Epidemiology and Infection A foodborne norovirus outbreak in a nursing cambridge.org/hyg home and spread to staff and their household contacts I. Parrón1, J. Álvarez1, M. Jané2,3, T. Cornejo Sánchez4, E. Razquin5, S. Guix6,7, Original Paper G. Camps1, C. Pérez1, À. Domínguez3,8 and the Working Group for the Study of *The Working Group for the Study of Outbreaks of Acute Gastroenteritis in Outbreaks of Acute Gastroenteritis in Catalonia* Catalonia (PI16/02005) is composed of: 1 Miquel Alsedà, Josep Álvarez, Irene Barrabeig, Sub-Direcció Regional a Barcelona del Departament de Salut, Barcelona, Spain; 2Sub-Direcció General de Isabel Belver, Neus Camps, Sofia Minguell, Vigilància i Resposta a Emergències de Salut Pública, Barcelona, Spain; 3CIBER Epidemiology and Public Health, Monica Carol, Pere Godoy, Conchita Izquierdo, Carlos III Health Institute, Madrid, Spain; 4Departament de Microbiologia, Vall d’Hebrón Hospital, Barcelona, Mireia Jané, Ana Martínez, Ignacio Parrón, Spain; 5Laboratori de l’Agència de Salut Pública de Barcelona, Barcelona, Spain; 6Departament de Genètica, Grup Cristina Pérez, Ariadna Rovira, Maria Sabaté, M Rosa Sala, Núria Torner, Rosa M Vileu (Agència de Virus Entérics, Microbiología i Estadística, Universitat de Barcelona, Barcelona, Spain; 7Institut d’Investigación de Salut Pública de Catalunya); Anna de en Nutrició i Seguretat Alimentària (INSA-UB), Universitat de Barcelona, Barcelona, Spain and 8Departament de Andrés, Javier de Benito, Esteve Camprubí, Medicina, Universitat de Barcelona, Barcelona, Spain Montse Cunillé, M Lluïsa Forns, Antonio Moreno-Martínez, Efrén Razquín, Cristina Rius, Abstract Sara Sabaté, Mercé de Simón (Agència Salut Pública de Barcelona, CIBERESP); Rosa On 16 March 2018, a nursing home notified a possible acute gastroenteritis outbreak that Bartolomé, Thais Cornejo (Hospital Vall affected 11 people. Descriptive and case–control studies and analysis of clinical and environ- d’Hebron); Susana Guix, Rosa M Pintó, Albert mental samples were carried out to determine the characteristics of the outbreak, its aetiology, Bosch (Laboratori de Virus Entèrics, Universitat de Barcelona); Lorena Coronas, Àngela the transmission mechanism and the causal food. The extent of the outbreak in and outside Domínguez, Núria Soldevila (Departament de the nursing home was determined and the staff factors influencing propagation were studied Medicina, Universitat de Barcelona, by multivariate analysis. A turkey dinner on March 14 was associated with the outbreak (OR CIBERESP). 4.22, 95% CI 1.11–16.01). Norovirus genogroups I and II were identified in stool samples. The Cite this article: Parrón I et al (2019). A attack rates in residents, staff and household contacts of staff were 23.49%, 46.22% and foodborne norovirus outbreak in a nursing 22.87%, respectively. Care assistants and cleaning staff were the staff most frequently affected. home and spread to staff and their household Cohabitation with an affected care assistant was the most important factor in the occurrence contacts. Epidemiology and Infection 147, of cases in the home (adjusted OR 6.37, 95% CI 1.13–36.02). Our results show that staff in e225, 1–7. https://doi.org/10.1017/ S0950268819001146 close contact with residents and their household contacts had a higher risk of infection during the norovirus outbreak. Received: 3 December 2018 Revised: 5 May 2019 Accepted: 15 May 2019 Introduction Key words: Acute gastroenteritis; household contacts; Noroviruses are non-enveloped RNA viruses of the Caliciviridae family which have six norovirus; nursing home; outbreaks genogroups (GI to GVI), although only genogroups I, II and IV are human pathogens [1, Author for correspondence: I. Parrón, 2]. Norovirus infection is usually characterised by nausea, vomiting and a self-limiting evolu- E-mail: iparron@gencat.cat tion of about 48–72 h [3]. The viral capsid provides specific resistance to the external environment, including high levels of chlorine [4], heat and cold [5], acidic pH and organic solvents [6, 7]. These charac- teristics mean norovirus is highly infective and can survive a long time in the environment [8]. There are different modes by which transmission may occur (direct person-to-person or indir- ect via faecal contamination in the environment or on foods) [9]. The low infectious dose (mean of 18 viral particles) [7], and the lack of long-term immunity in infected persons (the duration of immunity has been considered to be 6–24 months, although a recent study suggests that immunity lasts 4–9 years following infection) [10], means that norovirus often causes outbreaks in institutions and closed and semi-closed groups. © The Author(s) 2019. This is an Open Access Norovirus is the main cause of viral acute gastroenteritis (AGE) outbreaks worldwide article, distributed under the terms of the Creative Commons Attribution- (>90% of AGE outbreaks are attributed to norovirus) [11], causing >1.8 million deaths in chil- NonCommercial-ShareAlike licence (http:// dren aged <5 years annually [12]. creativecommons.org/licenses/by-nc-sa/4.0/), As in other European countries [13], in Catalonia norovirus outbreaks are frequent in nurs- which permits non-commercial re-use, ing homes: in 2010–2011 nearly 30% of norovirus outbreaks occurred in this type of setting distribution, and reproduction in any medium, [9], where older age and multiple comorbidities can result in hospital admission and even provided the same Creative Commons licence is included and the original work is properly death [14]. The immediate introduction of infection control measures (hand hygiene, princi- cited. The written permission of Cambridge ples of food safety, disinfection of contaminated surfaces, isolation of ill persons and no return University Press must be obtained for to work until 2 days after the absence of symptoms) decreases the duration of outbreaks and commercial re-use. the attack rates in residents and staff [13]. In Spain, the institutionalised population increased by >90% between 2001 and 2011, and more than 60% of this population (2 70 000 people) are estimated to live in nursing homes [15]. Many studies have looked at the factors that cause outbreaks, but fewer have looked at transmission beyond the primary outbreak setting [16–19]. The objective of this study was https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press 2 I. Parrón et al. to investigate a foodborne outbreak of norovirus in a nursing evolution, in addition to maintaining the control measures indi- home and measure its impact on residents and the spread in cated. Information on the demographic and clinical variables of staff and their household contacts. new cases was collected. The health personnel of the home col- lected the information. The food-handling facilities were inspected, including collecting environmental samples from the Material and methods kitchen and common use areas. It was not possible to process Outbreak notification samples of the food potentially implicated in the outbreak as our laboratory does not have approved International On 16 March 2018, a nursing home notified a possible AGE out- Organization for Standardization certification for the food that break that affected nine residents and two staff. The onset of AGE the case–control study showed was associated with the outbreak. in the first cases occurred on the afternoon of March 15. The pre- Between March 26 and April 1, the extent of the outbreak in dominant symptoms were nausea, vomiting and watery diarrhoea household contacts of staff was quantified. We actively investigated without blood or fever. When the suspected outbreak was noti- how many staff were clinical cases using a survey that included age, fied, some affected individuals were already recovering and no sex, whether they had been infected (with date of onset and end), patient required hospitalisation number of household contacts of staff (with age and sex), whether these were clinical cases and date of onset. The aim of this survey, Outbreak setting which was self-completed by staff, was to determine the extent of ill- ness in staff and their household contacts. The care home had 166 residents on three floors. Residents with greater autonomy (116) lived on the first floor, semi-autonomous persons (27) on the second floor and those with the highest Laboratory analyses degree of dependency (23) on the third floor. The home had 119 staff: 42 on the first floor (three shifts of 14), 12 on the second Stool samples were collected on March 18. Samples were sent to floor (three shifts of 4) and 12 on the third floor (three shifts of 4). the Vall Hebrón University Hospital microbiology laboratory The remaining 53 staff (maintenance, laundry and cleaning, for testing for norovirus (if negative, testing for rotavirus, adeno- kitchen and medical) were not assigned to a specific floor. virus, astrovirus and sapovirus was made). Given the suspicion of The centre had a kitchen and dining room on the ground floor viral AGE, bacterial tests were not carried out. The specific pri- that was used by patients admitted to the first and second floors. mers described by Kageyama et al. [20] for the detection of nor- On the third floor, there was a second dining room for patients ovirus GI and GII were used for RT-PCR. Norovirus genogroup although they could have meals in their rooms. IV (GIV) was detected using a modification of the primers Various menus were prepared according to individual charac- described by Farkas et al. [21] and Kageyama et al. [20]. For geno- teristics (normal diet, diabetic, easy chewing, soft foods and low typing, the ORF1–ORF2 junction was sequenced from all samples calorie), although the menus were basically combinations of dif- laboratory-confirmed for norovirus. To amplify this region, a one- ferent dishes and only the soft food menu was markedly different. step RT-PCR assay was carried out using the One-Step RT-PCR The home had been in operation for some years; the structure kit (Qiagen, Hilden, Germany) with previously published primers and facilities were adequate for its stated activity and the number GISKF, GISKR for GI NoV, and G2SKF and G2SKR primers for of residents was below the maximum capacity. Routine inspec- GII NoV [20, 22]. PCR products were then purified using tions had detected no deficiencies. Exo-SAP-IT (USB, Affymetrix Inc., Cleveland, Ohio, USA) and sequenced by the ABI Prism Big Dye Terminator cycle sequen- cing kit v3.1 on the ABI PRISME 3130XL sequencer (Applied Definitions Biosystems, Foster City, California, USA). Nucleotide sequences A clinical case of norovirus infection was defined as a person with were assembled and edited using SeqMan 4.05 (Dnastar, onset of diarrhoea and/or vomiting between March 15 and 31 Madison, Wisconsin, USA). Norovirus typing tool v2.0 was who lived or worked in the nursing or was a household contact used to genotype norovirus. of a staff member. A confirmed case was defined as a clinical Environmental samples were collected with polyester swabs. case that was positive for norovirus in faeces by real-time poly- Total nucleic acids were extracted with BioMérieux NucliSENS merase chain reaction (RT-PCR). easyMag system. The reagents, primers and cycling conditions of the real-time RT-PCR used for the detection of norovirus GI and GII were those indicated in ISO 15216-2:2013 [23]. Study phases The data were stored and subsequently debugged in a Microsoft Access database. The study was carried out in three phases: The first, carried out on March 17 and 18, was aimed at verifying the aetiology and mechanism of the outbreak. An epidemiological survey was Statistical analysis designed to gather socio-demographic data, symptom onset and end and clinical data. A food survey was conducted to determine The mean age of clinical cases and controls was compared using the type of menu and the specific dishes consumed. The question- the two-sample t test and percentages of the distribution of sexes naire was filled in by the health staff of the centre. A case–control using the χ 2 test. Univariate analysis was used to determine the study was designed: cases were chosen from clinical cases in resi- associations between the consumption of each dish served and dents and controls were chosen from residents who did not AGE, using the odds ratio (OR) and 95% confidence intervals become ill. (95% CI). The second phase, carried out from March 19 to 25, was aimed The risk of AGE in household contacts of staff who were clinical at quantifying the size of the outbreak and monitoring its cases or not was calculated using the rate ratio (RR) and 95% CI. https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press Epidemiology and Infection 3 Fig. 1. Distribution of clinical cases by day of onset in residents, staff and household contacts. In staff, the association between professional category and the symptoms were vomiting (64.3%), diarrhoea (62.5%), abdominal risk of AGE was estimated by calculating the OR and 95% CI. In pain (37.5%) and fever (14.3%). Symptom duration was approxi- household contacts of staff that were clinical cases, the risk of mately 24 h (median 1 day, range 1 h 55 min to 4 days). infection and the determining factors were estimated by calculat- Stool samples were collected from 28 people: 14 were clinical ing the OR and 95% CI. Multivariate logistic regression was car- cases (10 residents and four caregivers) and 14 were not (six resi- ried out to control for the influence of possible confounding dents, three caregivers and five kitchen staff). Ten samples were variables: the variables age of household contact, sex of household positive for norovirus (two GI, six GII and two GI/GII). The contact, number of household contacts and the duration of illness genotype was identified in nine cases: seven were GII.17 and in staff were included in the adjustment. The statistical analysis two GI.3. Six positive samples came from confirmed cases and was made using the PASW Statistic 18.0.2 statistical package. four from asymptomatic persons. Eight environmental samples were collected (three from kitchen staff lavatories, two from the kitchen and three from common areas of the residence). No Results environmental sample was positive for norovirus. Information was collected on 361 people (54 residents, 119 staff The food consumption questionnaire was answered by 46 resi- and 188 household contacts of staff). Seventy-nine persons (25 dents (25 clinical cases and 21 controls), including the type of diet staff and 54 residents) were exhaustively surveyed, of whom 56 and the food served during the two suspect meals. In four people, were infected and 23 were not. For the remaining 94 staff and it was only possible to identify the type of diet followed. Twenty 188 household contacts of staff, socio-demographic information, per cent of clinical cases and 19% of controls were male: the mean professional category and, in clinical cases, the date of onset, age was 78.8 years (S.D. 22.4) in clinical cases and 71.2 years (S.D. was collected. 26.2) in controls: the differences were not statistically significant. The AGE outbreak affected 137 people (39 residents, 55 staff Table 1 shows the distribution of individuals who were clinical and 43 household contacts). The patients affected were mainly cases or not, according to the consumption of a specific food or residents of the first and second floors and some staff, with no diet. No significant differences were observed between different resident of the third floor being affected. The temporal grouping diets. However, when the consumption of each food was analysed, of the first reported cases suggested a common exposure that the turkey served on the night of March 14 was associated with might have occurred at dinner on March 14, although breakfast being a clinical case (OR 4.22, 95% CI 1.11–16.01). In contrast, on March 15 could not be ruled out. The clinical characteristics the alternative to turkey (cod fritters) showed an OR of 0.12 suggested norovirus as the cause of the outbreak. (95% CI 0.02–0.75). Figure 1 shows the epidemic curve, and clinical cases in resi- Table 2 shows the attack rate in household contacts of staff that dents, staff and household contacts. were clinical cases or not. The overall attack rate in household The attack rates in residents, staff and household contacts were contacts was 22.87%, although the rates clearly differed between 23.49%, 46.22% and 22.87%, respectively. The most frequent household contacts of staff with and without illness (38.09% vs. https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press 4 I. Parrón et al. Table 1. Distribution of clinical cases and controls according to food consumption Clinical cases Controls Consumption No consumption Consumption No consumption OR (95% CI) Food category Diabetic 5 20 4 17 1.06 (0.24–4.60) Easy chewing 5 20 4 17 1.06 (0.24–4.60) Low calorie 0 25 1 20 0 (0–15.96) Normal 8 17 3 18 2.82 (0.64–12.44) Soft food 3 22 1 20 2.73 (0.26–28.39) Foods Sandwich 15 6 12 9 1.81 (0.52–6.29) Coffee with milk 11 10 7 14 2.12 (0.63–7.14) Milk 2 19 1 20 1.75 (0.21–14.55) Biscuits 2 19 1 20 1.75 (0.21–14.55) Soup 10 11 12 9 0.69 (0.21–2.28) Turkey 11 10 4 17 4.22 (1.11–16.01)* Cod fritters 1 20 8 13 0.12 (0.02–0.75)* Mixed vegetables 2 19 0 21 5.51 (0.25–122.10) Custard 1 20 0 21 3.15 (0.12–81.72) Soft food 3 18 1 20 2.59 (0.34–19.36) OR, odds ratio. *Statistically significant values (P < 0.05). 3.61%), with an RR of 10.54 (95% CI 3.38–32.87; P < 0.001). centres and other institutions. Becker et al. described an AGE out- Table 3 shows the risk of being a clinical case in each professional break due to the consumption of turkey sandwiches in a football category, expressed as the OR and 95% CI. The administration team and transmission to the opposing team [25]. Marsh et al. and services categories had a protective effect (OR 0.07, 95% CI analysed three outbreaks of food poisoning in which secondary 0.01–0.53). Table 4 shows the risk of being a clinical case in cases due to person-to-person transmission were found in house- household contacts in each staff category, expressed as the OR hold contacts of persons affected: 25% of the homes of those and 95% CI and the level of significance. Household contacts of affected had secondary cases, with an attack rate of 20% among a care assistant had a 5.5-fold higher risk of being a clinical contacts [16]. case than household contacts of the remaining staff. The profes- The epidemic curve in staff showed a delay in the onset of ill- sional categories of the remaining staff did not influence the ness compared with residents, which suggests residents were risk of their household contacts being a clinical case. In the multi- involved first and there was secondary transmission to staff. variate analysis (Table 5), the administration and service categor- Cases in staff from the beginning of the outbreak suggest that, ies were too small for separate analysis and were therefore although the staff did not have dinner in the centre, some prob- grouped with the cleaning staff. After adjustment, the only factor ably consumed the foods that triggered the outbreak. A possible significantly associated with the risk of being a clinical case was reason for the absence of clinical cases in third floor residents being a household contact of a care assistant (adjusted OR 6.37, may be explained by the fact that these persons did not consume 95% CI 1.13–36.02). the food that caused the outbreak and, due to limitations in move- ment, did not have physical contact with the other residents. Norovirus GI and GII co-infection was detected in two Discussion patients. Co-infection by more than one genogroup during epi- Our results show that the AGE outbreak investigated originated demic norovirus outbreaks is not exceptional. Ushijima et al. in from common exposure to food and was subsequently spread a review of food poisoning due to norovirus in Japan found GI/ by person-to-person transmission. The epidemic curve showed GII co-infection in up to 10% of outbreaks [26]. Huang et al. ana- the rapid emergence of cases, mostly in residents, and then a lysed an outbreak that affected six groups of tourists and, of the 23 more pronounced peak including staff and spread to household stool samples analysed, 22 were positive for norovirus GI and/or contacts of staff. The distribution of clinical cases in residents GII (six patients were co-infected by the two genogroups) [27]. was typical of the distribution of cases in a common source out- The presence of more than one norovirus genogroup has also break due to a specific exposure [24]. been observed when possible sources of infection are analysed. Reports have described outbreaks that begin with food poison- In an outbreak of AGE due to norovirus whose origin was bottled ing and continue with person-to-person transmission in nursing mineral water distributed among 925 Spanish companies, both https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press Epidemiology and Infection 5 Table 2. Attack rates in household contacts of staff according to clinical case Table 3. Clinical cases according to professional category status in staff Not Number of Clinical clinical Number of household contacts cases cases OR (95% CI)a household who became clinical Attack contacts cases rate Professional category Status of staff Administration 1 15 0.07 (0.01–0.53)** and services Clinical 105 40 38.09% case Health staff 7 5 1.96 (0.58–6.62) Not 83 3 3.61% Care assistants 32 31 2.06 (0.93–4.56) clinical Cleaning staff 7 10 0.89 (0.31–2.55) case Administration 8 25 0.29 (0.12–0.74)** Total 188 43 22.87% and services + Rate ratio (RR): 10.54 (95% CI 3.38–32.87; P < 0.001). cleaning staff OR, odds ratio. a Comparing each professional category with the rest. **Statistically significant values (P < 0.05). the analysis of the water and the faeces of affected people were positive for norovirus GI and GII [28]. The attack rates in staff (46.22%) and residents (23.49%) are and service staff were the least affected (attack rate of 6.67%), those expected in a norovirus outbreak due to food in a nursing and this category was a protective factor against infection (OR home with these characteristics. A review by Lindsay et al. of nor- 0.07, 95% CI 0.01–0.53). ovirus infection in older people from middle- and high-income The greater involvement of care assistants could be due in part countries found the attack rate in outbreaks in nursing homes to the pressure of care to which they are subjected. According to a ranged from 3% to 45% [29]. Similar variability was found by 2011 report by the Organization for Economic Cooperation and Green et al. in a study of 20 AGE outbreaks between 1987 and Development (OECD), the percentage of staff assigned to care 1988, with the attack rate ranging between 5% and 59% (median for older people is below what is desirable, but in some countries, 27%) in residents of nursing homes and between 0.6% and 26% such as Spain, this is especially relevant. While Sweden allocates (median 9%) in staff [30]. Utsumi et al. in another review of out- 3.6% of staff to this sector, Spain allocated just over 1% [36]. breaks of infectious aetiology in long-stay centres between 1966 There were also AGE cases in household contacts of staff, with and 2008 found that, in norovirus outbreaks, the mean attack a higher attack rate in people who lived with infected staff than in rate was 45% (range 13–100%) in residents and 42% (range those who did not (38.09% vs. 3.61%). This result is consistent 9–100%) in staff [31]. with the study by Sukhrie et al. of five outbreaks of AGE due We found an attack rate in household contacts of clinical cases to norovirus in two care homes and a university hospital in in staff of 22.87%, similar to the results of other studies. Marsh Rotterdam, which described the role of health staff in the trans- et al. described a secondary attack rate of 20% in household con- mission of the virus, while noting the low importance of asymp- tacts of infected persons in three outbreaks of food poisoning tomatic carriers [37]. There was a significant association between [16]. In an outbreak of food poisoning due to norovirus related the risk of household contacts of care assistants becoming infected to the consumption of oysters in a restaurant in North Carolina and the professional category of the worker (OR 5.50, 95% CI in 2009, secondary cases were found in 20% of households 1.72–17.61). included in the analysis and the attack rate was 14% in household Multivariate analysis showed that household contacts of care contacts (who had not eaten in the restaurant) [17]. Heun et al. assistants had an increased risk of infection (adjusted OR 6.37, studied a 1984 outbreak of food poisoning in a school due to nor- 95% CI 1.13–36.02), independently of other variables such as ovirus and, as in our study, the risk in household contacts of those the number of people in the home, the age or sex of household affected was greater than the risk in household contacts of persons contacts and the duration of symptoms presented by staff. who did not become ill [18]. The study had some limitations. First, we could not confirm Although the association was not significant, we found the the greater risk of illness among cleaning staff, probably due to most frequently affected staff were care assistants (OR 2.06, 95% a lack of statistical power. Second, the number of clinical samples CI 0.93–4.56), who have the most direct, closest and longest con- did not allow to study the possible differences between people tact with residents. The intensity of contact plays a fundamental affected by GI, GII or co-infected by both genogroups. Third, role in the risk of infection during an AGE outbreak due to nor- we could not analyse the presence of norovirus in the foods ovirus. Petrignani et al. reviewed norovirus outbreaks in care involved in the outbreak, especially in the turkey dish served at homes and found a higher intensity of contact between staff dinner on March 15, which was statistically associated with the and residents was associated with higher attack rates [32]. appearance of AGE. Fourth, clinical samples were not available Godoy et al. found attack rates of 56.5% in care assistants in an for household contacts that became clinical cases; however, the outbreak in an assisted living facility [33] and González Moran attack rates of household contacts of ill and unaffected staff et al. found attack rates of 35.8% in health staff (mostly care assis- showed significant differences, suggesting that cases in household tants) in a nursing home [34]. These two studies also found that contacts of staff were related to the outbreak and not to other cleaning staff were frequently affected (attack rates of 55.6% and viruses circulating in the community. 40.0%, respectively). In our study, the attack rate in cleaning In conclusion, our results suggest that the study of AGE out- staff was 41.2%, similar to other studies [33, 35]: administration breaks in nursing homes may be extended to the household https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press 6 I. Parrón et al. Table 4. Risk of becoming a clinical case in household contacts of clinical cases in staff Number of household contacts of staff clinical cases Professional category of clinical Household contacts who became Household contacts who did not case staff clinical cases become clinical cases OR (95% CI)a P value Administration and services 0 5 0 (0–1.16) 0.069 Health personnel 2 6 0.46 (0.09–2.40) 0.293 Care assistants 35 35 5.50 (1.72–17.61) 0.005 Cleaning staff 2 11 0.23 (0.05–1.08) 0.091 OR, odds ratio. a Comparing each professional category with the rest. Table 5. Risk of becoming a clinical case in household contacts of the clinical cases in staff. Multivariate analysis OR (95% CI) P value aORa (95% CI) P value Health staff 2.67 (0.30–23.42) 0.38 2.99 (0.23–39.54) 0.40 Care assistants 8.00 (1.71–37.42) 0.01 6.37 (1.13–36.02) 0.04 Administration and services/cleaners Ref. Ref. aOR, adjusted odds ratio; Ref., reference group. a Adjusted for age of household contact, sex of household contact, number of household contacts and duration of illness in staff. contacts of staff. Staff that have more intense contact with resi- Racaniello VR and Roizman B (eds), Fields Virology, 6th Edn. dents, such as care assistants, are more likely to generate second- Philadelphia: Lippincott Williams & Wilkins, pp. 582–608. ary cases in household contacts, which has important health and 8. Wu HM et al. (2005) A norovirus outbreak at a long-term-care facility: the role of environmental surface contamination. Infection Control and economic consequences [38, 39]. Care assistants working in nurs- Hospital Epidemiology 26, 802–810. ing home staff should receive additional training in the applica- 9. Torner N et al. (2016) Epidemiology of acute gastroenteritis outbreaks tion of preventive protocols. caused by human calicivirus (Norovirus and Sapovirus) in Catalonia: a two year prospective study, 2010–2011. PLoS ONE 11, e0152503. Author ORCIDs. I. Parrón, 0000-0002-4875-0236; À. Domínguez, 0000- 10. Ramani S, Estes MK and Atmar RL (2016) Correlates of protection 0003-0219-1907. against norovirus infection and disease – where are we now, where do Financial support. This study was funded by the Carlos III Health Institute we go? PLoS Pathogens 12, e1005334. through the project PI16/02005 (Co-funded by the European Regional 11. Patel MM et al. (2009) Noroviruses: a comprehensive review. Journal of Development Fund ‘Investing in your future’) and the Catalan Agency for Clinical Virology 44, 1–8. the Management of Grants for University (AGAUR Grant Number 2017/ 12. Bryce J et al. (2005) WHO estimates of the causes of death in children. SGR 1342). The Lancet 365, 1147–1152. 13. Friesema I et al. (2009) Norovirus outbreaks in nursing homes: the evaluation Conflict of interest. None. of infection control measures. Epidemiology and Infection 137, 1722–1733. 14. Desai R et al. (2012) Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: a systematic literature review. Clinical Infectious Diseases 55, 189–193. References 15. Instituto Nacional de Estadística. Censos de Población y Viviendas 2011. 1. Atmar RL, Ramani S and Estes MK (2018) Human noroviruses: recent Población residente en establecimientos colectivos. Available at http:// advances in a 50-year history. Current Opinion in Infectious Diseases 31, www.ine.es/prensa/np777.pdf (Accessed 4 March 2018). 422–432. 16. Marsh ZA et al. (2018) The unwelcome houseguest: secondary household 2. International Committee on Taxonomy of Viruses (ICTV) (2017) ICTV transmission of norovirus. Epidemiology and Infection 146, 159–167. 9th Report. Available at https://talk.ictvonline.org/ictv-reports/ictv_9th_re- 17. Alfano-Sobsey E et al. (2012) Norovirus outbreak associated with under- port/positive-sense-rna-viruses-2011/w/posrna_viruses/253/caliciviridae cooked oysters and secondary household transmission. Epidemiology and (Accessed 24 September 2018). Infection 140, 276–282. 3. Heyman DL (ed) (2015) Control of Communicable Diseases Manual, 20th 18. Heun EM et al. (1987) Risk factors for secondary transmission in house- Edn. Washington: American Public Health Association, pp. 218–220. holds after a common-source outbreak of Norwalk gastroenteritis. 4. Keswick BH et al. (1985) Inactivation of Norwalk virus in drinking water American Journal of Epidemiology 126, 1181–1186. by chlorine. Applied and Environmental Microbiology 50, 261–264. 19. Gastañaduy PA et al. (2015) Transmission of norovirus within house- 5. Butot S, Putallaz T and Sánchez G (2008) Effects of sanitation, freezing holds in Quininde, Ecuador. Pediatric Infectious Disease Journal 34, and frozen storage on enteric viruses in berries and herbs. International 1031–1033. Journal of Food Microbiology 126, 30–35. 20. Kageyama T et al. (2003) Broadly reactive and highly sensitive assay for 6. Butot S et al. (2009) Inactivation of enteric viruses in minimally processed Norwalk-like viruses based on real-time quantitative reverse berries and herbs. Applied and Environmental Microbiology 75, 4155– transcription-PCR. Journal of Clinical Microbiology 41, 1548–1557. 4161. 21. Farkas T et al. (2015) Multiplex real-time RT-PCR for the simultaneous 7. Green KY (2013) Caliciviridae: the noroviruses. In Knipe DM, detection and quantification of GI, GII and GIV noroviruses. Journal of Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Virological Methods 223, 109–114. https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press Epidemiology and Infection 7 22. Kojima S et al. (2002) Genogroup-specific PCR primers for detection 31. Utsumi M et al. (2010) Types of infectious outbreaks and their impact in of Norwalk-like viruses. Journal of Virological Methods 100, 107–114. elderly care facilities: a review of the literature. Age and Ageing 39, 23. Anon (2013) Microbiology of the food chain – horizontal method for 299–305. determination of hepatitis A virus and norovirus in food using RT-PCR 32. Petrignani M et al. (2015) Norovirus introduction routes into nursing – Part 2: Method for qualitative detection. ISO 15216-2:2013. homes and risk factors for spread: a systematic review and meta-analysis International Organization for Standardization. Geneva. of observational studies. Journal of Hospital Infection 89, 163–178. 24. Fontaine RE and Goodman RA (2008) Describing the findings: descrip- 33. Godoy P et al. (2006) Brote de norovirus de transmisión persona a per- tive epidemiology. In Gregg MB (ed.), Field Epidemiology, 3rd Edn. sona en una residencia asistida. Medicina Clínica 127, 538–541. New York: Oxford University Press, pp. 156–198. 34. González Morán F et al. (2002) Nosocomial epidemic outbreak of 25. Becker KM et al. (2000) Transmission of Norwalk virus during a football acute gastroenteritis by Norwalk-like virus. Medicina Clínica 118, 611–615. game. The New England Journal of Medicine 343, 1223–1227. 35. Mayoral Cortés JM et al. (2000) Outbreak of gastroenteritis at an 26. Ushijima H et al. (2014) Norovirus and foodborne disease: a review. Food old people’s home in Albacete. Revista Española de Salud Pública 74, Safety 2, 37–54. 561–572. 27. Huang J et al. (2013) Serial foodborne norovirus outbreaks associated 36. Colombo F et al. (2011) Long-term Care: Growing Sector, Multifaceted with multiple genotypes. Serial norovirus outbreaks of tourists in Systems. In Help Wanted?: Providing and Paying for Long-Term Care, Xiamen. PLoS ONE 8, e63327. OECD Publishing, pp. 44–45. 28. Blanco A et al. (2017) Norovirus in bottled water associated with gastro- 37. Sukhrie FH et al. (2012) Nosocomial transmission of norovirus is enteritis outbreak, Spain, 2016. Emerging Infectious Diseases 23, 1531–1534. mainly caused by symptomatic cases. Clinical Infectious Diseases 54, 29. Lindsay L et al. (2015) A decade of norovirus disease risk among older 931–937. adults in upper-middle and high income countries: a systematic review. 38. Bartsch SM et al. (2016) Global economic burden of norovirus gastro- BMC Infectious Diseases 15, 425. enteritis. PLoS ONE 11, e0151219. 30. Green KY et al. (2002) A predominant role for Norwalk-like viruses as 39. Navas E et al. (2015) Economic costs of outbreaks of acute viral gastro- agents of epidemic gastroenteritis in Maryland nursing homes for the eld- enteritis due to norovirus in Catalonia (Spain), 2010–2011. BMC Public erly. Journal of Infectious Diseases 185, 133–146. Health 15, 999. https://doi.org/10.1017/S0950268819001146 Published online by Cambridge University Press