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A Prolonged Outbreak of Salmonella Typhimurium Infection Related to an Uncommon Vehicle: Hard Cheese Made from Raw Milk

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A Prolonged Outbreak of Salmonella Typhimurium Infection Related to an Uncommon Vehicle: Hard Cheese Made from Raw Milk Epidemiol. Infect. (2009), 137, 1548–1557. f Cambridge University Press 2009 doi:10.1017/S0950268809002337 Printed in the United Kingdom A prolonged outbreak of Salmonella Typhimurium infection related to an uncommon vehicle: hard cheese made from raw milk Y. T. H. P. VAN DUYNHOVEN 1*, L. D. ISKEN1,K.BORGEN1,2, M. BESSELSE3, K. SOETHOUDT3,O.HAITSMA3,B.MULDER4, D.W. NOTERMANS1, R. D E JONGE1,P.KOCK5, W. VAN PELT 1, O. STENVERS6 AND J. VAN STEENBERGEN1, on behalf of the Outbreak Investigation Team# 1 Centre for Infectious Disease Control Netherlands, National Institute of Public Health and the Environment (RIVM/CIb), Bilthoven, The Netherlands 2 European Programme for Intervention Epidemiology Training, European Centre for Disease Prevention and Control, Sweden 3 Public Health Service Region Twente, Enschede, The Netherlands 4 Laboratory for Medical Microbiology Twente Achterhoek, Enschede, The Netherlands 5 Animal Health Service, Deventer, The Netherlands 6 Food and Consumer Product Safety Authority, The Hague, The Netherlands (Accepted 4 February 2008; first published online 19 March 2009) SUMMARY In 2006, in The Netherlands, an outbreak of Salmonella Typhimurium phage type 561 (STM DT7, corresponding to the rare DT7 in the international typing scheme) was detected, accumulating to over 200 cases. By telephone interviews, data were collected from all laboratory-confirmed cases. In addition, in August 2006, a case-control study was performed in a subset of cases. Environmental and microbiological investigation was performed on a suspected dairy farm. In the case-control study (51 cases, 105 matched controls), hard cheese purchased from a farm, specifically farm X, and from a market stall were found to be associated with infection. The dairy production room of farm X tested STM DT7-positive in August. However, it was only in November, after earlier unsuccessful attempts, that a low-level contamination was confirmed in the hard farmhouse cheese, triggering control measures. A timely and adequate response was hampered during this outbreak for several reasons. Measures for improvement in handling future similar incidents are discussed. Key words: Hard cheese, outbreak, Salmonella. INTRODUCTION practitioner [2], and diagnostic practices lead to about 2200–3000 laboratory-confirmed cases annually [3, 4]. In The Netherlands, over 40 000 cases of gastroenter- The Dutch laboratory-based Salmonella surveillance itis from non-typhoidal Salmonella occur annually [1]. covers about 64% of the population, and is based on At least one in six of these cases consults a general 16 regional public health laboratories sending all pri- mary Salmonella isolates of patients to the Center for * Author for correspondence: Y. T. H. P. van Duynhoven, Ph.D., Head, Laboratory for Zoonoses and Environmental Microbiology, Infectious Disease Control of the National Institute RIVM, Centre for Infectious Disease Control Netherlands, of Public Health and the Environment (RIVM/CIb) PO Box 1, 3720 BA, Bilthoven, The Netherlands. for sero- and phage-typing [3]. A sample of Salmonella (Email: [email protected]) # The remaining team members are listed in the Appendix. isolates from food and animals are typed and included Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 25 Sep 2021 at 00:51:29, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268809002337 Salmonella outbreak from hard raw-milk cheese 1549 in the national surveillance database as well. In this questionnaire (Q3, from 3 April onwards). Finally, database, a computer algorithm automatically detects on 18 July the questionnaire was again amended to an increase in subtypes of human Salmonella isolates, include additional more detailed questions about rec- as well as uncommon clusterings by region or age reational activities and consumption of food outside group. the home (Q4). In all questionnaires, demographic From January 2006 onwards, an increase of a rare characteristics, clinical manifestation and hospital- phage type of Salmonella Typhimurium, ranging from ization were included. Questions about exposure none to 16 annual cases between 2000 and 2005, was covered the 7-day interval before onset of illness. observed. This Dutch phage type 561 (STM561), Cases were interviewed by telephone. translates to STM DT7 in the English typing scheme. From 2 July 2006 onwards, all cases with S. A request for information to the international sur- Typhimurium cultured at the regional laboratory veillance network Enternet showed this type to be rare were reported daily to the MHS, before determination in Europe as well, only regularly occurring in east of the phage type, to reduce the time interval between Germany. The outbreak accumulated to over 200 onset of illness and interview of the patients. In laboratory-confirmed cases by the end of the year. July, the MHS dispatched an information leaflet to Although cases were observed nationwide, more than all general practitioners, paediatricians, and child 55% of the cases originated from a small region in the health centres in the region, to inform them about eastern part of The Netherlands. This large outbreak the outbreak and encourage them to send stool speci- prompted an investigation, first regionally and sub- mens for laboratory testing of all suspected cases in sequently nationally, in order to identify and control order to increase the sensitivity of the surveillance the source. system. Case-control study in subset of cases METHODS Based on the questionnaires and a STM DT7-positive Alert and data collection of cases manure sample, farm X, a large dairy farm with open On 7 February 2006, RIVM/CIb registered an in- access to the public, located in the epicentre of the crease of S. Typhimurium phage type DT7 with cases outbreak, was hypothesized as the source of the out- almost exclusively originating from one geographical break. At this farm, non-pasteurized hard cheese (des- region designated ‘Twente’ (y616 000 inhabitants). ignated as ‘farmhouse cheese’) was produced (about The alert was sent to the responsible municipal public 500 cheeses produced daily) and sold. On 11 August, health service (MHS) to investigate the cause of this it was decided to perform a matched case-control increase. The alert was accompanied by a routine com- study in order to confirm and specify the vehicle and prehensive trawling questionnaire and background to prevent further transmission. A case was defined as information about products generally involved in an individual with gastroenteritis (diarrhoea and at STM cases. Moreover, the MHS was informed about least two additional predefined symptoms) and a lab- the recent detection of STM DT7 in a pork product oratory-confirmed STM DT7 infection with date of taken during routine monitoring from a supermarket arrival of the isolate at RIVM/CIb after 1 June 2006. in the same region in early February, which was en- A control was a person registered in the national tered into the national Salmonella database. At the internet phonebook matched for age group (0–5, 6–10, MHS a brief questionnaire, targeted at consumption 11–20, 21–64, o65 years) and 4-digit postcode, and of pork, was transcribed from the trawling question- who did not travel abroad in the week preceding the naire (Q1, used from 8 February onwards). It was date of onset of the matched case. For each case, two administered to laboratory-confirmed cases. When on controls were selected. All cases and controls were 13 March, a sample of cattle manure was found interviewed by telephone between 14 August and 1 positive for STM DT7 in the Salmonella database, the September, using a standardized questionnaire di- questionnaire was extended to include beef (products) rected at risk exposures to farms, animals and food as well (Q2, from 20 March onwards). The cattle products. Exposures referred to the 7 days prior to manure sample was found to originate from dairy onset of illness for cases, and the week (Monday– farm X, in the Twente region. Consequently, dairy Sunday) preceding the date of onset of the matched products and contact with animals were added to the case for the controls. Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 25 Sep 2021 at 00:51:29, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268809002337 1550 Y. T. H. P. van Duynhoven and others Case-case comparison on subset of cases the rind was examined as follows. All cheese samples were cut into five pieces of 25 g which were each sus- The immediate reporting of S. Typhimurium cases pended in 225 ml pre-warmed BPW (45 xC), using a before determination of the phage type allowed a stomacher for 30 s at normal speed. Stomacher bags comparison of data (Q4 questionnaire) for cases with were incubated 24 h at 37 xC. For selective enrich- STM DT7 (n=98) vs. cases infected with other phage ment, we used MSRV plates (see above), Rappaport– types (n=39). Vassiliadis soya peptone broth (RVS, Oxoid) and Muller–Kaufmann Tetrathionate broth, sup- Investigation of dairy cattle, cheeserie and dairy plemented with novobiocine (MKTTn; Oxoid). RVS products farm X and MKTTn were incubated for 48 h at 37 xC. After On 14 April, farm X was visited for hygiene inspection 24 h and 48 h, the possible presence of Salmonella was and three samples of hard farmhouse cheese, butter checked by streaking a small amount of sample from and milk were tested for the presence of Salmonella. MSRV, RVS and MKTTn on xylose, lysine, Na- For each product a 25-g sample was investigated ac- desoxycholate agar (XLD, Oxoid) and BGA plates, cording to ISO and NEN methods [5–7]. On 19 July, which were incubated for 24 h at 37 xC. Suspected co- farm X was visited again and 12 samples of hard cheese lonies were further identified using LDC, TSI and UA.
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