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Publication #FSHN13-08

Outbreaks of Foodborne Illness Associated with Common Berries, 1983 through May 20131

M. Palumbo, L. J. Harris, and M. D. Danyluk2

Introduction

Fresh and frozen common berries (i.e., blackberries, blueberries, raspberries, and strawberries) are popular and healthy foods. When berries are picked for fresh consumption, they are either placed directly in retail containers in the field or packed in a packinghouse without washing because they are highly perishable. Berries may be washed before freezing, but they are not usually blanched or heat-treated unless they are used in preserves or other processed products. Thus, there is typically no “kill step” that would eliminate pathogens in fresh or frozen berries.

Berries may be served mixed with other foods such as in salads or desserts, and these may contain more than one kind of berry or other fruit. Epidemiologists have more difficulty accurately determining the food vehicle during a foodborne illness outbreak when the outbreak is associated with mixed foods, such as mixed berries. The viral and parasitic pathogens that have caused outbreaks associated with consumption of berries are difficult to detect in foods. The laboratory methods used to detect these pathogens have only recently been developed or are still under development.

This publication serves as a reference for anyone concerned about the safety of fresh and frozen berry products. Providing information for those who grow, harvest, process, transport, and serve berries to consumers is important for improving science-based food safety programs for the entire supply chain. Table 1 lists the reported outbreaks of foodborne illness from 1983 through May 2013 in which specific berries and mixed berries have been identified as the food vehicle. Table 2 lists the reported outbreaks in which berries were likely the food vehicle.

Figure 1. 
[Click thumbnail to enlarge.]

References

Associated Press. 2012. “Germany: Batch of Frozen Strawberries Blamed for Outbreak of Gastroenteritis in Schools.” FoxNews.com. Accessed April 2013. http://www.foxnews.com/world/2012/10/06/germany-batch-frozen-strawberries-blamed-for-outbreak-gastroenteritis-in/.

Bourquin, L. 2012. “Strawberries Implicated in Massive German Norovirus Outbreak.” Michigan State University Food Safety. Accessed April 2013. http://michiganstateuniversityfoodsafety.wordpress.com/2012/10/07/strawberries-implicated-in-massive-german-norovirus-outbreak/.

Calder, L., G. Simmons, C. Thornley, P. Taylor, K. Pritchard, G. Greening, and J. Bishop. 2003. “An Outbreak of Hepatitis A Associated with Consumption of Raw Blueberries.” Epidemiol. Infect. 131 (1): 745–751.

Canadian Food Inspection Agency (CFIA). 2012. “Health Hazard Alert - Certain Western Family Brand Pomeberry Blend Berries May Contain Hepatitis A Virus.” Accessed April 2013. http://www.inspection.gc.ca/about-the-cfia/newsroom/food-recalls-and-allergy-alerts/complete-listing/2012-04-05/eng/1355956873367/1355956873399.

Centers for Disease Control and Prevention (CDC). 1996. “Update: Outbreaks of Cyclospora cayetanensis Infection—United States and Canada, 1996.” MMWR Weekly 45 (28): 611–612. http://www.cdc.gov/mmwr/preview/mmwrhtml/00043133.htm.

Centers for Disease Control and Prevention (CDC). 1997a. “Hepatitis A Associated with Consumption of Frozen Strawberries—Michigan, March 1997.” MMWR Weekly 46 (13): 288–295. http://www.cdc.gov/mmwr/preview/mmwrhtml/00047129.htm.

Centers for Disease Control and Prevention (CDC). 1997b. “Update: Outbreaks of Cyclosporiasis—United States, 1997.” MMWR Weekly 46 (21): 461–462. http://www.cdc.gov/mmwr/preview/mmwrhtml/00047716.htm.

Centers for Disease Control and Prevention (CDC). 1997c. “Outbreak of Cyclosporiasis—Northern Virginia-Washington, D.C.-Baltimore, Maryland, Metropolitan Area.” MMWR Weekly 46 (30): 689–691. http://www.cdc.gov/mmwr/preview/mmwrhtml/00048551.htm.

Centers for Disease Control and Prevention (CDC). 1998. “Outbreak of Cyclosporiasis—Ontario, Canada.” MMWR Weekly 47 (38): 806–809. http://www.cdc.gov/mmwr/preview/mmwrhtml/00055016.htm.

Centers for Disease Control and Prevention (CDC). 2013a. Foodborne Outbreak Online Database [CDC FOOD]. Accessed January 2013. http://wwwn.cdc.gov/foodborneoutbreaks/Default.aspx.

Centers for Disease Control and Prevention (CDC). 2013b. “Multistate Outbreak of Hepatitis A Potentially Associated with a Frozen Berry Blend Food Product.” Accessed October 2013. http://www.cdc.gov/hepatitis/Outbreaks/2013/A1b-03-31/index.html.

Colorado Department of Public Health and Environment. 2013. “May 31: Hepatitis A Outbreak Associated with Townsend Farms Organic Antioxidant Blend Frozen Berries Purchased from Costco.” Accessed June 2013. http://www.colorado.gov/cs/Satellite?c=Page&childpagename=CDPHE-Main%2FCBONLayout&cid=1251643026247&pagename=CBONWrapper.

Cotterelle, B., C. Drougard, J. Rolland, M. Becamel, M. Boudon, S. Pinede, O. Traore, K. Balay, P. Pothier, and E. Espie. 2005. “Outbreak of Norovirus Infection Associated with the Consumption of Frozen Raspberries, France, March 2005.” Euro Surveill. 10 (4): E050428.1.

DW.de. 2012. “Blame Falls on Strawberries in German Mass Food Poisoning.” DW.de website. Accessed April 2013. http://www.dw.de/blame-falls-on-strawberries-in-german-mass-food-poisoning/a-16288862-1.

European Centre for Disease Prevention and Control (ECDC) and European Food Safety Agency (EFSA). 2013a. “Outbreak of Hepatitis A Virus Infection in Four Nordic Countries, 15 April 2013.” Accessed April 2013. http://ecdc.europa.eu/en/publications/Publications/hepatitis-a-rapid-assessment-nordic-countries-april2013.pdf.

European Centre for Disease Prevention and Control (ECDC) and European Food Safety Agency (EFSA). 2013b. “Outbreak of Hepatitis A Virus Infection in Residents and Travellers to Italy.” Accessed June 2013. http://www.foodsafetynews.com/files/2013/06/439e.pdf.

Falkenhorst, G., L. Krusell, M. Lisby, S. B. Madsen, B. Bottiger, and K. Molbak. 2005. “Imported Frozen Raspberries Cause a Series of Norovirus Outbreaks in Denmark, 2005.” Euro Surveill. 10 (9): E050922.2.

Fell, G., M. Boyens, and S. Baumgarte. 2007. “Frozen Berries as a Risk Factor for Outbreaks of Norovirus Gastroenteritis. Results of an Outbreak Investigation in the Summer of 2005 in Hamburg.” Bundesgesundheitsblatt – Gesundheitsforschung – Gesundheitsschutz 50 (2): 230–236.

Fleming, C. A., D. Caron, J. E. Gunn, and M. A. Barry. 1998. “A Foodborne Outbreak of Cyclospora cayetanensis at a Wedding: Clinical Features and Risk Factors for Illness.” Arch. Intern. Med. 158 (10): 1121–1125.

Food Safety News. 2012. “Chinese Strawberries Sickened Thousands of German Students.” Food Safety News website. Accessed April 2013. http://www.foodsafetynews.com/2012/10/german-students-got-sick-on-chinese-strawberries/.

Gillesberg Lassen, S., B. Soborg, S. E. Midgley, A. Steens, L. Vold, K. Stene-Johansen, R. Rimhanen-Finne, M. Kontio, M. Löfdahl, L. Sundqvist, M. Edelstein, T. Jensen, H. T. Vestergaard, T. K. Fischer, K. Mølbak, and S. Ethelberg. 2013. “Ongoing Multi-strain Food-borne Hepatitis A Outbreak with Frozen Berries as Suspected Vehicle: Four Nordic Countries Affected, October 2012 to April 2013.” Euro Surveill. 18 (17) pii: 20467. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20467.

Herwaldt, B. L. 2000. “Cyclospora cayetanensis: A Review, Focusing on Outbreaks of Cyclosporiasis in the 1990s.” Clin. Infect. Dis. 31 (4): 1040–1057.

Herwaldt, B. L., and M. L. Ackers. 1997. “An Outbreak in 1996 of Cyclosporiasis Associated with Imported Raspberries.” N. Engl. J. Med. 336: 1548–1556.

Herwaldt, B. L., and M. J. Beach. 1999. “The Return of Cyclospora in 1997: Another Outbreak of Cyclosporiasis in North America Associated with Imported Raspberries. Cyclospora Working Group.” Ann. Intern. Med. 130 (3): 210–220.

Hjertqvist, M., A. Johansson, N. Svensson, P. E. Abom, C. Magnusson, M. Olsson, K. O. Hedlund, and Y. Andersson. 2006. “Four Outbreaks of Norovirus Gastroenteritis after Consuming Raspberries, Sweden, June-August 2006.” Euro Surveill. 11 (9): E060907.1.

Ho, A. Y., A. S. Lopez, M. G. Eberhard, R. Levenson, B. S. Finkel, A. J. da Silva, J. M. Roberts, P. A. Orlandi, C. C. Johnson, and B. L. Herwaldt. 2002. “Outbreak of Cyclosporiasis Associated with Imported Raspberries, Philadelphia, Pennsylvania, 2000. Emerg. Infect. Dis. 8 (8): 783–788.

Hutin, Y. J. F., V. Pool, E. H. Cramer, O. V. Nainan, J. Weth, I. T. Williams, S. T. Goldstein, K. F. Gensheimer, B. P. Bell, C. N. Shapiro, M. J. Alter, and H. S. Margolis. 1999. “A Multistate, Foodborne Outbreak of Hepatitis A. New Eng. J. Med. 340 (8): 595–602.

Katz, D., S. Kumar, J. Malecki, M. Lowdermilk, E. H. Koumans, and R. Hopkins. 1999. “Cyclosporiasis Associated with Imported Raspberries, Florida, 1996.” Public Health Rep. 114 (5): 427–438.

Korsager, B., S. Hede, H. Boggild, B. E. Bottiger, and K. Molbak. 2005. “Two Outbreaks of Norovirus Infections Associated with the Consumption of Imported Frozen Raspberries, Denmark, May–June 2005.” Euro Surveill. 10 (6): E050623.1.

Koumans, E. H., D. J. Katz, J. M. Malecki, S. Kumar, S. P. Wahlquist, M. J. Arrowood, A. W. Hightower, and B. L. Herwaldt. 1998. “An Outbreak of Cyclosporiasis in Florida in 1995: A Harbinger of Multistate Outbreaks in 1996 and 1997.” Am. J. Trop. Med. Hyg. 59 (2): 235–242.

Luna, R. E., and R. Mody. 2010. “Non-O157 Shiga Toxin-Producing E. coli (STEC) Outbreaks, United States.” CDC Memo to Record. Accessed April 2013. http://blogs.cdc.gov/publichealthmatters/files/2010/05/nono157stec_obs_052110.pdf.

Marler-Clark, LLP. 2012. Foodborne Illness Outbreak Database. Accessed April 2013. http://outbreakdatabase.com/details/pomeberry-blend-frozen-berries-2012/?outbreak=berries&vehicle=berries.

Maunula, L., M. Roivainen, M. Keranen, S. Makela, K. Soderberg, M. Summa, C. H. von Bonsdorff, M. Lappalainen, T. Korhonen, M. Kuusi, and T. Niskanen. 2009. “Detection of Human Norovirus from Frozen Raspberries in a Cluster of Gastroenteritis Outbreaks.” Euro Surveill. 14 (49) pii: 19435.

Miller, B. D., C. E. Rigdon, T. J. Robinson, C. Hedberg, and K. E. Smith. 2013. “Use of Global Trade Item Numbers in the Investigation of a Salmonella Newport Outbreak Associated with Blueberries in Minnesota, 2010.” J. Food Prot. 76 (5): 762–769.

Murrow, L. B., P. Blake, and L. Kreckman. 2002. “Outbreak of Cyclosporiasis in Fulton County, Georgia.Georgia Epidemiol. Rep. 18 (1): 1–2.

Niu, M. T., L. B. Polish, B. H. Robertson, B. K. Kanna, B. A. Woodruff, C. N. Shapiro, M. A. Miller, J. D. Smith, J. K. Gedrose, M. J. Alter, and H. S. Margolis. 1992. “Multistate Outbreak of Hepatitis A Associated with Frozen Strawberries.” J. Infect. Dis. 166 (3): 518–524.

Oregon Public Health. 2011. "Fresh Strawberries from Washington County Farm Implicated in E. coli O157 outbreak in NW Oregon." Accessed September 2013. http://www.fda.gov/Safety/Recalls/ArchiveRecalls/2011/ucm267667.htm.

Pönkӓ, A., L. Maunula, C. H. von Bonsdorff, and O. Lyytikӓinen. 1999a. “Outbreak of Calicivirus Gastroenteritis Associated with Eating Frozen Raspberries.Euro. Surveill. 4 (6): 66–69.

Pönkӓ, A., L. Maunula, C. H. von Bonsdorff, and O. Lyytikӓinen. 1999b. “An Outbreak of Calicivirus Associated with Consumption of Frozen Raspberries.” Epidemiol. Infect. 123 (3): 469–474.

Ramsay, C. N., and P. A. Upton. 1989. “Hepatitis A and Frozen Raspberries.” Lancet 1 (8628): 43–44.

Reid, T. M. S., and H. G. Robinson. 1987. “Frozen Raspberries and Hepatitis A.” Epidemiol. Infect. 98 (1): 109–112.

Rothschild, M. 2012. “BC Issues Warning about Pomeberry Frozen Berries.” Food Safety News. Accessed April 2013. http://www.foodsafetynews.com/2012/04/bc-issues-warning-about-pomeberry-frozen-berries/.

Sarvikivi, E., M. Roivainen, L. Maunula, T. Niskanen, T. Korhonen, M. Lappalainen, and M. Kuusi. 2012. “Multiple Norovirus Outbreaks Linked to Imported Frozen Raspberries.” Epidemiol. Infect. 140 (2): 260–267.

Terry, L. 2011. “Oregon Confirms Deer Droppings Caused E. coli Outbreak Tied to Strawberries.” The Oregonian. Accessed September 2013. http://www.oregonlive.com/washingtoncounty/index.ssf/2011/08/oregon_confirms_deer_droppings.html.

Tables

Table 1. 

Foodborne illness outbreaks associated with common berries as the food vehicle, 1983 through 2012

Berry

Form

Country of origin

Pathogen1

Year

Outbreak location

Number of cases (deaths2)

Isolated/

detected in product

Comments

References

Blueberry

Fresh

New Zealand

Hepatitis A

2002

New Zealand

43 (1)

Yes

Mode of contamination was likely infected food handlers or contaminated groundwater (pit latrines were located in and near orchard, with no hand-washing facilities).

Calder et al. 2003

Blueberry

NR3

NR

Salmonella Muenchen

2009

United States, multiple states

14 (0)

NR

Consumed in private home(s)

CDC 2013a

Blueberry

Fresh

United States (Georgia)

Salmonella Newport

2010

United States, Minnesota

6 (0)

NR

Traced to single grower

CDC 2013a; Miller et al. 2013

Raspberry

Fresh

Guatemala

C. cayetanensis

1996

United States (multiple states), Canada (Ontario)

850

No

Source of contamination unknown

CDC 1996; Herwaldt and Ackers 1997

Raspberry

Fresh

Guatemala

C. cayetanensis

1997

United States (multiple states), Canada (Ontario)

1,012 (0)

No

Source of contamination unknown

CDC 1997b; CDC 1997c; Herwaldt and Beach 1999

Raspberry

Fresh

Guatemala

C. cayetanensis

1998

Canada (Ontario)

192

No

Source of contamination unknown

CDC 1998

Raspberry

Fresh

Guatemala likely

C. cayetanensis

2000

United States (Georgia, Pennsylvania)

54

Yes (PCR4)

Source of contamination unknown

Ho et al. 2002; Murrow, Blake, and Kreckman 2002

Raspberry

Frozen

East Europe

Calicivirus

1988

Finland

509

No

Source of contamination unknown

Pönkä et al. 1999a; Pönkä et al. 1999b

Raspberry

Frozen

Scotland

Hepatitis A

1983

Scotland

24

No

Pickers were believed to be the source of contamination; cases were reported in the area at the time of picking.

Reid and Robinson 1987

Raspberry

Purchased fresh, then frozen

Scotland

Hepatitis A

1988

Scotland

5

No

Infection was confirmed in a picker at the farm; other pickers had been ill, some with jaundice.

Ramsay and Upton 1989

Raspberry

Frozen pieces

Poland

Norovirus

2005

Denmark

973

No

Six point source outbreaks occurred between June and September; five of these linked to the same large batch of frozen raspberries, which came from several small farms in Poland.

Falkenhorst et al. 2005; Korsager et al. 2005

Raspberry

Frozen, imported

NR

Norovirus

2005

France

75

No

Raspberries blended with fromage blanc, and a frozen raspberry placed on each dessert by hand; kitchen staff did not report GI illness before the outbreak.

Cotterelle et al. 2005

Raspberry

Frozen

China

Norovirus

2006

Sweden

43

NR

Four outbreaks between end of June and end of August in southwestern part of country; raspberries were same brand in each outbreak; lab results on leftover product were pending at time of report.

Hjertqvist et al. 2006

Raspberry

Frozen

Poland (some batches)

Norovirus

2009

Finland

900

Yes

Thirteen outbreaks linked to consumption of imported raspberries; two positive batches, one of which traced back to 62 different farms; source of contamination not known.

Maunula et al. 2009;

Sarvikivi et al. 2012

Strawberry

Frozen

United States (California)

Hepatitis A

1990

United States (Georgia, Montana)

28

No

Outbreaks in elementary school in Georgia and institution for disabled in Montana; molecular analysis of HAV from patients showed viral genomes genetically identical and distinct from other known U.S. strains; strawberries implicated in both outbreaks processed at same plant on same night; infected picker was believed to be the likely source.

Niu et al. 1992

Strawberry

Frozen

Mexico

Hepatitis A

1997

United States (Michigan, Maine)

242

No

Implicated strawberries were grown in Mexico, processed and frozen in California, and distributed through USDA school lunch programs and through distributors for commercial use; U.S. FDA conducted site visits of growing fields and found inadequate toilet and hand-washing facilities; workers did not wear gloves and removed berry calyx with fingernails.

CDC 1997a; Hutin et al. 1999

Strawberry

NR

NR

Norovirus

2005

United States (Georgia)

40 (0)

NR

Consumed at wedding reception

CDC 2013a

Strawberry

NR

NR

Norovirus

2007

United States (Georgia)

10 (0)

NR

Consumed in private home

CDC 2013a

Strawberry

Fresh

NR

Norovirus

2007

United States (California)

17 (0)

NR

Consumed with ice cream in restaurant

CDC 2013a

Strawberry

Fresh

United States

E. coli O157:H7

2011

United States (Oregon)

15 (2)

NR

Matching strain found by environmental sampling in field, including deer droppings

CDC 2013a; Oregon Public Health 2011; Terry 2011

Strawberry

Frozen

China

Norovirus

2012

Germany

11,200

NR

Berries delivered to almost 500 schools and day care centers in eastern Germany by catering firm

Associated Press 2012; Dw.de 2012; Bourquin 2012; Food Safety News 2012

Berry mixture (pomegranate seeds, strawberry, blueberry, cherry)

Frozen

NR

Hepatitis A

2012

Canada (British Columbia)

8

NR

Five of 8 cases recalled eating this product

CFIA 2012; Marler-Clark 2012; Rothschild 2012

Berries, mixed

NR

NR

C. cayetanensis

2008

United States (California)

59 (0)

NR

Consumed at workplace cafeteria and banquet facility

CDC 2013a

Berries

NR

NR

C. cayetanensis

2008

United States (Tennessee)

3 (0)

NR

Type of berry not described, consumed at banquet facility; outbreak occurred in same month (July) as California outbreak

Marler-Clark 2012; CDC 2013b

Berries

Frozen

NR

Hepatitis A

2012–2013

Denmark, Finland, Norway, Sweden

71 (as of April 17, 2013)

No

May be ongoing; type of berry not yet identified

ECDC-EFSA 2013a; Gillesberg Lassen et al. 2013

Berries, mixed

Frozen

NR

Hepatitis A

2013

Germany, the Netherlands, Poland

15

Yes, in package from case patient’s home

All cases had traveled to northern Italy, provinces of Trento and Bolzano. Hepatitis A subgenotype IB

ECDC-EFSA 2013b

Berries, mixed (contained pomegranate seeds)

Frozen

Berries from United States, Chile, and Argentina; pomegranate seeds from Turkey

Hepatitis A

2013

United States (Arizona, California, Colorado, New Mexico, and Nevada)

162

No

Genotype 1B. Same genotype as outbreak in British Columbia (2012) and northern Europe (2012-2013). Genotype reported to be rare in the United States, but circulates in Middle East and North Africa. Pomegranate seeds imported from Turkey considered the most likely source.

Colorado Department of Public Health and Environment 2013; CDC 2013b

Raspberry and blackberry

NR

NR

C. cayetanensis

2009

United States (Connecticut)

8

NR

Consumed in private home

CDC 2013a

Strawberry and/or blueberry

NR

NR

E. coli O26

2006

United States (Massachusetts)

5 (0)

NR

 

Luna and Mody 2010

Notes to Table 1:

1 Pathogen abbreviated as C. denotes Cyclospora.

2 Deaths are shown in parentheses (x) only if reported by literature sources. If no (x) appears, no information on deaths was reported.

3 NR, not reported

4 PCR, polymerase chain reaction

Table 2. 

Foodborne illness outbreaks suspected to be associated with common berries as the food vehicle, 1983 through May 2013

Berry

Form

Country of origin

Pathogen1

Year

Outbreak location

Number of cases (deaths2)

Isolated/

detected in product

Comments

References

Blackberry likely

Fresh

Guatemala

C. cayetanensis

1999

Canada (Ontario)

104

No

Implicated dessert contained blackberries, frozen Chilean raspberries, fresh U.S. strawberries

Herwaldt 2000

Blackberry likely

Frozen

NR3

Norovirus

2005

Germany

241

No

[Article in German]

Fell, Boyens, and Baumgarte 2007

Raspberry most likely (strawberry possible)

Fresh

Guatemala

C. cayetanensis

1996

United States (20 states and Washington, DC), Canada (2 provinces)

1,465 (0)

No

Possible contamination due to fruit spraying with insecticides and fungicides mixed with contaminated water

Fleming et al. 1998; Herwaldt and Ackers 1997; Katz et al. 1999

Raspberry likely

NR

Guatemala likely

C. cayetanensis

1995

Florida

87

No

Two social events; berries purchased from separate sources

Koumans et al. 1998

Notes to Table 2:

1 Pathogen abbreviated as C. denotes Cyclospora.

2 Deaths are shown in parentheses (x) only if reported by literature sources. If no (x) appears, no information on deaths was reported.

3 NR, not reported

Footnotes

1.

This document is FSHN13-08, one of a series of the Food Science and Human Nutrition Department, UF/IFAS Extension. Original publication date: November 2013. Visit the EDIS website at http://edis.ifas.ufl.edu.

2.

M. Palumbo, outreach coordinator, Western Center for Food Safety, University of California, Davis, CA 95616; L. J. Harris, cooperative extension specialist, microbial food safety, Department of Food Science and Technology, University of California, Davis, CA 95616; M. D. Danyluk, assistant professor, Food Science and Human Nutrition Department, Citrus Research and Education Center, Lake Alfred, FL 33850; UF/IFAS Extension, Gainesville, FL 32611.

This review was supported by Specialty Crops Research Initiative Grant 2009-51181-05783.


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