Salmonella Enteritidis PT 4 Infections among a Group of Finns Visiting Riga: Effective Collaboration between Latvian and Finnish Authorities Resolved an Outbreak

  Published: 15.11.04 Updated: 15.11.2004 15:36:42
Katri Jalava1, Jurijs Perevoscikovs2, Anja Siitonen3, Maija Hatakka4, Irina Lucenko2, Markku Kuusi1, Pekka Nuorti1
1Department of Infectious Disease Epidemiology, National Public Health Institute (KTL), Finland; 2National Environmental Health Centre, Latvia; 3Department of Microbiology, Laboratory of Enteric Pathogens, National Public Health Institute (KTL), Finland; 4National Food Agency (NFA), Finland
The authors present the collaboration among authorities in Latvia and Finland in resolving an outbreak of Salmonella Enteritidis PT 4 infection. It affected 19 persons according to the used case definition among a group of 46 elderly Finnish tourists on a 3-day trip to Riga. The case-control study was undertaken using a questionnaire on especially food items and sampling of faeces. It is concluded that it is important with strong collaboration between authorities of health and food control within countries as well as between countries


Infectious Disease Control in the Barents and Baltic Sea Regions is a project financed by the Nordic Council of Ministers. This project has created a network of epidemiologists in the Nordic countries, Baltic states and Northwest Russia. The outbreak investigation described here required collaboration between two countries, and most likely would not have been possible without this network.


A group of 46, mostly elderly Finnish tourists (mean age 64 years) belonging to the same family attended a three-day trip to Riga between the 8th and 10th of June 2001. On the morning of the 9th of June the first passengers showed signs of illness including nausea, diarrhoea, fever and vomiting. During the next few days more people became ill with the same symptoms and obtained care from the local health services after returning home to Finland. The course of the disease was severe in most affected patients and one person was hospitalised. A common point source outbreak was suspected, and the local food authority from the city of Porvoo contacted the National Public Health Institute (KTL) and National Food Agency (NFA). Because the first passenger became ill already during the second day of the trip, possible common sources were the snack served on the bus, a meal on the ferry between Helsinki and Tallinn or the evening meal in the old town of Riga. Meals in the hotels were excluded because the cases stayed in different hotels.

Materials and Methods


Both local and national Finnish and Latvian authorities participated in the investigation. The Finnish NFA organised the collection of data using a questionnaire together with the local Finnish food control authorities. KTL co-ordinated the outbreak investigation, analysed the questionnaire data and performed the further laboratory analyses of the salmonella strains. The Latvian Environmental Health Centre co-ordinated outbreak investigations in Riga.
Epidemiological investigation and survey
To determine the cause and magnitude of the outbreak, a retrospective cohort study was conducted among all the participants on the trip. Data was collected by a standard questionnaire. Participants were asked about consumption of food items during the trip, possible symptoms and treatment.
A case was defined as a member of the travelling group who had diarrhoea with onset of illness  between the 9th and 16th of June 2001. The collection of data was completed primarily by telephone interview, but some passengers filled in the questionnaire themselves. The results were analysed using the Epi-Info version 6.04b (CDC, 1996).
The Latvian National Environmental Health Centre in collaboration with Riga Environmental Health Centre organised and carried out epidemiological investigation in the restaurants and took samples (on June 14th) for microbiological analysis from food items and personnel working with the evening meal restaurant. The meals consumed during the boat trip from Helsinki to Tallinn were ruled out based on the knowledge that no other complaints were made among the other 700 passengers on the boat. All passengers ate the snack served on the bus.

Laboratory investigations

Faecal samples were asked from all participants of the travelling group. Thirty-nine (87% of the passengers) faecal samples were obtained. A standard panel of enteric bacterial and viral pathogens (salmonella, shigella, campylobacters, yersinias, Staphylococcus aureus, Bacillus cereus, other bacilli, Clostridium perfringens, calicivirus and astrovirus) was obtained and analysis was conducted using standard protocols in Finnish clinical microbiology laboratories. The isolated strains (27) were sent for further typing to the Laboratory for Enteric Bacteria at KTL.

Results and discussion

Forty-five of the 46 participants (98%) completed the questionnaire. Nineteen (42%) met the case definition. The incubation period and symptoms were typical of salmonella infection. The majority of the group ate the same food during the whole trip, making a comparison between the exposed and unexposed difficult. Members of the group had noticed themselves that none of the six lactose intolerants became ill.
Initial analysis of the data did not show a significant association between any food item and illness.
Based on the raw data from the questionnaires, 18 passengers ate fruit salad as dessert during the evening dinner on June 9th. However, the group leader had reported that the fruit salad was only served to the six lactose intolerants. To get more precise data a second round of telephone interviews was organised by KTL for the whole group. It was noticed that some of the passengers had inadvertently confused the fruit salad on June 9th with the evening dessert on June 10th when it was served for the whole group. In addition, the original information that the main dessert served for the non-lactose intolerants was curd ice cream was also incorrect, the true dessert was a cake containing raw egg cream. As a result of second interview, only 10 people ate the fruit salad as some passengers shared their desserts. This highlights the importance of the quality of the data collected through questionnaires and information obtained from the organisers of the trip.
In the analysis following the additional data collection the cake containing raw egg cream was the only food item that was significantly associated with the illness (p-value 0.03). Nineteen of the 38 (50%) persons eating the cake containing raw egg cream met the case definition as compared to none of the six non-exposed.
Sixty-nine percent (39/45) of the cultured faecal samples were positive for Salmonella enterica. The samples were negative for other enteric pathogens examined. All patient strains were of serovar Salmonella Enteritidis and belonged to the phage type PT 4.  Additionally, all strains were resistant to nalidixic acid, often implicating decreased susceptibility to fluoroquinolones. The minimum inhibitory concentrations (MICs) of all these strains to ciprofloxacin was 0.19 mg/L. This MIC value is slightly lower than the presently accepted resistance breakpoint (≥0.25 mg/L). However, MICs to ciprofloxacin of fully susceptible strains are ≤0.064 mg/L. This serovar of salmonella is very uncommon in indigenously acquired salmonella infections in Finland. In addition, no endemic reservoir has been recognised among domestic food animals in Finland. These findings thus implicate a foreign source. Salmonella Enteritidis of the same PT 4 with MIC 0.19 mg/L was also isolated from another cake of the same kind containing raw egg cream that the group had as a dessert during the dinner. The sample of cake containing raw egg cream was taken in the restaurant on the day of epidemiological investigation (June 14th), 6 days after the tourists were exposed. The mentioned cakes were produced in a bakery located within walking distance from the restaurant. Epidemiological investigation was also performed and samples taken in the bakery. All other samples from the restaurant, bakery, from the ingredients of the cake containing raw egg cream and personnel tested were negative. The Finnish patients were informed about the potential threat of secondary cases through incomplete hand-hygiene. No secondary cases were reported.
This investigation highlights how the rapid action of the local Latvian and Finnish authorities enabled us to trace this outbreak. It is especially remarkable as often, even within a country, food samples may be very difficult to obtain from the food consumed. This was only accomplished through personal relationships between National Environmental Health Centre in Riga and National Public Health Institute in Helsinki. This study illustrates on a general level the importance of networks between health and food control authorities among countries. The positive attitude of the passengers also contributed to the investigation. Very effective dissemination of information and high response rate to the questionnaires within the group was possible despite the fact that they lived scattered in southern Finland.