Assessment of the incidents of histamine intoxication in some EU countries. European Food Safety Authority (EFSA)

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1 TECHNICAL REPORT APPROVED: 25 September 2017 doi: /sp.efsa.2017.en-1301 Assessment of the incidents of histamine intoxication in some EU countries European Food Safety Authority (EFSA) Abstract According to its mission, the European Food Safety Authority (EFSA) shall provide scientific advice and scientific and technical support for the Community's legislation and policies in all fields that have a direct or indirect impact on food and feed safety, including the investigation of multinational foodborne outbreaks. Upon a request of the Commission, EFSA assessed the incidents of histamine intoxication in some European Union (EU) countries that were linked to consumption of tuna and were notified through the Rapid Alert System for Food and Feed (RASFF). The contribution provided by EFSA included provision of information from the monitoring of food-borne outbreaks as well as an indepth analysis of the food data and technical assistance to the Commission in the tracing-back analyses of implicated food in the affected Member States. Data and information on the food product implicated in the specific incidents, including tracing-back information as well as epidemiological and analytical data, were extracted from the notifications posted by the involved Member States in RASFF. The aim of the assessment was to evaluate all incidents of histamine intoxication to highlight common factors in the food distribution chain that have potentially contributed to the occurrence of human cases, and to verify the possible correlation upstream in the food supply chain through one of the food business operators involved. Due to the nature of histamine and the conditions that favour its production, it is likely that several concurrent factors have occurred in several stages along the food chain. It is recommended that adequate chilling rates, cold chain and hygienic conditions are maintained at each step of the supply chain of this product. Any relevant information on food investigations should be shared by the involved Member States by issuing relevant notifications in RASFF. European Food Safety Authority, 2017 Key words: histamine, tuna, intoxication, scombroid syndrome, food-borne outbreak, food poisoning Requestor: European Commission Question number: EFSA-Q Correspondence: zoonoses@efsa.europa.eu EFSA Supporting publication 2017:EN-1301

2 Acknowledgements: EFSA wishes to thank the EFSA members of staff: Domenico Deserio, Marta Hugas, Ernesto Liebana Criado, and Valentina Rizzi and external experts: RASFF contact points of Belgium, Croatia, Denmark, France, Germany, Greece, Italy, Luxemburg, the Netherlands, Poland, Portugal, Romania, Slovenia, Spain. Suggested citation: EFSA (European Food Safety Authority), Assessment of the incidents of histamine intoxication in some EU countries. EFSA supporting publication 2017:EN pp. doi: /sp.efsa.2017.en-1301 ISSN: European Food Safety Authority, 2017 Reproduction is authorised provided the source is acknowledged. Reproduction of the image listed below is prohibited and permission must be sought directly from the copyright holder: Figure 1: Rapid Alert System for Food and Feed (RASFF) 2 EFSA Supporting publication 2017:EN-1301

3 Summary According to Regulation (EC) No 178/2002, the European Food Safety Authority (EFSA) shall provide scientific advice and scientific and technical support for the Community's legislation and policies in all fields that have a direct or indirect impact on food and feed safety. It shall provide independent information on all matters within these fields and communicate on risks. In cases of multinational food-borne outbreak investigations, EFSA should give scientific assistance by providing information from the monitoring of zoonoses, zoonotic agents and food-borne outbreaks, an in-depth analysis of the food data based on epidemiological and analytical results, including the robustness of the link to the suspected food source, and technical assistance to the Commission in its conduct of tracing-back and forward analyses of implicated batches of animals, food or feed in the affected Member States. Upon a request of the European Commission, EFSA assessed the incidents of histamine intoxication in some European Union (EU) countries that were due to consumption of tuna, either chilled or frozen, and that were notified through RASFF. Given the nature of the hazard, the present request falls mainly within the remit of EFSA. Moreover, because of the wide spatial distribution of clusters of human cases and the fact that some clusters did not seem to be epidemiologically linked to the others, the hypothesis of a common source for all cases of histamine intoxication in humans needed to be carefully assessed. Therefore, the overriding principle in answering the request from the Commission was to perform an assessment of all incidents to highlight common factors/elements in the food production chain that have potentially contributed to the human cases and to verify the possible correlations upstream among the food business operators involved in the food supply chain. Data and information on the food product implicated in the specific incidents, including tracing-back information as well as epidemiological and analytical data, were extracted from the notifications posted by the involved Member States in the Rapid Alert System for Food and Feed (RASFF). RASFF has been searched to identify all RASFF notifications concerning histamine contamination in tuna and cases of histamine intoxication in humans linked to tuna consumption. A total of 30 RASFF notifications were identified and monitored; among these, 21 RASFF notifications were chosen for this assessment based on their connections and grouped into four different events (called cases ). Additional information provided directly to EFSA by the national competent authorities of the involved Member States in the context of these events was also included. To identify common causes and critical points along the food distribution chain that might have been responsible for the occurrence of the human cases, the assessment focused on RASFF notifications involving mutual food business operators. The evaluation took into account all food business operators at all stages in the food chain; particular attention was paid to the links observed upstream in the supply chain: at fishing vessel, transporter vessel, supplier and/or processing levels. Graphical representation has also been used to visualise the food products distribution chain and underline points of connection between cases. Due to the nature of histamine and the conditions that favour its production, it is likely that several concurrent factors have occurred in several stages along the food chain. In particular, being the temperature one of the main factor influencing the production of histamine, it is considered that the temperature abuse during post-harvest chilling, storage and/or processing has played an important role in these events. This could have been further amplified by the cumulative effect in case the temperature abuse occurred at multiple stages along the food chain. This instance may have a stronger effect for products with a long shelf life. Evidence for non-compliant temperature conditions was reported at different stages in the supply chain in the cases discussed in the present report. The presence of poor hygienic conditions is another contributory factor that could have led to the bacterial contamination of fish and later to the production of the enzyme responsible of the histamine production. It is recommended that adequate chilling rates are achieved after catching, and cold chain is maintained at each step of the production and distribution chain of this product, from the harvest to the consumers, to avoid or limit the production of histamine. The implementation of hygienic measures is also recommended to limit bacterial contamination after fish is caught, and thus to reduce the possible presence of bacterial histidine decarboxylase. 3 EFSA Supporting publication 2017:EN-1301

4 Any relevant information on food investigations (e.g. conditions of chilling, storage, processing, intended use and analytical results of the food products) should be shared by the involved Member States by issuing relevant notifications in RASFF. Further investigations are needed in order to evaluate the cumulative effect of concurrent conditions in the production of histamine in fish and fishery products, such as wrong chilling rates, inadequate storage temperatures, poor hygiene conditions, use of additives, long shelf life. 4 EFSA Supporting publication 2017:EN-1301

5 Table of contents Abstract... 1 Summary Introduction Background and Terms of Reference as provided by the European Commission Interpretation of the Terms of Reference Data and Methodologies Data Methodologies Assessment Disease background information Characteristics of histamine intoxication Food-borne outbreaks due to histamine reported in the EU Notifications of histamine intoxication in RASFF Event background information Food and environmental investigations Case 1 (RASFF, , , , , , , , , , , ) Processing companies in case Analyses and inspections at the processing companies in case Distribution to wholesalers and retailers in case Analyses and inspections at wholesalers and retailers in case Suppliers in case Analyses and inspections at suppliers in case Case 2 (RASFF , , , , Processing companies in case Analyses and inspections at the processing companies in case Distribution to wholesalers and retailers in case Analyses and inspections at wholesalers and retailers in case Suppliers in case Analyses and inspections at suppliers in case Case 3 (RASFF , , ) Processing companies in case Analyses and inspections at the processing companies in case Distribution to wholesalers and retailers in case Analyses and inspections at wholesalers and retailers in case Suppliers in case Analyses and inspections at suppliers in case Case 4 (RASFF , ) Processing companies in case Analyses and inspections at the processing companies in case Distribution to wholesalers and retailers in case Analyses and inspections at wholesalers and retailers in case Suppliers in case Analyses and inspections at suppliers in case Discussion Conclusions References Abbreviations Country codes (ISO ) Appendix A Traceability and testing information in case Appendix B Traceability and testing information in case Appendix C Traceability and testing information in case Appendix D Traceability and testing information in case EFSA Supporting publication 2017:EN-1301

6 1. Introduction 1.1. Background and Terms of Reference as provided by the European Commission On 5 July 2013 the European Food Safety Authority (EFSA) received a mandate from the European Commission on the request for scientific assistance in the investigation of multinational food-borne outbreaks. In multinational food-borne outbreak investigations, the European Commission and Member States are responsible for risk management activities such as control activities (inspections, sampling and analyses) aimed at the confirmation of suspected food sources, their tracing-back and forward, the management and use of the Rapid Alert System for Food and Feed (RASFF) and the adoption of possible trade restrictions. Several European risk assessment bodies are involved in the coordination of multinational investigations of outbreaks of food-borne pathogens to support Member States. While both the European Centre for Disease Prevention and Control (ECDC) and the European Food Safety Agency (EFSA) share activities and collaborate in the area of food-borne outbreak investigations, it is important that their respective tasks and responsibilities are clearly defined. EFSA is responsible for risk assessments in all fields that have a direct or indirect impact on food and feed safety and has been mandated by the European Commission to directly collect and publish information on the monitoring of zoonoses, zoonotic agents and food-borne outbreaks in accordance with Directive 2003/99/EC 1. The purpose of this mandate is to specify the contribution expected from EFSA in these investigations of multinational food-borne outbreaks. In accordance with Article 31 of EU Regulation 178/2002 2, EFSA is requested to provide scientific assistance in the area of food-borne outbreak investigation, particularly: 1. Contributing to the ECDC rapid outbreak assessments by providing information from the monitoring of zoonoses, zoonotic agents and food-borne outbreaks. When such information has not yet been published, EFSA should consult the relevant Member States on the use of the data through its Task Force on Zoonoses Data Collection. 2. When more information on a specific outbreak becomes available, and upon specific request of the Commission, to further collaborate with ECDC in the food-borne outbreak assessment by providing an in-depth analysis of the food data based on epidemiological and analytical results and including the robustness of the link to the suspected food source. 3. Upon specific request of the Commission, to provide technical assistance to the Commission in its conduct of tracing-back and forward analyses of implicated batches of animals, food or feed in the affected Member States. 4. Pending the further course/evolution of the outbreak and new information becoming available, to provide an update of the joint rapid outbreak assessment carried out jointly with ECDC. On 17 May 2017, EFSA received a request from the European Commission in the context of the mandate mentioned above. Taking into account the Early Warning and Response System (EWRS) notification 3 issued by Spain, the increasing number of RASFF notifications of the last weeks and the number of human cases reported by some countries in RASFF, the Commission asked EFSA to provide support in the investigation of incidents of histamine intoxication that were due to consumption of tuna in some EU countries and that were notified through RASFF. EFSA was also required to conduct an assessment on these events. ECDC was invited to take part in this exercise and expressed interest in participating as observer. 1 Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC. OJ L 325, , p Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. OJ L 31, , p EWRS ID ES EFSA Supporting publication 2017:EN-1301

7 1.2. Interpretation of the Terms of Reference This request to assess the incidents of histamine intoxication in some EU countries differs from the requests received in the past under the same mandate owing to the nature of the events. While histamine intoxication is indeed a food safety problem, it is not part of the list of communicable disease as provided in Annex I to Decision 2000/96/EC 4. According to Regulation (EC) No 178/2002 establishing EFSA and laying down procedures in matters of food safety, the Authority shall provide scientific advice and scientific and technical support for the Community's legislation and policies in all fields which have a direct or indirect impact on food and feed safety. It shall provide independent information on all matters within these fields and communicate on risks. Regulation (EC) No 851/ establishing ECDC, lays down the mission of ECDC in Article 3, stating that: In order to enhance the capacity of the Community and the Member States to protect human health through the prevention and control of human disease, the mission of the Centre shall be to identify, assess and communicate current and emerging threats to human health from communicable diseases. In the case of other outbreaks of illness of unknown origin which may spread within or to the Community, the Centre shall act on its own initiative until the source of the outbreak is known. In the case of an outbreak which clearly is not caused by a communicable disease, the Centre shall act only in cooperation with the competent authority upon request from that authority. Taking into account the specific missions of the two European Agencies, the present request falls mainly within the remit of EFSA as histamine intoxication is not currently listed within the communicable diseases of Decision 2000/96/EC. Therefore, the European Commission asked EFSA to provide support in the food investigation. ECDC was invited to participate and agreed to take part in the exercise as observer. Owing to the wide spatial distribution of clusters of human cases and the fact that some clusters did not seem to be epidemiologically linked to the others, the hypothesis of a common source for all human cases of histamine intoxication needed to be carefully assessed. The overriding principle in answering the request from the Commission was therefore to perform an assessment of all incidents that were notified in the RASFF system to identify and evaluate common factors/elements in the food distribution chain that have potentially contributed to the human cases and to verify the possible correlation upstream in the food supply chain through one of the food business operators involved. The contribution requested of EFSA included the provision of information from the monitoring of foodborne outbreaks as well as an in-depth analysis of the food data based on epidemiological and analytical results and including the robustness of the link to the suspected food source. Technical assistance was also provided to the Commission in the tracing-back analyses of implicated food in the affected Member States. 2. Data and Methodologies 2.1. Data Data included in this report comprise that provided by Member States in the context of routine investigation and reporting of food-borne outbreaks as well as specific data and information collected on the investigated incidents. Data on food-borne outbreaks caused by histamine in the period were provided to EFSA by the Member States according to Article 8 of Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 and published in the European Union Summary Report on Zoonoses, Zoonotic Agents and Food-borne Outbreaks for the years /96/EC: Commission Decision of 22 December 1999 on the communicable diseases to be progressively covered by the Community network under Decision No 2119/98/EC of the European Parliament and of the Council. OJ L 28, , p Regulation (EC) No 851/2004 of the European Parliament and of the Council of 21 April 2004 establishing a European Centre for disease prevention and control. OJ L 142, , p EFSA Supporting publication 2017:EN-1301

8 Information about the notifications of incidents of histamine intoxication due to consumption of tuna in the period was extracted from RASFF. Specific background information on the human cases in the investigated incidents was extracted from ECDC s Epidemic Intelligence Information System Food- and Waterborne Disease (EPIS-FWD) platform (last updated 18 September 2017) and approved by the National Focal Points for Food- and waterborne diseases and zoonoses in France, Italy and Spain. Data and information on the food implicated in the specific incidents, including tracing-back and forward information as well as epidemiological and analytical data, were extracted from the notifications and related follow-ups posted by the involved Member States in RASFF. Analytical data for histamine include results obtained during sampling performed by competent authorities ( official control ) and food business operators ( own-check ). The evaluation of compliance was based on the Commission Regulation (EC) No 2073/ for food category 1.25 ( fishery products from fish species associated with high amount of histidine ). Additional information provided directly to EFSA by the national competent authorities of the involved Member States in the context of these events was also included Methodologies RASFF was searched to identify all RASFF notifications concerning histamine contamination in tuna and human cases of scombroid syndrome linked to tuna consumption; the key words used were histamine, food-borne outbreak, food poisoning, and tuna. As of 16 August 2017, a total of 30 RASFF notifications were identified and monitored. Among these, 21 RASFF notifications were chosen for this assessment based on their connections, and were grouped into four different events (called cases from now on), as follows: Case 1 (RASFF , , , , , , , , , , ); Case 2 (RASFF , , , , ); Case 3 (RASFF , , ); Case 4 (RASFF , ). The other RASFF notifications were the following: , , , , , , , and Because of the absence of a link at upstream level between these and the four cases mentioned, these nine RASFF notifications were only monitored and not included in the assessment. The different incidents were analysed separately. Starting from the cases of human intoxication, the suspected products were followed backward along the food chain to identify all food business operators that were involved in the production/distribution chain. Then, to identify common causes and weak points along the food distribution chain that may have been responsible of the occurrence of the clusters of human cases, the assessment focused on RASFF notifications involving mutual food business operators. The evaluation took into account all food business operators at all stages in the food chain; particular attention was paid to the links observed at upstream levels (fishing vessel, transporter vessel, supplier and/or processing company). This choice is due to several factors: Owing to the high level of branching of the distribution chain, a weak point upstream in the food supply chain could have an impact on many food business operators downstream, including the occurrence of interrelated human cases. The processing step could represent a critical point in the food chain, as temperatures applied during food processing are often higher than those applied during storage (potentially increasing the risk of histamine production). 6 Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. OJ L 338, , p EFSA Supporting publication 2017:EN-1301

9 If high levels of histamine are detected downstream in the food chain (e.g. at retailer and wholesaler level), this could be due to the cumulative effect of the amount of histamine or histidine decarboxylase (the enzyme responsible for histamine production) produced at different stages further up the food chain. For the contaminated batches of tuna with the expiry date already passed, interest was mainly on the overall food distribution chain to identify possible connections upstream in the food chain, rather than on the distribution of the specific batches on the market. The food business operators (fishing vessels, transporter vessels, suppliers, processing companies, wholesalers and retailers) mentioned in this report are limited to those either linked to the human cases or included in the distribution chain of the suspected batches of product. Therefore, this list does not include all food business operators involved in the very broad tuna distribution chain of the aforementioned food business operators. The food business operators mentioned have been anonymised. Unless otherwise specified, all tuna batches mentioned in this document had passed their expiration dates. All batches mentioned in the report have been anonymised. Graphical representation was used to visualise the distribution chain of food products and underline points of connection between the cases. The clusters of human cases reported in the graphs are the ones for which the trace-back exercise up the food distribution chain was possible based on the information provided. Therefore, the list of these human cases can neither be comprehensive nor can it match the number of human cases reported in the Public Health sector through the EPIS-FWD platform. In addition, to improve their readability, the graphs in this document do not include all the analytical results for histamine communicated by the involved Member States. To produce a graphical representation of the incidents that still includes the most relevant information, only the results of the official controls have been included as well as the non-compliant analyses observed in the context of the own check programmes. 3. Assessment 3.1. Disease background information Characteristics of histamine intoxication Histamine is a compound that naturally occurs in the human body. It is involved in biological processes such as allergic response, and acts as a neurotransmitter or chemical messenger in synaptic transmissions. Nevertheless, histamine may be hazardous to human health if its levels reach a critical threshold. Apart from endogenous production, histamine is introduced to the organism from exogenous sources by ingestion of food containing high concentrations of this compound. Foods likely to contain high levels of histamine include fish, fish products and fermented foodstuffs (fermented meat, dairy products, vegetables, and alcoholic beverages such as beer and wine). In healthy persons, dietary histamine is rapidly detoxified by amine oxidases, but consumers may develop severe symptoms of histamine intoxication if high amounts are ingested with food. Histamine is a thermostable biogenic amine and is mainly produced at temperatures above 0 C in a wide variety of pelagic fish (e.g. tuna, swordfish, mackerel, sardine, herring, and anchovy) by decarboxylation of free histidine under the action of a bacterial enzyme, histidine decarboxylase. The implementation of hygiene measures helps to limit bacterial contamination after fish are caught, and thus reduces the possible presence of bacterial histidine decarboxylase. The cold chain also plays an essential role in reducing the production of histamine. Histamine intoxication is among the most common toxicities related to fish ingestion and results from the consumption of inadequately preserved and improperly refrigerated fish and it resembles an allergic reaction. Previous terms for histamine intoxication were scombroid fish poisoning, pseudoallergic fish poisoning, histamine overdose, or mahi-mahi flush. The term scombroid was used because the first fish species implicated in this poisoning were from the family Scombridae, which includes mackerel, tuna, marlin, 9 EFSA Supporting publication 2017:EN-1301

10 swordfish, albacore, bonito, skipjack and almost 100 other species. Other non-scombroid fish (e.g. mahi mahi, bluefish, sardines and pilchards) also have a high content of naturally occurring histidine that is decarboxylated by bacteria when the fish are improperly processed and stored. Intoxication is characterized by an incubation period ranging from a few minutes to hours, with symptoms that are usually noticeable for a few hours only. Typical manifestations of histamine intoxication include skin flushing on the upper half of the body, rash, gastrointestinal complaints and throbbing headache. Generally, the diagnosis is made on clinical grounds; no laboratory tests are necessary. If confirmation is required, histamine levels in uneaten portions of the suspect fish can be measured. In addition, elevated histamine levels can be measured in patients urine Food-borne outbreaks due to histamine reported in the EU In 2015, a total of 80 outbreaks of histamine intoxication were reported by 7 EU Member States, involving 437 cases of which 43 were hospitalised (EFSA and ECDC, 2016). The proportion of cases hospitalised was low (9.8%). The number of outbreaks reported in 2015 represents an increase compared with 2014, when 75 outbreaks caused by histamine were reported. The evidence implicating the food vehicle was reported to be strong for 23 out of 80 outbreaks, with 193 human cases and 11 hospitalisations (Table 1). No deaths due to histamine were reported in In all these outbreaks, the evidence reported was the detection of causative agent in food vehicle or its component or the detection of causative agent in food chain or its environment in combination with symptoms and onset of illness pathognomonic to causative agent ; descriptive epidemiological evidence was reported in one outbreak. These outbreaks were associated with the consumption of fish and fish products (20 outbreaks), cheese (2 outbreaks), and mixed food (1 outbreak). Tuna was reported as the specific food vehicle in 5 outbreaks (tuna in oil in 1 case and salad with tuna in 2 cases). The setting was reported to be restaurant or cafe or pub or bar or hotel or catering service in 13 cases, school or kindergarten in 4 cases, household in 3 cases, canteen or workplace catering in 2 cases. No information on setting was given for 1 outbreak. During the period , 306 food-borne outbreaks caused by histamine were reported by 12 EU Member States. For 168 of these food-borne outbreaks, the evidence implicating the food vehicle was reported to be strong (Table 1). During this 5-year period, the most frequently reported food vehicles were fish and fishery products (156 outbreaks), mixed food (5 outbreaks, but a dish with tuna in 3 of these), and cheese, buffet meal, crustaceans, shellfish, molluscs and products thereof, dairy products (other than cheeses), vegetables and juices and other products thereof (1 outbreak each). Detailed information on the implicated food vehicle was not provided for 2 of the reported strongevidence outbreaks (reported as other foods ) EFSA Supporting publication 2017:EN-1301

11 Table 1: Reported strong-evidence food-borne outbreaks caused by histamine in the EU, Year Food category Number of outbreaks Number of cases Number of hospitalisations Number of deaths Year 2010 Cheese Fish and fish products Other foods Vegetables and juices and other products thereof Year 2011 Crustaceans, shellfish, molluscs and products thereof Fish and fish products Mixed food Year 2012 Fish and fish products Year 2013 Buffet meals Dairy products (other than cheeses) Fish and fish products Mixed food Year 2014 Fish and fish products Mixed food Other foods Year 2015 Cheese Fish and fish products Mixed food Total 191 1, Note: information summarised in this table is based on Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC (EFSA and ECDC, 2016) Notifications of histamine intoxication in RASFF Information about the notifications concerning histamine contamination in tuna and human cases of scombroid syndrome linked to tuna consumption was extracted from RASFF. The extraction covered the period and data were analysed per quarter. Since 2014 it is evident a rise of notifications with a sharp increase in the second quarter of 2017 (Figure 1). The number of notifications for the third quarter 2017 is not yet final as the period as not yet ended and data collection is still on-going EFSA Supporting publication 2017:EN-1301

12 Q1 Q2 Q3 Q4 Q1 Q2 Q3 Q4 Q1 Q2 Q3 Q4 Q1 Q2 Q Figure 1: RASFF notifications concerning histamine contamination in tuna and human cases of scombroid syndrome linked to tuna consumption (source: Rapid Alert System for Food and Feed - RASFF) 3.2. Event background information Information about human cases was extracted from ECDC s FWD EPIS platform (last update available 18 September 2017). In May 2017, Spain and France reported cases of scombroid poisoning after consuming yellowfin tuna from Spain. Additional countries were also known to have received the product and therefore additional cases may have arisen. The shelf life of the fresh tuna was however short and has expired for the involved batches. According to Spain, on 12 th May 2017, 61 cases of scombroid syndrome (histamine poisoning) were detected in Spain and 11 in Italy; all cases presented with mild episodes. All cases had eaten yellowfin tuna of a specific brand imported from Spain which had been frozen and later thawed and sold as fresh vacuum packed tuna. An investigation started on 3 rd of May in Spain and is undergoing. Six lots produced between 1 st and 6 th May were withdrawn. The company was closed and all product batches produced between 1 st and 6 th May were withdrawn from the market. Parts of these batches were distributed to Croatia, France, Germany, Italy, Portugal and Romania. Three RASFF were launched: Spain (RASFF from 8 May), Italy (RASFF from 8 May), and France, (RASFF from 9 May). In addition, Spain posted an EWRS and an urgent inquiry in EPIS on 12 th May. On 18 th September 2017, France updated the information related to this event in EPIS reporting 11 outbreaks between the 12 th April and 5 th July with 40 associated cases, of which 15 had been hospitalised and rapidly discharged. The Spanish tuna was consumed in restaurants in different regions of the country and at least two Spanish suppliers were identified, and suspected batches were withdrawn from the market EFSA Supporting publication 2017:EN-1301

13 3.3. Food and environmental investigations The aim of the assessment of data from food and environmental investigations is to highlight common factors/elements in the food production chain that have potentially contributed to the human cases, and to verify the possible correlation upstream in the food supply chain through one of the food business operators involved. In these incidents of histamine intoxication, the food implicated was marketed as tuna, either chilled or frozen. The assessment summarises, by different levels of the distribution chain, relevant information on food and environmental investigations related to the following incidents and related RASFF notifications: case 1 (RASFF , , , , , , , , , , ); case 2 (RASFF , , , , ); case 3 (RASFF , , ); case 4 (RASFF , ). The graphical representation of the traceability information for the four cases is illustrated in Figures 2, 3, 4 and 5 (summarised versions) and Appendices A, B, C and D (detailed versions), respectively Case 1 (RASFF, , , , , , , , , , , ) Processing companies in case 1 The main notification on this case (RASFF ) was triggered by the frozen tuna received on 21 April 2017 by processing company A (ES) from two different suppliers: suppliers A (ES) and B (ES) (Figure 2). At processing company A, the frozen tuna was defrosted, cut into pieces (loins, tails, etc.), injected with antioxidants (E331 - sodium citrate, E300 - ascorbic acid) and vacuum-packed. At least 28 human cases were reported in Italy (between 21 April 2017 and 5 May 2017) and Spain, and were linked to tuna distributed by processing company A. Suppliers A and B also provided unprocessed tuna to processing company/wholesaler C (ES), and supplier B provided tuna to processing company B (ES). At least 35 cases of histamine intoxication (in Croatia and France) were linked to tuna distributed by these processing companies Analyses and inspections at the processing companies in case 1 Analyses Analytical tests carried out at processing company A highlighted some anomalies. During official controls at processing company A, histamine was detected at concentrations above 600 mg/kg in tuna samples taken on 10 May 2017 from a batch of product that had been delivered from supplier A on 20 April Other official analyses performed the same day on batches delivered from supplier A and supplier B gave compliant results (< 10 mg/kg of histamine). Non-compliant results for histamine were detected during official controls at processing company B (565 mg/kg on 7 April 2017 and 293 mg/kg on 15 June 2017). Inspections Inspections carried out at processing company A highlighted some anomalies. Grouping the main aspects, the serious non-compliances detected during inspections performed by the competent authorities at processing company A, they generally correspond to the following factors: The enterprise's hazard analysis and critical control points (HACCP) system was reviewed and the production records for processed tuna requested, with specific regard to records of thawing and processing, from the cutting by hand of the thawed tuna, through injection, weighing, packing in ice, labelling and transfer from the cold store. A single record provided did not correspond to the HACCP records that would report the time and temperature checks on the product during thawing and processing EFSA Supporting publication 2017:EN-1301

14 The record provided does not give the time and temperature information necessary to check the process described in its HACCP, and the two records are combined in a single one. Hygiene in the production process: the processor s own-checks system defines production processes that do not correspond to what is actually done. Labelling: the labelling includes an incomplete batch number as described in the batch numbering system, in that it does not include the date of processing in the enterprise. Training of staff handling product: given the errors described in labelling and traceability, the staff handling product have not been trained to apply the processor s HACCP system. Traceability: the enterprise's traceability plan in its own-check system does not ensure that the information provided is full and correct. The traceability and distribution lists for the products processed and packed proved to be incomplete and/or incorrect, so that there is no guaranteed link or internal traceability between the products received from the processing and packing line to the products that are labelled and distributed. Statements given indicate that the HACCP system is not fully implemented, some records are missing and others are badly drawn up. Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs 7, Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs, and Law 17/2011 of 5 July 2011 on Food Safety and Nutrition 8 are being infringed Distribution to wholesalers and retailers in case 1 Processing company A distributed the implicated tuna to retailers and restaurants in at least eight Member States (DE, ES, FR, HR, IT, PT, RO, SI) and in Andorra, mainly through wholesalers F (ES) and G (ES). However, the tracing-back exercise was made unreliable by the failure of processing company A s labelling machine to write the digits of the batch numbers. In light of this, the competent authorities decided to consider all the batches originating from processing company A to be covered by this alert (RASFF , follow-up 24). With follow-up 23 (RASFF ), it was notified that processing company A had started withdrawal of the implicated product from the market. On 5 May 2017, the company also suspended the production line and applied an extraordinary disinfection plan. As for the product provided by supplier A, it is distributed by processing company/wholesaler C (ES) to at least eight Member States (BE, DE, ES, FR, GR, IT, LU, NL) and Monaco. With regard to the product provided by supplier B, it is distributed by processing company B and processing company/wholesaler C to at least seven Member States (DE, ES, FR, HR, IT, PT, RO). Processing company B processes tuna while still frozen, and distributes it to wholesalers Q (ES) and R (ES), processing company/wholesaler D (ES) and other wholesalers and retailers. Processing company/wholesaler C trades the tuna directly or through other wholesalers/processing companies. Wholesaler Q places the tuna on the market defrosted; wholesaler R sold a batch with an expiration date of 10 November 2018; processing company/wholesaler D is connected to 7 human cases in Croatia and 19 in France. Processing company/wholesaler C is also involved in case 2 (Section 3.3.2) Analyses and inspections at wholesalers and retailers in case 1 Analyses 7 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs. OJ L 139, , p Law 17/2011, of 5 July 2011 on Food Safety and Nutrition. Boletín Oficial del Estado nº 160, Miércoles 6 de julio de EFSA Supporting publication 2017:EN-1301

15 For the batches under investigation, non-compliances with the histamine food safety criterion were identified at wholesaler and retailer level, both for food business operators involving processing companies A, B and processing company/wholesaler C. Indeed, between April and June 2017, during official analysis by competent authorities, histamine was detected at particularly high concentrations (up to 5,020 mg/kg) at wholesalers and retailers supplied by processing company A. Also, food business operators supplied by processing company B and processing company/wholesaler C gave non-compliant results in official analyses of histamine (highest results above 2,500 mg/kg). Inspections Inappropriate storage conditions have been notified in only one retailer in France linked to processing company B Suppliers in case 1 With regard to suppliers, tuna is delivered to processing companies A, B and processing company/wholesaler C separately by suppliers A, B and C (ES). These companies are supplied with unprocessed tuna caught in FAO areas 34, 47, 51 and 87 that enters Spain via the ports of Malaga (ES) and Pobra do Caramiñal (ES). Table 2 summarises the origins of the aforementioned tuna. Table 2: Tuna supply chains in case 1 Vessel FAO area (a) Place of transhipment vessel BIP Supplier(s) involved vessel A (Colombia) vessel B (Colombia) vessel C (Panama) vessel D (ES) vessel E (ES) vessel F (ES) vessel G (FR) vessel H (FR) vessel I (FR) vessel J (El Salvador) 87 Colombia vessel A vessel B (Panama) vessel C (PT) 87 Colombia vessel A vessel B (Panama) vessel C (PT) 34 Ivory Coast vessel D (Panama) 34/47 Ivory Coast vessel D (Panama) 34/47 NA vessel E (Panama) 34 Ivory Coast vessel F (Bahamas) Malaga Malaga Pobra do Caramiñal Pobra do Caramiñal Pobra do Caramiñal Pobra do Caramiñal 51 NA vessel G Pobra do Caramiñal 51 Seychelles vessel H (Panama) Pobra do Caramiñal 51 Seychelles vessel I Pobra do Caramiñal 34/47 Ivory Coast vessel J Pobra do Caramiñal Supplier A Supplier A Supplier B Supplier B Supplier B Supplier B Supplier B Supplier C Supplier B Supplier C Supplier B Supplier C Processing company B BIP: Border Inspection Point; NA: information not available (a): Food and Agriculture Organization of the United Nations (FAO) area 34: Atlantic, Eastern Central; FAO area 47: Atlantic, Southeast; FAO area 51: Indian Ocean, Western; FAO area 87: Pacific, Southeast vessel C (owned by owner/operator B (ES)) and fishing vessel D also provide tuna to food business operators involved in case 2 via the supply chain described in Section vessel J and transporter vessel E are also involved in case 4 (Section 3.3.4). vessels B and C are owned by owner/operator C, which also owns transporter vessel P involved in case 3 (Section 3.3.3) EFSA Supporting publication 2017:EN-1301

16 Analyses and inspections at suppliers in case 1 Analyses Own-check analyses carried out on the implicated tuna delivered to supplier B on 17, 20 and 21 March 2017 measured histamine at below 10 mg/kg. Other own-checks at fishing vessel A, fishing vessel B and supplier A detected histamine at below 25 mg/kg. Inspections Official inspections at suppliers A and B yielded satisfactory findings both for hygiene conditions and storage temperatures applied (RASFF , follow-up 68). Minor non-compliances were detected only on 19 December 2016 in a risk-based inspection at the supplier A. This, however, did not cause interruption of the cold chain. It has been reported that transporter vessels D and F applied storage temperatures below 18 C during transportation. Inspections of the establishment of the vessels owner/operator A, owner of fishing vessels A and B, revealed compliance with the plant s procedures in relation to export product temperature conditions and microbiological parameters (RASFF , follow-up 64). According to what is stated in follow-up 65 (RASFF ), storage temperatures of the fishing vessels are 18 C. However, information provided in RASFF (follow up 64) indicates that, for a certain period, storage temperatures in fishing vessels A, B, and C were higher (between 9.9 C and 14 C) than those recommended for storage of such product ( 18 C) (Table 3). Table 3: Vessels storage temperatures reported as higher than 18 C in case 1 Vessel Range of temperature Period of concern vessel A (Colombia) Between 10 C and 12 C 21/12/16 23/12/16 vessel B (Colombia) Between 9.9 C and 14 C 31/1/17 3/2/17 vessel C (Panama) Between 11.5 C and 13.4 C (in brine) 29/3/17 30/3/17 It has been reported that fishing vessels C and D stored tuna in brine. Some temperatures were reported for the tuna distribution from the port of entry in Europe (port of Pobra do Caramiñal) to supplier B (between 16.4 C and 20.9 C) EFSA Supporting publication 2017:EN-1301

17 T between 10 C and 14 C Vessels owner/operator A Colombia FAO area 87 vessel A Colombia vessel A Colombia vessel B Colombia Vessels owner/operator C Switzerland vessel B vessel C Panama PT Port of Malaga T between 9.9 C and 14 C Vessels owner/operator B FAO area 34 Storage in brine vessel C T between 11.5 C and Panama 13.4 C Storage in brine T: < 20 C Ivory Coast vessel D Panama T delivery: < 17.8 C Hygiene conditions satisfactory Connection with case 2 FAO areas vessel D ES Storage in brine Supplier B vessel E ES vessel E Panama FAO area 34 T: < 20 C vessel F ES Ivory Coast vessel F Bahamas Port of Pobra do Caramiñal (ES) T transportation: < 16.4 C Connection with case 4 vessel G FR vessel G FAO area 51 vessel H FR vessel H Panama Supplier C Seychelles Connection with case 4 vessel I FR vessel I FAO areas vessel J El Salvador Ivory Coast vessel J Connection with case 2 Tuna loins and tacos Processing company/ wholesaler C Other food business operators Countries: BE, DE, ES, FR, GR, IT, LU, NL, Monaco 2 cases FR ES- Histamine: 20 mg/kg Sampling: 22/6/17 Non compliances Histamine: < 10 mg/kg Sampling: 10/5/17 Histamine: > 600 mg/kg Sampling: 10/5/17 IT- Histamine: 1,845 mg/kg Sampling: 22/4/17 IT- Histamine: 1,798 mg/kg Sampling: 27/4/17 IT- Histamine: 3,927 mg/kg Sampling: 5/5/17 IT- Histamine: 405 mg/kg Sampling: 5/5/17 Supplier A T transportation to processing company A and storage temperatures compliant Vacuum packed fresh tuna Processing company A Batches from Batches from Supplier A Supplier B Wholesalers Retailers Countries: DE, ES, FR, HR, IT, PT, RO Histamine: < 10 mg/kg Sampling: 10/5/17 Histamine: < 10 mg/kg Sampling: 10/5/17 Wholesalers Countries: ES, FR, IT Other food business operators Countries: ES, FR, HR, IT, PT, SI, Andorra IT- Histamine: 2,112 mg/kg Sampling: 5/5/17 IT- Histamine: mg/kg Sampling: 5/5/17 IT- Histamine: 848 mg/kg Sampling: 5/5/17 IT- Histamine: 804 mg/kg Sampling: 25/4/17 IT- Histamine: 5,020 mg/kg Sampling: 28/4/17 12 cases IT 16 cases ES Histamine: < 50 mg/kg Sampling: 2/2/17 Histamine: < 50 mg/kg Sampling: 12/5/17 Histamine: < 50 mg/kg Sampling: 25/5/17 Histamine: < 50 mg/kg Sampling: 25/5/17 FR- Own check Histamine: 208 mg/kg Sampling: 11/5/17 FR- Own check Histamine: 217 mg/kg Sampling: 11/5/17 FR- Own check Histamine: 240 mg/kg Sampling: 11/5/17 Processing company/ wholesaler C Wholesalers Countries: ES, FR, IT, PT Retailer AG IT Histamine: 1,701 mg/kg Sampling: 20/5/17 Wholesaler P Retailer AH IT Histamine: mg/kg Sampling: 23/6/17 7 cases HR Retailers HR Connection with case 2 Wholesalers/retailers Countries: DE, ES, FR, HR, IT Processing 1 case FR company B Histamine: 565 mg/kg Sampling: 7/4/17 6 cases FR Wholesalers/ retailers Countries: ES, FR, IT Processing company/ wholesaler E HR Histamine: 440 mg/kg Sampling: 12/6/17 19 cases FR Wholesaler Q Histamine: > 2,500 mg/kg Sampling: 3/7/17 Retailer AJ IT Vacuum packed frozen tuna Exp date 10/11/18 Histamine: 293 mg/kg Sampling: 15/6/17 Wholesaler R Wholesaler S Wholesaler T Other wholesalers/retailers Countries: ES, FR, IT, RO FR- Inappropriate storage conditions Processing company/ wholesaler D Food Business Operators Batch Human cases Compliant inspection/temperature information Not satisfactory inspection/temperature information Geographical location The complete graphical representation is available in Appendix A. Compliant test information Not satisfactory test information Connection Connection between cases Food/process description Distribution of the product Figure 2: Summary of graphical representation of traceability and testing information available for case 1 as of 16 August 2017 according to information in RASFF ( , , , , , , , , , , , and follow-ups) or provided to EFSA by the involved Member States EFSA Supporting publication 2017:EN-1301