We estimated the magnitude of the reporting excess of laboratory-confirmed norovirus illness in Germany that paralleled a large outbreak of STEC O104:H4. Based on a count data time series analysis, the weekly incidence of reported norovirus illness increased overall by a factor of 1.76 (i.e., 76%) for the first three weeks of the outbreak before the outbreak vehicle was publicly communicated, with the highest excess in males aged 20–29 years (factor 2.88). Because it is highly unlikely that all persons suffering from gastroenteritis consulted a physician and received laboratory testing for norovirus during this outbreak, we interpret these estimates to be minimal under-reporting factors. This explains – apart from differing structures of surveillance systems – why our estimated overall under-reporting factor is lower than factors reported from other countries, e.g. factor 12.7 from England and Wales [8].
The estimated under-reporting varied by sex and by age-group and was highest in 20–29 year-olds. However, it was not as high as we had expected based on the fact that younger age-groups, especially women, were communicated to be highly represented among cases early during the outbreak. Our assumption was that especially women aged 20–39 years presented more frequently to their physician when suffering from gastroenteritis during the outbreak than usually. There are two possible explanations: either, the public, and especially the younger age-groups, did not perceive the risk communication message as it was intended, and patients did not consult physicians more often when suffering from diarrhoea, or physicians did not initiate laboratory testing more often for these younger age-groups. Alternatively, the message was perceived and physician consultations and laboratory testing increased, but norovirus infections were not that prevalent in this age-group. For the youngest (0–9 years) and the oldest age-group (70 years and above), the differences were less pronounced, or even absent, compared to previous years. The discrepancy between the crude reporting excess reported in Table 1 and the (smaller) model-based under-reporting factors for these two age-groups can be explained by the increasing trend of reported case numbers over time (see Additional file 1: Mathematical Appendix). Furthermore, we did not find any significant geographic variation of our estimates (data not shown). The Mathematical Appendix also contains a more detailed analysis and visualisation of the model fit together with a discussion of possible model limitations including autocorrelation.
Our approach is unusual in that it used data from the passive surveillance system of infectious diseases to estimate this systems’ own degree of under-ascertainment (with regard to norovirus illness). Enabled by the occurrence of a public health emergency event, this inexpensive approach cannot distinguish between the effects of increased health care-seeking behaviours by cases, stool collection by clinicians, or testing by laboratories. It furthermore remains unclear whether physicians who collected patients’ stool during the outbreak specifically ordered testing for norovirus or whether they simply ordered testing for a panel of infectious enteric pathogens, which then also included norovirus. The observed parallel reporting increase of other enteric pathogens, e.g., Campylobacter spp., gives weight to the hypothesis that norovirus testing was often an unintentional by-product of increased stool testing initiated to search primarily for STEC during the outbreak. How detailed physicians need to specify the pathogens when ordering laboratory testing is influenced by health insurance reimbursement policies, which vary across Germany. At any rate, more complex study designs are needed, e.g., cohort studies, to specifically address under-reporting at the different levels of the surveillance pyramid.
We deem it unlikely that the increase in reported case numbers reflects a true increase in norovirus activity in the outbreak period. First, increased case numbers were also reported for other reportable infectious enteric diseases for this period [7], supporting our hypothesis that fear of STEC infection led to more diagnostic testing. Second, the increase was higher before the public announcement that sprouts were the likely vehicle of infection, suggesting less pressure for testing after the announcement. Third, the increase differed across age-groups. It was less pronounced in young children and older women who usually have the highest incidences of reported norovirus illness [14] due to their exposure in child-care facilities and residential homes, whereas it was stronger in young adults who are usually not that frequently affected in these classical norovirus outbreak settings. A fourth argument against a true increase in norovirus activity during the outbreak period is that, although large fluctuations of the incidence of norovirus illness between the seasons exist and have been hypothesized to be influenced by the emergence of new virus variants [15], the season 2010/2011 altogether was one with lower norovirus activity compared to 2009/2010 in Germany [7] and other countries in Europe, e.g. in England and Wales [16].
Due to the temporal occurrence of the STEC O104:H4 outbreak, our estimates apply to a specific time-period outside the peak of the norovirus season (which is classically in winter). Hence, our analyses cannot show, whether under-reporting factors are time dependent and, if so, in what direction they would tend to go in other time periods, e.g. during the peak season. It is conceivable that they were smaller during winter because the health-care system would be more aware of norovirus infections and more likely to detect them. On the other hand, increased norovirus circulation and a higher familiarity with gastroenteritis symptoms during winter could lead to lower consultation rates of patients and stool collection rates by physicians, and therefore to larger under-reporting.
