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A Bit(e) of History of Hepatitis A and Frozen Fruits and Vegetables

Saturday, March 18, 2023 5:22

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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

Source: https://www.marlerblog.com/case-news/a-bite-of-history-of-hepatitis-a-and-frozen-fruit/

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