Another Hepatitis A outbreak appears to be brewing in the US linked to imported frozen strawberries. Here is a bit(e) of a compilation of past outbreaks.
Hepatitis A outbreaks associated with fresh, frozen, and minimally processed produce worldwide from 1983 to 2022—adapted and expanded from Sivapalasingam et al., 2004 and Fiore, 2004. Italics indicate instances where the food was locally sourced with respect to the cases. The implicated foods were raw unless listed otherwise.
Hepatitis A outbreaks associated with fresh, frozen, and minimally processed produce, worldwide, from 1983 to 2022
Year | # Cases | Implicated food | Location of cases | Source of implicated food | Suspected cause of contamination | Reference |
1983 | 24 | Raspberries (frozen) | Scotland | Scotland | Infected pickers or packers | Reid et al., 1987[1] |
1987 | 5 | Raspberries (frozen) | Scotland | Tayside, Scotland | Infected pickers | Ramsay and Upton, 1989[2] |
1988 | 202 | Iceberg lettuce | Kentucky | Unknown, suspected to be from Mexico | Believed to have occurred prior to distribution, since multiple restaurants involved | Rosenblum et al., 1990[3] |
1990 | 35 | Strawberries (frozen) | Montana, Georgia | California | Suspect an infected picker at farm | Sivapalasingam et al., 2004;[4]Niu et al., 1992[5] |
1996 | 30 | Salad ingredients | Finland | Imported salad ingredients | Unknown | Pebody et al., 1998[6] |
1997 | 256 | Strawberries (frozen) | Michigan, Maine, Wisconsin, Arizona, Louisiana, Tennessee | Grown in Mexico,processed and frozen at a single California facility a year before consumption | Inconclusive due to time between harvest and consumption, suspect barehanded contact with berries at harvesting, coupled with few latrines and handwashing facilities on site | Hutin et al., 1999[7] |
1998 | 43 | Green onions | Ohio | One of two Mexican farms or a farm in California | Believed to be contaminated before arrival at restaurant | Dentinger et al., 2001[8] |
2000 | 31 | Green onions or tomatoes | Kentucky, Florida | Green onions: California or MexicoTomatoes: Unknown | Unknown | Wheeler et al., 2005[9]; Datta et al., 2001[10]; Fiore, 2004[11] |
2002 | 81 | Blueberries | New Zealand | New Zealand, one orchard | Inadequate bathroom facilities in fields, workers had barehanded contact with product, polluted groundwater from nearby latrines a possibility | Calder et al., 2003[12] |
2003 | 601 | Green onions | Pennsylvania, Tennessee, Georgia, North Carolina | Mexico, two farms | Contaminated during or before packing at farm | CDC, 2003[13]; Wheeler et al., 2005[14] |
2009 | 562 | Tomatoes (semidried) | Australia | Unknown; imported and domestic product involved | Product suspected to be imported due to concurrent outbreaks elsewhere at the time, source of contamination unknown | Donnan et al., 2012[15] |
2009 | 13 | Tomatoes (semidried) | Netherlands | Unknown; imported product suspected | Identical strain to the 2009 Australian outbreak | Petrignani et al., 2010[16] |
2010 | 59 | Tomatoes (semidried) | France | Likely Turkey, single batch of product | Unable to determine when and where contamination occurred. Virus was slightly different from one in the 2009 Australian and Dutch outbreaks. | Gallot et al., 2011[17] |
2012 | 9 | Pomegranate seeds (frozen) | Canada | Egypt | Suspect product contamination before export. Some history of travel to endemic areas among workers at Canadian processing facility, but less likely as only one product was associated with illness. | CDC 2013[18]; Swinkels et al., 2014[19] |
2013 | 103 | Strawberries (frozen)Other frozen berries may have been involved | Denmark, Finland, Norway, Sweden | Suspected Egypt and Morocco based on virus strain and import history | Unknown, some cases matched the strain of the larger 2013 European outbreak (see below) | Nordic Outbreak Investigation Team, 2013[20] |
2013 | 1589 | Berries (frozen) | Italy (90% of cases), Austria, Bulgaria, Denmark, England, Finland, France, Germany, Ireland, the Netherlands, Norway, Poland, Sweden | Multiple food items containing frozen mixed berries (cakes, smoothies); Bulgarian blackberries and Polish redcurrants were the most common ingredients in the implicated lots | Unknown, no single source found. Some cases also related to travel to Italy. | Severi et al., 2015[21]; EFSA 2014[22]; Chiapponi et al., 2014[23]; Rizzo et al., 2013[24]; Guzman-Herrador et al., 2014[25]; Fitzgerald et al., 2014[26] |
2013 | 165 | Pomegranate arils (frozen) | Arizona, California, Colorado, Hawaii, New Hampshire, New Jersey, New Mexico, Nevada, Utah, Wisconsin | Turkey | Unknown | Collier et al., 2014[27]; CDC 2013[28] |
2016 | 143 | Strawberries (frozen) | Arkansas, California, Maryland, New York, North Carolina, Oregon, Virginia, West Virginia, Wisconsin | Egypt | Unknown | CDC 2016[29] |
2022 | 19 | Strawberries(frozen) | CaliforniaArizonaNorth DakotaMinnesota | Mexico | Unknown | CDC 2022[30] |
[1] Reid, T., Robinson, H. (1987). Frozen raspberries and hepatitis A. Epidemiol Infect, 98: 109–112.
[2] Ramsay, C. N. and Upton, P. A. (1989). Hepatitis A and frozen raspberries. Lancet, 1: 43–44.
[3] Rosenblum, L. S., Mirkin, I. R., Allen, D. T., Safford, S., Hadler, S. C. (1990). A multifocal outbreak of hepatitis A traced to commercially distributed lettuce. American Journal of Public Health, 80(9): 1075-1079.
[4] Sivapalasingam, S., Friedman, C. R., Cohen, L., Taube, R. V. (2004). Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot, 67: 2342-2353.
[5] Niu, M. T., Polish, L. B., Robertson, B. H. (1992). Multistate outbreak of hepatitis A associated with frozen strawberries. J Infect Dis 166: 518-524.
[6] Pebody, R. G., Leino, T., Ruutu, P., Kinnunen, L., Davidkin, I., Nohynek, H., & Leinikki, P. (1998). Foodborne outbreaks of hepatitis A in a low endemic country: an emerging problem? Epidemiology and infection, 120(1): 55-59.
[7] Hutin, Y. J., Pool, V., Cramer, E. H., Nainan, O. V., Weth, J., Williams, I. T. et al. (1999). A multistate, foodborne outbreak of hepatitis A. New England Journal of Medicine, 340(8): 595-602.
[8] Dentinger, C. M., Bower, W. A., Nainan, O. V., Cotter, S. M., Myers, G., Dubusky, L. M., Fowler, S., Salehi, E. D. P., and Bell, B. P. (2001). An outbreak of hepatitis A associated with green onions. J Infect Dis, 183: 1273-1276.
[9] Wheeler, C., Vogt, T. M., Armstrong, G. L., Vaughan, G., Weltman, A., Nainan, O. V. et al. (2005). An outbreak of hepatitis A associated with green onions. New England Journal of Medicine, 353(9): 890-897.
[10] Datta, S. D., Traeger, M. S., & Nainan, O. V. (2001). Identification of a multi-state outbreak of hepatitis A associated with green onions using a novel molecular epidemiologic technique [abstract 896]. In Program and abstracts of the 39th Annual Meeting of the Infectious Diseases Society of America. Alexandra, VA: Infectious Diseases Society of America (Vol. 192).
[11] Fiore, A. E. (2004). Hepatitis A transmitted by food. Clinical Infectious Diseases, 38(5): 705-715.
[12] Calder, L., Simmons, G., Thornley, G. (2003). An outbreak of hepatitis A associated with consumption of raw blueberries. Epidemiol Infect,131: 745-751
[13] Centers for Disease Control and Prevention (CDC). (2003). Hepatitis A outbreak associated with green onions at a restaurant–Monaca, Pennsylvania, 2003. MMWR, 52(47): 1155-1157. Available at https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5247a5.htm
[14] Wheeler, C., Vogt, T. M., Armstrong, G. L., Vaughan, G., Weltman, A., Nainan, O. V. et al. (2005). An outbreak of hepatitis A associated with green onions. New England Journal of Medicine, 353(9): 890-897.
[15] Donnan, E. J., Fielding, J. E., Gregory, J. E., et al. (2012). A multistate outbreak of hepatitis A associated with semidried tomatoes in Australia, 2009. Clin Infect Dis, 54: 775–781.
[16] Petrignani, M., Harms, M., Verhoef, L. (2010). Update: a food-borne outbreak of hepatitis A in The Netherlands related to semi-dried tomatoes in oil, January-February 2010. Euro Surveillance, 15(20): 19572.
[17] Gallot, C., Grout, L., Roque-Afonso, A., Couturier, E., Carrillo-Santisteve, P., Pouey, J. et al. (2011). Hepatitis A Associated with Semidried Tomatoes, France, 2010. Emerging Infectious Diseases, 17(3): 566-567.
[18] Centers for Disease Control and Prevention (CDC). (2013). Multistate outbreak of hepatitis A virus infections linked to pomegranate seeds from Turkey (Final Update). Available at: https://www.cdc.gov/hepatitis/outbreaks/2013/a1b-03-31/
[19] Swinkels, H. M., Kuo, M., Embree, G., Andonov, A., Henry, B., Buxton, J. A. (2014). Hepatitis A outbreak in British Columbia, Canada: the roles of established surveillance, consumer loyalty cards and collaboration, February to May 2012. Euro Surveillance, 19: 20792.
[20] Nordic Outbreak Investigation Team C (2013). Joint analysis by the Nordic countries of a hepatitis A outbreak, October 2012 to June 2013: frozen strawberries suspected. Euro Surveillance, 18(27): 20520.
[21] Severi, E., Verhoef, L., Thornton, L., Guzman-Herrador, B. R., Faber, M., Sundqvist, L. et al. (2015). Large and prolonged food-borne multistate hepatitis A outbreak in Europe associated with consumption of frozen berries, 2013 to 2014. Euro Surveillance, 20(29): 1-9.
[22] European Food Safety Authority (EFSA). (2014). Tracing of food items in connection to a multinational hepatitis A virus outbreak in Europe. EFSA Journal, 12(9): 3821-4007. Available at http:// www.efsa.europa.eu/en/efsajournal/pub/3821.htm
[23] Chiapponi, C., Pavoni, E., Bertasi, B., Baioni, L., Scaltriti, E., Chiesa, E., et al. (2014). Isolation and genomic sequence of hepatitis A virus from mixed frozen berries in Italy. Food Environ Virol, 6(3): 202-206.
[24] Rizzo, C., Alfonsi, V., Bruni, R., Busani, L., Ciccaglione, A., De Medici, D., et al. (2013). Ongoing outbreak of hepatitis A in Italy: preliminary report as of 31 May 2013. Euro Surveillance, 18(27): 20518.
[25] Guzman-Herrador, B., Jensvoll, L., Einoder-Moreno, M., Lange, H., Myking, S., Nygard, K., et al. (2014). Ongoing hepatitis A outbreak in Europe 2013 to 2014: imported berry mix cake suspected to be the source of infection in Norway. Euro Surveillance, 19(15): 20775.
[26] Fitzgerald, M., Thornton, L., O’Gorman, J., O Connor, L., Garvey, P., Boland, M., et al. (2014). Outbreak of hepatitis A infection associated with the consumption of frozen berries, Ireland, 2013 – linked to an international outbreak. Euro Surveillance: European communicable disease bulletin, 19(43).
[27] Collier, M. G., Khudyakov, Y. E., Selvage, D., Adams-Cameron, M., Chiepson, E., Cronquist, A., et al. (2014). Outbreak of hepatitis A in the USA associated with frozen pomegranate arils imported from Turkey: an epidemiological case study. Lancet Infectious Diseases, 14(10): 976-981.
[28] Centers for Disease Control and Prevention (CDC). (2013) – Multistate outbreak of hepatitis A virus infections linked to pomegranate seeds from Turkey (Final Update), supra note 85.
[29] Centers for Disease Control and Prevention (CDC). (2016). 2016 – Multistate outbreak of hepatitis A linked to frozen strawberries (Final Update). Available at https://www.cdc.gov/hepatitis/outbreaks/2016/hav-strawberries.htm
[30] Centers for Disease Control and Prevention (CDC). (2016). 2016 – Multistate outbreak of hepatitis A linked to frozen strawberries (Final Update). Available at https://www.cdc.gov/hepatitis/outbreaks/2022/hav-contaminated-food/index.htm