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On 20 April 2017, an outbreak of histamine food poisoning occurred in a French military unit located near Paris. A total of 40 cases were identified (attack rate: 16.6%). We conducted a case–control study on 31 cases and 63 controls. Multivariate analysis pointed to cooked yellowfin tuna fillet as the very likely source of food poisoning (odds ratio = 156.8; 95% confidence interval: 18.4–1,338.4). The fresh yellowfin tuna was from Reunion Island and was supplied vacuum-sealed and packed with ice at the principal food market of Paris. No cold chain issues could be established in the upstream and downstream supply chains. Histamine concentration was found to be 1,720 mg/kg in leftover raw tuna, and 3,720 mg/kg in control cooked tuna, well above the threshold limit values defined by European regulations (200 mg/kg). The presence of and microorganisms of the Enterobacterales order that have been reported to produce histamine, was confirmed in the leftover raw tuna. This type of food poisoning is rarely recognised and confirmed. We describe the outbreak to highlight the specific key points of this type of investigation.


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  1. Schirone M, Visciano P, Tofalo R, Suzzi G. Histamine Food Poisoning. Handb Exp Pharmacol. 2017;241:217-35.  https://doi.org/10.1007/164_2016_54  PMID: 27752845 
  2. Feng C, Teuber S, Gershwin ME. Histamine (Scombroid) Fish Poisoning: a Comprehensive Review. Clin Rev Allergy Immunol. 2016;50(1):64-9.  https://doi.org/10.1007/s12016-015-8467-x  PMID: 25876709 
  3. Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO). WHO | Public health risks of histamine and other biogenic amines from fish and fishery products. Geneva: WHO; 2013. Report No.: ISBN: 9789240691919. Available from: http://www.who.int/foodsafety/publications/histamine_risk/en/
  4. Visciano P, Schirone M, Tofalo R, Suzzi G. Biogenic amines in raw and processed seafood. Front Microbiol. 2012;3:188.  https://doi.org/10.3389/fmicb.2012.00188  PMID: 22675321 
  5. Hungerford JM, Arefyev AA. Flow-injection assay of enzyme inhibition in fish using immobilized diamine oxidase. Anal Chim Acta. 1992;261(1-2):351-9. https://doi.org/10.1016/0003-2670(92)80213-Q 
  6. Hungerford JM. Scombroid poisoning: a review. Toxicon. 2010;56(2):231-43.  https://doi.org/10.1016/j.toxicon.2010.02.006  PMID: 20152850 
  7. Gardini F, Özogul Y, Suzzi G, Tabanelli G, Özogul F. Technological Factors Affecting Biogenic Amine Content in Foods: A Review. Front Microbiol. 2016;7:1218.  https://doi.org/10.3389/fmicb.2016.01218  PMID: 27570519 
  8. European Food Safety Authority/European Centre for Disease Prevention and Control (EFSA/ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018;16(12):5500.
  9. European Food Safety Authority (EFSA). Assessment of the incidents of histamine intoxication in some EU countries. EFSA Support Publ.2017;14(9):EN-1301.
  10. Santé publique France. Epidemiological data. Foodborne outbreak. Paris: Santé publique France. [Accessed: 13 Mar 2018]. Available from: http://invs.santepubliquefrance.fr/fr./Dossiers-thematiques/Maladies-infectieuses/Maladies-a-declaration-obligatoire/Toxi-infections-alimentaires-collectives/Donnees-epidemiologiques
  11. Duflos G, Dervin C, Malle P, Bouquelet S. Relevance of matrix effect in determination of biogenic amines in plaice (Pleuronectes platessa) and withing (Merlangus merlangus). J AOAC Int. 1999;82:1097-101.
  12. Mietz J, Karmas E. Chemical Quality Index of Canned Tuna as Determined by High-Pressure Liquid-Chromatography. J Food Sci. 1977;42(1):155-8.  https://doi.org/10.1111/j.1365-2621.1977.tb01240.x 
  13. Seng P, Drancourt M, Gouriet F, La Scola B, Fournier P-E, Rolain JM, et al. Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis. 2009;49(4):543-51.  https://doi.org/10.1086/600885  PMID: 19583519 
  14. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D. 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol. 2000;38(10):3623-30. PMID: 11015374 
  15. European Commission. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union. Luxembourg: Publications Office of the European Union. 22.12.2005:L 338. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:02005R2073-20180101
  16. JORF. French Ministry of Food, Agriculture and Fisheries, Ministry of Economy, Industry and Employment, Ministry of Defense, Ministry of Health and Sports. Arrêté du 21 décembre 2009 relatif aux règles sanitaires applicables aux activités de commerce de détail, d’entreposage et de transport de produits d’origine animale et denrées alimentaires en contenant [Decree of 21 December 2009 on the health rules applicable to the retail trade, storage and transport of products of animal origin and foodstuffs containing them]. Paris; 2009. French. Available from: https://www.legifrance.gouv.fr/affichTexte.do?cidTexte=JORFTEXT000021573483&categorieLien=id
  17. Grinda J-M, Bellenfant F, Brivet FG, Carel Y, Deloche A. Biventricular assist device for scombroid poisoning with refractory myocardial dysfunction: a bridge to recovery. Crit Care Med. 2004;32(9):1957-9.  https://doi.org/10.1097/01.CCM.0000139921.38352.3D  PMID: 15343026 
  18. D’Aloia A, Vizzardi E, Della Pina P, Bugatti S, Del Magro F, Raddino R, et al. A scombroid poisoning causing a life-threatening acute pulmonary edema and coronary syndrome in a young healthy patient. Cardiovasc Toxicol. 2011;11(3):280-3.  https://doi.org/10.1007/s12012-011-9115-1  PMID: 21567294 
  19. Coppola G, Caccamo G, Bacarella D, Corrado E, Caruso M, Cannavò MG, et al. Vasospastic angina and scombroid syndrome: a case report. Acta Clin Belg. 2012;67(3):222-5. PMID: 22897074 
  20. Borade PS, Ballary CC, Lee DKC. A fishy cause of sudden near fatal hypotension. Resuscitation. 2007;72(1):158-60.  https://doi.org/10.1016/j.resuscitation.2006.05.021  PMID: 17084013 
  21. Yu Y, Wang P, Bian L, Hong S. Rare Death Via Histamine Poisoning Following Crab Consumption: A Case Report. J Forensic Sci. 2017; 2018;63(3):980-2. PMID: 28833161 
  22. Colombo FM, Cattaneo P, Confalonieri E, Bernardi C. Histamine food poisonings: A systematic review and meta-analysis. Crit Rev Food Sci Nutr. 2018;58(7):1131-51.. PMID:27791395
  23. Lerke PA, Werner SB, Taylor SL, Guthertz LS. Scombroid poisoning. Report of an outbreak. West J Med. 1978;129(5):381-6. PMID: 569397 
  24. Ohnuma S, Higa M, Hamanaka S, Matsushima K, Yamamuro W. An outbreak of allergy-like food poisoning. Intern Med. 2001;40(8):833-5.  https://doi.org/10.2169/internalmedicine.40.833  PMID: 11518138 
  25. Demoncheaux J-P, Michel R, Mazenot C, Duflos G, Iacini C, de Laval F, et al. A large outbreak of scombroid fish poisoning associated with eating yellowfin tuna (Thunnus albacares) at a military mass catering in Dakar, Senegal. Epidemiol Infect. 2012;140(6):1008-12.  https://doi.org/10.1017/S0950268811001701  PMID: 21875451 
  26. Bédry R, Gabinski C, Paty M-C. Diagnosis of scombroid poisoning by measurement of plasma histamine. N Engl J Med. 2000;342(7):520-1.  https://doi.org/10.1056/NEJM200002173420718  PMID: 10691498 
  27. Laroche D. Histamine. Allergie aux médicaments: Tests immuno-biologiques [Histamine. Drug allergy: Immuno biological tests]. French. John Libbey Eurotext; 2006.
  28. Ricci G, Zannoni M, Cigolini D, Caroselli C, Codogni R, Caruso B, et al. Tryptase serum level as a possible indicator of scombroid syndrome. Clin Toxicol (Phila). 2010;48(3):203-6.  https://doi.org/10.3109/15563651003649177  PMID: 20230333 
  29. Ridolo E, Martignago I, Senna G, Ricci G. Scombroid syndrome: it seems to be fish allergy but... it isn’t. Curr Opin Allergy Clin Immunol. 2016;16(5):516-21.  https://doi.org/10.1097/ACI.0000000000000297  PMID: 27466827 
  30. EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on risk based control of biogenic amine formation in fermented foods. EFSA J. 2011;9(10):2393.
  31. Biji KB, Ravishankar CN, Venkateswarlu R, Mohan CO, Gopal TKS. Biogenic amines in seafood: a review. J Food Sci Technol. 2016;53(5):2210-8.  https://doi.org/10.1007/s13197-016-2224-x  PMID: 27407186 
  32. Chen H-C, Kung H-F, Chen W-C, Lin W-F, Hwang D-F, Lee Y-C, et al. Determination of histamine and histamine-forming bacteria in tuna dumpling implicated in a food-borne poisoning. Food Chem. 2008;106(2):612-8.  https://doi.org/10.1016/j.foodchem.2007.06.020 
  33. Kung H-F, Lee Y-C, Huang Y-R, Lin W-F, Lin C-M, Chen W-C, et al. Biogenic amines content, histamine-forming bacteria, and adulteration of pork and poultry in tuna dumpling products. Food Control. 2010;21(7):977-82.  https://doi.org/10.1016/j.foodcont.2009.12.011 
  34. Lin C-S, Tsai H-C, Lin C-M, Huang C-Y, Kung H-F, Tsai Y-H. Histamine content and histamine-forming bacteria in mahi-mahi (Coryphaena hippurus) fillets and dried products. Food Control. 2014;42:165-71.  https://doi.org/10.1016/j.foodcont.2014.02.004 
  35. Özogul F, Özogul Y. Formation of biogenic amines by Gram-negative rods isolated from fresh, spoiled, VP-packed and MAP-packed herring (Clupea harengus). Eur Food Res Technol. 2005;221(5):575-81.  https://doi.org/10.1007/s00217-005-0064-4 
  36. Naila A, Flint S, Fletcher G, Bremer P, Meerdink G. Control of biogenic amines in food--existing and emerging approaches. J Food Sci. 2010;75(7):R139-50.  https://doi.org/10.1111/j.1750-3841.2010.01774.x  PMID: 21535566 
  37. Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, Kersters K, et al. Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and Description of Pantoea dispersa sp. nov. Int J Syst Evol Microbiol. 1989;39:337-45.
  38. Masiello SN, Martin NH, Trmčić A, Wiedmann M, Boor KJ. Identification and characterization of psychrotolerant coliform bacteria isolated from pasteurized fluid milk. J Dairy Sci. 2016;99(1):130-40.  https://doi.org/10.3168/jds.2015-9728  PMID: 26547640 
  39. Centre for the Promotion of Imports from developing countries (CBI). Exporting fresh tuna to Europe. The Hague; CBI. [Accessed: 13 Mar 2018]. Available from: https://www.cbi.eu/market-information/fish-seafood/fresh-tuna/

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