Epidemiological investigation of two parallel gastroenteritis outbreaks in school settings

Viral gastroenteritis is a major health problem worldwide. Viruses cause both seasonal acute gastroenteritis and occasional outbreaks associated with the consumption of contaminated food or water [1]. These outbreaks involve a number of high-risk groups, particularly young children, the elderly and immunocompromised patients [2–6]; they are frequent in semi-enclosed environments, such as school settings due to the increased number of people and the increased personal contacts among them. However, there is not a clear picture on the aetiological agents and source of infection in several outbreaks occurring in school settings because of underreporting and incomplete epidemiological and laboratory investigation of the reported ones. Regarding the source, a few publications refer to waterborne viral outbreaks in such settings [7–9].

In Greece, viral gastroenteritis outbreaks are generally under-reported [10–13] even though clusters of non-bacterial gastroenteritis cases are included in the mandatory notification system of the Hellenic Center for Disease Control and Prevention (HCDCP). To our knowledge no epidemiological studies have been published referring to viral outbreaks regarding a Greek school setting.

On 16 January 2012, HCDCP was informed on an increased number of pupils with gastroenteritis at an elementary school of Nea Santa Kilkis, a village with 1,538 residents, in Northern Greece. The reported symptoms were mild (mainly vomiting and diarrhoea), and supportive of a viral origin. Recommended pre-investigation interventions included the adoption of strict personal hygiene standards, disinfection of shared environmental surfaces, and exclusion of ill persons from school during their illness and for at least 48 hours after resolution of symptoms. A neighboring to the elementary school kindergarten was also contacted to ask for gastroenteritis cases in pupils or staff members and cases of gastroenteritis were confirmed.

The Public Health Department (PHD) of Kilkis informed HCDCP that there had been an increased occurrence of viral gastroenteritis after New Year’s Eve in the community but most of the cases had not visited a medical service. This increase was considered to be inside the limits of the expected for this time of year increase of viral gastroenteritis.

According to the results of the initial investigation of the outbreak at the elementary school, there were no shared meals and children were allowed to consume only the food brought by their home. Cases were almost simultaneously reported by the eight classes of the school and children of different classes did not have any common school activities the days that preceded the occurrence of the first cases. Furthermore, the cases occurred after the school was closed for 15 days for Christmas and New Year’s Eve holidays with the first cases experiencing symptoms late at night of the first day back to school. Initial investigation was against the hypothesis that a pupil or teacher could have been the source of the outbreak since no teacher was included among the first cases based on the reported onset date of symptoms, and the first children that developed symptoms were from different classes, were not family members or friends and had not participated to a common activity. Local public health authorities and teachers suspected that the heavy snowfall and the low temperature may have caused problems to the public water supply system that became obvious at the school as the tap water was not used for two weeks.

Further epidemiological investigation of the outbreak was decided as: a) attack rate of gastroenteritis was high in the elementary school and many cases occurred almost simultaneously, b) the source of the outbreak was not clear, c) outbreaks like this are rarely investigated in Greece and little information can be found in the literature, and d) cases also occurred in the neighboring to the school kindergarten. The objectives of the investigation were to identify the mode and the vehicle of transmission in both settings and also the possible connection between them.

We report on the investigation of two gastroenteritis outbreaks, in an elementary school and a neighboring kindergarten in a village with 1,538 residents in Northern Greece. Even though information from epidemiological and molecular investigation is of utmost importance to guide outbreak control measures and to prevent future outbreaks, gastroenteritis outbreaks at school settings are rarely investigated [19].

Evidence did not support the hypothesis of food-borne origin of the outbreak in the elementary school and cases could not be attributed to a single pupil or teacher. According to the results of the analytical epidemiological study, those who consumed tap water at school were more likely to develop gastroenteritis symptoms than those who did not consume tap water. The shape of the epidemic curve was compatible with a point source outbreak followed by secondary transmission. Even though the aetiological agent of the outbreak, was not verified, the epidemic curve in combination with the descriptive data, and the detection of NoV GI NoV GII, and AdVs in clinical samples collected from the elementary school pupils support the hypothesis of a mixed viral gastroenteritis outbreak. The detection of a viral pathogen/s was not possible at the tap water sample of the elementary school, but evidence of faecal contamination was found in one sample of tap water from the kindergarten, which was positive for hAdV; since the two schools have the same water supply system this finding is supportive of our hypothesis. Noroviruses (NoVs) and adenoviruses (AdVs) are common causative agents of gastroenteritis outbreaks in both children and adults and are believed to be implicated to several community outbreaks [20]. AdVs have been detected in waters of various origins and have been responsible for many waterborne outbreaks [21]. In addition, they have been proposed as indicators of human fecal contamination in water and food, since they are excreted by the populations of all geographical areas and are the most abundant viruses detected in urban sewage [22].

The fact that no Norovirus was detected in the analyzed water samples and that only the water sample from the kindergarten was found positive for AdVs can be explained by the fact that the two tap water samples were collected on 17 January, several days after the outbreak onset on 09 January and after the outbreak peak on 12/01/2012. NoVs and AdVs present different stability characteristics in the environment.

Financial constraints did not allow the molecular typing of the detected viral agents by sequencing.

Verification of the aetiological agent of waterborne outbreaks is always challenging since most of them are of mixed etiology [23–25] and sampling is usually performed with delay [25, 26]. In this outbreak, viruses could have already disappeared from the water or been present at much diluted concentrations in the supposed case of a transient contamination at the day of water sampling. Moreover, despite improvements in the methodology used, detection of viruses in water remains challenging and NoVs are not identified in water in most suspected Norovirus related waterborne outbreaks [27].

Based on the revised strength-of-evidence classification of waterborne outbreaks of the Centre for Diseases Control of USA [28], this outbreak could be considered as a class II waterborne outbreak based on the available epidemiological data. It is believed that heavy snowfall while the school was closed for 15 days and the fact that the water system of the schools was not used during that period contributed to an increased microbial load of the water that was consumed by teachers and pupils on the first day after holidays (9th January). Heavy rains and snowfalls contribute to run-off of water from the fields into the rivers through mobilization of pathogens in the environment [29–31]. The hypothesis that the water was contaminated with human or animal waste and that pathogens were multiplied during that period need further investigation.

Regarding gastroenteritis cases at the kindergarten, the shape of the epidemic curve refers to a person-to-person transmission and univariate analysis did not reveal a statistically significant risk factor. Diarrheic fecal samples were not collected, although recommended. The results of the investigation were not conclusive regarding the mode of transmission of the outbreak in the kindergarten. This was mainly because contacts were difficult to be defined due to the young age of children, many children were in diapers, and practices followed by the personnel inside the kindergarten could not be accurately documented. This viral gastroenteritis outbreak investigation is one of the very few that combined epidemiological, laboratory and environmental data in Greece; it highlights the value of molecular methods in outbreak investigations, and illustrates the importance of inter-agency collaboration.

Despite the limitations of this investigation, such as the delayed notification, the difficulty in collecting clinical and environmental samples early in the course of the outbreak, it clearly showed that the local public health authorities should play a more active role in the investigation of such outbreaks and that training of the personnel on the different aspects of outbreak investigation should be a future goal of HCDCP. Furthermore, since viral gastroenteritis outbreaks are frequent in school settings, school boards should be provided with a written protocol for timely notification of public health authorities and implementation of preventive measures. Recording of absenteeism at schools should be done on a daily basis and in a structured manner.

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

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