University of FloridaSolutions for Your Life

Download PDF
Publication #FSHN12-04

Outbreaks of Foodborne Disease Associated with Fruit and Vegetable Juices, 1922–20101

M. D. Danyluk, R. M. Goodrich-Schneider, K. R. Schneider, L. J. Harris, and R. W. Worobo2

In response to several outbreaks of illness in the 1990s associated with raw juices processed at commercial facilities, the U.S. Food and Drug Administration (FDA) introduced regulation (21 Code of Federal Regulations 120; FDA, 2001) mandating that all 100% fruit/vegetable juices sold wholesale 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). The juice HACCP regulation applies to domestic and imported 100% juice products and therefore has implications for juice producers in countries that export juice to the United States.

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:

Photo by Nathan Reading CC BY-NC-ND 2.0 http://flic.kr/p/9TtH1V


[Click thumbnail to enlarge.]

References

Alarcón de Noya, B., Z. Díaz-Bello, C. Colmenares, R. Ruiz-Guevara, L. Mauriello, R. Zavala-Jaspe, J. A. Suarez, T. Abate, L. Naranjo, M. Paiva, L. Rivas, J. Castro, J. Márques, I. Mendoza, H. Acquatella, J. Torres, and O. Noya. 2010. Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. Journal of Infectious Disease 201:1308–1315.

Besser, R. E., S. M. Lett, J. T. Weber, M. P. Doyle, T. J. Barrett, J. G. Wells, and M. P. Griffin. 1993. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. Journal of the American Medical Association 269:2217–2220.

Birkhead, G. S., D. L. Morse, W. C. Levine, J. K. Fudala, S. F. Kondracki, H. G. Chang, M. Shaydgani, L. Novick, and P. A. Blake. 1993. Typhoid fever at a resort hotel in New York: A large outbreak with an unusual vehicle. Journal of Infectious Diseases 167:1228–1232.

Butler, M. E. 2000. Salmonella outbreak leads to juice recall in Western states. Food Chemical News April 24, 2000.

Buzby, J. C., and S. R. Crutchfield. 1999. New Juice Regulations Underway. Food Review. http://www.ers.usda.gov/publications/foodreview/may1999/frmay99f.pdf. Accessed October 5, 2011.

CDC (Centers for Disease Control and Prevention). 1975. Salmonella typhimurium outbreak traced to a commercial apple cider—New Jersey. Morbidity and Mortality Weekly Report 24:87–88.

CDC. 1991. Cholera associated with imported frozen coconut milk—Maryland. Morbidity and Mortality Weekly Report 40:844–843.

CDC. 1995. Outbreak of Salmonella Hartford infections among travelers to Orlando, Florida. EPI-AID Trip Report 95–62.

CDC. 1996. Outbreak of Escherichia coli O157:H7 infections associated with drinking unpasteurized commercial apple juice—British Columbia, California, Colorado, and Washington, October 1996. Morbidity and Mortality Weekly Report 45:975.

CDC. 1997. Outbreaks of Escherichia coli O157:H7 infection and cryptosporidiosis associated with drinking unpasteurized apple cider—Connecticut and New York, October 1996. Morbidity and Mortality Weekly Report 46:4–8.

CDC. 1999. Outbreak of Salmonella serotype Muenchen infections associated with unpasteurized orange juice—United States and Canada, June 1999. Morbidity and Mortality Weekly Report 48:582–585.

CDC. 2006. Botulism associated with commercial carrot juice—Georgia and Florida. Morbidity and Mortality Weekly Report 55:1098–1099.

CDC. 2010. Investigation Update: Multistate Outbreak of Human Typhoid Fever Infections Associated with Frozen Mamey Pulp. http://www.cdc.gov/salmonella/typhoidfever/index.html. Accessed October 4, 2011.

CDC. 2011. Foodborne Outbreak Online Database (FOOD). http://wwwn.cdc.gov/foodborneoutbreaks/Default.aspx. Accessed October 4, 2011.

Cody, S. H., K. Glynn, J. A. Farrar, K. L. Cairns, P. M. Griffin, J. Kobayashi, M. Fyfe, R. Hoffman, A. S. King, J. H. Lewis, B. Swaminathan, R. G. Bryant, and D. J. Vugia. 1999. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Annals of Internal Medicine 130:202–209.

Cook, K. A., T. E. Dobbs, W. G. Hlady, J. G. Wells, T. J. Barrett, N. D. Puhr, G. A. Lancette, D. W. Bodager, W. L. Toth, C. A. Genese, A. K. Highsmith, K. E. Pilot, L. Finelli, and D. L. Swerdlow. 1998. Outbreak of Salmonella serotype Hartford infections associated with unpasteurized orange juice. Journal of the American Medical Association 280:1504–1509.

Duncan, T. G., J. A. Coull, E. R. Miller, and H. Bancroft. 1946. Outbreak of typhoid fever with orange juice as the vehicle illustrating the value of immunization. American Journal of Public Health 36:34–36.

Eisenstein, A. B., R. D. Aach, W. Jacobson, and A. Goldman. 1963. An epidemic of infectious hepatitis in a general hospital. Journal of the American Medical Association 185:171–174.

FDA (U.S. 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. http://www.fda.gov/Food/FoodSafety/HazardAnalysisCriticalControlPointsHACCP/JuiceHACCP/ucm082031.htm. Accessed October 4, 2011.

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.

FDA. 2010. DHMH Issues Consumer Alert Regarding Recall of Baugher’s Apple Cider. http://www.fda.gov/Safety/Recalls/ucm232878.htm. Accessed October 4, 2011.

IFT/FDA (Institute of Food Technologists/U.S. Food and Drug Administration). Outbreaks associated with fresh and fresh-cut produce: Incidence, growth, and survival of pathogens in fresh and fresh-cut produce. In Analysis and Evaluation of Preventive Control Measures for the Control and Reduction/Elimination of Microbial Hazards on Fresh and Fresh-Cut Produce, A Report of the Institute of Food Technologists for the Food and Drug Administration of the United States Department of Health and Human Services, September 30, 2001. http://www.fda.gov/Food/ScienceResearch/ResearchAreas/SafePracticesforFoodProcesses/ucm091270.htm. Accessed October 4, 2011.

INS DOH (Indiana State Department of Health). Summary of Special Disease Outbreak Investigations—1997, Appendix E. http://www.in.gov/isdh/21186.htm. Accessed October 5, 2011.

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.

Lester, R., T. Stewart, J. Carnie, S. Ng, and R. Taylor. 1991. Air travel-associated gastroenteritis outbreak, August 1991. Communicable Disease Intelligence 15:292–293.

LSDEPC (Laboratory Surveillance Data for Enteric Pathogens in Canada). Annual summary 2005. http://www.nml-lnm.gc.ca/NESP-PNSME/index-eng.htm. Accessed October 4, 2005.

Millard, P. S., K. F. Gensheimer, D. G. Addiss, D. M. Sosin, G. A. Beckett, A. Houck-Jankoski, and A. Hudson. 1994. An outbreak of cryptosporidiosis from fresh-pressed apple cider. Journal of the American Medical Association 272:1592–1596.

National Centre for Disease Control/Communicable Diseases Network Australia New Zealand, Australian Department of Health and Aged Care. 1999. Salmonellosis outbreak, South Australia. Communicable Diseases Intelligence 23(3):73.

Paquet, P. 1923. Épidémie de fièvre typhoïde: Déterminée par la consommation de petit citre. Revue d’Hygiène 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.

SVS (Secretaria de Vigilância em Saúde do Ministério da Saúde, Brasil). 2005a. Doença de Chagas Aguda relacionada à ingestão de caldo de cana em Santa Catarina. Nota Técnica, 4 de abril de 2005. http://portal.saude.gov.br/portal/saude/visualizar_texto.cfm?idtxt=21270.

SVS. 2005b. Doença de Chagas Aguda no município de Santana—Amapá. Nota Técnica, 4 de abril de 2005. http://portal.saude.gov.br/portal/saude/visualizar_texto.cfm?idtxt=21310.

SVS. 2007a. Doença a de Chagas Aguda. Nota Técnica, 9 de outubro de 2007. http://portal.saude.gov.br/portal/arquivos/pdf/nota_chagas_091007.pdf.

SVS. 2007b. Surto de doença de Chagas agudo (DCA) em Coari/Amazonas—abril de 2007. Nota Técnica, 11 de maio de 2007. http://portal.saude.gov.br/portal/saude/visualizar_texto.cfm?idtxt=26087. Accessed December 12, 2007.

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 1922–2010

Type

Product

Pathogena

Year

Location

Venue

Cases (deaths)b

Referencec

Açaí

Unspecified

Trypanosoma cruzid

2004

Brazil

Retail

27

SVS, 2005b; Pereira et al., 2009

 

Unspecified

Trypanosoma cruzi

2007

Brazil

Retail

25

SVS, 2007b; Pereira et al., 2009

 

Apple

Unpasteurized

S. Typhi

1922

France

NRe

23 (0)

Paquet, 1923

 

Unpasteurized

S. Typhimurium

1974

USA (NJ)

Farm, small retail outlets

296 (0)

CDC, 1975

 

Unpasteurized

E. coli O157:H7 (suspected)

1980

Canada (ON)

Local market

14 (1)

Steele et al., 1982

 

Unpasteurized

E. coli O157:H7

1991

USA (MA)

Small cider mill

23 (0)

Besser et al., 1993

 

Unpasteurized

Cryptosporidium

1993

USA (ME)

School

213 (0)

Millard et al., 1994

 

Unpasteurized

C. parvum

1996

USA (NY)

Small cider mill

31 (0)

CDC, 1997

 

Unpasteurized

E. coli O157:H7

1996

USA (CT)

Small cider mill

14 (0)

CDC, 1997

 

Unpasteurized

E. coli O157:H7

1996

USA (WA)

Small cider mill

6 (0)

FDA, 2001

 

Unpasteurized

E. coli O157:H7

1996

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

Retail

70 (1)

CDC, 1996; Cody et al., 1999

 

Unpasteurized

E. coli O157:H7

1997

USA (IN)

Farm

6

INS DOH, 1997

 

Unpasteurized

E. coli O157:H7

1998

Canada (ON)

Farm/Home

14 (0)

Tamblyn et al., 1999

 

Unpasteurized

E. coli O157:H7

1999

USA (OK)

NR

25

CDC, 2011

 

Unpasteurized

C. parvum

2003

USA (OH)

Farm/Retail

144

Vojdani et al., 2008

 

Unpasteurized

E. coli O111 and C. parvum

2004

USA (NY)

Farm/Home

212

Vojdani et al., 2008

 

Unpasteurized

E. coli O157:H7

2005

Canada (ON)

NR

4

LSDEPC, 2005

 

Unpasteurized

E. coli O157:H7

2007

USA (MA)

NR

9

CDC, 2011

 

Unpasteurized

E. coli O157:H7

2008

USA (IA)

Fair

7

CDC, 2011

 

Unpasteurized

E. coli O157:H7

2010

USA (MD)

Retail

7

FDA, 2010

 

Carrot

Homemade

C. botulinum

1993

USA (WA)

Home

1 (0)

Buzby and Crutchfield, 1999

 

Pasteurized

C. botulinum

2006

USA

Retail

4

CDC, 2006

 

Coconut

Milkf

Vibrio cholerae

1991

USA (MD)

Home/picnic

4

CDC, 1991; Taylor et al., 1993

 

Guava

Unspecified

Trypanosoma cruzi

2007

Venezuela

School

103 (1)

Alarcón de Noya et al., 2010

 

Mamey

Frozen Puree

S. Typhi

1999

USA

NR

19

Katz et al., 2002

 

Frozen Pulp

S. Typhi

2010

USA

Retail

9

CDC, 2010

 

Mixed Fruit

Unspecified

Shigella sonnei

2002

Canada, USA, UK, British West Indies

Resort

78

CDC, 2011

 

Açaí, sugar cane

Trypanosoma cruzi

2006

Brazil

NR

94 (6)

SVS, 2007a; Pereira et al., 2009

 

Acai, banana, strawberry, sugar cane

Hepatitis A

2007

USA (FL)

Food Service

3

CDC, 2011

 

Mixed Fruit /Vegetable

Clover, sweet potato leaf, apple

Angiostrongylus cantonesisg

2001

Taiwan

Home

5

Tsai et al., 2004

 

Orange

Unpasteurized

Enterotoxigenic

1992

India

Roadside vendor

6 (0)

Singh et al., 1995

 

Unpasteurized

Salmonella Gaminara, Hartford and Rubislaw

1995

USA (FL)

Retail

63 (0)

CDC, 1995; Cook et al., 1998; Parish, 1998

 

Unpasteurized

Shigella flexneri

1995

South Africa

Restaurant

14

Thurston et al., 1998

 

Unpasteurized

Virus suspected

1996

USA

Food Service

2

Parish, 2000

 

Unpasteurized

S. Muenchen

1999

Canada and USA

Restaurant

423 (1)

CDC, 1999

 

Unpasteurized

S. Anatum

1999

USA (FL)

Roadside stand

6 (0)

Krause et al., 2001

 

Unpasteurized

S. Typhimurium

1999

Australia

Retail

405 (0)

National Centre for Disease Control, 1999

 

Unpasteurized

S. Enteritidis

2000

USA (6 states)

Retail and Food Service

88

Butler, 2000

 

Unpasteurized

Salmonella Typhimurium and Saintpaul

2005

USA (23 states)

Retail and Food Service

152

Jain et al., 2009

 

Reconstituted

S. Typhi

1944

USA (OH)

Hotel

18 (1)

Duncan et al., 1946

 

Reconstituted

Hepatitis A

1962

USA (MO)

Hospital

24

Eisenstein et al., 1963

 

Reconstituted

Unknown

1965

USA (CA)

Football game

563

Tabershaw et al., 1967

 

Reconstituted

S. Typhi

1989

USA (NY)

Hotel

69

Birkhead et al., 1993

 

Unspecified

Norwalk-like virus

1991

Australia

Airline

3,053

Lester et al., 1991

 

Sugar cane

Unspecified

Trypanosoma cruzi

2005

Brazil

Roadside kiosk

25 (3)

SVS, 2005a; Pereira et al., 2009

 

Watermelon

Homemade

Salmonella spp

1993

USA (FL)

Home

18 (0)

FDA, 1998

a Pathogens abbreviated and associated with outbreaks include S. – Salmonella; E. – Escherichia; C. parvum – Cryptosporidium parvum; C. botulinum – Clostridium botulinum.

b The number in parenthesis 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 cantonensis, 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, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Published January 2012. Visit the EDIS website at http://edis.ifas.ufl.edu.

2.

Michelle D. Danyluk, assistant professor, Department of Food Science and Human Nutrition, Citrus Research and Education Center, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Lake Alfred, FL 33850. Renée M. Goodrich-Schneider, associate professor; Keith R. Schneider, associate professor; Department of Food Science and Human Nutrition, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Gainesville, FL 32611-0290. Linda J. Harris, Cooperative Extension specialist–microbial food safety, Department of Food Science and Technology, University of California, Davis, CA 95616. Randy W. Worobo, associate professor, Department of Food Science and Technology, Cornell University, Geneva, NY 14456.


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.