ginsberg et al., 2009; Liu et al., 2017; van de Belt et al., 2018).
FI G U R E 2 Schematic depiction of natural playground area. Water from the nearby river (A) is pumped into a natural playground area (B) from where it flows into the adjacent lake (C). Waterfowl (insert) reside near the playground area. Map: © OpenStreetMap contributors https ://www. opens treet map.org/copyr ight
F I G U R E 3 Phylogenetic tree demonstrating norovirus interrelatedness. Maximum-likelihood trees of ORF 2 were inferred by phyml
3.0 software using the general time reversible nucleotide substitution model. Scale bars indicate nucleotide substitutions per site. The sequences of two outbreak samples are depicted in red
0.02 MG023244.1_NoV/Hu/GI.2/VIR725F/BRAZIL/2015 KX245177.1_Sewage/SD143−10/GI.2/2014/CHN MF787207.1_PTBP2016−116 KX245173.1_Sewage/SD143−6/GI.2/2014/CHN HM047093.1_lettuce/GI.2/CE−V−09−0042/2009/CAN KX245192.1_Sewage/SD214−8/GI.2/2014/CHN KR107763.1_sewage/SD0405/2013/CHN KX154763.1_202.HMI/2014/GO/BR_isolate_202.HMI KR107811.1_sewage/SD7609/2013/CHN KX245187.1_Sewage/SD210−7/GI.2/2014/CHN KR107782.1_sewage/SD6602/2013/CHN KR107766.1_sewage/SD0501/2013/CHN KR107760.1_sewage/SD0102/2013/CHN KT383941.1_GI/Hu/KR/2015/GI.2/20150122GL02_1 KR107767.1_sewage/SD0502/2013/CHN KY427646.1_strain_groundwater/GI.2/GGN30/2010/KOR MF784792.1_NoV/Env/BRA/1610760/2016 KX245157.1_Sewage/SD102−4/GI.2/2014/CHN KR107795.1_sewage/SD6908/2013/CHN MF784782.1_NoV/Env/BRA/1528341/2015 MF784790.1_NoV/Env/BRA/1610747/2016 KT383887.1_GI/Hu/KR/2014/GI.2/20140519FL01_1 KX245193.1_Sewage/SD210−4/GI.2/2014/CHN KX245167.1_Sewage/SD142−5/GI.2/2014/CHN KR107752.1_sewage/SD0303/2013/CHN KU821045.1_66230/ATH/GI.2 HM047091.1_lettuce/GI.2/CE−V−09−0005/2009/CAN MF784778.1_NoV/Env/BRA/1524863/2015 KX245189.1_Sewage/SD210−2/GI.2/2014/CHN KX245179.1_Sewage/SD149−10/GI.2/2014/CHN KX245185.1_Sewage/SD141−6/GI.2/2014/CHN KR107755.1_sewage/SD0306/2013/CHN KR107802.1_sewage/SD7304/2013/CHN MF784771.1_NoV/Env/BRA/1520785/2015 MF784794.1_NoV/Env/BRA/1610763/2016 MF996720.1_Hu/GI.2/Pingtung/10−1/2015/TW KT383882.1_GI/Hu/KR/2014/GI.2/20140512EL03_1 MF784788.1_NoV/Env/BRA/1528525/2015 KR107776.1_sewage/SD1109/2013/CHN KC954432.1_oyster/GI/HAR13.2/2012/IE KX245166.1_Sewage/SD141−9/GI.2/2014/CHN KX245168.1_Sewage/SD142−6/GI.2/2014/CHN KR107753.1_sewage/SD0304/2013/CHN KX245156.1_Sewage/SD101−3/GI.2/2014/CHN KT150999.1_Hu/GI.2/NZ13844/2013/NZ KX245190.1_Sewage/SD214−3/GI.2/2014/CHN KX245181.1_Sewage/SD148−6/GI.2/2014/CHN MF784798.1_NoV/Env/BRA/1610784/2016 KU821055.1_80286/ATH KT383951.1_GI/Hu/KR/2015/GI.2/20150223EL06_2 KR107793.1_sewage/SD6904/2013/CHN KX245178.1_Sewage/SD149−5/GI.2/2014/CHN HQ201648.1_water/GI.2/09−07−06b/2009/ZAF MF787208.1_PTBP2016−117 KR107810.1_sewage/SD7606/2013/CHN KX245183.1_Sewage/SD147−5/GI.2/2014/CHN KR107759.1_sewage/SD0202/2013/CHN MH916772.1GI/BCCDC_PHL/CAN/2016/GI.2/1−20161123 KX245191.1_Sewage/SD214−4/GI.2/2014/CHN KR107932.1_sewage/SD7107/2013/CHN KR107800.1_sewage/SD7010/2013/CHN MF784793.1_NoV/Env/BRA/1610761/2016 KX775422.1_Pingtung/GI.2/201503/ROC KX245159.1_Sewage/SD101−4/GI.2/2014/CHN KR107757.1_sewage/SD0308/2013/CHN patient 2 KP064095.1_E2818 MF787206.1_PTBP2016−115 MH916781.1_GI/BCCDC_PHL/CAN/2017/GI.2/9−20170105 KR107779.1_sewage/SD1209/2013/CHN MF787205.1_PTBP2016−114 KR107933.1_sewage/SD7503/2013/CHN MF784791.1_NoV/Env/BRA/1610751/2016 KT383933.1_GI/Hu/KR/2015/GI.2/20150116FL01_2 KR107751.1_sewage/SD0205/2013/CHN KR107798.1_sewage/SD7004/2013/CHN KR107931.1_sewage/SD6901/2013/CHN KR107808.1_sewage/SD7508/2013/CHN KR107768.1_sewage/SD0503/2013/CHN KR107785.1_sewage/SD6702/2013/CHN MF784799.1_NoV/Env/BRA/1613691/2016 KX652372.1_Chiayi/GI.2/2015/ROC MH916776.1_GI/BCCDC_PHL/CAN/2016/GI.2/5−20161128 KR107930.1_sewage/SD6807/2013/CHN MF784773.1_NoV/Env/BRA/1520794/2015 MF784797.1_NoV/Env/BRA/1610773/2016 KT383934.1_GI/Hu/KR/2015/GI.2/20150116FL03_1 MF996721.1_Hu/GI.2/Pingtung/11−1/2015/TW MF787209.1_PTBP2016−118 KT239553.1_Hu/GI.2/NSW757Y/2014/AU MH916782.1_GI/BCCDC_PHL/CAN/2017/GI.2/10−20170105 KX245164.1_Sewage/SD106−6/GI.2/2014/CHN MF784780.1_NoV/Env/BRA/1528316/2015 KR107807.1_sewage/SD7502/2013/CHN KX245163.1_Sewage/SD106−2/GI.2/2014/CHN KR107775.1_sewage/SD1103/2013/CHN MF784762.1_NoV/Env/BRA/1520723/2015 KX245170.1_Sewage/SD142−10/GI.2/2014/CHN KR107765.1_sewage/SD0410/2013/CHN patient 1 KT383902.1_GI/Hu/KR/2014/GI.2/20140811EL06_2 MF784760.1_NoV/Env/BRA/1610787/2016 KR107774.1_sewage/SD1101/2013/CHN KR107934.1_sewage/SD7506/2013/CHN MF182347.1_GI/wastewater/ZA/2016/GI.2/OV_E_Feb KR107801.1_sewage/SD7204/2013/CHN KY427652.1_Hu/GI.2/GG0379/2010/KOR KR107758.1_sewage/SD0309/2013/CHN MF784795.1_NoV/Env/BRA/1610769/2016 KT151000.1_Hu/GI.2/NZ14079/2014/NZ MF784783.1_NoV/Env/BRA/1528343/2015 MF182344.1_GI/wastewater/ZA/2015/GI.2/FF_R_Dec KF361440.1_94L KR904271.1_GI/Hu/ZA/2012/GI.2/Cape_Town_8676 MF182349.1_GI/wastewater/ZA/2016/GI.2/DV_E_Mar MF182346.1_GI/wastewater/ZA/2016/GI.2/OV_E_Jan KX245186.1_Sewage/SD210−6/GI.2/2014/CHN MF784789.1_NoV/Env/BRA/1528526/2015 KC954403.1_Hu/GI/2761.2/2012/IE KX245169.1_Sewage/SD142−9/GI.2/2014/CHN KX245182.1_Sewage/SD144−9/GI.2/2014/CHN
From a One Health perspective, an outbreak related to surface water warrants a multidisciplinary approach investigating human, environmental and animal factors (Graciaa et al., 2018; Summa, Henttonen, & Maunula, 2018). As surface water is not routinely tested for NoVs, water specimens were only included for NoV-testing following notifications of disease when the playground water had already been refreshed. In future outbreak settings, it is advisable to obtain water specimens directly following disease outbreaks near recreational water. These can be stored under cold conditions and tested at a later moment. The same holds true for other environmental specimens, such as subsurface sand speci-mens, which can be positive for NoV while the water is negative (Schets et al., 2018).
In light of a recent publication on detection of human norovi-rus (HuNoV) in bird faeces in non-outbreak settings, it is of impor-tance that, in our case, bird faecal specimens underwent testing for HuNoV-testing as part of the outbreak investigation and were found to be negative (Summa et al., 2018). There has been a lot of historical attention on the disease-transmitting potential of bird faeces with a focus on bacteria and parasites (Benskin, Wilson, Jones, & Hartley, 2009; Elmberg, Berg, Lerner, Waldenstrom, & Hessel, 2017; Gorham & Lee, 2016; Graczyk, Majewska, & Schwab, 2008; Meerburg, Koene, & Kleijn, 2011). In this respect, however, a recent review found evidence suggesting HuNoV-transmission could in principle rather be directed from humans or the environment towards animals (Villabruna, Koopmans, & de Graaf, 2019).
Overall, our findings may serve to stress the fact that routine water testing for faecal bacteria and harmful algal blooms are not always a good indicator of viral-contamination which is in line with previous publications (Rose, Mullinax, Singh, Yates, & Gerba, 1987; Sinclair, Jones, & Gerba, 2009). It is advisable to collect a variety of environmental specimens, such as water specimens, subsurface sand specimens and animal stool, as soon as possible following an outbreak. Non-outbreak-related routine collection can increase knowledge on the background presence and relevance of norovirus.
In an era in which all sorts of natural recreation are gaining pop-ularity, it is prudent that clear guidelines are developed describing minimal requirements for recreational areas. In this case, the play-ground was well-designed and thoroughly constructed but a pump that was crucial for water refreshment went defunct. In general, though, measures should incorporate minimal hygiene facilities, such as a sufficient amount of garbage containers, simple shower, toilet, and diaper-changing facilities and a system avoiding poorly circulating shallow water. The public should be advised to avoid rec-reational activities in natural water when sick.
Ultimately, in accordance with the One Health approach de-scribed here, it should also be realized that these leisure areas are situated in the natural habitat of animals, keeping them in mind in our designs and interventions.
CONFLIC T OF INTEREST None.
ORCID
Gregorius J. Sips https://orcid.org/0000-0003-4506-983X
My V. T. Phan https://orcid.org/0000-0002-6905-8513
Marion P. G. Koopmans https://orcid.org/0000-0002-5204-2312
REFERENCES
Benskin, C. M., Wilson, K., Jones, K., & Hartley, I. R. (2009). Bacterial pathogens in wild birds: A review of the frequency and effects of infection. Biological Reviews of the Cambridge Philosophical Society,
84(3), 349–373. https ://doi.org/10.1111/j.1469-185X.2008.00076.x
de Graaf, M., van Beek, J., & Koopmans, M. P. (2016). Human norovi-rus transmission and evolution in a changing world. Nature Reviews
Microbiology, 14(7), 421–433. https ://doi.org/10.1038/nrmic
ro.2016.48
Elmberg, J., Berg, C., Lerner, H., Waldenstrom, J., & Hessel, R. (2017). Potential disease transmission from wild geese and swans to live-stock, poultry and humans: A review of the scientific literature from a One Health perspective. Infection Ecology and Epidemiology, 7(1), 1300450. https ://doi.org/10.1080/20008 686.2017.1300450 Ginsberg, J., Mohebbi, M. H., Patel, R. S., Brammer, L., Smolinski, M. S.,
& Brilliant, L. (2009). Detecting influenza epidemics using search engine query data. Nature, 457(7232), 1012–1014. https ://doi. org/10.1038/natur e07634
Gorham, T. J., & Lee, J. (2016). Pathogen loading from Canada geese faeces in freshwater: Potential risks to human health through recre-ational water exposure. Zoonoses Public Health, 63(3), 177–190. https ://doi.org/10.1111/zph.12227
Graciaa, D. S., Cope, J. R., Roberts, V. A., Cikesh, B. L., Kahler, A. M., Vigar, M., … Hlavsa, M. C. (2018). Outbreaks associated with untreated rec-reational water – United States, 2000–2014. MMWR. Morbidity and
Mortality Weekly Report, 67(25), 701–706. https ://doi.org/10.15585/
mmwr.mm6725a1
Graczyk, T. K., Majewska, A. C., & Schwab, K. J. (2008). The role of birds in dissemination of human waterborne enteropathogens. Trends in
Parasitology, 24(2), 55–59. https ://doi.org/10.1016/j.pt.2007.10.007
Kroneman, A., Vennema, H., Deforche, K., Avoort, H., Peñaranda, S., Oberste, M. S., … Koopmans, M. (2011). An automated genotyping tool for enteroviruses and noroviruses. Journal of Clinical Virology,
51(2), 121–125. https ://doi.org/10.1016/j.jcv.2011.03.006
Lewis, G. D., & Metcalf, T. G. (1988). Polyethylene glycol precipita-tion for recovery of pathogenic viruses, including hepatitis A virus and human rotavirus, from oyster, water, and sediment samples.
Applied and Environment Microbiology, 54(8), 1983–1988. https ://doi.
org/10.1128/AEM.54.8.1983-1988.1988
Liu, K., Huang, S., Miao, Z.-P., Chen, B., Jiang, T., Cai, G., … Jiang, J. (2017). Identifying potential norovirus epidemics in China via internet sur-veillance. Journal of Medical Internet Research, 19(8), e282. https :// doi.org/10.2196/jmir.7855
Matthews, J. E., Dickey, B. W., Miller, R. D., Felzer, J. R., Dawson, B. P., Lee, A. S., … Leon, J. S. (2012). The epidemiology of published noro-virus outbreaks: A review of risk factors associated with attack rate and genogroup. Epidemiology and Infection, 140(7), 1161–1172. https ://doi.org/10.1017/S0950 26881 2000234
Meerburg, B. G., Koene, M. G., & Kleijn, D. (2011). Escherichia coli con-centrations in feces of geese, coots, and gulls residing on recreational water in the Netherlands. Vector-Borne and Zoonotic Diseases, 11(6), 601–603. https ://doi.org/10.1089/vbz.2010.0218
Meldpunt Water. Retrieved from https ://www.meldp untwa ter.nl/ Prikazsky, V. (Ed.). Field Epidemiology Manual. Outbreak Investigations: 10
steps, 10 pitfalls. Retrieved from https ://wiki.ecdc.europa.eu/fem/w/
wiki/outbr eak-inves tigat ions-10-steps-10-pitfalls
Rockx, B., De Wit, M., Vennema, H., Vinje, J., De Bruin, E., Van Duynhoven, Y., & Koopmans, M. (2002). Natural history of human
calicivirus infection: A prospective cohort study. Clinical Infectious
Diseases, 35(3), 246–253. https ://doi.org/10.1086/341408
Rose, J. B., Mullinax, R. L., Singh, S. N., Yates, M. V., & Gerba, C. P. (1987). Occurrence of rotaviruses and enteroviruses in recreational waters of Oak Creek, Arizona. Water Research, 21(11), 1375–1381. https :// doi.org/10.1016/0043-1354(87)90012-1
Schets, F. M., van den Berg, H., Vennema, H., Pelgrim, M. T. M., Colle, C., Rutjes, S. A., & Lodder, W. J. (2018). Norovirus outbreak associ-ated with swimming in a recreational lake not influenced by external human fecal sources in the Netherlands, August 2012. International
Journal of Environmental Research and Public Health, 15(11), 2550.
https ://doi.org/10.3390/ijerp h1511 2550
Sima, L. C., Schaeffer, J., Le Saux, J. C., Parnaudeau, S., Elimelech, M., & Le Guyader, F. S. (2011). Calicivirus removal in a membrane bioreactor wastewater treatment plant. Applied and Environment Microbiology,
77(15), 5170–5177. https ://doi.org/10.1128/AEM.00583-11
Sinclair, R. G., Jones, E. L., & Gerba, C. P. (2009). Viruses in rec-reational water-borne disease outbreaks: A review. Journal
of Applied Microbiology, 107(6), 1769–1780. https ://doi.
org/10.1111/j.1365-2672.2009.04367.x
Sukhrie, F. H., Beersma, M. F., Wong, A., van der Veer, B., Vennema, H., Bogerman, J., & Koopmans, M. (2011). Using molecular epidemiol-ogy to trace transmission of nosocomial norovirus infection. Journal
of Clinical Microbiology, 49(2), 602–606. https ://doi.org/10.1128/
JCM.01443-10
Summa, M., Henttonen, H., & Maunula, L. (2018). Human noroviruses in the faeces of wild birds and rodents-new potential transmission routes. Zoonoses and Public Health, 65(5), 512–518. https ://doi. org/10.1111/zph.12461
The European Parliament and the Council of the European Union (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. Official Journal of the
European Union, L64, 37–51.
van Beek, J., de Graaf, M., Al-Hello, H., Allen, D. J., Ambert-Balay, K., Botteldoorn, N., … Koopmans, M. P. G. (2018). Molecular surveillance of norovirus, 2005–16: An epidemiological analysis of data collected from the NoroNet network. The Lancet Infectious Diseases, 18(5), 545–553. https ://doi.org/10.1016/S1473-3099(18)30059-8 van Beek, J., van der Eijk, A. A., Fraaij, P. L., Caliskan, K., Cransberg, K.,
Dalinghaus, M., … Koopmans, M. P. (2017). Chronic norovirus in-fection among solid organ recipients in a tertiary care hospital, the Netherlands, 2006–2014. Clinical Microbiology and Infection, 23(4), 265.e9–265.e13. https ://doi.org/10.1016/j.cmi.2016.12.010 van de Belt, T. H., van Stockum, P. T., Engelen, L. J. L. P. G., Lancee, J.,
Schrijver, R., Rodríguez-Baño, J., … Voss, A. (2018). Social media posts and online search behaviour as early-warning system for MRSA outbreaks. Antimicrobial Resistance and Infection Control, 7, 69. https ://doi.org/10.1186/s13756-018-0359-4
Villabruna, N., Koopmans, M. P. G., & de Graaf, M. (2019). Animals as reservoir for human norovirus. Viruses, 11(5), 478. https ://doi. org/10.3390/v1105 0478
World Health Organization (2017). One Health. Retrieved from https :// www.who.int/featu res/qa/one-healt h/en/
How to cite this article: Sips GJ, Dirven MJG, Donkervoort JT, et al. Norovirus outbreak in a natural playground: A One Health approach. Zoonoses Public Health. 2020;00:1–7. https ://doi.org/10.1111/zph.12689
