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Outbreaks of Foodborne Disease Associated with Fruit and Vegetable Juices, 1922–20191

Matthew D. Krug, Travis K. Chapin, Michelle D. Danyluk, Renée M. Goodrich-Schneider, Keith R. Schneider, Linda J. Harris, and Randy W. Worobo2

In response to several outbreaks of illness in the 1990s associated with raw juices processed at commercial facilities, the US Food and Drug Administration (FDA) introduced regulation (21 Code of Federal Regulations 120; FDA 2001) mandating that all 100% fruit/vegetable juices be produced under a Hazard Analysis and Critical Control Point (HACCP) plan. The juice HACCP regulation applies to domestic and imported 100% juice products and has implications for juice producers in countries that export juice to the United States.

HACCP plans must have supporting good manufacturing practices (GMPs) and sanitation standard operating procedures (SSOPs). In addition, the regulation requires juice processors apply a treatment that results in at least a 5-log reduction of the “pertinent microorganism,” which is defined as “the most resistant microorganism of public health significance that is likely to occur in the juice.” Identification of the pertinent microorganism for a particular juice may be based upon foodborne illness outbreak data or other appropriate information such as survey or recall reports involving isolation of pathogens from juices or the fruits or vegetables used to produce those juices. Currently, Salmonella is generally accepted as the pertinent pathogen in citrus juices, whereas Escherichia coli O157:H7 as well as Cryptosporidium parvum are both considered pertinent for apple juice (FDA 2001).

Outbreaks reported to the US Centers for Disease Control and Prevention (CDC) are compiled in the CDC National Outbreak Reporting System (NORS) database available at https://wwwn.cdc.gov/norsdashboard (CDC 2018). This tool was used, in part, for the preparation of the table presented here and may also be a useful resource when conducting a hazard analysis. A microbial risk assessment for unpasteurized fruit juices and cider prepared by Health Canada may also be a useful resource (Mihajlovic et al. 2013). This document is intended to highlight juice-related outbreaks, aid juice processors in the identification of “pertinent microorganisms,” and review the locations, venues of juice preparations, and severity of juice-associated outbreaks.

Figure 1. 

Salmonella species on X.L.D. agar.


Credit:

Nathan Reading, CC BY-NC-ND 2.0 (http://flic.kr/p/9TtH1V)


[Click thumbnail to enlarge.]

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CFIA (Canadian Food Inspection Agency). 2014. “Food Recall Warning - Unpasteurized apple cider processed by Rolling Acres Cider Mill recalled due to E. coli O157:H7.” https://web.archive.org/web/20181204022225/http://www.inspection.gc.ca/about-the-cfia/newsroom/food-recall-warnings/complete-listing/2014-10-30/eng/1414720185030/1414720197088. Accessed August 8, 2018.

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FDA (US Food and Drug Administration). Federal Register Proposed Rules – 63 FR 20449 April 24, 1998 – HACCP; Procedures for the Safe and Sanitary Processing and Importing of Juice; Food Labeling: Warning Notice Statements; Labeling of Juice Products. Federal Register: April 24, 1998 63:20449–20486. https://www.federalregister.gov/documents/1998/04/24/98-11025/hazard-analysis-and-critical-control-point-haccp-procedures-for-the-safe-and-sanitary-processing-and. Accessed August 7, 2018.

FDA. Federal Register Final Rule – 66 FR 6137, January 19, 2001: Hazard Analysis and Critical Control Point (HACCP); Procedures for the Safe and Sanitary Processing and Importing of Juices. Federal Register: January 19, 2001 66:6137–6202.

Frank, C., J. Walter, M. Muehlen, A. Jansen, U. van Treeck, A. M. Hauri, I. Zoellner, E. Schreier, O. Hamouda, and K. Stark. 2005. “Large outbreak of hepatitis A in tourists staying at a hotel in Hurghada, Egypt, 2004 – orange juice implicated.” Eurosurveillance 10:2720.

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IDPH (Iowa Department of Public Health). 2014. Iowa surveillance of notifiable and other diseases: Annual report 2013. http://publications.iowa.gov/17797/1/IDPH_Annual_Rpt_2013.pdf. Accessed August 7, 2018.

Jain, S., S. A. Bidol, J. L. Austin, E. Berl, F. Elson, M. L. Williams, M. Deassy III, M. E. Moll, V. Rea, J. D. Vojdani, P. A. Yu, R. M. Hoekstra, C. R. Braden, and M. F. Lynch. 2009. “Multistate outbreak of Salmonella Typhimurium and Saintpaul infections associated with unpasteurized orange juice—United States, 2005.” Clinical Infectious Diseases 48:1065–1071.

Katz, D. J., M. A. Cruz, M. J. Trepka, J. A. Sarez, P. D. Filrella, and R. M. Hammond. 2002. “An outbreak of typhoid fever in Florida associated with an imported fruit.” Journal of Infectious Diseases 186:234–239.

Krause, G., R. Terzagian, and R. Hammond. 2001. “Outbreak of Salmonella serotype Anatum infection associated with unpasteurized orange juice.” Southern Medical Journal 94:1168–1172.

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Noël, H., A. Hofhuis, R. De Jonge, A. E. Heuvelink, A. De Jong, M. E. Heck, C. De Jager, and W. van Pelt. 2010. “Consumption of fresh fruit juice: How a healthy food practice caused a national outbreak of Salmonella Panama gastroenteritis.” Foodborne Pathogens and Disease 7:375–381.

Paquet, P. 1923. “Épidémie de fièvre typhoïde: Déterminée par la consommation de petit citre.” Revue d’Hygine 45:165–169.

Parish, M. E. 1998. “Coliforms, Escherichia coli, and Salmonella serovars associated with a citrus-processing facility implicated in a salmonellosis outbreak.” Journal of Food Protection 61:280–284.

Parish, M. 2000. “Relevancy of Salmonella and pathogenic E. coli to fruit juices. Proceedings IFU-Workshop ‘Microbiology.’” Fruit Processing 10:246–250.

Pereira, K. S., F. L. Schmidt, A. M. A. Guaraldo, R. M. B. Franco, V. L. Dias, and L. A. C. Passos. 2009. “Chagas’ disease as a foodborne illness.” Journal of Food Protection 72:441–446.

Schaffzin, J. K., F. Coronado, N. B. Dumas, T. P. Root, T. A. Halse, D. J. Schoonmaker-Bopp, M. M. Lurie, D. Nicholas, B. Gerzonich, G. S. Johnson, B. J. Wallace, and K. A. Musser. 2012. “Public health approach to detection of non-O157 Shiga toxin-producing Escherichia coli: summary of two outbreaks and laboratory procedures.” Emerging Infectious Diseases 140 (2): 283–289. https://doi.org/10.1017/s0950268811000719

Singh, B. R., S. B. Kulshreshtha, and K. N. Kapoor. 1995. “An orange juiceborne outbreak due to enterotoxigenic Escherichia coli.” Journal of Food Science and Technology-India 34:504–506.

Steele, B. T., N. Murphy, and C. P. Rance. 1982. “An outbreak of hemolytic uremic syndrome associated with ingestion of fresh apple juice.” Journal of Pediatrics 101:963–966.

Tabershaw, I. R., L. L. Schmelzer, and H. B. Bruhn. 1967. “Gastroenteritis from an orange juice preparation.” Archives of Environmental Health 15:72–77.

Tamblyn, S., J. de Grosbois, D. Taylor, and J. Stratton. 1999. “An outbreak of Escherichia coli O157:H7 infection associated with unpasteurized non-commercial, custom-pressed apple cider – Ontario, 1998.” Canada Communicable Disease Report 25:113–117; discussion 117–120.

Taylor, J. L., J. Tuttle, T. Pramukul, K. O’Brien, T. J. Barrett, B. Jolbaito, Y. L. Lim, D. J. Vugia, J. G. Morris, Jr., R. V. Tauxe, and D. M. Dwyer. 1993. “An outbreak of cholera in Maryland associated with imported commercial frozen fresh coconut milk.” Journal of Infectious Diseases 167:1330–1335.

Thurston, H., J. Stuart, B. McDonnell, S. Nicholas, and T. Cheasty. 1998. “Fresh orange juice implicated in an outbreak of Shigella flexneri among visitors to a South African game reserve.” Journal of Infectious Diseases 36:350.

Tsai, H.-C., S. Lee, C.-K. Huang, C.-M. Yen, E.-R. Chen, and Y.-C. Liu. 2004. “Outbreak of eosinophilic meningitis associated with drinking raw vegetable juice in southern Taiwan.” American Journal of Tropical Medicine and Hygiene 71:222–226.

Vojdani, J., L. Beuchat, and R. Tauxe. 2008. “Juice-associated outbreaks of human illness in the United States, 1995 through 2005.” Journal of Food Protection 71 (2): 356–364.

Tables

Table 1. 

Outbreaks of human foodborne disease from various microorganisms associated with juices during the period of 1922–2019.

Type

Product

Year

Pathogena

Location

Venue

Cases (Deaths)b

Referencec

Açaí

Unspecified

2004

Trypanosoma cruzid

Brazil

Retail

27

Pereira et al. 2009

 

Unspecified

2007

Trypanosoma cruzi

Brazil

Retail

25

Pereira et al. 2009

Apple

Unpasteurized

1922

S. Typhi

France

NRe

23 (0)

Paquet 1923

 

Unpasteurized

1974

S. Typhimurium

US (NJ)

Farm, small retail outlets

296 (0)

CDC 1975

 

Unpasteurized

1980

E. coli O157:H7 (suspected)

Canada (ON)

Local market

14 (1)

Steele et al., 1982

 

Unpasteurized

1991

E. coli O157:H7

US (MA)

Small cider mill

23 (0)

Besser et al. 1993

 

Unpasteurized

1993

Cryptosporidium

US (ME)

School

213 (0)

Millard et al. 1994

 

Unpasteurized

1996

C. parvum

US (NY)

Small cider mill

31 (0)

CDC 1997

 

Unpasteurized

1996

E. coli O157:H7

US (CT)

Small cider mill

14 (0)

CDC 1997

 

Unpasteurized

1996

E.coli O157:H7

US (WA)

Small cider mill

6 (0)

FDA 2001

 

Unpasteurized

1996

E. coli O157:H7

Canada (BC), US (CA, CO, WA)

Retail

70 (1)

CDC 1996, Cody et al. 1999

 

Unpasteurized

1997

E. coli O157:H7

US (IN)

Farm

6

INS DOH 1997

 

Unpasteurized

1998

E. coli O157:H7

Canada (ON)

Farm/Home

14 (0)

Tamblyn et al. 1999

 

Unpasteurized

1999

E. coli O157:H7

US (OK)

NR

25 (0)

CDC 2018

 

Unpasteurized (ozonated)

2003

C. parvum

US (OH)

Farm/Retail

144 (0)

Blackburn 2006, Vojdani et al. 2008, CDC 2018

 

Unpasteurized

2004

E. coli O111 and C. parvum

US (NY)

Farm/Home

212 (0)

Vojdani et al. 2008, Schaffzin et al. 2012, CDC 2018

 

Unpasteurized

2005

E. coli O157:H7

Canada (ON)

NR

4

LSDEPC 2005

 

Unpasteurized

2007

E. coli O157:H7

US (MA)

NR

9 (0)

CDC 2018

 

Unpasteurized

2008

E. coli O157:H7

US (IA)

Fair, festival

5 (0)

CDC 2018

 

Unpasteurized

2010

E. coli O157:H7

US (MD)

Retail

7 (0)

CDC 2018

 

Unpasteurized

2011

Cryptosporidium, E. coli O111:NM

US (MN)

Farm

14 (0)

MDH 2014, CDC 2018

 

Unpasteurized

2011

Cryptosporidium

US (OH)

NR

4 (0)

CDC 2018

 

Unpasteurized

2012

E. coli O157:H7

US (MI)

Home

3 (0)

CDC 2018

 

Unpasteurized

2013

Cryptosporidium

US (IA)

Home

10 (0)

IDPH 2014, CDC 2018

 

Unpasteurized

2013

Cryptosporidium

US (OH)

NR

8 (0)

CDC 2018

 

Unpasteurized

2013

S. Typhimurium

US (PA)

NR

10 (0)

CDC 2018

 

Unpasteurized

2014

E. coli O157:H7

Canada (ON)

Farm, cider mill, local farmer’s market

3

CFIA 2014

 

Unpasteurized

2014

Campylobacter jejuni

US (AZ)

Fair, festival

6 (0)

CDC 2018

 

Unpasteurized

2015

E. coli O157

US (MN)

Farm

2 (0)

CDC 2018

 

Unpasteurized

2015

E. coli O45

US (MI)

NR

2 (0)

CDC 2018

 

Unpasteurized

2016

E. coli O157:H7

US (KS)

Fair, festival

56 (0)

CDC 2018

 

Unspecified

2015

E. coli O111:NM

US (CA)

NR

15 (0)

CDC 2018

Carrot

Homemade

1993

C. botulinum

US (WA)

Home

1 (0)

Buzby and Crutchfield 1999

 

Pasteurized

2006

C. botulinum

US (FL, GA)

Retail

4 (1)

CDC 2006, CDC 2018

Coconut

Milkf

1991

Vibrio cholerae

US (MD)

Home/picnic

4

CDC 1991, Taylor et al. 1993

Guava

Unspecified

2007

Trypanosoma cruzi

Venezuela

School

103 (1)

de Noya et al. 2010

Mamey

Frozen Puree

1999

S. Typhi

US (FL)

NR

16 (0)

Katz et al. 2002, CDC 2018

 

Frozen Pulp

2010

S. Typhi

US (CA, NV)

Restaurant

12 (0)

CDC 2010, CDC 2017

Mixed Fruit

Unspecified

2002

Shigella sonnei

Canada, US, UK, British West Indies

Resort

78

CDC 2018

 

Açaí, sugar cane

2006

Trypanosoma cruzi

Brazil

NR

94 (6)

Pereira et al. 2009

 

Açaí, banana, strawberry, sugar cane

2007

Hepatitis A

US (FL)

Restaurant

3 (0)

CDC 2018

Mixed Fruit /Vegetable

Clover, sweet potato leaf, apple

2001

Angiostrongylus cantonesisg

Taiwan

Home

5

Tsai et al. 2004

Orange

Unpasteurized

1992

Enterotoxigenic E. coli

India

Roadside Vendor

6 (0)

Singh et al. 1995

 

Unpasteurized

1995

Salmonella Gaminera, Hartford and Rubislaw

US (FL)

Retail

63 (0)

CDC 1995, Cook et al. 1998, Parish 1998

 

Unpasteurized

1995

Shigella flexneri

South Africa

Restaurant

14

Thurston et al. 1998

 

Unpasteurized

1996

Virus suspected

US

Food Service

2

Parish 2000

 

Unpasteurized

1999

S. Muenchen

Canada and US

Restaurant

398 (0)

CDC 1999, CDC 2018

 

Unpasteurized

1999

S. Anatum

US (FL)

Roadside stand

10 (0)

Krause et al. 2001, CDC 2018

 

Unpasteurized

1999

S. Typhimurium

Australia

Retail

405 (0)

National Centre for Disease Control 1999

 

Unpasteurized

2000

S. Enteritidis

US (6 states)

Retail and Food Service

88

Butler 2000, CDC 2018

 

Unpasteurized

2004

Hepatitis A

Egypt

Hotel

351

Frank et al. 2005

 

Unpasteurized

2005

S.Typhimurium and S. Saintpaul

US (23 states)

Retail and Food Service

157 (0)

Jain et al. 2009, CDC 2018

 

Unpasteurized

2008

S. Panama

The Netherlands

Retail

33

Noël et al. 2010

 

Reconstituted

1944

S. Typhi

US (OH)

Hotel

18 (1)

Duncan et al. 1946

 

Reconstituted

1962

Hepatitis A

US (MO)

Hospital

24

Eisenstein et al. 1963

 

Reconstituted

1965

Unknown

US (CA)

Football game

563

Tabershaw et al. 1967

 

Reconstituted

1989

S. Typhi

US (NY)

Hotel

69

Birkhead et al. 1993

 

Unspecified

1991

Norwalk-like virus

Australia

Airline

3,053

Lester et al. 1991

Sugarcane

Unspecified

2005

Trypanosoma cruzi

Brazil

Roadside kiosk

25 (3)

Pereira et al. 2009

Watermelon

Homemade

1993

Salmonella spp.

US (FL)

Home

18 (0)

FDA 1998

a Pathogens abbreviated and associated with outbreaks include S.Salmonella; E.Escherichia; C. parvumCryptosporidium parvum; C. botulinumClostridium botulinum.

b The number in parentheses represents the number of deaths, if reported.

c References for each outbreak appears in the following reference list.

d Trypanosoma cruzi is the causative agent of Chagas’ Disease.

e NR—Not Reported

f Coconut milk is the liquid that is squeezed from the coconut meat; coconut juice or coconut water is the liquid obtained from a whole coconut when one breaks the shell.

g Angiostrongylus cantoneses, also known as rat lungworm, is the major cause of eosinophilic meningitis in the Pacific Islands and southeast Asia.

Footnotes

1.

This document is FSHN12-04, one of a series of the Food Science and Human Nutrition Department, UF/IFAS Extension. Original publication date January 2012. Revised June 2020. Visit the EDIS website at https://edis.ifas.ufl.edu for the currently supported version of this publication.

2.

Matthew D. Krug, state specialized agent, food science, UF/IFAS Southwest Florida Research and Education Center; Travis K. Chapin, state specialized agent, food safety; Michelle D. Danyluk, professor, Food Science and Human Nutrition Department, UF/IFAS Citrus REC; Renée M. Goodrich-Schneider, professor; Keith R. Schneider, professor, Food Science and Human Nutrition Department; Linda J. Harris, cooperative Extension specialist—microbial food safety, Department of Food Science and Technology, University of California; and Randy W. Worobo, associate professor, Department of Food Science and Technology, Cornell University; UF/IFAS Extension, Gainesville, FL 32611.


The Institute of Food and Agricultural Sciences (IFAS) is an Equal Opportunity Institution authorized to provide research, educational information and other services only to individuals and institutions that function with non-discrimination with respect to race, creed, color, religion, age, disability, sex, sexual orientation, marital status, national origin, political opinions or affiliations. For more information on obtaining other UF/IFAS Extension publications, contact your county's UF/IFAS Extension office.

U.S. Department of Agriculture, UF/IFAS Extension Service, University of Florida, IFAS, Florida A & M University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Nick T. Place, dean for UF/IFAS Extension.