Hepatitis A outbreaks associated with fresh, frozen, and minimally processed produce, worldwide, from 1983 to 2016—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 2016 | ||||||
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] |
Estimates of the annual costs (direct and indirect) of hepatitis A in the United States have ranged from $300 million to $488.8 million in 1997 dollars.[30] In one study conducted in Spokane, Washington, the combined direct and indirect costs for each case of hepatitis A from all sources ranged from $2,892 to $3,837.[31] In a 2007 Ohio study, each case of HAV infection attributable to contaminated food was estimated to cost at least $10,000, including medical and other non-economic costs.[32] Nationwide, adults who become ill miss an average of 27 workdays per illness, and 11 to 22 percent of those infected are hospitalized.[33] All of these costs are entirely preventable given the effectiveness of a vaccination in providing immunity from infection.[34]
THE OUTBREAK
An outbreak of hepatitis A was investigated by the Centers for Disease Control and Prevention (CDC), state public health partners, and the U.S. Food and Drug Administration (FDA).
As of July 18, 2023, a total of 10 outbreak-associated cases of hepatitis A have been reported from four states (CA (2), HI (1), OR (1), WA (6)). Illnesses ranged from November 24, 2022, to June 4, 2023. Cases ranged from 38 to 64 years of age, with a median age of 56.5 years. Thirty percent of cases were female. Of 10 cases with available information, 4 (40%) have been hospitalized. No deaths have been reported.
The hepatitis A virus strain causing illnesses in this outbreak is genetically identical to the strain that caused a foodborne hepatitis A outbreak in 2022, which was linked to fresh organic strawberries imported from Baja California, Mexico, and sold at various retailers.
Ten cases were interviewed, and 10/10 (100%) reported eating frozen, organic strawberries. This proportion was significantly higher than results from a survey of healthy people, in which 24% reported eating frozen berries in the week before they were interviewed. Traceback and epidemiological investigations showed that outbreak-associated cases purchased the same retail brand of frozen organic strawberries prior to becoming ill. The outbreak was linked to frozen organic strawberries, imported fresh from certain farms located in Baja California, Mexico in 2022 by a common supplier.
In response to this investigation, California Splendor, Inc. of San Diego, California voluntarily recalled certain lots of 4-lb. bags of Kirkland Signature Frozen Organic Whole Strawberries that were sold at Costco stores in Los Angeles, California; Hawaii; and two San Diego, California business centers. The lots subject to this recall include: 140962-08, 142222-23, 142792-54, 142862-57, 142912-59, 142162-20, 142202-21, 142782-53, 142852-56, 142902-58, 142212-22, 142232-24, 142842-55.
In response to this investigation, Scenic Fruit Company of Gresham, Oregon voluntarily recalled frozen, organic strawberries sold to Costco, Trader Joe’s, Aldi, KeHE, Vital Choice Seafood, and PCC Community Markets in certain states. Products subject to this recall include:
Simply Nature | Organic Strawberries | 24 oz. | 4099100256222 | 6/14/2024 | Arizona, Arkansas, California, Illinois, Iowa, Michigan, Minnesota, Missouri, North Dakota, Ohio, South Dakota, Wisconsin |
Vital Choice | Organic Strawberries | 16 oz. | 834297005024 | 5/20/2024 | Washington |
Kirkland Signature | Organic Strawberries | 4 lbs. | 96619140404 | 10/8/2024 | Alaska, Idaho, Montana, Oregon, Utah, Washington |
Made With | Organic Strawberries | 10 oz. | 814343021390 | 11/20/2024 | Illinois, Maryland |
PCC Community Markets | Organic Strawberries | 32 oz. | 22827109469 | 29/10/2024 | Washington |
Trader Joe’s | Organic Tropical Fruit Blend Pineapple, Bananas, Strawberries & Mango | 16 oz. | 00511919 | 04/25/24, 05/12/24, 05/23/24, 05/30/24, 06/07/24 | Nationwide |
On March 17, 2023, the retailer Meijer also issued a voluntarily recall of Made-With brand frozen, organic strawberries from certain market store locations.
In response to this investigation, on June 7, 2023, Wawona Frozen Foods of Clovis, California, initiated a voluntary recall of year-old packages of Wawona brand Organic DayBreak Blend 4-lb. bags that were distributed to Costco Wholesale stores in Arizona, California, Colorado, Utah, and Washington from April 15, 2022, to June 26, 2022, with “Use By” dates of 9/23/2023, 9/29/2023, 9/30/2023, and 10/18/2023:
Best If Used By 09/23/2023 | Best If Used By 09/29/2023 | Best If Used By 09/30/2023 | Best If Used By 10/18/2023 |
Affected Lot Codes: | Affected Lot Codes: | Affected Lot Codes: | Affected Lot Codes: |
20082D04 | 20088D04 | 20089D09 | 20108D04 |
20082D05 | 20088D05 | 20089D10 | 20108D05 |
20082D06 | 20088D06 | 20089D11 | 20108D06 |
20082D07 | 20088D07 | 20089D12 | 20108D07 |
20082D08 | 20088D08 | 20108D08 | |
20088D09 | |||
20088D10 | |||
20088D11 | |||
20088D12 |
In response to this investigation, on June 12, 2023, Willamette Valley Fruit Co. of Salem, Oregon, voluntarily recalled select packages of frozen fruit, containing strawberries, distributed to the following retailers: Walmart (from January 24, 2023 to June 8, 2023), Costco Wholesale Stores (from October 3, 2022 to June 8, 2023), and HEB (from July 18, 2022 to June 8, 2023). Products subject to this recall include:
Retailer | Product Name | Net weight | Lot Code | Best By Date | Distributed in States |
Walmart | Great Value Sliced Strawberries | 4 lbs. | 4018305 4019305 | 7/19/2024 7/20/2024 | AR, AZ, CA, CO, HI, IA, ID, IL, IN, KS, KY, LA, MD, MI, MN, MO, MT, ND, NE, NV, NY, OH, OK, OR, PA, SD, TX, UT, VA, WI, WV, WY |
Great Value Mixed Fruit | 4 lbs. | 4024205 4025305 4032305 4033305 4034305 4035305 | 7/25/2024 7/26/2024 8/2/2024 8/3/2024 8/4/2024 8/5/2024 | ||
Great Value Antioxidant Fruit Blend | 40 oz. | 4032305 | 8/2/2024 | ||
Costco Wholesale | Rader Farms Fresh Start Smoothie Blend | 48 oz. bag containing six 8 oz. pouches | 4224202 4313202 4314202 4363202 4364202 4017302 4018302 4042306 4043306 4060306 | 2/11/2024 5/10/2024 5/11/2024 6/29/2024 6/30/2024 7/18/2024 7/19/2024 8/12/2024 8/13/2024 8/30/2024 | AZ, CA, CO, TX |
HEB | Rader Farms Organic Berry Trio | 3 lbs. | 4153205 4283202 4284202 4058302 4059302 | 12/02/2023 4/10/2024 4/11/2024 8/28/2024 8/29/2024 | TX |
In sum, the Willamette Valley Fruit Co. voluntary recall affected Great Value Mixed Fruit, Sliced Strawberries, and Antioxidant Fruit Blend sold in Walmart stores in AR, AZ, CA, CO, HI, IA, ID, IL, IN, KS, KY, LA, MD, MI, MN, MO, MT, ND, NE, NV, NY, OH, OK, OR, PA, SD, TX, UT, VA, WI, WV, and WY from January 24, 2023, to June 8, 2023; Rader Farms Organic Fresh Start Smoothie Blend sold in Costco stores in CO, TX, CA, and AZ from October 3, 2022, and June 8, 2023; Rader Farms Organic Berry Trio sold in HEB stores in TX from July 18th, 2022, to June 8, 2023; the Wawona Frozen Foods voluntary recall affected packages of Organic DayBreak Blend distributed to Costco Wholesale stores in AZ, CA, CO, UT, and WA from April 15, 2022 to June 26, 2022; the Meijer recall affected MadeWith brand frozen, organic strawberries sold in Meijer stores in certain location; the California Splendor, Inc. voluntary recalled affected certain lots of 4-lb. bags of Kirkland Signature Frozen Organic Whole Strawberries that were sold at Costco stores in Los Angeles and Hawaii, and at two San Diego business centers; and the Scenic Fruit Company voluntary recall affected frozen, organic strawberries sold to Costco, Aldi, KeHE, Vital Choice Seafood, and PCC Community Markets in certain states and to Trader Joe’s nationwide.
California Splendor supplied product sold to Costco stores in Los Angeles and HI, and to two San Diego business centers; Scenic Fruit supplied product sold to Costco, Aldi, KeHE, Vital Choice Seafood, and PCC Community Markets in specific states, and to Trader Joe’s nationwide. [35] [36] [37] [38] [39] [40] [41] [42] [43]
[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 Dis166: 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] CDC, Summary, “Disease Burden from Viral Hepatitis A, B, and C in the United States,” supra note 44.
[31] Bownds, Lynne, et al., “Economic Impact of a Hepatitis A Epidemic in a Mid-Sized Urban Community: The Case of Spokane, Washington,” Journal of Community Health, Vol. 28, No. 4, pp. 233-46 (2003). Abstract at http://www.ncbi.nlm.nih.gov/pubmed/12856793; Fiore, Anthony, et al., Advisory Committee on Immunization Practices (ACIP), Prevention of Hepatitis-A Through Active or Passive Immunization: Recommendations,” supra note 20.
[32] Scharff, RL, et al., “Economic Cost of Foodborne Illness in Ohio,” Journal of Food Protection, Vol. 72, No. 1, pp. 128-36 (2009). Abstract available online at http://www.ingentaconnect.com/content/iafp/jfp/2009/00000072/00000001/art00018.
[33] CDC, “Surveillance for Acute Viral Hepatitis – United States 2007,” supra note 13; CDC, “Hepatitis A,” supra note 5.
[34] CDC, “Hepatitis A,” supra note 5; Fiore, Anthony, et al., Advisory Committee on Immunization Practices (ACIP), Prevention of Hepatitis-A Through Active or Passive Immunization: Recommendations,” supra note 20.
[35] Organic Strawberries Hepatitis A Outbreak | CDC
[36] Outbreak Investigation of Hepatitis A Virus Infections: Frozen Strawberries (February 2023) | FDA
[37] 2023 Hepatitis A Outbreak Associated with Frozen Organic Strawberries | Washington State Department of Health
[38] Gresham company recalling frozen strawberry products linked to hepatitis A cases in Washington (govdelivery.com)
[39] California Splendor, Inc. Recalls Kirkland Brand Bags of Frozen Organic Whole Strawberries Distributed by Costco in Los Angeles, Hawaii, and in Two San Diego Business Centers Because of Possible Health Risk | FDA
[40] Updated – Scenic Fruit Company Recalls Frozen Organic Strawberries and Frozen Organic Tropical Blend Because of Possible Health Risk | FDA
[41] 103441 – Made-With Frozen Strawberries (Market Format Locations Only) – Recalls – Meijer – Meijer Community
[42] Wawona Frozen Foods Voluntarily Recalls Organic Daybreak Blend Processed and Sold in 2022 Due to Possible Health Risk | FDA
[43] Willamette Valley Fruit Co. Recalls Great Value Sliced Strawberries, Great Value Mixed Fruit Great Value Antioxidant Blend, Rader Farms Organic Fresh Start Smoothie Blend, and Rader Farms Organic Berry Trio Because of Possible Health Risk | FDA