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CDC

Hepatitis A Outbreak Associated with Green Onions at a Restaurant ---

Monaca, Pennsylvania, 2003

On November 21, 2003, this report was posted on the MMWR website (

http://www.cdc.gov/mmwr ). However, two errors* were found. The text of the

report printed here has been corrected.

The Pennsylvania Department of Health and CDC are investigating an outbreak

of hepatitis A outbreak among patrons of a restaurant (Restaurant A) in

Monaca, Pennsylvania. As of November 20, approximately 555 persons with

hepatitis A have been identified, including at least 13 Restaurant A food

service workers and 75 residents of six other states who dined at Restaurant

A. Three persons have died. Preliminary sequence analysis of a 340

nucleotide region of viral RNA obtained from three patrons who had hepatitis

A indicated that all three virus sequences were identical. Preliminary

analysis of a case-control study implicated green onions as the source of

the outbreak.

Among 207 persons with hepatitis A who were interviewed and who ate at

Restaurant A only once during the 2--6 weeks (i.e., the typical incubation

period for hepatitis A) before illness, dates of illness onset were between

October 14 and November 12. These 207 patrons reported eating food prepared

in Restaurant A during September 14--October 17; a total of 181 (87%)

persons reported eating at Restaurant A during October 3--6 (Figure). All

infected Restaurant A food service workers became ill after October 26,

suggesting that a food service worker could not have been the source of the

outbreak. However, during late October--early November, these ill food

service workers were working in Restaurant A when they could have been

infectious. For this reason, immune globulin has been provided to

approximately 9,000 persons who ate food from Restaurant A during this time

or had exposures to ill persons involved in the outbreak. The restaurant has

been closed.

A case-control study was conducted to identify menu item(s) or ingredient(s)

associated with illness. A case-patient was defined as a person who had

illness onset during October 14--November 12, had laboratory confirmation of

acute hepatitis A virus (HAV) infection (i.e., positive IgM anti-HAV),

reported eating food prepared at Restaurant A during October 3--6, and had

eaten only once at Restaurant A during the 2--6 weeks before illness onset.

Controls included persons without hepatitis A who either had dined with

case-patients at Restaurant A or were identified through credit card

receipts as having dined at Restaurant A during October 3--6. Controls with

a previous history of hepatitis A, hepatitis A vaccination, or receipt of

immune globulin within 2 weeks after eating Restaurant A food were excluded.

Enrolled case-patients and controls were asked about Restaurant A food that

they had eaten.

The median age of the 181 case-patients in the study was 34 years (range:

4--73 years), and that of the 83 controls was 28 years (range: 2--81,

p>0.05). Of 133 menu items, only chili con queso and mild salsa were

associated significantly with illness. Mild salsa was eaten by 94% of

case-patients, compared with 39% of controls (odds ratio [OR] = 24.2; 95%

confidence interval [CI] = 11.4--51.4). Chili con queso was eaten by 15% of

case-patients, compared with 3% of controls (OR = 5.2, 95% CI = 1.5--17.8).

Both menu items associated with illness contained uncooked or minimally

heated fresh green onions. Among 11 case-patients who reported not eating

mild salsa, seven ate at least one of the other 52 menu items that contained

green onions. Of 103 ingredients used at the restaurant, 12 were associated

with illness in a univariate analysis. Of these, 10 had been consumed by

<50% of case-patients. Eating a menu item containing green onions was

reported by 98% of case-patients, compared with 69% of controls (OR = 20.2,

95%CI = 6.8--59.9). Eating a menu item containing white onions also was

associated with illness. However, among the 176 case-patients who reported

eating white onions, 174 (99%) also ate green onions. Among the four

case-patients and 28 controls who reported not eating green onions, white

onions were not associated with illness (OR = 2.5, 95% 0.3--20.9).

During interviews conducted at Restaurant A, food service workers described

green onion storage, washing, and preparation practices. Green onions were

shipped in 8.5-lb. boxes containing multiple small bundles (6--8 green

onions per bundle). Each box was unpacked, and bundles were stored upright

(root side down) and refrigerated in a bucket with ice included in the

shipment. Green onions were stored <5 days before processing, which

consisted of rinsing intact onion bundles, cutting the roots off, and

removing the rubber bands. Green onions from each box were chopped by

machine to yield approximately 8 qts. Chopped green onions were refrigerated

for approximately 2 days.

Periodically (i.e., every 1--3 days), salsas were prepared in batches of

40--80 qts. Mild salsa included chopped fresh green onions; hot salsa did

not. Salsas were refrigerated in 8-quart containers with a shelf life of 3

days. Mild and hot salsa were ladled into bowls and provided free with

tortilla chips upon seating at Restaurant A.

The Food and Drug Administration (FDA), CDC, and the state health

departments are investigating the source of the green onions associated with

this outbreak and how they became contaminated with HAV. Preliminary

traceback information indicates that green onions supplied to Restaurant A

were grown in Mexico.

Reported by: V Dato, MD, A Weltman, MD, K Waller, MD, Bur of Epidemiology,

Pennsylvania Dept of Health. MA Ruta, Ohio Dept of Health. U.S. Food and

Drug Administration. Div of Viral Hepatitis, National Center for Infectious

Diseases; A Highbaugh-Battle, C Hembree, S Evenson, Epidemiology Program

Office; C Wheeler, MD, T Vogt, PhD, EIS officers, CDC.

Editorial Note:

This report describes a large hepatitis A outbreak associated with eating a

food item containing green onions at a single restaurant. The majority of

ill patrons interviewed as of November 21 were exposed during a 3-day period

in early October. No ill food service worker identified could have been the

source of the outbreak. The green onions likely were contaminated with HAV

in the distribution system or during growing, harvest, packing, or cooling.

Traceback investigations completed to date have determined that the green

onion source is one or more farms in Mexico.

Both green onions and white onions were associated with illness in the

univariate analysis. However, white onions were not associated with illness

among those who did not eat green onions. This association with white onions

observed in the univariate analysis might not remain when multivariate

modeling is completed. Restaurant A purchases previously chopped white

onions and adds them to several menu items, including hot and mild salsa.

Mild salsa, which contains both green onions and white onions, was

associated with illness; however, hot salsa, which contains only white

onions, was not associated with illness.

The genetic sequence of the outbreak strain is very similar to viral

sequences obtained from persons involved in hepatitis A outbreaks in

Tennessee, Georgia, and North Carolina during September 2003 that were

linked epidemiologically to green onions. These sequences also were

identical or very similar to sequences observed among persons with hepatitis

A living along the United States-Mexico border and travelers returning from

Mexico, consistent with a source in Mexico (CDC, unpublished data, 2003).

Raw green onions from three firms in Mexico have been implicated in the

Tennessee and Georgia outbreaks. FDA is still reviewing records to determine

if additional firms are involved. The Mexican government is assisting with

the traceback investigation in Mexico and the investigation to determine the

source of the contamination.

Previous hepatitis A outbreaks linked to green onions have been reported and

have involved patrons of a single restaurant (1). However, the outbreak at

Restaurant A was unusually large. Several characteristics of the way food

was prepared and served in Restaurant A could have contributed to the

outbreak's size, including 1) multiple opportunities for intermingling of

uncontaminated and contaminated green onions in a common bucket for 5 days

with the ice in which they were shipped and 2) serving contaminated items

with a relatively long shelf life (e.g., mild salsa) to a large proportion

of patrons over several days.

HAV is transmitted by the fecal-oral route. Green onions require extensive

handling during harvesting and preparation for packing. Contamination of

green onions could occur 1) by contact with HAV-infected workers, especially

children, working in the field during harvesting and preparation and 2) by

contact with HAV-contaminated water during irrigation, rinsing, processing,

cooling, and icing of the product. Green onions and other selected produce

items (e.g., strawberries [2]) might be more vulnerable to contamination

because plant surfaces are particularly complex or adherent to viral or

fecal particles. Outbreaks of other enteric pathogens linked to green onions

have been reported (3).

On November 15, FDA issued an alert to consumers about the recent hepatitis

A outbreaks associated with green onions (available at

http://www.fda.gov/bbs/topics/ANSWERS/2003/ANS01262.html). FDA advised

consumers concerned about the possibility of getting hepatitis A from green

onions to cook green onions thoroughly before eating and to ask about use of

green onions in prepared foods. Unless directed otherwise by public health

officials, persons who have recently eaten green onions do not need

postexposure prophylaxis (i.e., immune globulin).

CDC is working with state health departments to identify other hepatitis A

outbreaks associated with green onions. As of November 21, no other

hepatitis A outbreaks have been identified. To identify other cases related

to these outbreaks, state and local health officials should interview

persons with hepatitis A with onset after October 1. Persons without typical

risk factors for hepatitis A (4) should be asked about food and restaurant

exposures during their incubation period. Because molecular epidemiologic

techniques have been useful for identifying related cases of foodborne

hepatitis A in previous outbreaks (2), health departments might consider

obtaining serum specimens for cases of interest.

An increasing proportion of reported foodborne outbreaks have been linked to

fresh produce (3). This increase might be attributed to increased

consumption of fresh produce or better surveillance techniques. HAV

contamination of fresh produce can be reduced by using approaches such as

the application of Good Agricultural Practices/Good Manufacturing Practices

recommended by FDA (5) Recommended control measures include providing

sanitary facilities for field workers, ensuring appropriate water quality,

use of properly treated manure or biosolids, and ensuring worker health.

Reducing HAV transmission in areas where produce is grown and discouraging

the presence of children in areas where food is harvested also will reduce

opportunities for HAV contamination. Further investigation of this and other

hepatitis A outbreaks linked to green onions, including observation of

cultivation and harvesting practices, can guide additional specific critical

control measures.

References

Dentinger CM, Bower WA, Nainan OV, et al. An outbreak of hepatitis A

associated with green onions. J Infect Dis 2001;183:1273--6.

Hutin YJF, Pool V, Cramer EH, et al. A multistate, foodborne outbreak of

hepatitis A. N Engl J Med 1999;340:595--602.

Tauxe RV. Emerging foodborne diseases: an evolving public health challenge.

Emerg Infect Dis 1997;3:425--34.

CDC. Prevention of hepatitis A through active or passive immunization:

recommendations of the Advisory Committee on Immunization Practices (ACIP).

MMWR 1999;48(RR-12).

U.S. Food and Drug Administration. Guidance to industry: guide to minimize

microbial food safety hazards for fruits and vegetables, 1998. Available at

http://www.foodsafety.gov/~dms/prodguid.html.

* In the fourth sentence of the fifth paragraph, green onions were stated to

have been stored for >5 days before processing rather than <5 days. In the

third sentence of the fifth paragraph of the Editorial Note, the word " of "

appeared before " plant surfaces are particularly complex or adherent to

viral or fecal particles. "

Figure

Return to top.

Use of trade names and commercial sources is for identification only and

does not imply endorsement by the U.S. Department of Health and Human

Services.

--------------------------------------------------------------------------------

References to non-CDC sites on the Internet are provided as a service to

MMWR readers and do not constitute or imply endorsement of these

organizations or their programs by CDC or the U.S. Department of Health and

Human Services. CDC is not responsible for the content of pages found at

these sites. URL addresses listed in MMWR were current as of the date of

publication.

Disclaimer All MMWR HTML versions of articles are electronic conversions

from ASCII text into HTML. This conversion may have resulted in character

translation or format errors in the HTML version. Users should not rely on

this HTML document, but are referred to the electronic PDF version and/or

the original MMWR paper copy for the official text, figures, and tables. An

original paper copy of this issue can be obtained from the Superintendent of

Documents, U.S. Government Printing Office (GPO), Washington, DC 20402-9371;

telephone: (202) 512-1800. Contact GPO for current prices.

**Questions or messages regarding errors in formatting should be addressed

to mmwrq@....

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CDC

Hepatitis A Outbreak Associated with Green Onions at a Restaurant ---

Monaca, Pennsylvania, 2003

On November 21, 2003, this report was posted on the MMWR website (

http://www.cdc.gov/mmwr ). However, two errors* were found. The text of the

report printed here has been corrected.

The Pennsylvania Department of Health and CDC are investigating an outbreak

of hepatitis A outbreak among patrons of a restaurant (Restaurant A) in

Monaca, Pennsylvania. As of November 20, approximately 555 persons with

hepatitis A have been identified, including at least 13 Restaurant A food

service workers and 75 residents of six other states who dined at Restaurant

A. Three persons have died. Preliminary sequence analysis of a 340

nucleotide region of viral RNA obtained from three patrons who had hepatitis

A indicated that all three virus sequences were identical. Preliminary

analysis of a case-control study implicated green onions as the source of

the outbreak.

Among 207 persons with hepatitis A who were interviewed and who ate at

Restaurant A only once during the 2--6 weeks (i.e., the typical incubation

period for hepatitis A) before illness, dates of illness onset were between

October 14 and November 12. These 207 patrons reported eating food prepared

in Restaurant A during September 14--October 17; a total of 181 (87%)

persons reported eating at Restaurant A during October 3--6 (Figure). All

infected Restaurant A food service workers became ill after October 26,

suggesting that a food service worker could not have been the source of the

outbreak. However, during late October--early November, these ill food

service workers were working in Restaurant A when they could have been

infectious. For this reason, immune globulin has been provided to

approximately 9,000 persons who ate food from Restaurant A during this time

or had exposures to ill persons involved in the outbreak. The restaurant has

been closed.

A case-control study was conducted to identify menu item(s) or ingredient(s)

associated with illness. A case-patient was defined as a person who had

illness onset during October 14--November 12, had laboratory confirmation of

acute hepatitis A virus (HAV) infection (i.e., positive IgM anti-HAV),

reported eating food prepared at Restaurant A during October 3--6, and had

eaten only once at Restaurant A during the 2--6 weeks before illness onset.

Controls included persons without hepatitis A who either had dined with

case-patients at Restaurant A or were identified through credit card

receipts as having dined at Restaurant A during October 3--6. Controls with

a previous history of hepatitis A, hepatitis A vaccination, or receipt of

immune globulin within 2 weeks after eating Restaurant A food were excluded.

Enrolled case-patients and controls were asked about Restaurant A food that

they had eaten.

The median age of the 181 case-patients in the study was 34 years (range:

4--73 years), and that of the 83 controls was 28 years (range: 2--81,

p>0.05). Of 133 menu items, only chili con queso and mild salsa were

associated significantly with illness. Mild salsa was eaten by 94% of

case-patients, compared with 39% of controls (odds ratio [OR] = 24.2; 95%

confidence interval [CI] = 11.4--51.4). Chili con queso was eaten by 15% of

case-patients, compared with 3% of controls (OR = 5.2, 95% CI = 1.5--17.8).

Both menu items associated with illness contained uncooked or minimally

heated fresh green onions. Among 11 case-patients who reported not eating

mild salsa, seven ate at least one of the other 52 menu items that contained

green onions. Of 103 ingredients used at the restaurant, 12 were associated

with illness in a univariate analysis. Of these, 10 had been consumed by

<50% of case-patients. Eating a menu item containing green onions was

reported by 98% of case-patients, compared with 69% of controls (OR = 20.2,

95%CI = 6.8--59.9). Eating a menu item containing white onions also was

associated with illness. However, among the 176 case-patients who reported

eating white onions, 174 (99%) also ate green onions. Among the four

case-patients and 28 controls who reported not eating green onions, white

onions were not associated with illness (OR = 2.5, 95% 0.3--20.9).

During interviews conducted at Restaurant A, food service workers described

green onion storage, washing, and preparation practices. Green onions were

shipped in 8.5-lb. boxes containing multiple small bundles (6--8 green

onions per bundle). Each box was unpacked, and bundles were stored upright

(root side down) and refrigerated in a bucket with ice included in the

shipment. Green onions were stored <5 days before processing, which

consisted of rinsing intact onion bundles, cutting the roots off, and

removing the rubber bands. Green onions from each box were chopped by

machine to yield approximately 8 qts. Chopped green onions were refrigerated

for approximately 2 days.

Periodically (i.e., every 1--3 days), salsas were prepared in batches of

40--80 qts. Mild salsa included chopped fresh green onions; hot salsa did

not. Salsas were refrigerated in 8-quart containers with a shelf life of 3

days. Mild and hot salsa were ladled into bowls and provided free with

tortilla chips upon seating at Restaurant A.

The Food and Drug Administration (FDA), CDC, and the state health

departments are investigating the source of the green onions associated with

this outbreak and how they became contaminated with HAV. Preliminary

traceback information indicates that green onions supplied to Restaurant A

were grown in Mexico.

Reported by: V Dato, MD, A Weltman, MD, K Waller, MD, Bur of Epidemiology,

Pennsylvania Dept of Health. MA Ruta, Ohio Dept of Health. U.S. Food and

Drug Administration. Div of Viral Hepatitis, National Center for Infectious

Diseases; A Highbaugh-Battle, C Hembree, S Evenson, Epidemiology Program

Office; C Wheeler, MD, T Vogt, PhD, EIS officers, CDC.

Editorial Note:

This report describes a large hepatitis A outbreak associated with eating a

food item containing green onions at a single restaurant. The majority of

ill patrons interviewed as of November 21 were exposed during a 3-day period

in early October. No ill food service worker identified could have been the

source of the outbreak. The green onions likely were contaminated with HAV

in the distribution system or during growing, harvest, packing, or cooling.

Traceback investigations completed to date have determined that the green

onion source is one or more farms in Mexico.

Both green onions and white onions were associated with illness in the

univariate analysis. However, white onions were not associated with illness

among those who did not eat green onions. This association with white onions

observed in the univariate analysis might not remain when multivariate

modeling is completed. Restaurant A purchases previously chopped white

onions and adds them to several menu items, including hot and mild salsa.

Mild salsa, which contains both green onions and white onions, was

associated with illness; however, hot salsa, which contains only white

onions, was not associated with illness.

The genetic sequence of the outbreak strain is very similar to viral

sequences obtained from persons involved in hepatitis A outbreaks in

Tennessee, Georgia, and North Carolina during September 2003 that were

linked epidemiologically to green onions. These sequences also were

identical or very similar to sequences observed among persons with hepatitis

A living along the United States-Mexico border and travelers returning from

Mexico, consistent with a source in Mexico (CDC, unpublished data, 2003).

Raw green onions from three firms in Mexico have been implicated in the

Tennessee and Georgia outbreaks. FDA is still reviewing records to determine

if additional firms are involved. The Mexican government is assisting with

the traceback investigation in Mexico and the investigation to determine the

source of the contamination.

Previous hepatitis A outbreaks linked to green onions have been reported and

have involved patrons of a single restaurant (1). However, the outbreak at

Restaurant A was unusually large. Several characteristics of the way food

was prepared and served in Restaurant A could have contributed to the

outbreak's size, including 1) multiple opportunities for intermingling of

uncontaminated and contaminated green onions in a common bucket for 5 days

with the ice in which they were shipped and 2) serving contaminated items

with a relatively long shelf life (e.g., mild salsa) to a large proportion

of patrons over several days.

HAV is transmitted by the fecal-oral route. Green onions require extensive

handling during harvesting and preparation for packing. Contamination of

green onions could occur 1) by contact with HAV-infected workers, especially

children, working in the field during harvesting and preparation and 2) by

contact with HAV-contaminated water during irrigation, rinsing, processing,

cooling, and icing of the product. Green onions and other selected produce

items (e.g., strawberries [2]) might be more vulnerable to contamination

because plant surfaces are particularly complex or adherent to viral or

fecal particles. Outbreaks of other enteric pathogens linked to green onions

have been reported (3).

On November 15, FDA issued an alert to consumers about the recent hepatitis

A outbreaks associated with green onions (available at

http://www.fda.gov/bbs/topics/ANSWERS/2003/ANS01262.html). FDA advised

consumers concerned about the possibility of getting hepatitis A from green

onions to cook green onions thoroughly before eating and to ask about use of

green onions in prepared foods. Unless directed otherwise by public health

officials, persons who have recently eaten green onions do not need

postexposure prophylaxis (i.e., immune globulin).

CDC is working with state health departments to identify other hepatitis A

outbreaks associated with green onions. As of November 21, no other

hepatitis A outbreaks have been identified. To identify other cases related

to these outbreaks, state and local health officials should interview

persons with hepatitis A with onset after October 1. Persons without typical

risk factors for hepatitis A (4) should be asked about food and restaurant

exposures during their incubation period. Because molecular epidemiologic

techniques have been useful for identifying related cases of foodborne

hepatitis A in previous outbreaks (2), health departments might consider

obtaining serum specimens for cases of interest.

An increasing proportion of reported foodborne outbreaks have been linked to

fresh produce (3). This increase might be attributed to increased

consumption of fresh produce or better surveillance techniques. HAV

contamination of fresh produce can be reduced by using approaches such as

the application of Good Agricultural Practices/Good Manufacturing Practices

recommended by FDA (5) Recommended control measures include providing

sanitary facilities for field workers, ensuring appropriate water quality,

use of properly treated manure or biosolids, and ensuring worker health.

Reducing HAV transmission in areas where produce is grown and discouraging

the presence of children in areas where food is harvested also will reduce

opportunities for HAV contamination. Further investigation of this and other

hepatitis A outbreaks linked to green onions, including observation of

cultivation and harvesting practices, can guide additional specific critical

control measures.

References

Dentinger CM, Bower WA, Nainan OV, et al. An outbreak of hepatitis A

associated with green onions. J Infect Dis 2001;183:1273--6.

Hutin YJF, Pool V, Cramer EH, et al. A multistate, foodborne outbreak of

hepatitis A. N Engl J Med 1999;340:595--602.

Tauxe RV. Emerging foodborne diseases: an evolving public health challenge.

Emerg Infect Dis 1997;3:425--34.

CDC. Prevention of hepatitis A through active or passive immunization:

recommendations of the Advisory Committee on Immunization Practices (ACIP).

MMWR 1999;48(RR-12).

U.S. Food and Drug Administration. Guidance to industry: guide to minimize

microbial food safety hazards for fruits and vegetables, 1998. Available at

http://www.foodsafety.gov/~dms/prodguid.html.

* In the fourth sentence of the fifth paragraph, green onions were stated to

have been stored for >5 days before processing rather than <5 days. In the

third sentence of the fifth paragraph of the Editorial Note, the word " of "

appeared before " plant surfaces are particularly complex or adherent to

viral or fecal particles. "

Figure

Return to top.

Use of trade names and commercial sources is for identification only and

does not imply endorsement by the U.S. Department of Health and Human

Services.

--------------------------------------------------------------------------------

References to non-CDC sites on the Internet are provided as a service to

MMWR readers and do not constitute or imply endorsement of these

organizations or their programs by CDC or the U.S. Department of Health and

Human Services. CDC is not responsible for the content of pages found at

these sites. URL addresses listed in MMWR were current as of the date of

publication.

Disclaimer All MMWR HTML versions of articles are electronic conversions

from ASCII text into HTML. This conversion may have resulted in character

translation or format errors in the HTML version. Users should not rely on

this HTML document, but are referred to the electronic PDF version and/or

the original MMWR paper copy for the official text, figures, and tables. An

original paper copy of this issue can be obtained from the Superintendent of

Documents, U.S. Government Printing Office (GPO), Washington, DC 20402-9371;

telephone: (202) 512-1800. Contact GPO for current prices.

**Questions or messages regarding errors in formatting should be addressed

to mmwrq@....

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